Walnuts may not seem like summer fruits, but they are – as long as you have the right recipe.  Katherine takes you to the heart of French walnut country for green walnut season.

Public domain, via wikimedia commons

English walnuts do not come from England. The English walnut came to American shores from England, but the English got them from the French. The (now) French adopted walnut cultivation from the Romans two millennia ago, back when they were still citizens of Gallia Aquitania. Some people call this common walnut species “Persian walnut,” a slightly better name, as it does seem to have evolved originally somewhere east of the Mediterranean. But the most accurate name for the common walnut is Juglans regia, which means something like “Jove’s kingly nuts.” I think of them as queenly nuts, in honor of Eleanor of Aquitaine, because if any queen had nuts, she certainly did. During her lifetime the Aquitaine region of France became a major exporter of walnuts and walnut oil to northern Europe, and it remains so more than 800 years later.

French walnut culture may actually predate the Romans by tens of millennia, as archeological and paleobotanical evidence places walnut trees and early modern humans in the same locations at the same time. The Périgord region of Aquitaine in south western France is home to the original Cro-Magnon site and some of the richest archeological remains of early modern humans in Europe. Prehistoric pollen deposits show that walnuts grew wild in this same area, and that isolated walnut populations in France and Spain may have survived the last ice age (Carrion & Sanchez-Gomez 1992; refs in Henry 2010). Thus the earliest modern humans in Europe could have gathered the nuts. It probably would have been worth their effort since even wild walnuts are abundant, large, nutritious, caloric, and easy to process.

But did they? The romantic notion that Cro-magnons gathered walnuts has passed from mere plausibility into cherished legend in French walnut country. The professional organization of Périgord nut producers  suggests that the same people who adorned the walls of Lascaux with animal paintings 17 thousand years ago may have enjoyed their roasted aurochs encrusted with a golden layer of crushed walnuts.

“Lascaux painting” by Prof saxx – Own work. Licensed under CC BY-SA 3.0 via Wikimedia Commons.

(I eventually found a likely source for this claim: a brief mention, in a 1963 note in the bulletin of the French Prehistorical Society, of broken walnut shells in a cave dated to about 12 to 14 thousand years before present.) Whatever their role in early modern human diets, there is solid evidence that walnuts gained importance in Roman times (Figueiral & Séjalon 2013), and today they are deeply embedded in the culture of south west France.

From Jove to John
On an afternoon in late June, deep in French walnut country, I stood on the street and wondered aloud about “nut wine.” The street was the only navigable one in La Roque-Gageac, a tiny medieval town carved into a cliff face over the Dordogne river. Within a block I had already seen vin de noix, walnut wine, offered at two shops and the restaurant of the hotel where our small band of pilgrims would stay that night. Our friend Pascal explained that walnut wine was a regional specialty, made at home by just about everyone in his grandparents’ generation and many generations before them. When the woman who greeted our table at the hotel told us that they made their own vin de noix following an old recipe, I had to try it. It was served slightly cool, cellar temperature, but it tasted warm and rich and honey-spiced. After one sip I knew I would be making this at home myself.

As it turns out, late June was the perfect time of year to discover nut wine. Vin de noix is not fermented walnut juice. It is Bordeaux wine that has been augmented with crushed macerated young walnut fruits, green husks and all. The recipe also includes eau de vie, among other things, and requires several months to mellow (see recipe below). According to tradition, the best young walnuts are harvested around the feast day of St. Jean-Baptiste on the 24th of June. After that, the shells inside start to harden, and cutting them becomes impossible or dangerous.

What is a walnut?
In their natural state, the sculptured shells of walnuts are covered in a thick green rind or husk, derived from the walnut flower.  Since the husk is sticky, stinky, and makes terrible stains, it is removed before walnuts are sent to market.  To make walnut wine, then, you have to find your own walnut tree.  More on that below.

The next most natural and inclusive form of walnut would be those still in the shell.  You might buy walnuts in the shell if you like the way they look in a bowl or want to slow the pace of your snacking.  About a third of US production is sold this way (NASS 2014).  The hard shells are derived from the ovary, so in botanical terms the shells are part of the fruit proper (pericarp, and specifically endocarp).  The shell layer starts out as living tissue whose cells have soft walls and the capacity for growth.  As the walnut fruits reach full size, however, the specialized cells of the shell start to thicken their own walls by adding layers from the inside, until the living part of each cell is reduced to a tiny little pocket inside a ridiculously well defended fortress.  Eventually the cells cannot communicate with the outside world and they die.  If you harvest walnuts right after John-the-Baptist day, though, the shell will still be alive and soft, and the nuts will be easy to cut.

The most prized part of a walnut fruit is the rich oily seed inside.  The fat brain-shaped walnut halves are mostly the cotyledons, which would have become the first leaves of a walnut seedling had the seed been allowed to germinate.   [As reader Dianne points out below, the cotyledons in this species stay below ground and do not photosynthesize, but rather provide nutrients to the seedling.  You would not see them above ground, as with a common bean cotyledon, for example.]  The central body of the walnut embryo lies along the tear-drop shaped area where the two halves were joined in the shell.  The seed is covered with a thin brown seed coat, shot through with branching veins that once carried nutrients to the developing seed.  That seed coat also contains a lot of phenolic compounds, and at least one of them can leach into dough and give bread a purple cast.

Although we rarely see it, the husk (or “hull”) is the most interesting part of our walnut story.  For one thing, the husk is complicated because it is composed of several different types of tissue fused together in a way that undermines its straightforward classification as a fruit. 

Walnuts as pseudodrupes. Click to enlarge

If the husk were derived from ovary tissue alone, the fruit would be called a drupe; however only the very inner part of the husk comes from the ovary.  Surrounding that layer are four thick sepals fused side-to-side, which are in turn covered by a layer of fused bracts. 

click to enlarge

To me, the husk of a young fruit looks like a thick green sweater over a green shirt, with the tips of the sepals emerging liked a popped collar.  (Stretching the comparison, the ovarian layer might be the undershirt you never see.)  All that extra-ovarian tissue has led most botanists to classify walnuts as pseudo-drupes.  In this way, the walnut is similar to its cousin, the pecan, albeit simpler.  (The pecan husk splits open, further complicating the fruit type.  See here for more of that story.  It also turns out that J. regia is probably the only walnut species with a splitting husk.  Things are getting really complicated now.)

Loving and hating the husks
The keepers of nut lore fondly repeat the saying that “Nothing is lost from the Perigord walnut except the sound of its cracking.”  (Rien n’est perdu dans la Noix du Périgord sauf le bruit qu’elle fait en se cassant.)  The nutmeats, shells, and husks all have their uses, as it turns out.

Walnut husks are sticky with resinous glandular hairs, and their flesh is full of the compounds juglone and gallic acid.  Juglone is a famously bad party guest because it kills other plants and stains everything it touches.  Juglone is present throughout the walnut tree, from leaves to roots, and the soil under a walnut tree can be extremely toxic to tomatoes and a wide array of other plants.  Black walnuts (J. nigra), native in much of the eastern US, are especially potent.  There were a couple of black walnut trees in the back yard of my childhood home, encroaching upon the most obvious spot for a vegetable garden.  Our tomatoes did well in fresh soil in a raised bed, unless their roots found their way into the deeper walnuty soil.  Then, in my dad’s words, they looked like they’d been “hit with a blow torch.”  I also remember stained bare feet and spots on the carpet, but it was worth it – those black walnuts tasted like caramel and anise.

Gallic acid is a much nicer component of the husk.  It is a phenolic acid found in many plants, including tea leaves, grape skins, and oak bark.  It is astringent and seems to make up the largest fraction of what leaches out of the walnut husks and into our nut wine, with juglone also contributing some flavor and color (Stampar et al. 2006, Mrvcic et al. 2012).  Although the etymology gods missed a great opportunity, gallic acid is not named for the people of Gallia Aquitania and their famous walnuts.  It was originally obtained from oak galls.

Making walnut wine
As soon as I returned from France in early July I hurried to collect my own green walnuts.  Walnut trees grow abundantly along the creek beside the public trail where I run, and their fruits were still small and green.  These trees are not English walnuts, but the descendants of native California walnuts (Juglans hindsii) planted by the 19th century owners of the parcels along the creek.

Making vin de noix is simple, although you need good tools.  As long as the shells are still soft, they are not hard to cut, but a large sharp knife and a solid cutting board are essential.  I found out the hard way that I should have worn gloves and an old apron, since there’s no getting around the juglone.  I spent two weeks hiding my henna-colored thumbs.  The stains looked especially nasty because Juglone has a way of finding dead skin – cuticles, fingerprint ridges, the stuff right under your nails, and the rough places on the sides of your fingers.  A pumice stone and patience help.

Green walnuts, staining the cutting board. Husks start to brown (oxidize) as soon as they are cut.

Vin de Noix
One bottle (750 ml) of ordinary Bordeaux wine
200 g sugar (approximately 1 cup)
100 ml (2 mini bottles) of Poire Williams or pear-flavored vodka
4 green walnuts, quartered
a cinnamon stick

Collect the walnuts the last week of June. Traditionalists prefer June 24th, St. Jean-Baptiste day; pagans may opt for the summer solstice.  As the planet warms, collecting earlier in June will probably be necessary.

Wash the walnuts and quarter them with a large butcher’s knife.  They will stain your fingers and cutting board a greenish brown color unless you wear gloves and protect the board with thick paper.

Pour all of the ingredients into a pitcher and stir to dissolve the sugar.  Cover the pitcher and let the mixture sit for a Biblical 40 days and 40 nights of soaking.  Stir once a week and remove any floating fruit flies.

Strain the mixture, put it back into an empty wine bottle, and seal it with a cork.  Allow the wine to mellow until Christmas or the winter solstice, whichever suits your worldview.

Serve as an aperitif and make a toast to old friends and summer adventures

References
Carrion, J.S. and P. Sanchez-Gomez (1992) Palynological data in support of the survival of walnut (Juglans regia L.) in the western Mediterranean area during last glacial times. Journal of Biogeography 19: 623-630

Cheynier André. Présence du noyer à l’époque azilienne. In: Bulletin de la Société préhistorique de France. 1963, tome 60, N. 1-2. p. 74.
doi : 10.3406/bspf.1963.3885

Figueiral, I. and P. Séjalon (2013) Archaeological wells in southern France: Late Neolithic to Roman plant remains from Mas de Vignoles IX (Gard) and their implications for the study of settlement, economy and environment. Environmental Archaeology

Henry, A. G. (2010) Plant foods and the dietary ecology of Neandertals and modern humans. PhD dissertation for The George Washington University

Mrvcic, J. et al. (2012) Spirit drinks: a source of dietary polyphenols. Croat. J. Food Sci. Technol. 4: 102-111

National Agricultural Statistics Service of the USDA (2014)

Stampar, F, et al. (2006) Traditional walnut liqueur – cocktail of phenolics
Food Chem., 95 (2006), pp. 627–631

Other vin de noix recipes:
http://www.atelierdeschefs.fr/fr/recette/15505-vin-de-noix.php
http://lacuisinedelilly.canalblog.com/archives/2014/06/23/30112218.html
http://tomatesansgraines.blogspot.com/2014/06/vin-de-noix-maison.html

Coconut palms grow some of the biggest seeds on the planet (coconuts), and the tiny black specks in very good real vanilla ice cream are clumps of some of the smallest, seeds from the fruit of the vanilla orchid (the vanilla “bean”). Both palms and orchids are in the large clade of plants called monocots. About a sixth of flowering plant species are monocots, and among them are several noteworthy botanical record-holders and important food plants, all subject to biological factors pushing the size of their seeds to the extremes.

People seem innately fascinated by biological extremes—what is biggest, smallest, fastest, slowest, oldest, smelliest, most dangerous or most of whatever other adjective is of interest. The satisfaction of parameterizing our known world with this trivia motivates us to leaf through The Guinness Book of World Records and stand in awe of the General Sherman tree, and perhaps it similarly inspired Christ to invoke extreme seed size in the “Mustard Seed Parable” (Matthew 13:31-32):

“He set another parable before them, saying, ‘The Kingdom of Heaven is like a grain of mustard seed, which a man took, and sowed in his field; which indeed is smaller than all seeds. But when it is grown, it is greater than the herbs, and becomes a tree, so that the birds of the air come and lodge in its branches.’”

yellow and brown mustard seeds, on a saucer

We’ll forgive his smudging of botanical fact into allegory. After all, though mustard seeds are not the smallest seeds on Earth (and grow into decent-sized weeds, not trees), they are pretty small, and it’s unlikely that his audience of farmers in the Holy Land were familiar with tropical epiphytic orchids. The range of seed size in the modern flora should capture our interest beyond metaphor, however, as it happens to be extraordinary and involves some interesting evolutionary history, and seed size affects many aspects of a plant’s life. Seed size in the modern flora spans 11.5 orders of magnitude by mass (Moles et al. 2005), and the entire range is encompassed by a single group of plants that consists of about a sixth of modern flowering plant species.

Double coconut seed

Both the species with the largest seeds (the double coconut palm, Lodoicea maldivica, family Arecaceae) and the species with the smallest seeds (various epiphytic orchids, Orchidaceae) in the world are monocots, members of the large, monophyletic (derived from a single common ancestor) Monocotyledon clade, which split from the rest of the angiosperms and began diversifying relatively early in angiosperm (flowering plant) evolution. Technically, the double coconut and the orchid species with the tiniest of the microscopic orchid seeds are beyond the usual scope of this blog, as they’re not food plants.

squirrel monkey in a coconut palm

Another very large-seeded palm, however, the coconut (Cocos nucifera), and another orchid with exceedingly small seeds, the vanilla orchid (Vanilla planifolia), could very well be in your pantry right now (or will be soon, if you decide to bake the Extreme Monocot Cookies from the recipe below) and are certainly representative of the tail ends of the seed size range. Boasting the biggest and smallest seeds alone would make the monocots noteworthy. Monocots also, however, are directly or indirectly (as animal forage) responsible for a large fraction (most?) of the calories consumed by people worldwide. Before we speculate about what forces may have pushed seed sizes in monocots, we should take a moment to further appreciate the clade.

The monocots (and a sort of stream-of-consciousness account of some botanical record holders)

In addition to the single (“mono”) cotyledon (embryonic leaf) that gives the clade its name, most of the 60,000+ monocot species are characterized by a list of features that you probably had to memorize at some point for a test (summarized here), including, in part, parallel leaf veins, flower parts in groups of threes, pollen with a single pore, unique vasculature and lack of true secondary growth (described by Katherine in her asparagus post), and adventitious roots (which are mechanically impressive, as Katherine explains in her post about leeks). The monocots of particular interest here are vanilla, which is one of the 20,000+ species of orchids (family Orchidaceae; order Asparagales), and the palms (family Arecaceae; order Arecales), which provide coconuts, dates, palm oil, and numerous tropical fruits, include acaí. Monocots also include the 15,000+ species in the grass family (Poaceae; Poales), which covers a large fraction of the planet in pasture and provides the world with grains, sugarcane, and bamboo. Other edible monocots are on the phylogeny below.

Phylogenetic relationships among the 11 monocot orders (names ending with “ales”) and common monocot food plants, shown with phylogenetic position of taxa basal to the monocots (ferns, gymnosperms and basal angiosperms), and the split between monocots and the rest of the angiosperms, notably eudicots. Seeds (instead of spores) first appeared in gymnosperms, so gymnosperms and angiosperms are seed plants. Order and family topology is from the Missouri Botanical Garden’s Angiosperm Phylogeny website; subfamily phylogeny within the Poaceae from my gluten post; note that the yam here is not sweet potato, which is an unrelated eudicot.

Monocots incidentally also include the smallest flowering plant species, the aquatic duckweed Wolffia (Araceae), which also makes the smallest flowers, which mature into the smallest fruit, but these smallest fruits do not contain the smallest seeds. That distinction goes, as I have mentioned and will explain below, to the orchids. The Wolffia fruit is a thin husk that barely coats the single seed inside it, which is about the same size as a grain of table salt (sodium chloride). Orchid fruits, in contrast, are pods that can contain up to multiple millions of seeds, each of which can be smaller than a grain of salt and weigh less than a microgram. That is, tiny seeds in not-so-tiny fruits.

In The Private Life of Plants, David Attenborough claims that, at 34 square feet, the world’s largest undivided leaves belong to a giant Bornean arum (I think he’s talking about Alocasia robusta), which is awesomely in the same plant family as the miniscule Wolffia (and therefore also a monocot). “Undivided” means that the leaf lacks the feathery dissections like a palm leaf or division into leaflets, like in a clover. As much as I admire Attenborough, though, the A. robusta leaf is probably not the biggest. The undivided circular leaves of the giant water lily (Victoria amazonica; Nymphaceacea), a basal angiosperm, can have a 10-foot diameter (78 square feet in surface area) and are therefore larger than the arum leaves, as noted by botanist Wayne Armstrong on his fabulous page on botanical trivia. Interestingly, both the very large size of the waterlily pad and the very tiny body of duckweed may be construed as alternative adaptations to living in water, so maybe on terra firme the point goes to Attenborough.

titan arum

Not to be easily dismissed, though, the arum family, Araceae, also boasts the largest unbranched inflorescence (flower stalk), on the Bornean titan arum. Its Latin name, Amorphophallus titanium, means “giant mis-shapen penis,” a reference to that inflorescence. This guy is responsible for that name (I think). The titan arum is also in the running for the stinkiest flower. Its inflorescence strongly smells of rotting carrion to attract flies that pollinate the flowers as they’re searching for the source of the smell. More importantly, though, the arum family gives us taro root (Colocasia esculenta), an important staple food throughout the tropics. The largest branched inflorescence? From a palm. The largest single flower, though, Rafflesia arnoldii, is a eudicot, but like the titan arum, it also lives in the rainforests of Borneo and strongly reeks of carrion to attract flies. Being on an island (Borneo) might have something to do with the large size of these flower structures, although that’s just rampant speculation on my part. Island life often evolutionarily pushes taxa to be exceptionally larger or smaller than their mainland relatives (see David Quammen’s The Song of the Dodo for a great discussion of the biological consequences of island habitats). Such appears to be the case for the double coconut palm, which has a very limited natural range in the Seychelles and is much larger than its closest relatives.

Colocasia leaves

Back to leaves for a moment, though. The matter of the species with the smallest leaf is complicated, but 80 feet in length, the biggest dissected leaves, along with those largest seeds, are from palms (family Arecaceae; those 80-footers are from an African palm, Raphia regalis). Those super large palm seeds, though, don’t house particularly large plant embryos. According to Armstrong, the biggest embryo is in the seed of the legume Mora oleifera, a eudicot. The Mora seed is probably the largest eudicot seed, but with a weigh around a kilogram, it’s an order of magnitude lighter than the double coconut, whose mass can top out around 20kg. The ecological factors pushing seed size evolution likely similarly affect all major clades of flowering plants, and most flowering plant species are eudicots, not monocots. Therefore, it seems remarkable to me that the monocots hold so many botanical size records, including seed size records. I’d love to know what makes them so seemingly structurally labile.

Seed size variation

a vanilla bean and a coconut (in a lab exercise about seed size)

So why are orchid seeds so small, and coconut seeds so big? The job of the seed is to help maximize the chances that it will land in a good place for the embryo within it to grow, to protect the plant embryo until conditions are right for germination, and to help the newborn seedling establish. All of these components of that job can push seed size toward being large or small. As Katherine noted in her excellent post about black-eyed peas (seeds), it would seem that the interests of the embryo should determine seed characteristics. In most species, however, a mother plant produces more than one seed, and she must hedge her bets across all her offspring, and seed size is under maternal control. The seeds of most species store a certain amount of nutritive tissue (endosperm or cotyledon, depending on the taxon) to support the seedling after germination until it can photosynthesize on its own. Producing seeds, therefore, is energetically and nutritionally expensive for the mother plant, and she only has a certain amount of energy and nutrients to allocate to seed production. She can therefore either invest a large fraction of that allocated amount into each of a few large seeds, or she can invest a smaller fraction into each of several smaller seeds. There is cool math that describes this seed size vs. number tradeoff with reasonably well supported predictions (Leishman et al. 2000) about how the mother plant should allocate her reproductive effort across her seeds under different scenarios. Across all species, however, there are a few trends in the relationship between seed size and a plant’s habitat and life history (Leishman et al. 2000, Moles et al. 2005).

Rose family fruit (in a lab exercise). Smallest seeds are in the blackberries and raspberries in the petri dish in the far right corner, the largest in the tree-borne stone fruits peach and plum on the left.

Bigger plants tend to produce bigger seeds. This trend seems to be especially true among closely-related species. Think about the seeds of familiar fruit species in the rose family (Rosaceae): strawberry plants are herbaceous and have very small seeds; roses, Saskatoon berries, raspberries and blackberries grow on woody shrubs or vines, and their seeds are a bit bigger than those of strawberries; and the biggest seeds are in the tree species within the family (almonds, peaches, plums, nectarines, apricots, cherries, apples, pears, loquats, quince, medlar). The palms (family Arecaceae) are the only tree-sized woody monocots, so large plant size may be one factor pushing large seed size in coconuts. Incidentally, coconut fruit and seed structure is fairly uncomplicated and is well explained here.

Seeds tend to be larger for species that germinate under stressful conditions, for example, in shade, or in saline or nutrient-poor soils, or in dry places. Several plant families, for example, have species that became mangrove trees, living in coastal areas in wet soils of various salinities. In every case, seed size is bigger in the mangrove species than in its closest relatives (Moles et al. 2005). Under stressful conditions, a seedling may require more time or support until it can produce enough of its own food, so the seed supplies a large amount of nutritive reserve, which increases seed size. Double coconuts sprout exclusively on granitic outcrops on their islands, and coconuts, of course, inhabit sandy tropical beaches. The former probably involves shade and perhaps drought stress, and the latter sounds pretty appealing to me, but only because I’m not a seedling, so maybe environmental stress has helped push seed size in coconuts.

vanilla flower (photo from Kew)

Orchids and some other plant taxa have arrived at an alternative arrangement for fueling their seedlings: taking advantage of fungus. Instead of relying on nutrients packed into a seed, the embryo becomes a parasite on a fungus, which in turn gets its nutrients and energy from decaying organic matter or by being a parasite itself upon other plants. After seedling establishment these mycotrophic (fungus parasitizing) plants may become partially or entirely parasitic on another plant, and they become independent of their fungal symbiont, or they may maintain the relationship, often repaying the fungus with sugar from photosynthesis. Many plants form symbiotic relationships with soil fungus, in which the fungus receives photosynthate in exchange for soil nutrients, but only a few plants forego seed nutrient reserves and rely on fungal support for seedling establishment. So, without the burden of nutritive tissue, seeds can get very small, and a mother plant can make millions of such seeds. The epiphytic orchids have made this a fine art, as is well explained here and here, but some parasitic eudicots do it, too, if not quite so spectacularly.

vanilla bean split under a microscope

Dispersal strategy affects seed size, too. Seeds transported by wind tend to be smaller than those dispersed by animals or those that, well, don’t fall far from the tree (mother plant). This is true in orchids. The tiniest dust-like orchid seeds are wind-dispersed, but the seeds of the vanilla orchid (a beautiful neotropical vine) are relatively big for an orchid and are coated in a sticky resin, which adheres itself to the coats of animals or detritus after the fruit (vanilla “bean” or “pod”) splits upon maturity. That sticky resin in the fermented and dried vanilla fruit is the origin of the delicious vanilla flavor. The tiny black specks in good vanilla ice cream or other desserts are clumps of seeds scraped from the vanilla pod. Coconuts, on the other hand, are dispersed by floating across the ocean. Part of their large size and morphology obviously helps them make the voyage. Double coconuts, though, don’t disperse across the ocean. They stay close to home, which is apparently exactly where mother wants them.

The cookie recipe below, modified from Heidi Swanson’s animal cracker recipe, combines coconut and vanilla and only uses plant ingredients from monocot species (grains, sugar, coconut, vanilla). I recently made these for the party favor bags for my daughter’s birthday party, but, ironically, I used a cookie cutter in the shape of an oak leaf, a eudicot.

Extreme Monocot Cookies

1 cup whole wheat pastry flour or oat flour

¾ cup unsweetened finely shredded coconut, ground in a blender or food processor into coarse flour

¼ cup extra-virgin coconut oil, softened

¼ to ½ cup sugar (from sugar cane, not sugar beets), as you wish
¼ teaspoon salt
1 large egg, lightly beaten

½ teaspoon vanilla extract, or seeds scraped from 1 inch of vanilla bean, if you’re feeling indulgent

turbinado or large-crystal sugar for sprinkling (optional)

Whisk the flour and shredded coconut together in a medium bowl. Set aside. In a separate medium bowl, beat the coconut oil with the sugar and salt until it’s smooth . Beat in the egg and vanilla until everything is uniform in appearance. Add the flour mixture and stir just until incorporated. Turn the dough out onto the counter-top, knead it once or twice and gather it into a ball. Cut the dough in half, flatten each piece, wrap and refrigerate for at least an hour.

When you are ready to bake the cookies, preheat the oven to 350F degrees. Place the racks in the middle and line a couple baking sheets with parchment paper. On a floured work surface roll the dough out 1/8-inch thick. If the dough cracks, let it sit and warm up for a couple more minutes. Stamp out shapes with floured cookie cutters and place the cookies an inch apart on the baking sheets, sprinkle with a bit of the turbinado sugar, if using. Bake until the cookies are just beginning to color at the edges, 7-8 minutes. Remove from the oven and cool the cookies on racks.

References

Leishman, M. R., I. J. Wright, A. T. Moles, and M. Westoby. 2000. The evolutionary ecology of seed size. Seeds: The ecology of regeneration in plant communities, 2^nd edition. Pages 31-57. CAB International 2000. Ed. M. Fenner.

Moles, A. T., et al. 2005. A brief history of seed size. Science 307: 576-580.

If it smells like onion or garlic, it’s in the genus Allium, and it smells that way because of an ancient arms race. Those alliaceous aromas have a lot of sulfur in them, like their counterparts in the crucifers. You can combine them into a Brimstone Tart, if you can get past the tears.

The alliums

garlic curing

The genus Allium is one of the largest genera on the planet, boasting (probably) over 800 species (Friesen et al. 2006, Hirschegger et al. 2009, Mashayehki and Columbus 2014), with most species clustered around central Asia or western North America. Like all of the very speciose genera, Allium includes tremendous variation and internal evolutionary diversification within the genus, and 15 monophyletic (derived from a single common ancestor) subgenera within Allium are currently recognized (Friesen et al. 2006). Only a few have commonly cultivated (or wildharvested by me) species, however, shown on the phylogeny below.

Phylogeny of my edible alliums: genus Allium with subgenera (“subg.”) and sections within subgenera (“sect.”) labeled (data from Friesen et al. 2006 and Hirschegger et al. 2010). Click to enlarge.

Some popular allium species, including onion (A. cepa var. cepa), shallots and potato onion (A. cepa var. aggregatum), garlic (A. sativum), and leek (A. ampeloprasum), are among the oldest domesticated plants and have been employed since at least the beginning of written history throughout the large region spanning the Mediterranean through at least central Asia. Onions (A. cepa), garlic (A. sativum), and scallion (A. fistulosum) are only currently known in their cultivated forms, having changed so substantially for so long under domestication that their wild ancestry is ambiguous (Vaughan and Geissler 2009).

There are guesses, of course, for the responsible parties among the many wild species in central Asia (such as A. longicuspis for garlic; Volk et al. 2004), where both onions and garlic probably got their starts, but it’s not clear. Some other allium species that are still abundant in the wild are widely cultivated as vegetables and herbs, such as leek and other vegetables derived from wild A. ampeloprasum, chives (A. schoenoprasum), which is one of the only alliums native to both North America and Eurasia, garlic chives (A. tuberosum), and A. polyanthum. Some alliums are simply grown for their handsome flower umbels, but they’re edible, too.

ramps getting washed

The vast majority of the 800ish allium species smell garlicky or oniony, and, as far as I know, all parts of all of them are edible. To paraphrase what Greene Deane said in his post about eating some wild alliums native to the eastern U.S., if it looks and smells like garlic or onion, it’s edible. Many wild allium species were important food sources for indigenous peoples, and some are still popular wild vegetables today. I’ve used the wild garlic (A. vineale) and wild onion (A. canadense) that grow in the yard as chives in the kitchen and nibbled them on camping trips, and before we moved two years ago, we had a spot (in New Jersey) to harvest ramps (wild leeks; A. tricoccum) in the spring, but we don’t have a spot now (near DC), and ramp spots are like morel or other awesome mushroom spots: nobody divulges his or her spot. You have to find one on your own (and not overharvest). If you’re curious about harvesting wild alliums, do use your nose. The alliums are closely related to many very poisonous wild lilies (Allium is in the same family as amaryllis, Amaryllidaceae) and superficially resemble them, with similar long, thin leaves and umbels of star-like flowers. None of the poisonous lilies smell like garlic or onion, though.

A. vineale with curious chicken–they peck at it but don’t decimate it

Some wild alliums, including A. vineale, are noxious weeds that affect wheat and dairy farmers. The little bulbils (tiny bulbs, see below) that form alongside flowers in the umbels (cluster of flowers on the top of a stalk) of A. vineale mature around the same time as wheat seeds and are about the same size, so bulbils are often harvested along with wheat seeds and are difficult to separate from them, leading to contamination of the wheat crop (and garlic bread?) (Block 2010). Nursing mothers are often warned that compounds from certain foods they eat, including alliums, can end up in their milk and may upset a baby’s digestion. This is apparently also the case for cows. If dairy cows eat wild alliums growing in their pastures, the aromatic compounds can end up in their milk, causing an oniony flavor (Block 2010). The oniony flavor in milk is described as a bad thing, and it would be for many uses of milk, but I wonder if it wouldn’t in fact be a good thing for savory applications, like hard cheeses or ricotta destined for something like the filling of a greens pie (such as the brimstone tart, below). Wild alliums, like the wild relatives of many cultivated species, have higher concentrations of defense compounds, and therefore stronger flavors, than domesticated alliums (Fritsch and Keusgen 2006). And for those strong flavors, love them or hate them, we can thank their wild enemies.

 If you like spices, thank bugs

homegrown garlic

I designed a lab for an undergraduate evolution course that demonstrated general evolutionary principles using edible plant examples. One module presents culinary spices as chemical warfare agents in plants’ ongoing evolutionary arms races against the pathogens and herbivores that would consume them. The story goes like this: a plant arrives on a chemical that harms or detracts some or all of its attackers, and, in evolutionary retaliation, some subset of those attackers arrive at a way to circumvent said chemical. In response, the defense compound in the plant changes, causing a reactionary change in the pathogens or herbivores. The process is an example of coevolution, in which different species mutually evolutionarily respond to one another, and repeats itself over generations. Over time this ratcheting can lead to extreme specialization of an herbivore or pathogen on a particular plant species and is a reason why many pathogens or herbivorous insects can only eat one plant species or one set of closely related species with similar defense chemistry (see the famous landmark paper on the topic using butterflies and their hostplants as an example by Ehrlich and Raven (1964)). For example, I’ve whined on the blog already (here and here) about the Pieris cabbage butterfly caterpillars whose ancestors bequeathed to them the physiology necessary to counteract the glucosinolate defense compounds in the cruciferous vegetables (family Brassicaceae) in my garden. This specialization of different insects on different plant lineages also contributes to diversity of defense compounds within plants, of which there is a dizzying array across the global flora.

Some plant defense chemicals are toxic to people, too, and some of these are famous poisons (see Amy Stewart’s Wicked Plants for awesome descriptions). Other plant defense compounds, however, are nontoxic to humans, at least in small quantities. The flavorful constituents of our culinary spices are among these latter compounds. Similarities of defense compounds among closely related plants, variations on a chemical theme, explain why closely related plants often have similar flavors. It turns out that some of those spicy chemicals also inhibit the bacteria that can cause food to spoil or cause foodborne illness in people, and there’s some support for the hypothesis that humans have long incorporated spices into food in part to preserve it and prevent food poisoning, especially before modern refrigeration. Jennifer Billings and Paul Sherman (1998) compiled the literature on the ability of 30 spices to inhibit foodborne bacteria (see chart below).

Antimicrobial properties of 30 spices, from Billings and Sherman 1998. The spice species are arrayed from the greatest to least effectiveness at inhibiting microbes. Each bar indicates the fraction of all food-spoilage bacterial species (which ranged from 4 to 31) on which the spice or its phytochemicals have been tested (in any concentration) in the laboratory that were killed or whose growth was inhibited. Garlic and onion (along with allspice and oregano) killed all of the tested spices.

Billings and Sherman used those data to determine that typical recipes from places with hot climates, where foodborne bacteria might proliferate to the most devastating effect, have a tendency to incorporate spice combinations or concentrations that are more effective against bacteria than do recipes from cooler climates. Antimicrobial capacity is not, of course, the only reason we choose spices for our food, but perhaps it is or was a contributing factor.

homegrown garlic

In the lab I asked students to choose one of the 30 spice species from that graph from Billings and Sherman and to look up some primary literature about the compounds it uses against its enemies. Every time we did the lab, nearly all the students chose garlic or onion, the two most common of the many alliums. More than one student essay included the heartwarming sentence “I love garlic,” or “I put it in everything.” One student, however, chose allspice from the list because: “it kills as many microbes as garlic and onion, and I hate garlic and onion.” For the record, I didn’t ask students to justify their choice in their lab reports; they just volunteered this commentary. Student comments such as these contributed to my own sense of justification in creating a lab that forced them to contemplate biological perspectives of familiar plants that were emotionally evocative or about which they already had strong opinions.

onion bulbs growing in a planter box

Given their near-ubiquity in cuisines from across the globe, few plants imprint our memories like garlic and onion and other members of the genus Allium. Like in many spice species, the antimicrobial defense compounds in the alliums give them their characteristic pungent flavors and the aroma that fills up a kitchen, announcing the world over that dinner will be ready soon. Those allium defense compounds, though, may also hurt a chef’s eyes when he or she cuts an onion. At least for me, though, even that is sentimental because of what my mother would always say, sniffing and wiping the tears away from her eyes with the back of her hand, when an onion made her cry: “Whew! Good onion!”

Why onions make you cry and garlic tastes hot

Onion slices macerating with salt and apple cider vinegar while I do other stuff. All my coleslaws and grain or bean salads begin with this quick onion pickle. Like heat, acid and salt must transform the thiosulphinates into less aggressive sulfurous compounds.

Chemically, the defense compounds in alliums start out as cysteine sulphoxides (Fritsch and Keusgen 2006, Block 2010). In addition to being sulfurous like the glucosinolate defense compounds in crucifers, allium cysteine sulphoxides are activated in the same way as glucosinolates. Both are kind of like an industrial glue in which two inert components stored in different containers only become sticky when mixed together. To become the final (smelly) defense chemical form, an enzyme, called alliinase, needs to transform the cysteine sulphoxides into sulfenic acids, which then transform into thiosulphinates, which give alliums their scent and presumably repel the enemies. Alliinase is stored separately from the cysteine sulphoxides within allium cells (the enzyme is stored in little packets called vacuoles, while the cysteine sulphoxides are stored in the cytoplasm, the liquid inside cells; Lancaster and Collin 1981). When the cell is broken apart, from the action of an herbivore or a knife in the kitchen, the vacuole breaks open, bringing the cysteine sulphoxides into contact with the enzyme, and voila! The irritating/aromatic/smelly/delicious/hateful (depending on your opinion about the smell and flavor of alliums and whether or not you are a susceptible herbivore) thiosulphinates are released into the smashed allium tissue and into the air surrounding it (Fritsch and Keusgen 2006, Block 2010, Scott 1999). The defense compounds are stored in a mucilaginous matrix within special large “laticifer” cells, the exact position of which varies across plant tissues and species but is invariably close to the surface (Mashayehki and Columbus 2014)

There are a handful of different cysteine sulphoxides that accumulate in notable concentrations in alliums (Fritsch and Keusgen 2006). Different mixes of cysteine sulphoxide derivatives (thiosulphinates) characterize the aroma and flavor of individual allium species (or groups of closely related allium species) (Fritsch and Keusgen 2006). This is why the flavor of garlic is distinct from that of onion or leek or some of the wild species. Alliin is the dominant cysteine sulphoxide in garlic; isoalliin dominates onion; and isoalliin and propiin dominate leek. Another cysteine sulphoxide, methiin, has a particularly unpleasant flavor and characterizes the flavor of many wild species, which may explain why many of them are not utilized more frequently as food (Fritsch and Keusgen 2006).

In garlic, alliinase transforms alliin into allicin, the thiosulphiate that gives raw garlic its characteristic aroma and “hot” flavor. Allicin feels “hot” because it activates two of the neural pain receptors in our mouths (TRPV1 and TRPA1) that are responsible for sensing excessive thermal heat (Macpherson 2005). TRPV1 is the receptor also triggered by capsaicin in chili peppers (Capsicum), and TRPA1 is triggered by glucosinolate-derived mustard oils. Allicin and other thiosulphinates in alliums are thermally unstable and break down when heated into various diallyl sulfides. These derivative sulfurous compounds are still flavorful and aromatic (they’re what you smell over time when something with onions is roasting or braising in your kitchen), but they lack that bite in the mouth because they can no longer activate those pain receptors in this form (Macpherson 2005). Incidentally, thiosulphinates may attach themselves to the pain receptors in the same way that they attach themselves to bacterial cellular machinery, which ends up inhibiting bacterial growth (Block 2010).

chopped leak pseudostem generates painful compounds, too

In onions, an alliinase transforms the cysteine sulphoxide isoalliin into the sulfenic acid 1-Propenesulfenic acid. Then a second enzyme, appropriately named lachrymatory factor synthase, transforms the 1-Propenesulfenic acid into the highly volatile gas thiosulphinate syn-propanethial-S-oxide. The nerve endings in the cornea of the eye respond to syn-propanethial-S-oxide in proportion to its concentration in the air wafting up from a cut onion and prompt the tear ducts to produce tears to flush the irritant (Scott 1999, Block 2010).

Tearless onions have been genetically engineered by a simple, surgical mechanism: “silencing” the gene that encodes for the lachrymatory factor synthase enzyme. These transgenic onions produce all of the sulfur-containing compounds that give alliums their antimicrobial and putatively health-enhancing benefits with less pungency and without causing tears (Block 2010). You may find that “Vidalia” or other “sweet” onions, which were not produced transgenically, smell and taste less pungent and are quite sweet. These cultivars do not take up sulfulr from the soil as effectively or allocate sulfur to cysteine sulfoxides as much as the more pungent cultivars. Additionally, they may be grown in certain locations with low-sulfur soils, which demonstrably reduces cysteine sulfoxide content in all cultivars (Block 2010).

sweet, cooked leeks + greens, destined for brimstone tart

All onions, regardless of cysteine sulfoxide content, can produce large bulbs with high sugar contents (like a Vidalia); that’s why caramelized onions taste sweet no matter the variety they’re made from. They are, after all, organs designed to store the plant’s energy over the dormant period in the form of sugars. The size of the bulb and its sugar content ultimately depend on how much photosynthesis (sugar generation) the leaves were able to do during the growing season. Garlic cloves and leek pseudostems are also carbohydrate storage organs and also therefore have sweetness behind the sulfur.

Allium morphology

Leek pseudostem, with leaf bases growing from a flat, think disk stem

The parts of onions, shallots, garlic and elephant garlic that we eat are botanically bulbs, carbohydrate storage organs composed of highly modified stems and leaves that grow underground or on the soil surface. Bulbs are employed by many monocot species in the orders Liliales and Asparagales (think tulip and amaryllis) and one eudicot genus (Oxalis). Plants that make bulbs start out as green shoots with leaves and a flowering shoot (inflorescence) originating from a very short, squat disk-like stem, so that it looks like they’re all coming out of the same place. The bases of the leaves might even be tightly overlapping and long, forming a pseudostem around the flowering stalk, evident in leek, garlic, and onion plants (and banana plants). The bulb stores carbohydrates and other nutrients during the dormant part of the year to fuel shoot and flower growth in the following growing periods. To make an onion bulb, the tightly overlapping leaf bases in the onion plant swell with stored carbohydrate, and the bases of the outermost leaves becomes brittle, paper-like “tunicas.” Inside the swelling leaf bases, new leaves are continuously being formed from the apical meristem growth point on the disk-like stem, and most of them will never sprout but only exist to store carbohydrate and other compounds. The bulb grows as the leaf bases swell and the new storage leaves grow. The storage leaves surround the developing shoot of new leaves and a flower stalk that will sprout the following year.

Many allium species reproduce asexually by producing small bulbs that sprout from the outside of the squat disk stem, from axial meristems (see the B. oleracea post for a description of the various meristems in a shoot). In garlic and elephant garlic, these new bulbs are called “cloves” and consist of a new growing shoot surrounded by a single large storage leaf encased within a single tunicate leaf (the garlic “peel”). The new small bulbs grow in a ring around the disk stem, encased within the papery tunicate leaf bases from the parent plant (see labeled photos of garlic and onion below).

structures in garlic and onion bulbs. Photo of garlic bulb from Southern Exposure

The new small bulbs in the multiplier onions (shallot, potato onion) develop similarly to garlic but can consist of many storage leaves within the new tunic. If left to their own devices, eventually the garlic cloves and new shallots would outgrow the maternal tunicate case and will develop their own root system from their own little disk stems and send up their own shoots. This is why you can plant individual garlic cloves (or individual shallots or potato onions or small onion bulbs) in the fall and get big heads of garlic or shallot (or an onion bulb) from each one the following summer.

two potato onions (multiplier onions; fun to grow!), showing new small bulbs encased in a tunic growing from axillary buds on a disk stem, with roots growing on the underside of the disk stem

Impressive morphological variation exists within individual Allium species, including the domesticated species A. ampeloprasum and A. cepa. The common single-bulb onion is a variant of A. cepa distinct from conspecific multiplier onions, which include shallots and potato onions. The multiplier onions get their name from their tendency to produce clumps of small bulbs from a single planted bulb, more like garlic. Domestication of four subspecies of A. ampeloprasum modified different plant structures in each lineage. Domestication of the leek subspecies amplified the pseudostem, formed by tightly packed overlapping leaf bases, just like in the plants of fellow monocot banana. The aerial, photosynthesizing portions of the leek leaves become too tough to eat, so to increase the amount of tender pseudostem in the harvested crop, dirt is piled up over the pseudostem, a farming technique called “hilling” that blanches the pseudostem, making it pale and tender.

leek

Pearl onions from A. ampeloprasum are small lateral bulbs that develop off the main stem, each with a tunica encasing multiple, thin storage leaves and an immature shoot. Elephant garlic develops cloves like A. sativum garlic, from lateral buds off the disk stem, each with a tough, dry tunicate leaf covering a single, large storage leaf and an immature shoot. Kurrat varieties, popular throughout the Middle East, don’t develop a large pseudostem like leek or lateral bulbs but instead are grown for their leaves, which are much more tender than leaves in the other varieties.

garlic chives blooming

Species we typically grow for leaves or bulbs (onions, chives, garlic, leeks) have beautiful flower clusters, too, and also contain lots of sweet nectar to complement their oniony-garlicky flavor and make attractive edible flowers for garnishes or salads. The immature flowering stalks (inflorescences) are called “scapes.” Garlic scapes can be found in farmer’s markets in the spring. They have a mild garlic flavor and can be used like a scallion or ground into sauces, like pesto, or soup.

garlic scapes

If left to develop, the garlic inflorescence would produce an umbel composed mostly or entirely of bulbils, tiny bulbs, instead of flowers. A garlic bulbil is like a very tiny garlic clove, with a tunica leaf covering a starchy storage leaf surrounding buds that could become leaf and inflorescence, if the bulbil were planted in the ground. Because bulbils replace most or all garlic flowers, most garlic varieties rarely or never produce viable seeds and have almost exclusively been propagated asexually from cloves and bulbils for millennia. Picking the scapes forces the garlic plant to invest energy it would have allocated to the flowers and bulbils into the bulb, which is where most people want it.

bulbils and flowers in the umbel of a cultivated onion

Garlic and wild garlic are far from the only alliums that produce bulbils. Walking onions, or “tree” onions, have such large bulbils in their inflorescences that they can be picked and peeled like pearl onions. The umbels (flower head with clustered bulbils and flowers) becomes so heavy with these large bulbils that they nod down to the ground, whereupon the bulbils sprout roots and shoots and become progenitors of a new plant, as if the onion plants were “walking” across the landscape. Commercially available walking onions are considered hybrids of A. cepa and A. fistulosum, which itself is called “scallions” and is grown for its tender greens and very tiny bulbs, although the young aerial parts of a great many cultivated and wild alliums can be harvested and used fresh like “scallions” as well.

green garlic; the immature bulb and pseudostem are tender and can be cooked; the leaves were used to flavor stock

Along with the scapes, you may also see early season “green” garlic available in markets, perhaps as a whole plant. This is the young, immature plant with a soft bulb, picked before the tunicate leaves have become coarse, and the garlic flavor is mild. The whole immature bulb and tender lower portions of the stalk can be sliced and used like a leek, and, like with leek tops, the upper stalk and leaves should be saved for making a lovely garlicky soup stock (the leaf tops are too tough to eat as a vegetable).

hollow terete leaf of chive (left), and flat leaf of garlic chive (right)

Leeks, garlic and garlic chives all have flat leaves instead of hollow, tapered, cylindrical “terete” leaves in onions, chives and scallions. Both leaf types appear to evolutionarily wax and wane within the genus, perhaps partially in response to habitat aridity (Mashayekhi an Columbus 2014).

 Brimstone Tart

Cysteine sulphoxides are found in many cruciferous species (family Brassicaceae), too (Fritsch and Keusgen 2006, Kubec et al. 2001), although I don’t know which enzyme acts on them in crucifers. The Latin name of the cruciferous genus Allaria means “garlic-like” and includes the weed commonly called “garlic mustard” (Alliaria petiolata), which is known for its “garlicky” aroma.

crucifer cabbage (Brassica oleracea) intercropped with allium garlic (A. sativum), National Arboretum

Alliums, which are monocots, are only distantly related to cruciferous vegetables, which are eudicots. Therefore, the separately-compartmentalized enzyme activation of sulfur-based defense chemistry, and the occurrence of cysteine sulphoxides in alliums and crucifers specifically, likely evolved independently in both groups (Fritsch and Keusgen 2006). Since both cruciferous glucosinolates and cysteine sulphoxides are rich in sulfur, both crucifers and alliums need more sulfur-rich soil than do other crops to produce the most flavorful and nutritious (and large) vegetables. This is similar to caffeine production, in that caffeine is very nitrogen-rich defense compound, and plants that make it vary caffeine production according to soil nitrogen availability. So, my mother was kind of right about particularly tear-inducing onions being “good.” The defense chemicals in onion give them flavor and are potentially medically beneficial (Block 2010). Higher concentrations of them in an onion cause more tears but also might be more nutritious, more flavorful and potentially indicative of soil fertility. Ergo, “good.”

brimstone tart, made with leeks, radish greens (cruciferous), and chard (not)

I think that crucifers and alliums taste awesome together in a multitude of species combinations and preparations, from a raw coleslaw with cabbage and onions to a leek-and-greens tart (recipe below). Maybe their high sulfur content has something to do with their affinity for one another. You can only call the concoction below brimstone tart if you use a cruciferous vegetable for the greens, thereby including two genera with sulfurous defense chemistry: Brassica and Allium.

Recipe for Brimstone Tart

Kale, mustard greens, turnip greens, and radish leaves seem like good choices for the greens in this recipe. You can make this with any set of greens that will cook down, though (chard, spinach, and amaranth greens are also good choices here). You may find it easier to steam the greens just until they wilt before you chop them and mix them in with the sautéed leeks, but it’s okay to coarsely chop them first and then wilt them in with the leeks, but you have to make sure you’ve got enough room for that in your pan (and probably a lid). If you’re using chard, you can use the entire midrib and petiole (often informally incorrectly called “stem”), diced fine. I tend to remove the toughest parts of the midribs and petioles from the cruciferous greens, though. I like an egg-enriched pastry dough for the shell, but use whatever crust recipe you’d like. If you don’t have leeks, use onions. The dairy in this, too, is really flexible. I’ve made this with all cream, half strained (“Greek”) yogurt and half cream, half cream and half milk, half ricotta and half cream. Sour cream or crème fraiche for part of it would work well, too.

Pastry:

1.25 cups whole-wheat flour

3 oz. cold unsalted butter

½ tsp. salt

3 tablespoons ice-cold water in which 1 egg is whisked

Filling:

3 leeks (white and pale green pseudostem only), or 1-2 onion bulbs, chopped

About 2 cups steamed greens (from about 1.5-2 typical grocery bunches), coarsely chopped.

1 tablespoon fresh thyme leaves (or 1.5 teaspoons dried)

3 T butter

salt and black pepper

1 cup heavy cream

4 eggs

4 T grated cheese (I like Parmesan, Gruyere or Gouda)

Sautee the leeks or onion with the thyme in the butter on medium-low heat while you do the rest, stirring occasionally, letting them soften and begin to caramelize. Steam and chop the greens (or add chopped greens to the leeks after about 10 minutes and put a lid over them to wilt them before stirring them) and add them to the leeks with some salt and pepper, stirring occasionally on low heat, to dry them out a bit, while you make the custard. Whisk the eggs and cream until frothy and liberally season with more salt and pepper. Take the greens and leeks off the heat to cool a bit while you make the pastry and preheat oven to 400 degrees (Farenheit). Cut the butter into the flour and salt with a pastry cutter, butter knives or a food processor until the mixture looks like breadcrumbs. Pour the water with egg over it and mix it together with your hands until it forms a ball. Put some flour on the surface you’ll use to roll out the dough and do so. Press the dough into your tart pan or baking dish (9-inch) and trim off excess dough. Stir the leek and greens mixture into the cream and egg mixture and pour into the pastry shell. Top with cheese and bake until golden brown on the top, about 45 minutes. Cool for a bit (10-15 minutes) before eating.

References

Billings, J., and Sherman, P. W. 1998. Antimicrobial Functions of Spices: Why Some Like It Hot.” Quarterly Review of Biology 73.

Block, E. 2010. Garlic and Other Alliums: The Lore and the Science.

Fritsch, R. M., and M. Keusgen. 2006. Occurrence and taxonomic significance of cysteine sulphoxides in the genus Allium L. (Alliaceae). Phytochemistry 67:1127-1135.

Friesen, N., R. M. Fritsch, and F. R. Blattner. 2006. Phylogeny and new intrageneric classification of Allium (Alliaceae) based on nuclear ribosomal DNA ITS sequences. Aliso 22:372-395.

Kubec, R., M. Svobodová, and J. Velísek. 2001. Gas-chromatographic determination of S-methylcysteine sulfoxide in cruciferous vegetables. European Food Research and Technology 213:386-388.

Lancaster J. E., and H. A. Collin. 1981. Presence of alliinase in isolated vacuoles and alkyl cysteine sulphoxides in the cytoplasm of bulbs in onion (Allium cepa). Plant Sci. Lett. 22:169–176

Macpherson, L. J., B. H. Geierstanger, . Viswanath, M. Bandell, S. R. Eid, S. Hwang, and A. Patapoutian. 2005. The pungency of garlic: activation of TRPA1 and TRPV1 in response to allicin. Current Biology 15:929-934.

Mashayehki, S., and J. T. Columbus. 2014. Evolution of leaf blade anatomy in Allium(Amaryllidaceae) subgenus Amerallium with a focus on the North American species. American Journal of Botany 101:63-85.

Scott, T. 1999. What is the chemical process that causes my eyes to tear when I peel onion? Scientific American 21 October 1999.

Vaughan, J. G., and C. A. Geissler. 2009. The new Oxford book of food plants. 2^nd ed. Oxford University Press.

Volk, G.M., A. D. Henk, and C. M. Richards. 2004. Genetic diversity among U.S. garlic clones as detected using AFLP methods. J. Amer. Soc. Hort. Sci. 129:559-569.

Infinity scarves? No. They won’t keep doctors away. Apples are the ultimate everyday accessory (fruit). Katherine explains where the star in the apple comes from. Could it be due to a random doubling of chromosomes? We also give readers the chance to test their apple knowledge with a video quiz.

Although apples are not particularly American – nor is apple pie – they color our landscape from New York City to Washington State, all thanks to Johnny Appleseed. Or so goes the legend. Everyone already knows a lot about apples, and for those wanting more, there are many engaging and beautifully written stories of their cultural history, diversity, and uses. See the reference list below for some good ones. There is no way I could cover the same ground, so instead I’ll keep this post short and sweet (or crisp and tart) by focusing on apple fruit structure and some interesting new studies that shed light on it.
Of course if you do want to learn more about apple history but have only 5 minutes, or if you want to test your current knowledge, take our video quiz! It’s at the bottom of this page.

Apple structure
Depending on your approach to eating apples, you may not actually consume any fruit at all. If you nibble the outer part, warily avoiding the core, then you might be missing the true fruit entirely. If, on the other hand, you eat all the way down to the core (or even eat the core itself like the Foodbeast guy) then you are definitely getting to the fruit.

Mature apple fruits in longitudinal and cross-section. The “true fruit” is the part derived from the ovary. It is visible in a cut apple as a ring of vascular tissue. Click to enlarge.

Apples are pomes, meaning that what’s commonly considered the “true” fruit – the part derived from the ovary – is buried inside a large fleshy hypanthium that developed from other apple parts. The bulk of what we eat is that sweet and crunchy hypanthium (Greek for “under the little flower”). In spite of what some people assume, though, the actual ovary is not just the plasticky bits that surround the seeds and form the star in a cross-cut apple. Most of the ovary is fleshy and blends almost seamlessly into the rest of the apple. Its boundary is subtle, but you can see it in a cut apple as a ring of vascular tissue (veins) surrounding the core.

Pome-like fruits are found in apples, pears, quinces, loquats, and medlars, which are all members of the same clade (branch) within the rose family (Rosaceae).

Pomes of Heteromeles arbutifolia, with a penny for scale. The fruit at bottom left still has an old petal attached at the distal end, illustrating the inferior position of the ovary. Click to enlarge.

Also in the clade are typically wild-growing or ornamental plants such as hawthorne, cotoneaster, Heteromeles, Pyracantha, Photinia, and Raphiolepis. All of these species have flowers with inferior ovaries – ovaries buried within a hypanthium – and are unique within the rose family in this respect.

It’s easy to spot an inferior ovary because the leftover flower parts (or their scars) can be found opposite the stem on the mature fruit. In the rose family, a useful comparison is between apples and cherries or strawberries.

Cherry flowers have superior ovaries, visible within the floral cup. Apple flowers’ inferior ovaries are buried within a hypanthium and fused to it. Click to enlarge

The sepals and petals of a cherry generally fall off, but they leave scars in a ring close to where the stem meets the fruit. The sepals of a strawberry always persist, and petals can often be found on fresh berries, right around the stem.

By contrast, the floral bits of an apple are at the “bottom,” opposite the stem end. There you can see a ring of sepals surrounding a bunch of pollen-bearing stamens and sometimes even the styles that lead down to the ovary. Occasionally a shriveled petal remains there. Sometimes that little floral hole is filled with spider webs or dirt, but not as often as some people fear. And indeed I have noticed that some people do fear apples just a little bit, or at least eye them suspiciously. I don’t think we can blame the fate of Adam and Eve or the evil queen in Snow White for apples’ tainted reputation. I honestly think it’s anxiety over what might lurk in the little eye at the bottom of the fruit.

Sepals and a shriveled petal are visible at the flower end of an apple.

What we have learned from the apple genome
A pome is a type of fruit, and regular readers will know that fruit types are artificial categories with fuzzy boundaries and no regular or necessary relationship to evolutionary history or phylogenetic relatedness. That said, close relatives often produce the same type of fruit, and there are some fruit types restricted by convention to specific plant families or clades. Citrus fruits (hesperidia) are a good example of fruit type mapping perfectly onto a natural plant group.

Phylogenetic relationships among common fruits from the rose family.  Click to enlarge.

Within the rose family, the occurrence of pome fruits does reflect evolutionary history: pomes are present in only one clade, the apple tribe (called the Pyreae or Maleae). Intriguingly, this fruit type may be the result of a huge genetic shift within the family about 50 million years ago (Velasco et al. 2010). In 2010, a team of researchers published a draft of the apple genome, showing that the ancestor of the apple tribe experienced a duplication of its entire set of chromosomes (Velasco et al. 2010). The duplication was followed by an expansion and diversification of a set of genes (MADS-box genes) that control flower and fruit development by regulating the expression of other genes.

But how do a few genetic switches turn the ancestral dry fruit into an apple? It turns out that one of these MADS-box genes is particularly important for making a fleshy fruit, and that when it is experimentally turned off, the resulting fruit is dry. Even more impressive, though, is that the same gene is also required for other fruit qualities – exactly those qualities that would make a fleshy fruit attractive to animal dispersers: color, aroma, and sugar content (Ireland et al. 2013).  How do you like them apples?

All you wanted to know about apples in 5 minutes

References and further reading
Ireland, H. et al. (2013) Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. Plant Journal 73: 1044-56.

Jacobsen, R. (2014) Apples of Uncommon Character: Heirlooms, Modern Classics, and Little-Known Wonders. Bloomsbury USA

Juniper, B.E. & Mabberley, D. J. (2006) The Story of the Apple. Timber Press

Pollan, M. (2001) The Botany of Desire: A Plant’s-Eye View of the World. Random House

Potter, D. et al. (2007) Phylogeny and classification of Rosaceae. Plant Systematics & Evolution 266:5-43.

Spjut, R. (1994) A Systematic Treatment of Fruit Types. NYBG. 

Velasco, R. et al. (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nature Genetics 42: 833–839

The rapunzel plant (Campanula rapunculus; Campanulaceae). Photo from Wikipedia.

I never suspected that I’d learn something about edible botany by indulging my 3-year-old’s princess obsession, but I have. According to the Brothers Grimm, Princess Rapunzel is named after the cultivated  vegetable of the same name, growing in a witch’s garden. Formally the rapunzel plant is Campanula rapunculus, native from southwestern Asia through central Europe to North Africa. The genus Campanula contains upwards of 500 species of what are commonly called bluebells, bellflowers, or harebells, widely distributed throughout the northern hemisphere. Many if not most of those species have edible flowers, leaves and roots (see links here, here, here and here). The Brothers Grimm don’t specify which parts of the plant were particularly enticing to Princess Rapunzel’s mother.

Our princess, in the Tangled-inspired dress from Santa

Many species in the closesly-related genus Adenophora also have edible roots, leaves and flowers. These genera add a taxonomic family, Campanulaceae, to our list of taxa with culinary species. Campanulaceae joins the sunflower family (Asteraceae) as culinary families in the order Asterales. Rapunzel seeds are for sale, and it can grow in Anchorage, where we will be moving this spring. My little Rapunzel will have to beat the moose to it in the garden next summer.

The Cooks Illustrated recipe masters recently added nutmeg and orange zest to a pepper-crusted steak to replace two flavorful terpenes, pinene and limonene, lost from black pepper when simmered in oil. In doing so they take advantage of convergent evolution of terpenoids, the most diverse group of chemical products produced by plants. Nutmeg and orange zest, though, were hardly their only options.

The terpene swap

Black pepper growing (photo by L. Osnas)

To develop satisfying crunch, the Cooks Illustrated recipe for pepper-crusted beef tenderloin requires a prodigious quantity of coarsely ground black pepper (Piper nigrum; family Piperaceae). If applied to the meat raw, however, in the recipe authors’ view, this heap of pepper generates an unwelcome amount of spicy heat. To mellow it, the recipe authors recommend simmering the pepper in oil and straining it out of the oil before adding it to the dry rub. The hot oil draws out the alkaloid piperine, which makes black pepper taste hot, from the cracked black pepper fruits (peppercorns).

Nutmeg seed

To their dismay, however, the recipe authors discovered that the hot oil also removes flavorful compounds from the cracked pepper, in particular the terpenes pinene and limonene. To rectify this flavor problem, the recipe authors added pinene-rich nutmeg (Myristica fragrans; Myristicaceae) and limonene-rich orange (Citrus x sinensis; Rutaceae) zest to the dry rub, along with the simmered black pepper. In doing so they take advantage of widespread and diverse array of terpenoids in the plant kingdom.

Terpene what and why

Extra-terpenoid-y Bloody Mary: carotenoids in the carrot and tomato juices are terpenoids, as are major flavor constituents in its black pepper, lemon, celery, and lovage garnish

Terpenoids and isoprene, the building block molecule of terpenoids, escape plants and comprise a consequential component of atmospheric chemistry (Guenther et al. 1995). When he learned this, Ronald Reagan declared that trees cause more air pollution than cars. He was wrong about that, but his alarm does raise the question about what all those terpenoids are doing in the air, and in the plant.

Enzymes called terpene synthases combine particular numbers of isoprene molecules (actually slightly modified isoprene) and other constituents in particular arrangements to create terpenes. There is some ambiguity about the use of the terms “terpene” and “terpenoid,” but hereafter we’ll use “terpenoids” to include isoprene-derived terpenes as well as their chemical derivatives. Chemists have identified over 30,000 different terpenoids, making them the largest and most diverse class of natural products (Trapp and Croteau 2001). Most of them are naturally produced within organisms, with at least half of them synthesized by plants. Some terpenoids contribute to primary plant structure and function, such as gibberellin plant hormones, carotenoid pigments (vitamin A precursors), the phytol component of chlorophyll, and cell membrane phytosterols. Most terpenoids, however, are considered secondary metabolites, meaning that they do not directly contribute to plant growth and may serve other ecological functions, including defense and communication. Pinene and limonene likely fall into this category.

Thyme

The defense function is intuitively obvious, as many terpenoids are powerful antimicrobial and insecticidal compounds, and terpenoids, especially those in viscous plant resins, seal wounds when the plant is damaged (Martin et al. 2003). Terpenoids mediate plant communication because many of them are highly volatile, meaning they readily diffuse into the air and thereby come into contact with neighboring plants, potential pollinators, or carnivorous insects, such as parasitoid wasps, that would fly to the rescue of a besieged plant under assault by herbivorous insects (Paré and Tumlinson 1999). Whereupon receiving these airborne terpenoid distress signals from a damaged plant, neighboring plants may increase their own production of defense chemicals in anticipation of being attacked themselves (Paré and Tumlinson 1999).

Black swallowtail caterpillar inducing defense compound synthesis in dill. Swallowtail (Papilio spp.) caterpillars make their own stinky terpenes for defense, too, including pinene, deployed via osmeteria.

Isoprene and some of its volatile terpenoid derivatives may also escape plant tissue as a byproduct of internal physiological processes, or in response to thermal or other environmental stress, and not necessarily as a defense or communication tactic (Niinemets et al. 2004).

White pine (Pinus strobus)

Terpenoids have diverse commercial applications and are employed industrially, in perfumes, in food, as antimicrobials and insecticides, and pharmacologically (Kumari et al. 2014). Fragrant essential oils, turpentines and plant resins, all derived from plants, are mixtures with high terpenoid content. In addition to enjoying the fragrant and flavorful orange-scented limonene as a perfume and food flavoring agent (when bound in spices), humans use it as an insecticide ingredient and cleaning solvent.

Hops vine

Like limonene, many terpenoids are strongly aromatic and are main ingredients in many flower fragrances. As we discussed in the Allium post, both the aromatic and antimicrobial characteristics of terpenoids (and other flavorful compounds) probably contribute to their popularity as spices. Anti-malarial drug artemesinin (which we talked about in our Artemisia post), and anti-cancer drug Taxol (from yew, Taxus spp.) are terpenoids. The flavorful and psychoactive/medicinal components of species in the Cannabaceae family (order Rosales), with includes hops (Humulus lupulus), the popular beer ingredient, and cannabis/hemp (Cannabis sativa), are terpenoids. There are many more examples of charismatic terpenoids, but we’ll stop for now.

Sticking with the pinene and limonene theme 

The ingredients of CI’s steak crust are far from the only plants, or even the only spices, that contain pinene and limonene, which are two of the most common terpenoids encountered on the planet (Guenther et al. 1995).

Possible side dish options for a pinene-limonene themed dinner: Carrots (Daucus carota) contain both pinene and limonene, as do fellow umbellifers celery root and fennel bulb

A given terpenoid, however, is hardly ever the only aromatic component of a given plant. Plant species vary in how many and which kinds of terpenes they produce, but it can be dozens (Niinemets et al. 2004). Therefore, even though there may be more pinene in needles of its namesake pine (Pinus spp.) than in the nutmeg seed, taken as a whole, nutmeg may be a tastier ingredient here than pine needles because of all of the other flavorful components in both plants. Pine nuts, however, also contain pinene, so perhaps chopped pine nuts would have been a welcome (and nerdier) addition to the crust.

Oregano

In my culinary opinion, other potential pinene donors to the crust could have included any of the following palatably compatible and pinene-rich (according to the addictive Dr. Duke’s Ethnobotanical and Phytochemical Databases) spices: juniper berry (Juniperus communis), some members of the mint family (Lamiaceae: rosemary, Rosmarinus officinalis; sage, Salvia spp.; thyme, Thymus spp.; oregano/marjoram, Origanum vulgare; basil, Ociumum spp.; savory, Satureja spp.), some members of the carrot or umbellifer family (Apiaceae: coriander, Coriandrum sativum; fennel, Foeniculum vulgare), epazote (Chenopodium ambrosioides; Chenopodiaceae), bay (Laurus nobilis; Lauraceae), or tarragon (Artemisia dracunculus; Asteraceae).

Epazote

There are several other spices and familiar aromatic plants that have pinene or limonene or both (have fun with Dr. Duke’s database to figure that out, but be aware that you may have to put in the name of a particular terpenoid isomer, e.g. “alpha pinene” instead of just “pinene,” to get comprehensive results). These are just those that I think might work in the CI steak crust.

Parsley, flowering

Many of these other potential pinene donors contain both pinene and limonene. The umbellifer species whose leaves are used as a fresh herb (parsley, Petroselinum crispum; celery, Apium graveolens; lovage, Levisticum officinale; cilantro/coriander; and fennel) have respectable amounts of both pinene and limonene, too, so a gremolata employing them would likely be an appropriate accompaniment to the crusted meat, at least from a terpenoid perspective. In fact, tissues of both citrus and pine boast respectable amounts of both pinene and limonene. One of the terpenoids in hops is pinene, so for a limonene- and pinene-themed dinner, serve a hoppy beer with your crusted steak and gremolata. And for dessert have something with ginger (Zingiber officinale), which contains both pinene and limonene, or Katherine’s Basal Angiosperm cake, all ingredients of which contain at least pinene.

Meyer lemons

As its name suggests, the orange-scented limonene is a signature aroma in citrus (Citrus spp.: lemon, lime, orange, etc.). I’ve pointed out before that limonene is one of a few citrus-smelling compounds that repeatedly pops up in distantly related lemony-smelling plants. The large pool of potential pinene and limonene donors to the CI steak crust are distantly related and include both evolutionarily old (e.g. conifers and bay) and recently derived (e.g. mints, umbellifers) lineages (see our plant phylogeny page for details). This phylogenetic diversity in terpenoid source species demonstrates the ubiquity of terpenoid synthesis capacity across all plants and the repeated convergent evolution (independent evolution of the same thing in different species) of pinene and limonene production in particular.

References

Degenhardt, J., T. G. Köllner, and J. Gershenzon. 2009. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70:1621-1637.

Guenther, A., C. N. Hewitt, D. Erickson, R. Fall, C. Geron, T. Graedel, P. Harley, L. Klinger, M. Lerdau, W. A. McKay, T. Pierce, B. Scholes, R. Steinbrecher, R. Tallmaraju, J. Taylor, and P. Zimmerman. 1995. A global model of natural volatile organic compound emissions. J. Geophysical Research 100: 8873-8892.

Kumari, S., S. Pundhir, P. Priya, et al. 2014. EssOilDB: a database of essential oils reflecting terpene composition and variability in the plant kingdom. Database 2014: article ID bau120.

Martin, D. M., J. Gershenzon, and J. Bohlmann. 2003. Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiology 132:1586-1599.

Niinemets, U., F. Loreto, and M. Reichstein. 2004. Physiological and physiochemical controls on foliar volatile organic compound emissions. Trends in Plant Science 9:1360-1385.

Paré, P. W., and J. H. Tumlinson. 1999. Plant volatiles as a defense against insect herbivores. Plant Physiology 121:325-331.

Trapp, S. C., and R. B. Croteau. 2001. Genomic organization of plant terpene synthases and molecular evolutionary implications. Genetics 158:811-832.

What’s in a name?  An apple with an old fashioned name could taste as sweet, but it might not sell.  The most sought after branded varieties reveal what people look for in an apple: sweet and crunchy and bright white inside.  Do the fruits live up to their names?  Are Honeycrisp apples crunchier than others?  Do Arctics actually stay white?  We zoom in on the cells to find out.

Some of you will remember the era when the Superbowl halftime show repeatedly featured Up With People.  That was around the time when Granny Smiths arrived in our supermarkets and finally gave Americans a third apple, a tart and crunchy alternative to red and golden delicious.  Those were simple days. 

Forty years later, left-shark GIFs and crisp pink honey sweet snow white candy crunch goodness have exploded onto the stage.  Red delicious and grannies are still around, but now we can easily find another dozen familiar varieties, along with new name-branded apples streaking up the sales charts: Honeycrisp, Pink Lady ®, Jazz ™, SweeTango ®, Envy™, Ambrosia ™, Opal®, and Kanzi® (the apple, not the 35-year-old linguistically advanced bonobo).  As the marks suggest, the production or sale of many of these varieties are controlled to some extent by marketing groups or clubs that actively promote the brands and sometimes control quality.  So far, all have been bred conventionally, however a pair of genetically modified varieties were approved this winter (2015), with more likely on the way.

Do these new varieties live up to the hype?  Read our dramatically spectacular Shakespearean Superbowl edition XLVII to find out.

Honeycrisp and SweeTango ®

Honeycrisps seem to have shot out of nowhere lately, even though they have been available for nearly 25 years.  In many states, its acreage is expanding very rapidly (www.nass.usda.gov), and in 2013-14, it was the 7th best selling variety (usapple.org). The Honeycrisp was bred and developed by the University of Minnesota and had patent protection until 2008, generating millions of dollars for the university in licensing fees.  Even off-patent, it’s often more expensive than other varieties – online, Costco charges for Honeycrisp nearly three times what Fuji and Gala cost.

Why are people so crazy for an apple that they are willing to pay that much more?  I know at least one grower who credits the name, which is pretty much a direct translation of what people want in an apple.

But what is the evidence that Honeycrisp apples actually are crisper and juicier than others?  A study (done at Honeycrisp’s birthplace, the University of Minnesota) used a panel of 12 tasters, a microscope, and a texture analyzer to compare 10 apple varieties, both commercial and in development (Mann et al. 2005).  Some test varieties had Honeycrisp as a parent and were expected to share some of its qualities.  Apples were tested fresh and after 4 months of cold storage.  When the data came in, Honeycrisp apples (and their progeny) were rated as firmer and crisper than most other varieties, even after 4 months of storage.  They were also juicier.

In the study, juiciness was related to cell size, and Honeycrisp had the largest cells of the ten tested varieties (statistically larger than most).  Larger cells contain larger sugar-filled pockets of water (vacuoles) that burst open when you bite into them.  But for pretty much all plant tissues, “crunch” is related to three additional properties: cell wall stiffness, the integrity of the middle lamella, and turgor pressure.

Cells of the apple flesh contain a large central vacuole full of water, sugars, and other compounds. The pressure of the water against the cytoplasm (light blue) and ultimately against the cell wall supports the wall and adds to tissue stiffness. The middle lamella keeps cells from sliding apart and feeling “mealy.”  Click to enlarge.

Turgor is the pressure exerted against the walls of the cells by the water inside of them, and this pressure helps keep the whole tissue stiff.  Imagine the difference between standing on a stack of empty shoe boxes (which would collapse under you) and a stack of shoe boxes each containing a large water balloon (which might support you).  When you forget to water your peace lily and its leaves droop, it’s because turgor has been lost through dehydration.  Similarly, when a slice of fruit starts to dry out, it gets limp because the turgor is not there.  Sometimes when apples are stored for a while, they start to lose turgor and they feel softer.  Their juice is also under less pressure so they don’t explode in your mouth.  Somehow Honeycrisp apples are unusually good at maintaining their turgor pressure over time (Tong et al., 1999).

For the turgor mechanism to work, the walls must be stiff enough to resist the pressure.  Wall stiffness also contributes directly to tissue firmness.  During ripening, enzymes in cell walls tend to soften them, but again, Honeycrisp resists this change and stays firm in storage (Tong et al., 1999; Harb et al., 2012).

Stiff walls and turgid cells don’t make a tissue crisp if the middle lamella doesn’t hold the cells together.  With a good middle lamella, a fruit can have smaller cells, less turgor, and more flexible walls without feeling mushy and grainy in your mouth.  Peaches prove this point.  They get very soft when ripe, but they don’t usually feel like an old wool sweater.  As long as the middle lamella is holding the cells together, your teeth can break into the cells and release their juices.  When that cement has dissolved, the individual cells come apart, and the tissue feels dry and even a bit grainy.  Again, Honeycrisp seems to have extraordinarily long-lasting lamellae (Tong et al. 1999).  

We always love an excuse to run experiments in the kitchen, and Honeycrisp presents one.  The middle lamella is made of pectin, and as Jeanne describes near the end of her Vaccinium post, overripe fruit sometimes fails to gel, probably because the pectin has broken down.  It would be interesting to compare the gelling capacity of Honeycrisp to that of other varieties whose lamellae are not as resistant.  Let us know if you try it.

How do Honeycrisp apples taste?  Their sugar is well-balanced by some tangy acid, but I haven’t spent enough time with this variety to have a vocabulary for it.  Beyond the sweet-tart balance, apple flavors can be extraordinarily complex, with both tropical flavors and notes from other members of the rose family (peach, almond, rose, cherry).  Flavors and aromas change with storage and growing conditions.  As anyone who has tasted wine can tell you, your own mood and your companions’ suggestions strongly influence your ability to name what you taste.  John Seabrook describes the origins and qualities of the Honeycrisp and its offspring SweeTango ® in a fabulous New Yorker piece, and I’m still not sure what to think of them.  I’m just happy that there are now so many varieties to choose from, and that between August and February I can pretty much buy what I like.

Arctic ® Goldens and Arctic ® Grannies

Arctic ® apples are not crisper or more refreshing than other varieties – just eternally whiter.  They are also shaping up to be far more controversial, and if you haven’t heard about them yet, you will.  Arctic ® Goldens and Arctic ® Grannies were derived from familiar old Golden Delicious and Granny Smith varieties using a very hot new method for modifying gene expression called RNA interference.  I’ll explain how that works below.  This spring (2015), the USDA determined that the new varieties are not plant pests in need of special regulation, and the FDA concluded that the fruits raise no food safety concerns.  With last month’s approval by Canadian regulatory boards, Arctic apples may now go into commercial production and be sold for human consumption in the US and Canada.  We could see them in a few years once trees mature and start producing fruit.

The “problem” with ordinary apples –

When you cut or bite into an apple, it slowly starts to turn brown, and some people can’t quite get over that.  But the color has nothing to do with the apple’s freshness, only its storage temperature and the time it has been exposed to oxygen.  You might even say that the apple is showing off its stress-induced tan, since one of the brown pigments produced is melanin.  In apples and other fruits, the pigment doesn’t protect the plant from UV rays, but it does seem to interfere with insects’ digestion and may deter further damage.  Enzymatic browning begins when cells are damaged (bitten or cut) and small phenolic compounds sequestered in one part of the cell (the vacuole) are liberated.  The phenols are then free to react with enzymes called PPOs (polyphenol oxidases) which link them together into larger molecules that go on to form the dark colored polyphenols that insects and some people find objectionable. 

This pink pearl apple is pink all the way through. That’s one solution to browning.

You hardly notice the totally natural browning reaction if you eat your apples promptly and completely.  But all across North America it is allegedly a big problem, and Okanagan Specialty Fruits, Inc. have a solution: two new “Arctic ®” apple varieties whose genes endow them with everlasting snow-white flesh.  The scientists at Okanagan argue that if apples won’t brown then there is no need to treat them with sour-tasting acid or to throw out slightly tanned abandoned fruit.  Pre-cut apples are a surprisingly big business.  The three dominant hamburger chains offer apple slices in their kids menus, lots of restaurants offer them on food bars, and grocery chains sell bags of pre-sliced apples for home use.  Thus an apple variety that always looks freshly cut could give its producers a huge stake in the growing market for nutritious convenience foods.

I say “could” because Arctic Goldens and Arctic Grannies are genetically modified organisms, and not all consumers are open to eating GMOs.  Even consumers who love the idea of Arctic apples might not be able to buy them if their main supply of fresh apples comes from the drive-through.  That’s because McDonalds could reject Arctics the way they rejected GMO potatoes, produced using similar technology (as reported by several reliable news outlets last fall).

On the other hand, consumers are likely to hear the claim that Arctic apples are different from other GMOs in a way that makes them more acceptable, and if that claim sticks, Arctics could enjoy an easy entry into the mainstream food system.  For example, the method for creating Arctic apples involves a clever use of the apples’ own genes and quality-control mechanisms.  Unlike the modifications that produce Bt corn and Roundup Ready soy, the non-browning trait involves no “foreign” genes or novel proteins that might end up in food.  (Well, there is that marker gene and presumably present but undetectable levels of its protein product.)  Arctic apples also probably entail fewer ecological risks than current GMO crops.  Since Arctics do not produce a pesticide (like Bt) or resist an herbicide (like Roundup) they shouldn’t promote insect resistance or problem weeds.  Moreover, since apples are propagated through cuttings, not seeds, they are very unlikely to spread genes to neighboring orchards in a way that endangers other producers’ non-GMO status. 

Whatever your view of this application or of GMOs more generally, it’s fair to note that Okanagan has been unusually transparent about its GM technology, and their researchers have written many pages explaining the science to a broad public.  Without their openness, I would not know which of several possible techniques they used and therefore which to explain here.  For further exploration of the ecological issues, see Bettenhausen, 2013.

The technological solution –

For a review of DNA, RNA, and proteins, click to enlarge

Cut apples will stay white if there are no functional PPO enzymes to turn phenols into brown pigments.  In your kitchen, you can disable PPOs temporarily by adding lemon juice or vitamin C to your cut fruit.  Some commercial fruit washes (using calcium and vitamin C) are designed to retard browning for 3 weeks (!).  Plant geneticists can turn off a cell’s ability to make the enzymes in the first place.  It turns out that there is a whole family of genes that code for slightly different PPOs, and Okanagan scientists had to target all four of the most important genes to shut down browning nearly completely (OSF petition, 2012).  (For an overview/review of how the information in DNA gets translated into enzymes and other proteins, see the box to the right.)

One increasingly popular way to keep a protein from being made is to leave the normal gene intact but to silence it by killing its messenger RNA.  Researchers do this by manipulating a fundamental control mechanism used by plants, animals, fungi, and essentially all eukaryotes: RNA interference (or RNAi).  In nature, there are various reasons that a cell might want to stop an RNA message from being translated into a protein, and there are various versions of RNA interference.  In some cases, RNAi protects the organism from certain viral infections (e.g. polio) that depend on host cells to reproduce double-stranded viral RNA.  In other cases, cells target their own RNA as a way to stop gene expression after the DNA has already sent out its message.  In both situations, the cell deploys a complex of interconnected proteins to search and destroy RNA messengers carrying specific bits of code.

When I think about RNAi I like to imagine those doomed messengers Rosencrantz and Guildenstern, carrying a letter to the King of England.  During their journey conditions change, and their original orders (kill Hamlet) are never carried out.  Instead, the very message they are carrying marks them for execution by a large mass of protein that cuts them to bits.   (OK so the comparison is not perfect.  Hamlet changed the letter, whereas the RNA message is not altered en route.)

Oddly enough, a gene can be silenced by introducing an additional copy of it into the chromosome.  With this technique, the extra copy is simply a much shorter version of the original gene.  Arctic apples carry at least one extra shortened copy of each of its own native PPO genes.  When the cell tries to make an RNA messenger from these short copies, the messenger doubles back and sticks to itself, forming a hairpin loop.  The cell recognizes that something has gone wrong with this message and deploys the RNAi system to destroy any messages that look similar.  The normal RNA messages from the normal PPO genes get caught up in the search and are likewise destroyed.  (Like when Hamlet kills Polonius after he makes a Claudius-like noise behind the curtain…) No messages mean that none of the targeted PPO enzymes are made and no pesky browning will occur.

The technology is very powerful, but the actor I admire most in this whole tale is the plant cell, with its clever defense strategy and its tricks for finely controlling gene expression.  And given the intricacy of this drama, we’d be stupid to think that the apple cells didn’t have more secrets to reveal.  For example, there are many different PPOs, and they do a lot more than make pigments (Sullivan, 2015).  Most occur in chloroplasts and are associated with essential parts of the photosynthetic machinery.  What happens if and when those functions are undermined?  Okanagan Specialty Fruits did not report any growth problems in their trial plants, and maybe commercial trees planted on a wide scale will do just fine.  It will be interesting to watch the story unfold.  Now the company says it is developing non-browning varieties based on Fujis and Galas.  If these work out, I hope OSF’s marketing team looks to Hamlet’s haplessly meddling friends for inspiration.  I think Rosy Crown and Golden Star would make wonderful apple names.  (Certainly better than Arctic Granny, who would admirably grit her way through a Yukon winter with a single pair of high-waisted wool undies.  No Juicy Pink sweatpants for her.)

The other non-browning apple: Opal®

Opal lost its luster as a girls’ name towards the end of the Second World War, but despite its old-fashioned connotations, the Opal® has become a much sought-after apple.  Opals, like Arctics, stay white for a long time thanks to their low levels of polyphenol oxidases (PPOs).  The big difference, which is heavily advertised, is that they are conventional hybrids, not genetically modified.  The Opal® website makes very clear that “they are the first U.S. apple variety to be verified by the Non-GMO Project, the only independent verification in North America for non-GMO food.”  Until Arctics are available in stores, there are no GM apples for sale anywhere, but it’s obvious why Opal would want to clear up any confusion before Arctics hit the market.  And it’s not only the non-browning insides that are similar.  Since Opals are derived in part from Golden Delicious (crossed with Topaz), they strongly resemble Arctic Goldens in having rich amber-toned skin.  One difference is that Opals have a bit of russeting (rough brown surface markings) around their stems. 

Interestingly, Opals have not already pre-empted Arctics in the pre-cut apple market.  They seem to be sold primarily as whole fruits directly to consumers, perhaps because of their limited supply.  Although they were developed about 15 years ago in Europe (the Czech Republic) Opals have been available in the U.S. only about 5 years, and they are supplied by a single licensed grower in Washington State.  They are available for just a few months of the year.  I have never tried one, but I’m keeping my eyes out for them.  Eventually it will be fun to compare them to Arctic Goldens.

The last apple of the season, stored for 6 weeks, has lost its turgor. I ate it anyway. It tasted amazing.

My favorite apple supplier closed his stand in mid-February this year.  I stocked up, but this week I ate the last apple from my stash.  It was as old and wrinkly as Polonius, and slightly rubbery, but the concentrated flavor was amazing.  Exeunt.

References

Arctic apple documents:

Petition for Determination of Non-regulated Status http://www.aphis.usda.gov/brs/aphisdocs/10_16101p.pdf

Draft Environmental Assessment http://www.aphis.usda.gov/brs/aphisdocs/10_16101p_dea.pdf

Bettenhausen, C. (2013) Engineered Apples Near Approval. Chemical and Engineering News 91:31-33 http://cen.acs.org/articles/91/i14/Engineered-Apples-Near-Approval.html

Constabel, C.P., et al. (1996) Polyphenol oxidase as a component of the inducible defense response in tomato against herbivores. Ch. 9 in Romeo et al. (eds) Phytochemical Diversity and Redundancy in Ecological lnteractions. Plenum Press, New York.

Harb, J. et al. (2012) Molecular analysis of softening and ethylene synthesis and signaling pathways in a non-softening apple cultivar, ‘Honeycrisp’ and a rapidly softening cultivar, ‘McIntosh.’ Postharvest Biology and Technology 64: 94–103

Jin, Y. and Guo, H-S. (2015) Transgene-Induced Gene Silencing in Plants Ch. 7 in K. S. Mysore and M. Senthil-Kumar (eds.), Plant Gene Silencing: Methods and Protocols, Methods in Molecular Biology, vol. 1287, Springer, New York. DOI 10.1007/978-1-4939-2453-0_7

Mann, H., D. Bedford, J. Luby, Z. Vickers, and C. Tong (2005) Relationship of instrumental and sensory texture measurements of fresh and stored apples to cell number and size. Hort Science 40: 1815-1820

Seabrook, J. (2011) Crunch: building a better apple.  New Yorker Magazine http://www.newyorker.com/magazine/2011/11/21/crunch

Sullivan, M. L. (2015) Beyond brown: polyphenol oxidases as enzymes of plant specialized metabolism Front. Plant Sci. doi: 10.3389/fpls.2014.00783

Tong et al. (1999) Comparison of Softening-related Changes during Storage of ‘Honeycrisp’ Apple, Its Parents, and ‘Delicious.’ Journal of the American Society of Horticultural Science 124(4):407–415. 1999

Waltz, E. (2015) USDA approves next-generation GM potato. Nature Biotechnology 33: 12–13 doi:10.1038/nbt0115-12 http://www.nature.com/nbt/journal/v33/n1/full/nbt0115-12.html

Will seedless watermelons make us superhuman or turn our children into giants?  Hardly, but they do give home cooks the power to count chromosomes without a microscope.   Just a knife or a hard thunk on the sidewalk are enough to get a watermelon to spill its genetic guts.

If you were reading a Hearst Corporation newspaper in late 1937, you might have thought humanity would eventually be swallowed up by giant carnivorous plants, unwittingly unleashed by uncontrolled biotechnology.  The San Francisco Examiner reported on November 21st of that year that the discovery of an “elixir of growth,” meant that “…science may at last have a grip on the steering wheel of evolution, and be able to produce at will almost any kind of species…”  including “…a plague of man-eating ones.”  In 1937 Americans had much more important things to worry about, just as we do now.  Still, that discovery may in fact have threatened one cherished aspect of the American way of life by triggering the slow demise of late summer state fair watermelon seed spitting contests.  It doubtlessly paved the way for seedless watermelons, and in 2014 the total harvest of seedless watermelons on American farms – nearly 700 thousand tons – outweighed the seeded watermelon harvest more than 13 to 1 (USDA National Watermelon Report). A similar pattern is emerging this year.  Is there no stopping the attack of the seedless watermelons?

CLICK to read. Image from microfilm of an actual page in the San Francisco Examiner, published Sunday November 21, 1937. Found in the Media and Microtext Center of Stanford University Libraries.

And more important, how is it even possible to get seedless fruit from an annual plant?  From a plant whose only mode of reproduction is through those very seeds?  From a plant that cannot make suckers as bananas do and cannot be perpetuated endlessly through grafts like fruit trees and vines?   Such is the challenge posed every single year by watermelons, but thanks to the “elixir of growth” discovered by Albert Blakeslee and subsequent work by Hitoshi Kihara, one of the most prominent agricultural geneticists of the 20th century, the world has an elegant solution. Breeders continually improve the varieties available, and consumer demand keeps growing, yet seedless watermelon production methods have remained essentially unchanged for three quarters of a century.

This watermelon definitely has seeds

Pollination without procreation

Seeds normally develop when pollen grains germinate on the stigma of a flower and pollen tubes grow down into the ovary to deliver sperm cells to the eggs inside the potential seeds (ovules).  (see Jeanne’s fuller explanation here) The surrounding ovary is then stimulated to develop into a fruit.  You might think that seeds could be avoided if pollination could be avoided.  No pollen, no sperm, no seeds.  But also no fruit.  Large sweet fleshy fruits are expensive for a plant to produce, but the investment pays off if the fruit entices animals to disperse its seeds.  Natural selection generally favors a high return on investment, and accordingly, watermelon fruits develop only if their flowers are amply pollinated and the chance of producing seeds seems high. (Although wild watermelon fruits are smaller than commercial varieties and not sweet, they still represent a serious investment of resources; see Paris 2015)

Preventing pollination is not a solution.  It turns out, though, that a big load of pollen is enough to send the hormonal signals that promote watermelon fruit development, even if seeds ultimately never develop.  What’s needed, then, is some way to trick the plant by providing a full pollen load while preventing the sperm in the pollen from fertilizing the egg and producing a viable embryo-filled seed. 

Right now some of you are imagining thousands of microscopic condoms for the pollen tubes.  It’s an amusing image, but the much more effective way to block embryo development is to start with defective egg cells.  Plant egg cells are produced inside ovules (which would become seeds if fertilized) after a sequence of cell divisions that includes meiosis, the type of cell division that halves the number of chromosomes in a cell.  Messing up meiosis will produce defective eggs.  The geneticist Hitoshi Kihara knew that meiosis would be disrupted in every ovule of a plant if the plant body had three copies of each chromosome (a condition known as triploidy) instead of the usual two.  On that point he seems to have been inspired by triploid seedless bananas (Crow, 1994).  His great contribution was developing a technique to produce those triploid watermelon plants that would bear seedless fruit.

A seedless watermelon

Why triploids don’t make seeds

Humans normally have 23 pairs of homologous chromosomes, for a total of 46 chromosomes in most cells.  One set of 23 is inherited from one parent, and the homologous set comes from the other.  Similarly, watermelons normally have 11 pairs of chromosomes, for a total of 22.  Having two copies of each chromosome makes us and watermelons diploid (Greek for 2-ply, written as 2N).  Unless our parents are completely genetically identical (impossible in humans), the chromosomes in a pair are similar – “homologous” – but not identical.  They carry the same sequence of genes, but will have different versions (alleles) of many of those genes.  For example, both homologs of chromosome 6 in watermelon carry a gene influencing striping pattern, but a watermelon plant may have inherited the allele for defined stripes from one parent and the allele for diffuse stripes from the other.

A full set of human chromosomes, with homologous pairs brought together and digitally arranged in order of chromosome number.

Like humans, watermelons are normally diploid; however (unlike humans) a plant with three copies of each chromosome (3N, or triploid) does perfectly well doing its everyday thing, growing and photosynthesizing.  Plants in general are remarkably tolerant of extra chromosomes, and polyploidy is rampant in the plant world.  For example, bread wheat is hexaploid (6N) and common commercial strawberries are octoploid (8N).  The trouble starts with meiosis.

Small undeveloped seeds can be found in a seedless watermelon, but most people just eat these

Polyploids with even numbers of chromosomes, such as wheat and strawberries, can produce normal gametes (more on this below), but triploids (or pentaploids, etc.) mostly do not.  When all three homologs are properly matched and lined up on the equator ready to separate, they cannot be divided equally.  Sometimes only two homologs find each other, but then the third is left floating around on its own, which also prevents normal meiosis.  With 11 sets of three homologs, in a given cell there may be a combination of indivisible triplets and pairs-plus-singles.  In any case, the egg and its supporting cells fail to form, and the ovule remains small and soft and inoffensive enough to be ignored.  The desired watermelon fruit develops in response to the pollen load, but the unwanted seeds never do.

CLICK to enlarge. Plants that grow from triploid seeds grow normally, but they are sterile. Pollen from a diploid plant is used to stimulate fruit growth, but seeds never develop.

How we make triploids (but not giant rats)

Seedless triploids are beautiful in theory, but they don’t occur naturally in watermelons.  How do breeders make a triploid plant from a diploid species? By bringing together a typical haploid (N) gamete from one parent and a diploid (2N) gamete from another.  The most reliable way to produce diploid gametes is to start with a tetraploid parent (4N).  Recall that even-numbered polyploids, unlike triploids, can make functional gametes through meiosis.

Tetraploid plants come about through various mechanisms, both natural and artificial.  Sometimes ploidy is increased through hybridization between species (called “allopolyploidy,” as in bread wheat) and sometimes spontaneously within a species, even within a single plant (“autopolyploidy”). 

The earliest written report of successful chemical induction of autopolyploidy was made in 1937 by Blakeslee and Avery, who were working at the Carnegie Institution at Cold Spring Harbor in New York.  Following up on a tip from a colleague, they found that they could induce chromosome doubling by applying a plant-derived alkaloid called colchicine to either seeds or seedlings.  Some of their experiments charmingly involved an atomizer “purchased in Woolworths for twenty cents.” 

Applying colchicine with an atomizer from Woolworth. Excerpt from figure 5 of Blakeslee and Avery 1937.

What started innocently enough at Woolworths ended up splashed across the nation’s newspapers soon after Blakeslee and Avery’s discoveries became public.  The reports were so overblown that the editor of the Journal of Heredity was moved to include a comment at the end of the published article to quell “over-enthusiastic popularizations” resulting from “the tidal wave of wierdly [sic] misleading publicity distributed by the Hearst newspapers” involving giant babies and wheat as tall as a pine tree.  See below for an excerpt of his reassuring note.  Yellow journalism aside, colchicine is toxic.  Like many poisons, though, its properties are medically useful in low doses, and humans still take it for gout and some inflammatory diseases. 

Colchicine works by interfering with mitosis, the kind of cell division that goes on constantly in our bodies, creating (ideally) identical cells for growth, maintenance, and healing.  Before cells divide, they replicate their DNA so that each chromosome contains two copies of all the genetic material.  As in meiosis, the chromosomes are moved to the middle of the cell by microtubules.  In mitosis, however, the chromosomes line up single file and the two copies of the DNA are separated, not the homologs. A diploid cell becomes two diploid cells.

Colchicine-treated cells replicate their DNA as usual, but they are blocked from forming microtubules, so the cells do not divide; they just go on living with the extra copies of their chromosomes.  What Blakeslee and Avery identified was the right amount of the chemical for the right length of time to prevent one round of cell division and induce tetraploidy but allow cells to start dividing again soon after that.  With the correct protocol, plant parts that develop after colchicine treatment – including flowers – should all be tetraploid.  Tetraploid flowers will produce diploid gametes (through meiosis) to be joined with haploid gametes from diploid plants to create triploid offspring.

CLICK to enlarge. Triploid watermelon seeds are made by crossing a tetraploid maternal plant with a diploid paternal plant. The resulting embryos are triploid. The fruits containing the seeds are tetraploid and not harvested for food. The triploid seeds are harvested for sale to growers.

It didn’t take long for Hitoshi Kihara to apply the new and exciting colchicine technique to watermelons, but it took a while to perfect it (Crow, 1994).  One problem, as it turns out, is that tetraploid plants do still have some trouble making gametes, especially when all four copies of their chromosomes find each other and get tangled up.  Breeders therefore select the most fertile tetraploid lines to develop, and over time meiosis becomes more normal.  Once established, tetraploid lines can be maintained and propagated through seeds.  There is no need to use colchicine again except to initiate a new tetraploid variety.  Seed companies then use diploid plants to pollinate tetraploid flowers, which develop into fruit containing seeds with triploid embryos.  We in turn buy those seeds to plant in our gardens as seedless varieties.

Growing triploids

With many very tasty seedless varieties available, why would anyone grow seeded watermelons these days?  One reason is that triploid seeds cost about twice as much as diploid seeds because seed companies need to recoup their investment in developing tetraploid lines and generating seeds annually.  Another consideration is the opportunity cost of growing seedless watermelon varieties.  Alongside the triploid plants, farmers and gardeners have to plant diploid “pollinizer” plants, at a ratio of 2-to-1 triploids.  Doing so ensures that there is enough pollen deposited on the stigmas of the triploid flowers to trigger fruit formation.  Not only do farmers pay more for the triploid seeds, but they have to make room for the diploid vines to grow.  Their extra cost is often passed along to consumers at the market or grocery store, who may be reluctant to pay the higher price.

CLICK to enlarge. From top left, moving clockwise, the stages of creating a seedless watermelon. To make a tetraploid line, colchicine is applied to diploid seedlings. Resulting tetraploid growth is allowed to flower and produce seeds. Those seeds are planted and the best versions are selected for several generations to establish a strong tetraploid line. Every year, seed producers fertilize tetraploid plants with pollen from diploid plants to create triploid seeds. Triploid seeds are sold to growers as seedless varieties. These plants must be pollinated by a diploid plant in order to make the fruit we eat.

Counting chromosomes and thinking of bees

Through the magic of colchicine, you have the power to tell a diploid from a triploid watermelon in your kitchen.  If it has full-grown shiny black seeds, it’s a diploid.  If it does not, it’s a triploid.  That said, it is possible that in production, a tetraploid flower could be contaminated with pollen from another tetraploid flower and thus produce tetraploid seeds that accidentally get sold as triploids.  However, according to the Cucurbit Breeding Project at North Carolina State University, tetraploids are usually bred to have a grey rind exactly so that any tetraploid seeds sneaking through would be evident to growers as soon as fruits started to develop.

I’ll admit that old fashioned seed-filled watermelons have their charms.  Watermelon seeds are beautiful, especially against the deep red and sweet background of watermelon flesh.  And the zone of seeds conveniently demarcates the heart. On the other hand, I love to contemplate the genetic gymnastics required to produce a seedless watermelon.  If the biology of seedlessness is not enough to capture your own imagination, consider the bees.  One study found that bees have to visit a triploid flower 16 to 24 times before it will produce a good fruit (Walters, 2005).  That’s twice as many visits as a seeded variety requires.  Humans may have escaped a nightmare plague of six-foot-long carnivorous caterpillars, but the bees really are in serious trouble, and we’d better do all we can to keep those bees happy and healthy and abundant.

Excerpt of a note by the editor of the Journal of Heredity, 1937, at the end of the article by Blakeslee and Avery:

“MANY readers of the JOURNAL will be interested, we feel sure, in some expansion and explanation of certain points not touched on in Dr. Blakeslee’s article, which have come up in connection with this most interesting subject. The tidal wave of wierdly misleading publicity distributed by the Hearst newspapers on November 21, has doubtless aroused hopes and fears that have no foundation whatever. Colchicine is not a “growth elixer,” and evidence is lacking as to its effects on animal chromosomes, so that doctors may still make their calls safe from attack by giant rats, and ladies are in no danger of being gobbled up by caterpillars suddenly gone carnivorous.

Colchicine is a narcotic alkaloid, related chemically to morphine and codeine. It is a very potent and very poisonous substance whose immediate effect on growing tissues even in very small concentrations is to produce stunting and distortion. It offers no Magical Royal Road to the production of new varieties of plants and animals. In spite of the cold water which must be thrown on over-enthusiastic popularizations, the effect which colchicine has on doubling the number of chromosomes in the cells makes it unquestionably one of the most important genetic discoveries of the year.”

References

Agricultural Research Service, USDA. (1971) Production of seedless watermelons.  Technical Bulletin no. 1425. http://naldc.nal.usda.gov/download/CAT71326739/PDF

Blakeslee, A. F., & Avery, A. G. (1937). Methods of inducing doubling of chromosomes in plants by treatment with colchicine. Journal of Heredity, 28(12), 393-411. http://jhered.oxfordjournals.org/content/28/12/393.short

Crow, J.F. (1994) Hitoshi Kihara, Japan’s pioneer geneticist. Genetics 137: 891-894.  http://www.genetics.org/content/137/4/891.full.pdf

Gama, R. et al. (2015) Microsatellite markers linked to the locus of the watermelon fruit stripe patternGenetics and Molecular Research 14 (1): 269-276 (2015) http://dx.doi.org/10.4238/2015.January.16.11

Paris, H. S. (2015). Origin and emergence of the sweet dessert watermelon, Citrullus lanatus. Annals of botany, mcv077.

Science opens the way to make our children giants. San Francisco Examiner (1937, Nov. 21). Media and Microtext Center, Stanford University Libraries.

USDA National Watermelon Report.  Week ending Sept 4, 2015. http://www.ams.usda.gov/mnreports/fvdtvmelon.pdf

Walters, S. A. (2005). Honey bee pollination requirements for triploid watermelon. HortScience, 40(5), 1268-1270. http://hortsci.ashspublications.org/content/40/5/1268.short

Biologist Jessica Savage answers a few of our questions about her research on the physiology behind giant pumpkin size.

In October 2014, a giant pumpkin grown by Beni Meier of Switzerland tipped the scales at 1056 kilograms (2323 pounds) and set a new world record for the heaviest pumpkin ever weighed. Modern competitive pumpkin growers have been imposing very strong selection on pumpkin size for decades. Pumpkin fruit size keeps climbing, and old records are broken every year or two (Savage et al. 2015).

Beni Meier with his 2014 record-winning 2323-pound pumpkin, presumably a specimen of the Atlantic Giant variety of Cucurbita maxima. Photo from here.

The giant pumpkins breaking records are probably not the same kinds of squashes that are destined to be Halloween jack-o-lanterns or pumpkin pie. The behemoths are primarily fruit specimens of the Atlantic Giant variety of the species Cucurbita maxima (Savage et al. 2015). C. maxima varieties are collectively known as the hubbard squashes (see our post on squash diversity for information on the several squash species that earn the name “pumpkin”). Many hubbard squash varieties are grown as food and have been under selection for delicious, sweet, firm fruit. If you buy canned “pumpkin” for pie, you’re probably eating one of those sublime hubbard varieties.

Amish pie pumpkin, a large and delicious variety of hubbard squash, Cucurbita maxima. That’s a 12-inch chef’s knife for scale.

The edible hubbard varieties do produce impressively big fruit, but they are nowhere near the size of the Atlantic Giants (Savage et al. 2015). “These fruits really present an interesting study system because they have been under strong selection from humans for years for their size,” says Jessica Savage, a biologist who studies the evolution and physiology of giant pumpkins. Savage continues: “While it is desirable to breed many fruits to be large, in the case of edible fruits, there are other things to consider including taste. This is not a concern for the giant pumpkin growers. In fact, giant pumpkins tend to be fibrous and are not considered palatable to many. All that matters is size.”

The 2014 Topsfield Fair giant pumpkin weigh-in, Topsfield, MA (photo by J. Savage)

So, how did giant pumpkins get to be so large? What physiologically separates the giant pumpkin varieties from their brethren destined for pumpkin spice lattes? The short answer is that giant pumpkin plants produce more phloem than do plants of other squash varieties (Savage et al. 2015). Phloem is the component of a plant’s vascular system that moves solutes, mostly sugar, around the plant. Xylem is the other main component of plant vasculature, and its primary job is to move water and nutrients from the soil through the plant. We discussed xylem function in our post on maple syrup. Jessica Savage and her colleagues studied the anatomy and physiology of both phloem and xylem and a variety of other components of squash plants’ carbon acquisition and allocation in an effort to determine how Atlantic Giant squashes achieve giant size (Savage et al. 2015).

Large specimens of edible varieties of Cucurbita maxima and Cucurbita moschata, similar to the edible hubbard used in Savage’s research

Savage and her colleagues grew an edible hubbard squash variety and Atlantic Giants under identical conditions in a greenhouse and measured several aspects of the plants’ carbon (sugar) supply chain, from the carbon source in the leaves, through the vascular transport system, to the carbon sink: the fruit. Squashes and other species in the squash family (Cucurbitaceae) are particularly suited to studies of plant vasculature, as Jessica Savage explains below in a special interview post to explain phloem function and how it helps us understand the evolution of size in giant pumpkins.

Q&A with Jessica Savage about phloem and giant pumpkin physiology

Question 1: How do you like to explain phloem and its function to a general audience? “With pictures!” is a good beginning to an answer here.

Jessica Savage: “Plants are able to “feed themselves” by producing sugar in their leaves through photosynthesis but they need to be able to move this sugar to different parts of their body to sustain growth in various organs like roots and fruits/flowers. They achieve this using part of their vascular tissue, the phloem, which is specialized in transporting sugars. However, plants, different than animals do not have a heart to drive circulation of fluid in their vascular system, instead, they rely on mostly passive processes.”

Phloem function schematic diagram by J. Savage

“In the phloem, transport is driven by the movement of water into and out of the tissue in different parts of the plant. In their leaves, which we refer to as “source tissue” because it is the source of sugar, the phloem contains a high amount of sugar. This sugar draws extra water into the cells making them full and swollen. Meanwhile, other locations in the plant act as “sink tissues” (for example the roots or fruits) because they pull sugar out of the phloem to use for growth and other processes. In these locations, sugar concentrations are low inside the phloem. This causes water to leave the cells making them more limp. Because the source and sink tissue are connected, water moves from the full cells in the source to the more limp cells in the sink tissue. This “pressure-driven” pump allows for plants to move sugars from where it is plentiful to where it is more scarce.”

Question 2: Why do pumpkins (and other cucurbits) lend themselves to the study of plant vasculature?

Jessica Savage: “Pumpkins and cucurbits are great for studying sugar transport because the cells in their phloem are wide and have large pores connecting them. This makes them easy to see using a microscope. They also have some great properties which help us study their physiology, for example, the cells in their leaves are very connected. This seemingly simple characteristic is very important because if we want to put dye into the phloem to watch phloem transport in living plants, we can put the dye in any of the cells in the leaves and it will eventually get into the phloem.”

Question 3: On the other side of that coin, how does understanding phloem function and its evolution help us understand how giant pumpkins got so giant?

Jessica Savage: “The size of giant pumpkins to me is intriguing because it presents what I often refer to as a “traffic control problem”. In normal sized pumpkins, there are many small fruit and sugar is transport in different directions to feed them all. This is similar to traffic in the country where everyone is going to work in different directions and there is not too much traffic on any one road. However, in giant pumpkins a large amount of sugar is going into one fruit. This is more like the situation where you have a big city and everyone is going into this city for work in the morning. As a result, there needs to be either more roads or roads with a higher capacity to support the high amount of traffic entering the city. The same is true for giant pumpkins, either they need more phloem or phloem with a higher transport capacity to sustain these large fruits, especially considering that giant pumpkins can move a couple pounds of sugar into their fruit in a day.”

“When we look at giant pumpkins, we find that the solution that pumpkins have to this problem is producing more roads, or more phloem. When you compare different varieties of Cucurbita maxima, the giant varieties that have been bred for pumpkin competitions all produce more phloem. This allows them to move more carbon into individual organs than smaller fruited varieties. This changes is likely important in supporting the rapid growth rates we see in these fruits.”

Figuring out the mystery of how Atlantic Giants produce massive fruit

Excerpt from Figure 2 from Savage et al. (2015) of microscope slides of vascular anatomy of C. maxima. From their caption: “Vascular bundles of (a) Atlantic Giant and (b) Hubbard squash varieties. Bars are 250 micrometers. Pedicel cross sections of (c) Atlantic Giant and (d) Hubbard squash varieties. Bars are 500 micrometers. (e) Irregular vascular bundle in pedicel of an Atlantic Giant. Bar is 500 micrometers. Labels are as follows: EP and IP are external and internal fascicular phloem, respectively, F is fibres, and X is xylem.” Atlantic Giant have noticeably more phloem than does the hubbard.

To figure out how giant pumpkin size was achieved, Savage and her colleagues traced the anatomy of sugar production, transport and consumption from leaf to fruit. In their greenhouse study, Savage and her colleagues (2015) reported that the leaves from both varieties photosynthesized at about the same rate, so each square centimeter of leaf brought similar amounts of sugar into the plant in a given amount of time. And the hubbards actually produced slightly more leaf area than did the Atlantic Giants, so the total sugar inputs were similar or tipped slightly in favor of hubbards. The vascular system of both types had similar amounts of xylem (the amount of area in cross section occupied by xylem). Both the aboveground and belowground vegetative parts of the plants grew at roughly the same rate. The Atlantic Giant, though, made more flowers, and their fruits grew much faster than the hubbards. How? The vascular transport system—composed of stems, the petioles connecting the leaf blades to the stem, and the pedicels connecting the fruit to the stem (the “handle” of a ripe pumpkin)–of Atlantic Giants contained much more phloem than did the petiole-stem-pedicel pipe system of hubbards (Savage et al. 2015). The structure and function of the phloem itself was very similar for the different squash varieties. Only the amount of phloem changed, providing the capacity to transport the high volume of sugar needed to grow the giant fruit.

An Atlantic Giant pedicel, the narrow “stem” connecting the fruit to the main stem of the plant. Photo by J. Savage

Additionally, Atlantic Giants seem to take a substantially longer time to develop the ovary (the immature fruit prior to pollination, as well explained in Katherine’s post about watermelon, a close relative of pumpkin) and mature the fruit, with the longer maturation time translating to larger overall size (Savage et al. 2015). Further, Atlantic Giants have a thinner, softer outer fruit wall (exocarp) than do edible hubbards, which may increase the ability of Atlantic Giants to expand to large size (Savage et al. 2015). I imagine the softer, more elastic outer fruit wall would decrease its storage capacity, but that’s not important for these competitively grown pumpkins, unlike in the hubbards you expect to store for months to eat through the winter and spring.

Understanding how squashes have achieved the feat of large fruit size is interesting in and by itself, but the work of Savage and her colleagues also has strong implications for understanding the limits of agricultural yield and fruit and seed production strategies of wild plants (Savage et al. 2015).

Many thanks to Jessica Savage for helping us understand phloem function and her outstanding research on the physiology and evolution of giant pumpkins. We wish everyone a happy Halloween!

References

Savage, J. A., D. F. Haines, and N. M. Holbrook. 2015. The making of giant pumpkins: how selective breeding changed the phloem of Cucurbita maxima from source to sink. Plant, Cell and Environment 38:1543-1554.

We’ve got several posts in the pipeline – and this year we are contributing to Advent Botany – but meanwhile, we bring you posts from the past to nerd-up your kitchen as you cook. Don’t forget, nothing deflects from an awkward personal revelation or a heated political conversation like a well-placed observation about plant morphology.

We wish you a happy, healthy Thanksgiving!

Click a caption to serve up the whole post.

Brussels sprouts and kale

Whole sweet potatoes (NOT yams!)

Cranberries

Squash casserole

Pecan pie

Sugar plums dance, sugar cookies disappear from Santa’s plate, and candied fruit cake gets passed around and around. Crystals of sugar twinkle in the Christmas lights, like scintillas of sunshine on the darkest day of the year. Katherine and Jeanne explore the many plant sources of sugar.

Even at a chemical level, there is something magical and awe-inspiring about sugar. Plants – those silent, gentle creatures – have the power to harness air and water and the fleeting light energy of a giant fireball 93 million miles away to forge sugar, among the most versatile compounds on earth, and a fuel used by essentially all living organisms.

Sugar naturally occurs in various chemical forms, all arising from fundamental 3-carbon components made inside the cells of green photosynthetic tissue. In plant cells, these components are exported from the chloroplasts into the cytoplasm, where they are exposed to a series of enzymes that remodel them into versions of glucose and fructose (both 6-carbon monosaccharides). One molecule of glucose and one of fructose are then joined to form sucrose (a 12-carbon disaccharide). See figure 1.

Figure 1.

Sucrose is what we generally use as table sugar, and it is the form of sugar that a plant loads into its veins and transports throughout its body to be stored or used by growing tissues. When the sucrose reaches other organs, it may be broken back down into glucose and fructose, converted to other sugars, or combined into larger storage or structural molecules, depending on its use in that particular plant part and species. Since we extract sugar from various parts and species, the kind of sugar we harvest from a plant, and how much processing is required, obviously reflects the plant’s own use of the sugar.

Close to the source

The purest source of sugar in a plant is probably its veins, or more specifically, phloem cells making up the sieve tubes. Unlike other cells, they have little content besides sugar water, which is loaded directly from photosynthesizing leaves. Conveniently, the sugar water moves through the plant body in the phloem along a pressure gradient, so if you breach a bunch of sieve tubes, the sap will flow out of the plant and into a container. Just ask an aphid (Figure 2).

Figure 2. An aphid’s proboscis pierces a plant’s phloem to extract sugar water.

You would expect human sugar thieves to emulate our aphid friends and steal our sugar straight from plant veins. As it turns out, palm sugar is the only real commercial use of sweet sap taken directly from the phloem stream. Tropical palms (genera Cocos, Arenga, and Borassus; family Arecaceae; order Arecales) send a large amount of sugar-rich sap through their veins to fuel rapidly growing flowering stalks. While flowers are still immature and drawing lots of sap, harvesters cut the flowering stalks (either rachises or peduncles) and collect the dripping sugar water into containers. A mature tree can produce up to 50 liters (over 13 gallons) of sap a day. Although the sap is fairly concentrated – about 10% sucrose in solution – it must still be boiled down into syrup or crystallized into sugar. In fact, if sugar is the goal, it must be boiled right away to stop its fermentation into alcohol.

Maple sap collection: tubes run from a vacuum device to the tapped sugar maples and carry sap to the collection location.

Maple syrup and maple sugar are one additional step removed from the photosynthetic source. Although we harvest the sap directly from maple (Acer saccharum; Sapindaceae; Sapindales) plant veins, we take it from the xylem, not the phloem. As Jeanne detailed more fully in another post, the sucrose in maple syrup is synthesized during the summer and stored for the winter in the plant stem in cells adjacent to the xylem. When conditions are right, pressure within the stem pushes the sap into the xylem, from which it can be tapped.

Positive root pressure causes early spring sap flow in paper birch (Betula papyrifera)

Birch trees (Betula spp.; Fagaceae; Fagales) can also be tapped for sugary xylem sap in the spring, although birch sap flow results from root pressure, not stem pressure as in maple, and its primary sugars are fructose and glucose, unlike sucrose in maple. As we explain below, most stored carbohydrates are not easy to extract; however, maples (and some other species) naturally isolate and remobilize their stored carbohydrates for us. Still, maple sap is dilute (about 2% sugar), and concentrating it into useful syrup is hard work (birch sap is more than twofold more dilute than maple sap). Maple and birch sap also contain additional salts and various organic molecules that contribute to its flavor.

The nasturtium spur contains a very sugary nectar to reward hummingbird pollinators

Sap is a plant’s lifeblood, and it must be stolen, but plants offer their sugar freely in the form of floral nectar. Nectars make wonderful food because their sugars are augmented with minerals, amino acids, and other compounds that attract and reward pollinators. By volume, nectar offers a much greater sugar reward than sap does, with some bee-pollinated species producing a 30% sugar solution for their visitors. Still, it would be impossible for humans to harvest enough tiny droplets from individual flowers to be worthwhile, so we outsource the hard work to bees and then steal it from them as honey. Honey bees collect nectar, digest any sucrose into its component monosaccharides, make other enzymatic transformations, and concentrate the result by evaporating it with their beating wings. In the end, honey is over 80% sugar, but its high proportion of easily soluble fructose helps limit crystallization (McGee, 2004). The fructose also makes honey-sweetened foods prone to burning because of its low melting and caramelization point.

Pulling sugar out of storage

purple sugarcane

The overwhelming majority of our table sugar derives from carbohydrates stored in special parenchyma cells lying near the vascular tissue that runs through stems (sugarcane; Saccharum spp.; Poaceae; Poales) or into roots (sugar beet; Beta vulgaris; Polygonaceae; Caryophyllales). Both sugarcane and sugar beet are usefully unusual because they store carbohydrates as sucrose, whereas most plants use starch for long-term storage (and transitory storage in their leaves).

Starch is well-suited to its role: it is a long chain of glucose molecules (sometimes branched) that does not readily react with other molecules and which can be packed tightly with other starch molecules into granules within the cell. Enzymes erode a granule gradually, releasing glucose when short-term reserves are low, and rebuilding granules when supplies are adequate. See figure 3 (showing beets not staining but carrot and potato staining for starch).

Figure 3

We, also, can convert starch to sugar on an industrial scale (see below), but sugar beet and sugarcane save us that extra step. Both species push their sucrose into relatively large storage cells that can be broken open to release extraordinarily high concentrations of sugar. Sucrose molecules make up about 80% of the dry weight of sugarcane parenchyma (Wardlaw, 1990) and 50-75% of the dry weight of whole sugar beet root (Elliott & Weston, 1993; Turesson et al., 2014). Clearly, these plants are a rich source of sucrose, as long as the pure sugar can be separated from masses of crushed sugarcane stems and beet roots – a matrix of cell fragments, tough conducting tissues and fibers, and numerous organic molecules.

Sugarcane juice is about 15% sucrose and contains many more chemical components other than sucrose and water. If the sugarcane juice is processed like maple syrup, a simple process of cooking it and evaporating it, the result is dark brown, molasses-flavored crystals called rapadura or panela (see Figure 4). To get pure white sucrose, the other components of sugarcane juice (minerals, proteins, phytochemicals) are removed iteratively. The solution can be dehydrated at any stage in this process, resulting in a suite of sugarcane crystal products marketed under various names (evaporated cane juice, raw sugar, cristallino, golden treacle, brown sugars, muscovado). The end stage of most sugarcane juice processing, though, results in two products: pure white sucrose crystals and liquid blackstrap molasses (or dark treacle), a dark, thick syrup that has plenty of sugars to make it sweet plus all the other minerals and phytochemicals.

Figure 4. Alternative processing of sugarcane juice. Figure from the Rapunzel company, which manufactures rapadura.

The name “molasses” is also applied to thick syrups produced by cooking down juices of plants other than sugarcane, including the stalks of fellow grass sorghum (Sorghum bicolor), apples (Malus domestica; Rosaceae; Rosales), and pomegranates (Punica granatum; Lythraceae; Myrtales).

sorghum stalks can be almost as big as sugarcane

Other concentrated fruit juices are frequently used as sweeteners (for example: grape, Vitis vinifera; and pineapple, Ananas comosus), but usually not with the name “molasses” attached to it, perhaps because the modern industrial processes of concentrating those juices doesn’t involve cooking, which caramelizes some of the sugars. Those fruit juices are so very sweet, of course, because some plant species produce sweet fruit to entice seed-dispersing animals. Dates (date palm, Phoenix dactylifera; Arecaceae; Arecales) have a particularly high sugar content (and are delicious), and dried and ground date fruits are used as a sweetener (date sugar).

Agave is another plant with an unusual carbohydrate storage strategy. Instead of making long chains of glucose (starch), it transforms its sugars into short chains of fructose (fructans), specifically inulin. Inulin and starch differ in ways that matter for both plants and humans. In plant cells, inulin may provide some protection from drought stress and freezing (Van den Ende, 2013), both of which may be faced by Mexican agave plants growing at high-altitude on volcanic soils. Inulin is much less obviously useful to humans. Whereas we digest starch easily, starting in our mouths and continuing until the glucose components are absorbed through our small intestines, we lack the enzymes to digest inulin. Inulin moves through our bodies intact until it reaches our large intestines, where “helpful” bacteria that can make the relevant enzymes break it down and release a lot of nasty gas into our colons. (See McGee’s (1990) engaging advice for reducing inulin in sunchokes).

Blue agave (Agave tequilana) hearts ready to be turned into agave syrup and tequila, showing cross section of the base of the very thick leaves. Photo source unknown.

Agaves accumulate inulin in their squat, cone-shaped stems (piñas) for about a decade, until their piñas have achieved the weight of a smallish adult human. At harvest, leaves are removed and the stems are heated gently to soften them and release their juice. Fortunately, agave nectar and agave sugar are primarily fructose, derived from the inulin. Enzymes present in the harvested agave sap naturally break the inulin down into its component sugar (Willems & Low, 2012). This sugary solution may be transformed into agave syrup or “nectar” or fermented into tequila.

rice plant

Grains (technically fruits, usually thought of as seeds) store energy reserves for the seedling mostly as starch. Sprouting those grains, or “malting” them, unleashes an enzymatic cascade within the grain that converts the starch into sugar. In the case of grasses barley (Hordeum vulgare) and rice (Oryza sativa), most of this sugar is maltose. Toasting and boiling these malted grains results in a caramel-flavored sweet liquid that can be used in brewing or made into a sweet syrup (malt syrup, rice syrup).

Industrially-mediated enzymatic hydrolysis performs the starch-to-sugar transformation for starches bound in dry corn (Zea mays; Poaceae; Poales) grains and cassava (tapioca, Manihot esculenta) roots.

Non-sugar sweet plant extracts

stevia plant

Only a few plants have been identified that produce sweet compounds that are not sugar and are palatable as a sweetener for food and beverages, and none of them are perfect. To be perceived as sweet to our palates, a chemical compound must bind to and activate sweet flavor receptors in our taste buds on our tongues. Sugar does this, and only this, exceptionally well. Some sweet non-sugar compounds, like those in stevia (Stevia rebaudiana; Asteraceae; Asterales), unfortunately also bind other taste receptors, like bitter receptors in the case of stevia, or have an aromatic flavor that is difficult to remove. Miraculin, the very sweet compound in miracle fruit (Synsepalum dulcificum; Sapotaceae; Ericales), only tastes sweet under very acidic conditions.

Monk fruit extract in the store

Monk fruit (Siraitia grosvenorii; Cucurbitaceae; Cucurbitales) extract has some sugar (fructose and glucose) in it, but its exceptional sweetness is courtesy of a group of glycoside saponins. Monk fruit extract can be quite palatable, but as yet it has limited availability. Licorice (Glycyrrhiza glabra; Fabaceae; Fabales) root extract is also exceptionally sweet because of a saponin. In small doses, like in a few pieces of real, traditional licorice candy, this saponin and other chemical components of licorice root extract are not harmful. In large doses, though, they can cause medical problems. Licorice root extract also tastes like, well, licorice, having a mild anise or fennel (both in family Apiaceae) flavor, owing to its moderate content of anethole, the signature anise aromatic compound, which itself is quite sweet.

stevia in the store

These non-sugar sweet compounds likely serve the plant as storage compounds for chemicals with physiological or anti-pest-defense roles. That is, the plant likely does not use them for energy or as an attractant for a seed disperser, and their perception by us as sweet is likely coincidental. Glycoside saponins, for example, structurally, are a sugar molecule bonded to another compound. When the plant needs the bonded compound, it can enzymatically cleave off the sugar. In our mouths, the sugar component binds to our taste receptors, but we don’t break it off, so for us it is not a source of calories.

Plants also physiologically employ sugar alcohols. Many of these taste sweet to us but may or may not be metabolized (for example: xylitol and sorbitol). Some sugar alcohols are industrially produced from ground hardwood pulp and are commercially available as sweeteners.

Sugar overload

the sweetener aisle at a local health foods store

Standing in front of the sweetener section in the modern grocery store can be an overwhelming experience. The various sugar products extracted from plants sit alongside other non-sugar sweet plant extracts and various industrially-produced artificial sweeteners and sugar alcohols. The commercial diversity reflects the biological diversity of their plant sources. That said, however, there are over 300,000 plant species. All of them produce and employ sugars, but we only extract sugars from a very small subset of them. We use non-sugar sweet compounds from an even smaller subset. We even only bother to concentrate the fruit juice of a few species, a small subset of the species that produce edible sweet fruit. Modern industrial processes that can convert starches into sugars (for example, turning non-palatable corn varieties into high fructose corn syrup) may provide an avenue to turn more plant species into sugar sources, but as yet, again, we reserve this process for only a few plant species. Those starchy plants, incidentally, are perfectly good foodstuffs in their starchy original forms (corn, barley, rice, cassava).

Plant saps, extracts, and juices always contain many more chemical compounds other than sugars. Those other chemicals may make the plant extract inedible or unpalatable. The sugar in those plant extracts may also be quite dilute. Maple sap and sugarcane juice are exceptionally rich in sugars. And, in the case of sugarcane, the really sugary varieties are a result of domestication and have much sweeter juice than their wild relatives. So, is it the case that the vast majority of plant species on Earth produce juice or sap that is either too poisonous, undesirable, or dilute in sugars to make it worthy as a sugar source, much less commercially viable? The same question goes, too, for plant sources of non-sugar sweet compounds.

sugarcane plants are tall, even growing in Maryland, outside its usual tropical habitat

Like sugarcane, many of the sugar source species are from the tropics, or at least very warm places. Plant species diversity is highest in the tropics, anyway. Sugar beets, maple and birch trees, though, prefer cooler climates. And every continent (except Antarctica) has a native sugar source, so it is difficult to pinpoint definite geographical correlates of sugar source species.

Evolutionarily, the plant phylogeny doesn’t seem to give us a lot of clues, as we source sugar from several different disparate branches of the plant family tree (see phylogeny in Figure 5 below).

Figure 5. Position of plant species sources of sugar and sweet compounds on a phylogeny of large plant clades (taxonomic orders, mostly) containing edible species. Sugar sources are highlighted in red; sources of non-sugar sweet compounds are highlighted in blue. See our plant phylogeny page for a refresher on understanding phylogenies and plant evolutionary history, and our edibles list

Sugar sources do seem to be somewhat concentrated in the monocots, which boast the grasses (sugarcane, sorghum, barley, rice, corn), the palms (dates, coconut, other palm sources of sugary sap), and agave. There are, however, over ten thousand grass species. Carefully pluck any (herbaceous, non-woody) one of them out of the ground on a warm summer day and taste the pale meristem tissue that was growing at ground level, just above the roots. It is invariably sweet and delicious. Perhaps, under domestication, as with the sugarcane grass, some of them could become commercially viable sugar producers. It is hard to imagine, however, that another grass, let alone another plant species, could combine an incredibly fast growth rate with copious amounts of palatable, sugary extract, as in sugarcane, which is one of the fastest growing plant species on Earth, a key to its commercial success. And maybe there is some plant out there boasting a delicious, non-sugar sweet compound that is just waiting to put stevia and monk fruit to shame.

Whatever the future of sweet sources, Santa is the ideal taste tester. The man eats a lot of holiday cookies.

Summary Table

Table 1 below summarizes the information we discuss about and taxonomic details of sugar source species and plant sources of sweet non-sugar compounds.

Table 1. Summary of some plant species sources of sugar and non-sugar sweet compounds

References

Elliott, M. C., & Weston, G. D. (1993). Biology and physiology of the sugar-beet plant. In The Sugar Beet Crop (pp. 37-66). Springer Netherlands.

McGee, H. (2004). On food and cooking: the science and lore of the kitchen. Simon and Schuster.

McGee, H. (1990). Curious Cook. North Point Press.

Turesson, H., Andersson, M., Marttila, S., Thulin, I., & Hofvander, P. (2014). Starch biosynthetic genes and enzymes are expressed and active in the absence of starch accumulation in sugar beet tap-root. BMC plant biology,14(1), 104.

Van den Ende, W. (2013). Multifunctional fructans and raffinose family oligosaccharides. Frontiers in plant science, 4.

Wardlaw, I. F. (1990). Tansley Review No. 27. The control of carbon partitioning in plants. New Phytologist, 341-381.

Willems, J. L., & Low, N. H. (2012). Major carbohydrate, polyol, and oligosaccharide profiles of agave syrup. Application of this data to authenticity analysis. Journal of agricultural and food chemistry, 60(35), 8745-8754.

This is our second of our two contributions to Advent Botany 2015. All the essays are great!

An early image of candy canes. From Wikipedia

The candy cane, that red- and white-striped hard candy imbued with peppermint oil, is a signature confection of the winter holidays. Peppermint has a long history of cultivation and both medicinal and culinary use. Infusions of the plant or its extract have been used for so many hundreds of years throughout Europe, North Africa and Western Asia that the early history of peppermint candies, including cane-shaped ones, is murky. Fortunately, the biology behind peppermint’s famous aroma is more well known than the story of how it came to be a Christmas staple.

Botanically, peppermint is Mentha x piperata (family Lamiaceae). The “x” in the Latin name indicates that peppermint is a hybrid species, in this case a naturally-occurring hybrid of spearmint (M. spicata) and watermint (M. aquatica) (McGee 2004). There are around fifteen species of Mentha widely distributed across all continents except Antarctica and South America, all herbaceous plants that prefer rich, moist habitats (Bunsawat et al. 2004). All are aromatic, charismatic members of field and stream bank plant communities, but their exact number is difficult to infer because of rampant hybridization and genomic quirkiness within the genus, including polyploidy and variation in base chromosome numbers (Bunsawat et al. 2004). Peppermint and its parent species are native to a wide swath of Europe and western Asia. Like tarragon, peppermint is sterile and only reproduces vegetatively, spreading from underground rhizomes or sprouting from cuttings. So the peppermint in my garden is nearly genetically identical to its clonal progenitor identified from the wild hundreds of years ago.

peppermint

The signature aroma of peppermint essential oil comes from a group of monoterpenes dominated by menthol and related menthone and menthyl acetate. These and other components of peppermint’s essential oil are synthesized and stored in glandular trichomes, specialized projections of the epidermis covering all aerial parts of the plant (stem, leaves, flowers). The glandular trichomes sit like water balloons on the epidermal surface and are surrounded by different, hair-like trichomes, which may function in anti-herbivore defense or help plant energy balance by deflecting excess solar radiation or affecting the plant’s immediate micro-climate. Those hair-like trichomes make some mint family  plants look and feel a bit fuzzy. A mature peppermint leaf might have as many as 8000 glandular trichomes dotting its surface (Croteau et al. 2005).

SEM of peppermint trichomes. The glandular trichomes full of essential oil are yellow. The hair-like trichomes look like spikes. Photo source here.

As I discussed on our post on lemon flavor, these two types of trichomes are typical of Lamiaceae species. Each of the legion mint family culinary herbs (rosemary, thyme, oregano, marjoram, basil, savory, lavender, sage, mints, shiso, lemon balm) is characterized by a signature essential oil blend synthesized in glandular trichomes. Even what we might consider gentle handling of the plant will rupture the glandular trichome cuticle and release the aromatic essential oil. The oil is the plant’s defense against generalist insect herbivores and pathogens. An insect or fungal pathogen may experience the essential oil release as a caustic deluge, but for us it’s a culinary convenience. It also means that you should take care when you muddle your mints for mojitos or juleps or fresh mint syrup, and you shouldn’t steep your mint tea too long, as the desirable mint flavor is easily released from the surface of the plant, and too much bruising will release the plant’s juice, which may be bitter.

peppermint on the left, lemon balm on the right

Most of the components of mint family essential oils are monoterpenes or their derivatives. Monoterpene biosynthesis within the trichomes is typically characterized by many steps starting from primary metabolism in which an intermediate compound is modified by a particular enzyme. Many of the intermediates are terpenoids that are strongly aromatic in their own right and contribute to a plant’s essential oil bouquet. For example, the monoterpene limonene, which is a signature component of citrus (Rutaceae) essential oil, is one of the eight intermediate compounds in the biosynthesis of menthol and other monoterpenes (Croteau et al. 2005). Its accumulation contributes to the lemon or orange notes in many mint family herbs.

Even though spearmint is one of peppermint’s parent species, it has no menthol in its essential oil. The signature aromatic monoterpene in spearmint essential oil is carvone (specifically, the isomer of carvone denoted (-)-carvone). Limonene is an intermediate step in its biosynthesis, too, and the enzymes that modify limonene in spearmint and peppermint are similar, demonstrating how small genetic modifications to the genes encoding the enzymes responsible for monoterpene synthesis can lead to big changes in the resulting essential oils (Croteau et al. 2005). Interestingly, the other parent species of peppermint, watermint, also doesn’t produce menthol, but its essential oil is dominated by menthofuran (Bozin et al. 2006), which has a musty odor and is highly toxic. I haven’t seen a good description of how the two different monoterpne synthesis pathways in spearmint and watermint sire a completely different pathway in peppermint.

Menthol is perhaps the most recognizable monoterpene in the Western world and is hugely commercially important as a peppermint flavoring and ingredient in fragrances and topical medicines (Croteau et al. 2005). The refreshing peppermint aroma of menthol is not the only reason it is desirable in medicines applied to the skin and in confections. Menthol induces a cooling sensation on the skin and mucous membranes. It triggers our neural receptors that sense cold (TRPM8 receptors), and we perceive menthol to feel cool. Menthol, then, is the phytochemical opposite of capsaicin from chili peppers, which triggers heat-sensing neurons, making capsaicin feel hot. Menthol also triggers opioid receptors to function as a topical analgesic (Galeotti et al. 2002).

drying peppermint

Peppermint tea is still recommended as a folk herbal remedy for nausea or other digestive discomfort, and, of course, menthol clears the sinuses. I loved the part of the Celestial Seasonings factory tour in Boulder, CO, when they opened the garage door blocking the mint room, where they store all their dried peppermint, so its strong aroma doesn’t contaminate the other herbs. The wave of accumulated menthol that rolled over the waiting crowd brought tears to everyone’s eyes and forced us all to take a deep, minty cleansing breath. It has never really made sense to me that a cooling plant extract should be a hallmark of the coldest part of the year. Perhaps, however, peppermint’s long history as part of a home remedy for winter cold symptoms contributed to the tradition of peppermint holiday confections, and that resonates with me. And in the sense that the menthol wave in the tea factory brought the present moment sharply into focus, peppermint fostered a somewhat spiritual experience. So perhaps minty candy canes are not so incongruous this time of year after all.

References

Bozin, B., Mimica-Dukic, N., Anackov, G., Zlatkovic, B. and Igic, R., 2006. Variability of Content and Composition of Mentha aquatica L.(Lamiaceae) Essential Oil in Different Phenophases. Journal of Essential Oil Bearing Plants, 9(3), pp.223-229.

Bunsawat, J., Elliott, N.E., Hertweck, K.L., Sproles, E. and Alice, L.A., 2004. Phylogenetics of Mentha (Lamiaceae): evidence from chloroplast DNA sequences. Systematic botany, 29(4), pp.959-964.

Croteau, R.B., Davis, E.M., Ringer, K.L. and Wildung, M.R., 2005. (−)-Menthol biosynthesis and molecular genetics. Naturwissenschaften, 92(12), pp.562-577.

Galeotti, N., Mannelli, L.D.C., Mazzanti, G., Bartolini, A. and Ghelardini, C., 2002. Menthol: a natural analgesic compound. Neuroscience letters, 322(3), pp.145-148.

McGee, H. (2004). On food and cooking: the science and lore of the kitchen. Simon and Schuster.

This month we introduce a new feature to the Botanist in the Kitchen: Botany Lab of the Month, where you can explore plant structures while you cook. In our inaugural edition, Katherine explains why she would like to add her nominee, Solanum tuberosum, to the list of white guys vying for Best Supporting Actor.

In one of this year’s biggest and best movies, Matt Damon was saved by a potato, and suddenly botanists everywhere had their very own action hero. It’s not like we nearly broke Twitter, but when the trailer came out, with Damon proclaiming his fearsome botany powers, my feed exploded with photos of all kinds of people from all over the world tagged #Iamabotanist. The hashtag had emerged a year earlier as a call to arms for a scrappy band of plant scientists on a mission to reclaim the name Botanist and defend dwindling patches of territory still held within university curricula. Dr. Chris Martine of Bucknell University, a plant science education hero himself, inspired the movement, and it was growing pretty steadily on its own. Then came the trailer for The Martian, with Matt Damon as Mark Watney, botanizing the shit out of impossible circumstances and lending some impressive muscle to the cause. The botanical community erupted with joyous optimism, and the hashtag campaign was unstoppable. Could The Martian make plants seem cool to a broader public? Early anecdotes suggest it’s possible, and Dr. Martine is naming a newly described plant species (a close potato relative) for Astronaut Mark Watney.

In the film, that potato – or actually box of potatoes – was among the rations sent by NASA to comfort the crew on Thanksgiving during a very long mission to Mars. After an accident, when the rest of the crew leaves him for dead, Watney has to generate calories as fast as he can. It’s a beautiful moment in the movie when he finds the potatoes. In a strange and scary world, Mark has found a box of old friends. They are the only living creatures on the planet besides Mark (and his own microbes), and they are fitting companions: earthy, comforting, resourceful, and perpetually underestimated. At this point in the movie, though, the feature he values most is their eyes.

What is a potato?
Potatoes (Solanum tuberosum) are stem tubers, underground storage structures derived from stem tissue. As we explain elsewhere, potatoes store a lot of energy as starch, an extremely compact mode of storage. Each eye of the potato is a node on the stem capable of giving rise to a branch, which could eventually emerge from the soil and become a green, leafy shoot. A growing potato shoot fuels its early growth by drawing starch from the parent tuber (often mislabeled the “seed”), leaving the older tuber withered and empty. The new shoot meanwhile generates its own set of roots and underground stems (stolons) tipped with tubers. The new photosynthesizing shoot sends sucrose down to its tubers, where the sugar is converted to energy-rich starch and layered into pearl-like granules inside amyloplasts in the tuber’s storage cells. Each generation’s tubers thus give rise to the next generation of leafy shoots.

A closer look at the eyes
Chances are good that you have a potato in your pantry or refrigerator to use for this month’s botany lab. Standard russet baking potatoes have unremarkable eyes, so they aren’t the best specimens for our purposes. If possible, use a smooth-skinned red or yellow potato with prominent eyes. Fingerling potatoes are even better, if you have them, because their long thin tubers are the most obviously stem-like. You don’t need any other tools for this lab because you won’t be cutting anything up. Your potato will stay intact and available for whatever recipe you have in mind.

1. The first thing to note about a potato is that it has a proximal end, where it was attached to the parent plant by a thin length of stolon, and a distal end, representing the growing tip of the underground stem tuber. The proximal end often sports a cluster of stringy stolon fibers attached to a little scar. The distal end is where the eyes are close together and where new eyes would have originated had the potato continued to grow.

Figure 1. Click image to enlarge

2. Look closely at the distal end. Just as leaves are not randomly arranged on a stem, potato eyes are not scattered haphazardly over the tuber. Instead, they lie in a spiral around the stem. This pattern is less obvious along the fat middle part of the potato, but it can be seen clearly at the distal end where the eyes are close together.
3. Trace the spiral of eyes from the distal tip of the stem. Start by choosing a young eye close to the center of the tip as a starting point. Because new eyes are produced at the tip, the eyes are progressively older the farther they are from that tip. Now locate the next, slightly older, eye on the tuber. Keep moving from eye to eye around the stem, each time choosing the next one in the age sequence. (In the video shown below, the spiral runs counter-clockwise, but your particular spud could run clockwise.)

As you move into the wide part of the potato you will notice that the next eye is located not quite directly across the tuber from the previous eye. In fact, the angle formed by connecting successive eyes to the center of the tip (the vertex) should be about 137.5 degrees, the “golden angle.” This special angle describes the leaf arrangement of many (not all) species, and is derived from the “golden ratio,” which shows up in myriad beautiful objects, from nautilus shells to the Parthenon.

Figure 2. The angle between two successive eyes is about 137.5º, the “golden angle”

4. Since the eyes are arranged like leaves on a stem, you might wonder whether they themselves are sort of like leaves. Well, sort of. On typical leafy stems, there is a regular spatial relationship between leaves and buds/branches, and the same is true of potato tubers. The lumpy part of the eye is not a leaf, but rather a bud or cluster of buds that can grow out into a green leafy branch. But notice that each bud part of the eye sits in the curve of a thin ridge or lip (click to enlarge Figure 1 above). The ridge may even have a very short scaly extension on it. That ridge is the vestige of a short scale leaf subtending (lying below) the bud/branch. Each eye, then, corresponds to a leaf and its associated bud, which is potentially a branch.
5. Extra credit. If you have a potato to spare, put it out in the sun for a while to sprout and turn green. I’ve kept potatoes like that for nearly a year in my windowsill, without water or soil, and it’s fun to watch the growing shoots gradually draw down the reserves in the tuber.

Figure 3. This potato was left in the sun for a couple of months. Don’t eat green potatoes!

Potatoes turn green in the sun because the light signals them to produce chlorophyll and start photosynthesizing more sugar. Light exposure also triggers the production of toxic and bitter solanine, which you should avoid eating. Solanine tastes pretty bad, so you probably wouldn’t eat much of it accidentally even if you didn’t notice the chlorophyllous warning sign. Still, if you have obviously green potatoes, either peel them deeply or, better yet, plant them and see what comes up. Who knows when potato farming experience might actually save your life?

My pitch for Best Actor in a Supporting Role

The Oscars (are supposed to) recognize acting achievements and not the function of an actor’s character in the story. But let’s be literal for moment. Of all the nominees for Best Actor in a Supporting Role this year, only a couple of them (Stallone and Ruffalo) played parts that were at all supportive of the protagonists. Mark Watney’s potato friends, however, carried him through “overwhelming odds” both physiologically and psychologically. They gave him calories and nutrition, they gave him hope and inspiration, and they gave him something to worry about besides his own survival. He cared for those plants as true botanists do, recognizing their worth as fellow living creatures and missing them when they were gone.  

The hardworking and versatile S. tuberosum showed up in other films this year, too. Although it was disappointingly typecast in Brooklyn, fans will thrill to its cameo appearance in Minnie’s stew, an important plot element in The Hateful 8.

In 2016, the International Year of Pulses, we’ll be writing a lot about pulses (dried beans and peas), and we’ll also tackle the huge and diverse legume family more broadly. This weekend Katherine kicks things off with February’s Botany Lab of the Month: beans and chickpeas for your Superbowl bean dip and hummus.

The species name of Cicer arietinum means “ram’s head.”

Beans are a bit like football: a boring and homogeneous mass of protein, unless you know where to look and what to look for. In this lab, we’ll make the smashing of beans into bean dip or hummus much more interesting by taking a close look at some whole beans before you reduce them to paste. The directions are very detailed, but this whole lab can be completed in the time it takes to explain the onside kick.

Of course, if you have only pre-mashed refried beans in your pantry, it’s too late. Then again, if you are using canned refried beans for your recipe, you are probably not living in the moment or sweating the details right now. That’s OK. Go watch the game and let us know when someone scores.

1. For this Botany Lab of the Month, you can start with soaked dried beans, home cooked beans, or even whole canned beans if that’s what you’ve got. Uncooked soaked dried beans are definitely the best choice. You can even set a few aside and watch them become seedlings.

2. The first thing to consider about beans is that they are seeds and thus came out of a fruit – in this case a legume “pod.” Bean-dip beans (Phaseolus vulgaris, e.g. white, kidney, pinto, black) develop within a regular edible green bean and are harvested when the pod is fully mature. Chickpeas (Cicer arietinum = garbanzo beans) come in small inedible hairy pods that resemble one-seeded edamame or peanut shells. Each individual seed is tightly enclosed by a seed coat (the testa), which often slides off when beans are soaked or cooked.

Close up of Phaseolus beans showing parts we often overlook. Click to enlarge.

The same image, with parts labeled. Click to enlarge.

3. Look for evidence of the fruit connection right on the outside of the bean seed. Before harvest, a bean seed is attached to the inside of its fruit by a short little stalk (funiculus, or “slender rope”) through which it draws water, sugar, and nutrients. The same word is used for our umbilical cord (funiculus umbilicalis). Once the bean seed is mature, it becomes dry and separates from the fruit wall, but it carries a pale scar like a belly-button where its funiculus was attached. That scar is called a hilum, and it’s an obvious feature. In black-eyed peas, for example, the hilum stands out as a white scar in the middle of a black splotch. On the chickpea, the hilum is surrounded by a ridge so that it looks like one giant nostril under a beaky nose. Fun fact: Cam Newton won the Hilum Trophy in 2010.

Close up view of a chickpea flashing its hilum. Click to enlarge.

4. Several very interesting anatomical features appear when you look even more closely at a bean seed’s parts. On an ordinary Phaseolus type bean, the hilum sits in the center of the curved side of the seed. Extending from one end of the hilum is a narrow ridge, which may be easiest to see from the side. That ridge is the embryonic plant’s root (called a radicle) pressing out against the seed coat like overly tight clothing. When the seed germinates, the radicle will emerge from the seed coat, grow downward to anchor the seedling, and start drawing up water for rapid growth. The radicle of the chickpea is extremely obvious: it’s in the beaky nose of the seed overhanging the hilum.

5. Between the hilum and the radicle ridge is a tiny structure you may not be able to see: the micropyle (“tiny hole”). That’s where a pollen tube entered the seed (at that point still an “ovule”) and deposited its sperm. It may also be an entry point for water in some plant species, kicking off the process of germination. Finally, radicles generally emerge through the seed coat by way of the micropyle, which is usually found near the radicle tip. So if you can find the radicle in a seed, it will often guide you to the elusive micropyle. The micropyle is much more easily seen on Phaseolus beans than on chickpeas.

6. On the opposite side of the bean hilum is a pair of bumps called the strophiole. Allegedly, its Latin roots mean “little wreath,” which suggests that whoever named this structure was looking at some other species, and definitely not beans. Anyhow, in beans, there is some evidence that water enters the seed through the strophiole as well as through the micropyle (Smykal et al 2014).

7. Finally, running between the strophiole and the end of the seed is an elongated pleat or groove called the raphe. The raphe is a mark in the seed coat showing where, during development, the seed rested up against its funiculus (that umbilical-cord-like structure).

8. Oddly enough, the rest of the bean seed is much simpler than its outside. To get inside, first pull off the testa (seed coat). By the way, some hummus recipes suggest that you strip all your chickpeas of their coats (chefs usually call them hulls or skins) to make an elegant spread. If you mash by hand, it is nice not to have those tough testas scattered around in the hummus. If you plan to puree your beans or chickpeas, then it’s probably not worth the trouble.

9. Without the seed coat, you have a naked embryo. The radicle should be obvious now as a short thick curved root lying right where you expect it. On a chickpea, it’s in the nose. On a Phaseolus bean it runs halfway along the inside of the curve.

Chickpea embryo, with close-up showing the shoot tip (plumule) and its young leaves. Click to enlarge.

10. Now separate the two large lobes making up the bulk of the embryo. They are smooth in a bean and a little dimply in a chickpea. Those halves are the cotyledons, which store resources for the developing seedling. In beans, they are drawn out of the seed coat and carried above ground by part of the stem (the hypocotyl), where they become the first photosynthetic green leaves. In chickpea, they stay below ground while the rest of the seedling draws upon their stores for growth.

11. When you spread the cotyledons you will break one of them off, but you will still see that they were attached to each other near the top of the radicle and below a tiny little tuft of new leaves. The radicle grows out to become a root, and the tuft, or plumule, grows out to become the shoot.

12. Extra credit: If you do have soaked but uncooked beans, spread them in a shallow dish on wet paper towels to sprout. The seeds should not be submerged, but the water should pool around them on the paper towel. Keep the dish lightly covered (with a translucent plastic container lid, for example) and don’t let the seeds dry out. Change the water once a day so it doesn’t start to smell funny. You will see the root emerge first, followed by the shoot, which will turn green in the light, straighten up, and unfurl its young leaves.

From here you can continue with your favorite bean dip or hummus recipe or you can just go back to the game. I myself am a baseball fan, counting the days until spring training. Keep your eyes out for a peanut post.

Reference:

Smýkal, P., Vernoud, V., Blair, M. W., Soukup, A., & Thompson, R. D. (2014). The role of the testa during development and in establishment of dormancy of the legume seed. Frontiers in Plant Science, 5, 351. http://doi.org/10.3389/fpls.2014.00351

Shout out to my friend and partner in teaching 3 long lab sections in a day, Kay H, who taught me just how funny beans can be.

Dying Easter eggs with homemade vegetable dyes today made for some superb kitchen botany. Making the dyes is easy, fun, and offers insight into the fascinating evolution of plant pigments.

Pigments serve a variety of roles in plants. Many pigments protect plant tissues from sunburn and pathogens and herbivores or perform other physiological functions (see review by Koes et al. 2005). Most noticeably, however, their brilliant colors attract animal pollinators to flowers and seed dispersers to fruit. Humans are also interested in plant pigments, which color and sometimes flavor our food, are potentially medicinally active, and have been used as natural dyes and paints for millennia.

red cabbage

Today we made green dye from parsley, two different yellow dyes from turmeric and yellow onion skin, and three different pinkish-purplish dyes, from red cabbage, red onion skin, and beets. The basic recipe for all the vegetable dyes is the same: coarsely chop the vegetables, pour boiling water over it (about 2 cups vegetables or 1 tablespoon turmeric powder per quart of water), and stir in white vinegar (about a tablespoon per quart). Alternatively, put the chopped vegetables in a saucepan, cover with the water, and bring to a boil. You can either immediately add the hard-boiled eggs to the vegetable soup and let it sit for 12-48 hours, or you can let the vegetables steep for an hour and strain the vegetable solids out before adding the eggs and letting it sit.

The green color from the parsley comes from the pigment chlorophyll, a key component of the light-harvesting function of the photosynthetic apparatus. Grinding the parsley in the blender released the chlorophyll from the chloroplasts.

The spice turmeric comes from the rhizome (underground stem) of Cucurma longa (family Zingiberaceae), native to tropical southeastern India. Much (if not all) of turmeric’s yellow-orange color (and its distinctive earthy flavor) comes from its curcuminoids, natural phenols. These are likely defensive compounds that help the plant thwart herbivores and pathogens.

color courtesy carotenes

Curcuminoids are not widespread among plants, unlike other yellowish pigments, most notably the hydrocarbon carotenoids (xanthophylls and carotenes, including vitamin A precursors). The yellow-orange color of the yolks inside our Easter eggs came from the xanthophylls lutein and zeaxanthin that the chickens obtained from their food, ultimately from plant sources. Xanthophylls provide sunscreen to leaves. Carotenes have photosynthetic roles, but they’re mostly known for the color they give to many plant structures. Most carotenes confer yellow or orange color, but the carotene lycopene is bright red and is a primary pigment of tomatoes, red carrots, watermelons, and papayas. Although carotenoids are common, I don’t know much about their use as a dye. The yellow color from the yellow onion skins came not from carotenoids but from oxidative byproducts of flavonoid pigments, notably quercetin.

Red onion color from anthocyanins and quercetin

Red cabbage and red onion get their purple color from anthocyanins, the most common purple and blue pigments found in nature. Beets, however, get their red and yellow colors from betalain pigments, which replace anthocyanins, and to some extent carotenoids, as a pigment source in most families in the botanical order Caryophyllales (see our Food Plant Tree of Life phylogeny page for details on phylogenetic placement of the Caryophyllales; and see this excellent article for the comparative biology of anthocyanins and betalains within the Caryophyllales). That may initially sound obscure, but there are a lot of food plants in the Caryophyllales, all with betalains instead of anthocyanins (See our Food Plant Tree of Life list).

Betalains turn salads with beets bright pink

Extra Credit: At some point in your primary education you may have done a chemistry lab (like this one) using red cabbage-derived anthocyanins to learn about pH, as the anthocyanins can display an impressive range of color depending on pH. The acid (vinegar) in the dye may complicate this plan, but I wonder if there is a way to take advantage of the pH-sensitivity of anthocyanin pigments in dye making.

As part of our legume series, the Botanist in the Kitchen goes out to the ballgame where Katherine gives you the play-by-play on peanuts, the world’s most popular underground fruit. She breaks down peanut structure and strategy, tosses in a little history, and gives you a 106th way to eat them. Mmmmm, time to make some boiled peanuts.

Baseball is back, and so are peanuts in the shell, pitchers duels, lazy fly balls, and a meandering but analytical frame of mind. Is this batter going to bunt? Is it going to rain? What makes the guy behind me think he can judge balls and strikes from all the way up here? What does the OPS stat really tell you about a hitter? Is a peanut a nut? How does it get underground? What’s up with the shell?  A warm afternoon at a baseball game is the perfect time to look at some peanuts, and I don’t care if I never get back.

Peanuts fit baseball like an old glove fits your hand. Just as players through the ages have taken more clubhouse-friendly monikers, so Arachis hypogaea has many nicknames – peanuts, goobers, goober peas, groundnuts, etc. And fans love peanuts. Legend has it that San Francisco Giants fans leave four thousand pounds – two tons – of peanut shells behind after every home game. Over a season, that adds up to more than 160 tons of shells. (Fortunately, the Giants’ AT&T Park has a massive composting program). Shells make up only about a quarter of a peanut’s total mass, so at every game, six tons of edible peanut parts are consumed by the nearly 42 thousand fans typically in attendance. By my goobermetric calculations, that translates into more than a quarter pound and 700 Kcals of goober peas per person, not including any peanuts taken in as Cracker Jack. Consider that not everyone there is eating peanuts, and you have some fans hitting the peanuts pretty hard. Of course there are fans who are seriously, even dangerously, allergic to peanuts, and many teams now offer peanut-controlled sections for a few games per season. Personally, I like my peanuts best when they are boiled in brine and served in Georgia – just one of the ways you can get them at Turner Field in Atlanta.

Boiled peanuts at Turner Field in Atlanta. Click to enlarge.

Peanut seeds cradled in the fruit wall (shell)

Wherever your home team might be, imagine you are sitting there in the stands on a warm lazy day asking yourself “what is a peanut?” Most “nuts” are not botanical nuts, and neither are peanuts. You will have heard that peanuts are “peas,” and that’s mostly right. Arachis hypogaea is in the legume family (Fabaceae), and its botanical fruit type is also called a legume, along with green beans, snap peas, and edamame. The shell of a peanut develops from its ovary (making it a fruit), and it contains the edible peanut seeds inside, surrounded by a reddish brown papery seed coat. So peanuts in the shell are fruits, and we open them up and eat the seeds.

In fact, peanuts are among the rare fruits that develop underground, although they flower above ground. They start as beautiful aerial flowers, shaped like those of its sweet pea cousins, and strikingly bright yellow. Bees love them and occasionally spread their pollen, although the flowers typically fertilize themselves (Leuck & Hammons,1965).

Peanut flower (Wikimedia Commons)

The really weird part comes after pollination, when the flower petals fall off and the ovary (soon-to-be-shell) starts to push itself underground. It’s not the flower stalk (pedicel) that buries the fruit; rather the base of the ovary itself elongates into a structure called the “peg” (Smith, 1950). A recent study (Chen et al. 2015) found literally hundreds of genes involved at different stages in this odd developmental move. Genes that give plants a sense of gravity are important in turning the peg down into the ground. Once there, the tip of the peg uses another few hundred genes to know that it’s dark and that the ovary should start to develop into a fruit.

Peanut “pegs,” which will become peanut fruits. By Alain Busser from Wikimedia Commons

But developing underground (“subterranean fructification”) is pretty tough on a fruit, and a peanut ovary is exposed to fungi, bacteria, nematodes, and fluctuating moisture levels, so another large set of genes goes on the defense against these pathogens (Chen et al. 2015). The shells also become very tough with thick-walled cells and fibers that support the network of veins bulging at the surface of the shell (Halliburton et al. 1975).

So to recap, those peanut shells have to be tough enough to withstand intense physical challenges yet adept enough to adjust to subtle environmental cues. Sitting low in the dirt all that time has roughed up their epidermis and left them pretty well skinned. Sounds like a catcher to me.

Before you eat those edible seeds, take a closer look at them. The reddish brown papery layer surrounding a peanut seed is its seed coat. Just like other familiar bean seeds, the peanut has two distinct halves which are its cotyledons (“seed leaves”). The cotyledons store a lot of nutrients to support a developing seedling, a role that makes them dense sources of protein and fat calories. Because many legume species use symbiotic bacteria to fix nitrogen from the air, they can afford to pack their seeds full of nitrogen-rich protein.

Looking down at a peanut seed, slightly ajar. The tuft in the center is a set of new leaves that will emerge when the seedling germinates.

Between the cotyledons is a fascinating little structure that looks like a pale feathery mustache. That tiny tuft is the first set of leaves that appears above ground when you plant a fresh peanut.

Click to enlarge

But of course peanuts plant themselves, as described above. If you occasionally question a baseball manager’s strategy, just think about this insane move. When a flowering peanut pushes its fruits into the soil, the fruits remain tethered to the plant, and the seeds inside do not go far. They basically sit right under the parent plant, waiting for it to die, crowded by dozens and dozens of sibling seeds. Yes, it is a good spot, since those inbred seeds are genetically similar to their parents and would thrive where they did. Still, only a handful of them (at most) can occupy the family spot the following year. For a seed, that’s worse odds than a suicide squeeze. By contrast, most other plant species invest energy and cunning into dispersing their fruits and seeds as far as possible. They explode, or stick, or float, or travel through a gut. Bye bye baby. Peanuts’ odd reproductive habit is called “active geocarpy.” This strategy is rare in plants, but it seems to be associated with unstable soils, often at high altitudes, that are prone to freeze-thaw or extreme wet-dry cycles (Barker, 2005). Maybe active self-planting protects seeds from being buried too deeply or being unearthed when the ground shifts. Maybe sometimes they do roll away but stay in fair territory and colonize new ground.

My first recruit to the peanut farm team

In the US, we associate peanuts with the American South, and that’s where they are grown now. Although lots of American baseball players come from peanut country – San Francisco catcher Gerald “Buster” Posey grew up in Leesburg, not far from the famous peanut farms of Plains, GA – no major league baseball players have come from the original home of peanuts in southern Bolivia. Recent genetic work has narrowed the most likely origin of our cultivated peanuts (Arachis hypogaea) to a very small region in southern Bolivia, not far from where the borders of Bolivia, Paraguay, and Argentina come together (Bertioli et al. 2016). Peanut cultivation in that region began very early – almost as soon as people got there – and seems to have spread quickly. The Bertioli study estimates that our cultivated peanuts arose as a hybrid between two other groundnut species over 9 thousand years ago, and there is evidence of peanut cultivation in Peru not long after that, about 7800 years ago.

These days the US grows a lot of peanuts, and now we have a major goober glut that even baseball fans can’t soak up. The latest Farm Bill and other agricultural policies encouraged farmers to produce more peanuts and less cotton. We can’t eat all those peanuts, and we can’t store them all either. But peanuts are nutritional powerhouses, so an obvious solution is to give them away, and the USDA has made a deal to ship peanuts to Haiti. The heartbreaking part, as reported by the Washington Post, is that Haitian farmers have been growing peanuts themselves as part of that country’s agricultural recovery. Sending our peanuts to Haiti could undercut their efforts. Meanwhile, here at home, conditions continue to favor peanut production in spite of the oversupply.

Perhaps the most prominent promotor of peanut production was George Washington Carver, the long-time faculty chair of the Agriculture Department at the Tuskegee Institute in Alabama. He saw peanuts as a crop that could replace cotton and actually start to heal some of the damage cotton had brought to both soil and souls in the South. As part of his effort, Carver  published a booklet of 105 peanut recipes, including both savory and sweet preparations, and yet he somehow failed to mention peanut brittle or boiled peanuts.

Now, if you live in the south you can easily buy canned (meh) or roadside (mmm) boiled peanuts. But if you want something really good, here’s my pitch for making your own boiled peanuts.

Boiled Peanuts

Peanuts must be raw and still in the shell. They may be dried (not roasted) or they may still be damp and soft (“green”). With dried peanuts, it speeds cooking to soak them overnight in water to soften them a bit.

For every pound of peanuts, use a half-gallon of water and about 1/2 cup of salt. Put everything in a pot and bring it to a boil. Continue to boil until the peanut seeds are soft, with no residual crunch to them. Green peanuts will take up to two hours while dried peanuts may take 10 or 12 hours. Be sure to keep the water level high enough to keep all of the shells surrounded by water. Allow the peanuts to cool in the brine and then refrigerate them and eat them within a week.

Be sure to save a few to germinate, like I did. (It’s a video. Click it!):

References

Barker, N. P. (2005). A review and survey of basicarpy, geocarpy, and amphicarpy in the African and Madagascan flora. Annals of the Missouri Botanical Garden, 445-462.

Bertioli, D. J., Cannon, S. B., Froenicke, L., Huang, G., Farmer, A. D., Cannon, E. K., … & Ren, L. (2016). The genome sequences of Arachis duranensis and Arachis ipaensis, the diploid ancestors of cultivated peanut. Nature genetics. http://www.nature.com/ng/journal/v48/n4/full/ng.3517.html

Carver, G.W. (1925) How to Grow the Peanut and 105 Ways of Preparing it for Human Consumption. Tuskegee Institute Press, Bulletin no. 31 (revised from original 1918) http://aggie-horticulture.tamu.edu/fruit-nut/carver-peanut/

Chen X., Yang Q., Li H., Li H., Hong Y., Pan L., Chen N., Zhu F., Chi X., Zhu W., Chen M., Liu H., Yang Z., Zhang E., Wang T., Zhong N., Wang M., Liu H., Wen S., Li X., Zhou G., Li S., Wu H., Varshney R., Liang X. and Yu S. (2015) Transcriptome-wide sequencing provides insights into geocarpy in peanut (Arachis hypogaea L.). Plant Biotechnol. J., doi: 10.1111/pbi.12487

Leuck, D. B., & Hammons, R. O. (1965). Pollen-collecting activities of bees among peanut flowers. Journal of Economic Entomology, 58(5), 1028-1030. http://jee.oxfordjournals.org/content/jee/58/5/1028.full.pdf

Halliburton, B. W., Glasser, W. G., & Byrne, J. M. (1975). An anatomical study of the pericarp of Arachis hypogaea, with special emphasis on the sclereid component. Botanical Gazette, 219-223.

Smith, B. W. (1950). Arachis hypogaea. Aerial flower and subterranean fruit. American Journal of Botany, 802-815.

Is there anything good about green bean casserole? Not much beyond its association with Thanksgiving, so Katherine will be brief and just keep you company in the kitchen in case you are stuck assembling said casserole.

Since this year is the International Year of Pulses, we have been focusing on legumes, whether they count as pulses or not. Green beans do not count as pulses, but only because they are eaten as tender and fresh immature whole fruits. The very same species (Phaseolus vulgaris), when allowed to mature, could yield black beans, white beans, kidney beans, or pinto beans depending on their variety – dry seeds that are perfectly good examples of pulses.

This Thanksgiving week we are going to welcome green beans into the fold and give them a special place. It’s too bad that Thanksgiving so often presents them out of the can, overcooked, with funky flavors, and buried in a casserole. Even Wikipedia promotes this peculiar tradition : “A dish with green beans popular throughout the United States, particularly at Thanksgiving, is green bean casserole, which consists of green beans, cream of mushroom soup, and French fried onions.”

And once again, international observers ask themselves what on earth are Americans thinking? That cannot be good for them. But in the American spirit of inclusivity we invite green beans of all sorts to our tables and try to learn something from them. So if you are preparing green beans this week, take heart, take up your knives, and take a closer look.

The outside of the bean

If your beans have already been trimmed and packaged or will be sliding their way out of a can, you can skip ahead to the next step. If you are making fresh beans, though, then you have much to be thankful for, not the least of which is the bunch of flowers before you.

Fresh green beans still carry bits of the flowers that they outgrew

The end of the bean you normally discard – the stem end – still has tiny remnants of the flower that bore the bean fruit. Look closely and you can usually see a pair of tiny little wing-like sepals, the outermost whorl of flower parts. On very fresh beans, there is often a little bit of membranous stuff just right near the sepals, and this is of course what’s left of the petals.

While the stem end carries the floral bits, it is tough and should be removed. Some people insist on removing the opposite end as well because it instinctively makes them uncomfortable. That curved tapering end is the elongated stigma and style where pollen grains landed and grew down into the ovary, carrying sperm cells and stimulating fruit development. It is very soft and I always leave it on, but the more squeamish among us may in fact want to remove any whiff of plant sex from their Thanksgiving tables.

The inside of the bean

Even pre-cut and canned beans are good for dissections and anatomy demonstrations

Whether your beans are fresh, pre-trimmed, or canned, you can appreciate the inside of a green bean. Open it up carefully and you will see immature seeds inside, clinging to the inside of the bean fruit. The connecting structure, much like an umbilical cord, is a funiculus, which connects the developing seed to the placental tissue lining the fruit. On a mature dried bean, the scar from the funiculus is visible as a little eye on the concave side of the seed.

Alternative recipes

The traditional green bean casserole calls for cooking the beans in a matrix of cream of mushroom soup and topping them with French fried onions. It is possible to get all of these ingredients from a can, making it a cheap and fast dish. If you are fortunate enough, though, to have tender fresh beans on hand, you can serve them very simply with a bit of browned butter on top. Herbs and chopped almonds make them fancy. And for traditionalists, canned French fried onions do lend a nice fatty crunch to balance the freshness of the beans.

Jeanne and I have lots of other Thanksgiving themed posts here. Have a great holiday!

Enjoy Jeanne and Katherine’s holiday take on figs and figgy pudding which will appear on December 19th in Advent Botany 2016. For a longer read, check out our original 2013 version.

Figs reach their peak in summertime, growing fat enough to split their skins under the hot sun. It’s nearly impossible to keep up with a bountiful tree, and many a neglected fig is extravagantly abandoned to the beetles.  

Beetles gorge on a fig. Click to enlarge

But here we are, halfway around the calendar in dark and cold December, and we feel grateful for the figs we managed to set aside to dry. Their concentrated sweetness is balanced by a complex spicy flavor that makes dried figs exactly the right ingredient for dark and dense holiday desserts. As we mark another turn of the annual cycle from profligate to provident, what better way to celebrate than with a flaming mound of figgy pudding?

Well, except that the traditional holiday pudding contains no figs. More on that later, along with some old recipes. First, we’ll unwrap the fig itself to find out what’s inside.

Anatomy of the fig

To understand a fig, you have to recall the basic structure of a flower and imagine the various ways flowers can be grouped on a plant. Figs (and related mulberries) cluster their tiny flowers together into dense and well-defined inflorescences. And, in both, all the flowers on an inflorescence develop into a single fused unit, which we casually call a fruit. Before offering the details of what we eat, we’ll need to look at the individual flowers and fruit.

An idealized flower has four concentric rings of parts, or whorls. From the outside in, they are:

1) usually green, modified leaves, called sepals (collectively the calyx), which are prominent in the nightshade family and on persimmons;

2) petals, which are often colored or otherwise showy (together called the corolla);

3) the “male” stamens, consisting of a filament holding aloft a pollen-filled anther; and

4) one or more “female” pistils, anchored by an ovary.  The pistil catches pollen grains, which then grow down through a style to the ovary and the seeds within. The ovary matures into a fruit.

Not all flowers have all of these parts.  Figs make separate flowers with only one or the other sex: “female” flowers lack stamens and cannot make pollen, and “male” flowers lack pistils and cannot make fruit.  Both female and male flowers also lack petals.

Fig flowers are a bit like Christmas presents: you can’t see them without opening up the structure that encloses them, and sometimes the wrapping is more exciting than what’s inside. As it turns out, being hidden from view also means being hidden from all but the most specialized pollinators, which is a big part of the fig story (see below).

Cutaway view of a fig with a closeup of a female flower on the left. Flowers within the fig are shown without a calyx, which is not apparent anyhow. Click for full size image

Unwrapping the fig

A fig is essentially  an entire edible flower cluster turned inside out, tucked down inside its own stalk.  This fleshy stalk, the peduncle, is the delicious bulk of what we enjoy when we eat a fig. To understand how we get from a typical flower cluster to a fig, it is useful to imagine a topological transition. Better yet, imagine turning a plain brown dress sock – the ordinary inflorescence –  into a sock puppet – the fig. In your mind, put your hand into the sock. Now pretend that the toe end of the sock is covered with little fig flowers down to the base of your fingers. This structure would be equivalent to a short compact inflorescence with a long peduncle. Now make a sock puppet by pulling the flower-covered part of the sock into your hand until all the flowers are inside and completely surrounded by peduncle (plain sock) tissue. Finally, make your puppet pucker up its lips to close off the flowers inside. The head of the sock puppet is like the entire bulbous fig structure, technically called a syconium. If Santa brings you brown socks yet again this year, do something fun and educational with them. Make your own fig puppets for a family friendly way to learn about syconia.

Fig flowers make gritty little achenes for fruit. (Some sources classify the fruits as drupelets, which are basically achenes with a little flesh on them.) The flowers are attached to the inside of the syconium by flower stalks (pedicels), which get very soft as figs ripen. The sweet part of the fig is a combination of peduncle, pedicels, and sepals.  The crunchy parts are the achenes.  But what about the old legend that wasp parts add a little something to the texture?

Are there wasps in my figgy pudding?

Usually, before fruit can ripen, flowers must be pollinated. In most of the more than 800+ fig species, pollination happens courtesy of small wasps from the Agaonidae family. Figs and agaonid wasps have required one another for existence for at least 60 million years. And like many co-dependencies, this one isn’t pretty. Fig seeds feed wasp larvae. A large family of newborn wasps synchronously emerges from the seeds within a syconium. The wingless, blind males have two quick duties before dying: inseminating their sisters and chewing escape holes for them. Before leaving home, young females gather pollen from male flowers. A winged female has 48 hours to find and enter a new receptive fig, pollinate the flowers, and lay eggs. The fig doesn’t help her. The only opening, the narrow ostiole, is defended with sharp bracts. With specialized jaws and a strong head, she chews her way past this gauntlet and into the fig, but tears her wings and antennae in the process.

The ostiole defended by sharp bracts.

Figs make two kinds of female flowers: long-styled and short-styled. Wasps can lay eggs only in short-styled flowers, but they are able to transfer pollen to all flowers.  The short-styled flowers thus make wasps, whereas the long-styled flowers make fertile seeds.  Under this arrangement, both the plant and the pollinator may reproduce.  The mother wasp dies after her tasks are complete and fig enzymes devour her body during ripening.  The spent male offspring meet the same fate, while their gravid sisters fly off to other figs.

In about half of fig species, whole trees come in two different sexes: “male” plants are similar to those described above, and their syconia bear both male and short-styled female flowers.  (The ovaries of the female flowers serve mostly as wasp nurseries, so they tend to be forgotten by fig sexers.)  “Female” plants produce syconia containing only long-styled female flowers, and the poor wasp entering one of these cannot lay eggs before dying.  Although her own reproduction is thwarted, she brings pollen from a “male” plant that triggers seed and syconium development.  Some favored varieties (e.g. Calimyrna) fall into this category and are called gynodioecious.  Because they are pollinated, they produce viable seeds and a large sweet fig syconium, but their long-styled flowers preclude egg-laying, and we avoid a mouthful of baby wasps.

Mission fig showing its ostiole

Some mutant fig varieties can ripen syconia without pollination.  These parthenocarpic (“virgin fruit”) plants have been propagated asexually by humans for over 11,000 years and comprise most of our edible figs (e.g. Mission and Kadota). They may lack well-developed seeds, but the empty shells of their achenes provide some crunch and their flesh is free of liquified female wasp body. If your Christmas pudding is made with figs, they are probably wasp-free virgin figs.

Bring us some figgy pudding

So what is that round brown flaming mound we know as figgy pudding, plum pudding, or Christmas pudding? Various sources proclaim that figgy pudding contains no figs; however when a printed recipe for an English-style boiled pudding is specifically labeled Fig Pudding, it does include figs. Thanks to the Historic American Cookbook Project, we can look at all eight Fig Pudding recipes (dated between 1870 and 1914) available in the digitized portion of their cookbook collection and confirm that figs are the main fruit ingredient in all of them. Two more fig-filled fig pudding recipes appear in the Macon Cook Book (1936 reprint of 1909 edition) and are presented alongside four figless recipes for plum pudding and Christmas pudding.

Can we thereby conclude that true figgy pudding does contain figs and should not be confused with plum pudding, which does not contain figs and never claimed to?

It’s more complicated than that: the word figgy has been used for centuries to describe something very sweet or, in the 19th century, something made with raisins (Oxford English Dictionary online). Notably, Plum Puddings never include plums or prunes, but are instead full of raisins and could be described as figgy. Thus a plumless figless plum pudding could accurately be called figgy. So although we clearly shouldn’t take “figgy” literally as an adjective, somebody must have taken it as inspiration to transform a medieval English boiled pudding recipe into a fig-filled confection called Fig Pudding.

There’s one last twist to the story: perhaps the most popular early American cookbook, Fannie Farmer’s Boston Cooking School Cook Book (1896), contains a recipe for a holiday pudding bursting with figs and raisins. She calls it English Plum Pudding.

This season, if carollers come to your door demanding figgy pudding, give them whatever you have. Just be sure it’s warm and soaked in brandy.

Recipes

Note that these recipes include suet, which is not vegetarian. Some websites recommend frozen vegetable shortening or a commercial vegetarian version of suet  for those wanting to avoid the real thing. Butter’s melting point is too low to stand up to the long boil of the pudding.

From The Macon Cook Book: a collection of recipes tested principally by members of Benson-Cobb Chapter, Wesleyan College Alumnae, Macon, Georgia. J.W. Burke Company, Publisher. (1936 reprint of 1909 original edition)

Fig pudding n^o. 1

One fourth pound of figs chopped fine, one fourth pound of suet chopped fine, one cup of brown sugar, two cups of bread crumbs, two eggs, a rind and juice of one lemon, one-half grated nutmeg, one tablespoon of flour. Steam three hours and serve with sauce. It is splendid served with whipped cream, slightly flavored with vanilla. –Mrs. Mary Wimberly Robson

From Fannie Farmer’s 1896 The Boston Cooking School Cook Book. 

English Plum Pudding

1/2 lb. stale bread crumbs
1 cup scalded milk
1/4 lb. sugar
4 eggs
1/2 lb. raisins, seeded, cut in pieces, and floured
1/4 lb. currants
1/4 lb. finely chopped figs
2 oz. finely cut citron
1/2 lb. suet
1/4 cup wine and brandy mixed
1/2 grated nutmeg
3/4 teaspoon cinnamon
1/3 teaspoon clove
1/2 teaspoon mace

Soak bread crumbs in milk, let stand until cool, add sugar, beaten yolks of eggs, raisins, currants, figs, and citron; chop suet, and cream by using the hand; combine mixtures, then add wine, brandy, nutmeg, cinnamon, clove, mace, and whites of eggs beaten stiff. Turn into buttered mould, cover, and steam six hours.

Acknowledgements and references:

Thanks to James Preston for calling Katherine’s attention to the Macon Cook Book and to Nancy Anderson for providing a hard copy of it (and inducting Katherine into the tradition of flaming figgy pudding)

Thanks to Quentin Cronk for correspondence about the morphological delimitation of peduncles.

More information about fig pollination may be found at the wonderful site Wayne’s Word

An amazing collection of late 19th and early 20th century American cookbooks is available through Feeding America: The Historic American Cookbook Project based at Michigan State University.http://digital.lib.msu.edu/projects/cookbooks/

This year’s article is adapted from a longer version, posted in late summer of 2013, that compares in detail the anatomy of figs and their mulberry cousins and includes a summer recipe for fresh figs. This time of year, however, we revel in the charms of dried figs.

Sock puppet fig

The United Nations declared 2016 the International Year of Pulses. What’s a pulse? It’s the dry mature seed of a large number of species in the legume family (Fabaceae): various beans, peas, soybean, chickpeas, lentils, peanuts and other groundnuts. 2016 is days from ending, so it’s high time I get up the Fabaceae diversity post I’ve been meaning to write all year long. This rounds out our year of legume coverage, which included Katherine’s posts on bean anatomy, peanuts, and green beans. 

Christmas Lima beans (Phaseolus lunatus), soaking before cooking

One out of every 15 flowering plant (angiosperm) species is a legume, a member of the large plant family Fabaceae (Christenhusz and Byng 2016, LPWG 2013). Boasting around 19,500 species in 750-ish genera (LPWG 2013), the Fabaceae is the third-largest plant family in the world, trailing behind only the orchid (Orchidaceae: 27,800 species) and aster (Asteraceae: 25,040 species) families (Stevens 2016). By my count, people only use about 1% of legume species for food (my list of edible legume species is found here), but that small fraction of species is mighty. People eat and grow legumes because they are nutritional superstars, can be found in almost all terrestrial ecosystems around the world, and uniquely contribute to soil fertility in both wild and agricultural ecosystems.

A finger on the pulse of edible legume diversity

One out of every 20 grams of protein consumed by people across the planet is from pulses, the protein-rich mature (usually dried) seeds of several legume species: various beans, peas, lentils, soy, peanuts and other groundnuts (Heine 2016). In some regions, however, especially in the developing world and in cultures that do not consume animal protein, the contribution of pulses to dietary protein is considerably higher than that 5% global average (Heine 2016). Protein comprises 20-40% of pulse seed mass, compared to 7-15% of seed mass of grains from the grass family (Poaceae; see our takes on them here and here), which are responsible for most of the calories consumed around the world, mostly in the form of rice, wheat, and corn (Vitale and Bollini 1995).

Black-eyed peas, in a pot, a traditional New Year’s Day pulse. Make some Hoppin’ John!

Highlighting the importance of pulses to global diets is the main reason why the United Nations declared 2016 the International Year of Pulses (Their website has a really good pulse recipe section to which you can submit. Last year was the International Year of Quinoa; read Katherine’s excellent essay about quinoa and its relatives here).  There is a lot more to legume food than just pulses, so I’ll provide an overview of legume food before diving into how it is that legumes are nutritionally and agriculturally important (they do nitrogen fixation), which happen to be the same ultimate cause of why we only eat 1% of legume species (they use their nitrogen to make poison as well as protein). Finally I’ll do my best to elucidate the evolutionary pattern (phylogeny) of edible legume diversity.

Root to Shoot: Legume structural diversity in the cornucopia

While pulses—mature seeds—are nutritionally the most important legume food items we eat from a calorie and protein standpoint, they are far from the only plant structures we eat from the Fabaceae (see structures consumed in my list of edible legumes).

A fresh fava bean (Vicia faba), torn crosswise during shelling. Spongy pith (endocarp) protects the immature seeds.

The fruit of all legume species is a pod, a simple single chamber (carpel) with two seams, containing one to several seeds. The pod is called a legume, hence the family nickname. We eat all or part of the pod from several species in a few different ways.

tamarind (Tamarindus indica) pods in a Cambodian market (photo by L. M. Osnas)

Some legume species produce sweet or otherwise flavorful pulpy tissue in their pods that is eaten by itself without the seed (ice cream bean, tamarind, honey locust, huamúchil), or dried and ground into a flour with the seeds (mesquite, carob).

And as Katherine recently described, green beans (or French beans, string beans, snap beans, wax beans) are the immature fruits (pods) of several bean species, mostly: common bean (Phaseolus vulgaris), runner bean (Phaseolus coccineus), yardlong bean (Vigna unguiculata sesquipedalis), hyacinth bean (Lablab purpureus), and sword bean (Canavalia gladiata).

These Kentucky wonder beans (Phaseolus vulgaris) are a bit too mature to pick as a green bean; they were excellent left to ripen into a pulse, however.

Some varieties have a “string,” the hard fibrous strand running the length of the pod on one or both seams that can be removed before cooking (botanically the string is a lignified—woody—sclerenchyma cap outside the phloem of the vascular bundle running along one or both sutures of the fruit).

snap pea

Similarly, we eat the fresh, immature pod of some garden pea (Pisum sativum) varieties as snow peas or snap peas. With several varieties of both beans and peas, we can eat the immature seeds and pods when they are young and tender, or we can wait until the seeds mature and the pods dry, turning them from a vegetable into a pulse. This is a boon for gardeners who might not be completely diligent in harvesting all their green beans when young and tender. Also in the vegetable vein, young shoots and leaves of many legume species are eaten raw. Pea shoots are especially popular. A few species are eaten as sprouts, including alfalfa and mung bean.

Jicama is probably the most famous and widespread of several perennial legume herb or vine species that produce edible starchy root tubers that can be eaten raw or cooked. Well, in the southern United States, that honor probably goes to the ubiquitous invasive kudzu vine (eat that weed!), not jicama.

Caracalla bean flowers

The flowers of many species are edible, including the striking and fragrant flowers of the caracalla bean, which Thomas Jefferson grew at Monticello and described as “the most beautiful bean in the world.”

Rooibos (“red tea”) and honeybush are dried leaves/shoots from two South African legume shrubs used as herbal infusions (“tea”). Dried alfalfa leaf and red clover flowers are also used as tea.

Some pulses are multi-purpose. Peanuts and soy are pulses when consumed as whole seeds, but the seeds are also pressed for cooking oil. The nuña, a variety of the common bean, is a unique popping bean. When cooked dry over high heat, the nuña’s starchy cotyledons explosively puff up, like popcorn (although in popcorn the starchy puffing structure is endosperm, not cotyledon).

Some legume seeds are culinary spices (fenugreek, wattle) but might also be cooked in quantity like a pulse.

Polysaccharide compounds from some legume seeds (guar, cassia, tara, locust bean gum from carob) or resin (gum Arabic) or sap (gum tragacanth) are used as culinary gums and binders. The sticky-sweet root extract from the licorice plant is boiled to make the iconic candy.

mesquite  (Prosopis spp.) pod flour

Note that there are several plant foods that are not legumes whose common names nonetheless include “bean,” for example: coffee bean (Coffea; family Rubicaceae); cocoa bean (Theobroma; Malvaceae); vanilla bean (Vanilla; Orchidaceae); castor bean (Ricinus; Euphorbiaceae); and sea bean (Salicornia; Amaranthaceae).

legume shrubs and trees in the Sonoran Desert, including mesquite

The diversity of legume food plants reflects the fantastic morphological and life history variation in the family. In their 64 million years of existence, legumes have come to occupy most terrestrial ecosystems on Earth and exist in every botanical size and life history category: annual herbs and vines, perennial herbs and vines, shrubs, lianas (woody vines), and temperate and tropical trees (LPWG 2013, Stevens 2016). These life forms appear to be somewhat evolutionarily labile, waxing and waning into one another on what we currently understand to be the legume phylogeny (discussed below). We get food from all the different legume lifeforms and from many different branches of the legume family tree. One characteristic this motley set of edible legumes does share, though, is nitrogen fixation, which I will expound on a bit before we talk about legume phylogeny and domestication.

Prodigal sons of the plant world: Nitrogen fixation in legumes

Peanuts (Arachis spp.) are pulses that store seed resources primarily as protein and fat (photo by K. Preston).

Across all plants in the world, there is little rhyme or reason, as far as we’ve been able to figure out, as to why certain plants store their seed’s resources as protein, fat, or carbohydrates (Hanson 2015). Legumes store seed resources in all three forms. We get industrial quantities of both oil and protein from soy beans and peanuts, for example. My husband considers pulses to be the “starchy” side dishes to accompany meat instead of the respectable protein source much of the mostly vegetarian world recognizes them to be.

Lentils (Lens spp.) are pulses that store seed resources mainly as protein and carbohydrate

Within the legumes, though, part of the protein-versus-carbohydrate seed storage form seems dictated by environment and where the seed stores its resources. The most carbohydrate-leaning seeds are those of species that live in dry and drought-prone environments and store their seed resources in endosperm, like many other non-legume seeds including grains (see Katherine’s description here), instead of in enlarged cotyledons, which is the strategy favored by most legumes, including all culinary beans and peas (see Katherine’s bean posts here and here for the details). Some carbohydrates in those “endospermic” legume seeds (including alfalfa, fenugreek, carob, and guar) are highly branched complex polysaccharides that have high affinity for binding water for seed germination in places where water can be scarce. It turns out those complex water-binding carbohydrates make excellent emulsifiers, thickeners and binders for humans’ food and industrial products. We extract polysaccharide gums from many different legume species, and they show up in diverse products spanning the cultural gamut, from vegan ice cream to fracking fluid (Hanson 2015).

weedy wild Lathyrus latifolius: inedible but a good nitrogen fixer, contributing nitrogen to this meadow

Legume seeds are exceptionally good sources of protein because they can afford to throw around large quantities of nitrogen, an essential plant nutrient that is scare (limiting to plant growth) in most terrestrial ecosystems. Legumes are able to profligately live what my college ecosystem science professor called a “nitrogen-rich lifestyle” because they have their own little nitrogen fertilizer factories in their roots, full of specialized symbiotic bacteria (Rhizobium spp.) that perform nitrogen fixation. The bacteria, housed in specialized root nodules and fed a steady diet of sugar derived from the plant’s photosynthesis, with the aid of the plant, ultimately transform unusable nitrogen gas (N₂) from the atmosphere into biologically available nitrogen compounds: ammonium (NH₄⁺), nitrate (NO₃^–), or amino acids. The legume plant uses that nitrogen to build its own tissues (nitrogen is a main ingredient in proteins and DNA) and to imbue its seeds with large concentrations of specialized protein used for energy, defense, and amino acids.

scarlet runner bean (Phaseolus coccineus)

After a legume plant discards structures or dies, the substantial nitrogen in its tissues becomes part of the soil and available to other plants that do not form nitrogen-fixation symbioses, which is most plants. Legumes thereby uniquely contribute to soil fertility in both wild and agricultural ecosystems.  That is why legumes are popular as cover crops and in crop rotations, naturally improving the soil for the next crop and reducing the need for artificial nitrogen fertilizer. This food security and agricultural sustainability benefit of legume crops is the other beneficial aspect of pulses that the UN wanted to highlight in this International Year of Pulses.

Pairing grass family (Poaceae) grains and legume pulse crops for both the nutritional (complementary amino acids, both needed for human protein synthesis) and agricultural benefits is likely a very early feature of agriculture and independently emerged multiple times: in the Fertile Crescent and Europe, wheat, oats, rye, and barley were paired with chickpeas, lentils, fava/broad beans, grass peas, fenugreek, and garden/split peas; rice was paired with soy, azuki and mung beans in China; in the Americas the “three sisters” were squash, corn, and beans (common beans, Lima/butter beans, peanuts, lupines); cowpeas and Bambara groundnuts grew alongside sorghum and millet in Africa (Hanson 2015, Vaughan and Geissler 2009).

Two of the “Three Sisters”: bean (Phaseolus vulgaris) vines up corn stalks

Many widespread legume species underwent multiple independent domestication events, contributing to the dizzying variety of pulse and vegetable legume varieties. For example, the common bean P. vulgaris had two domestication centers, one in Mexico and another in the southern Andes (LPWG 2013). Following European exploration in the Americas, P. vulgaris and other American legumes underwent further domestication in Europe. This multi-staged domestication in P. vulgaris resulted in everything from haricot vert green beans to classic Latin American cooking beans (navy beans, black beans, kidney beans, white beans, Appaloosa beans, cranberry beans), to the nuña popping bean.

Protein and Poison in Pulses: why legume seeds are so big and nutritious, but also why we only eat 1% of legume species

The nutritious value of legume seeds to people is inextricably tied up with their dependence on nitrogen fixation, or at least their high dependency on nitrogen, as a small fraction of legumes don’t form nitrogen fixation symbioses. Nitrogen fixation allows legumes to colonize and grow well in soils that have little or no nitrogen. To do so, however, the new legume seedling requires a large initial amount of energy and nutritional resources to quickly construct the photosynthetic and root nodule apparatuses required to house and feed the nitrogen fixing bacterial symbionts. That initial investment comes from reserve material in the seed, stored, as I mentioned above, as a combination of starches or other polysaccharides, fats, and protein.

Katherine’s image of a germinating peanut seed (from her peanut post)

When the seed germinates the embryo will enzymatically break down or otherwise metabolize these compounds to fuel its initial growth (see Katherine’s description of bean seed anatomy, germination, and growth here and here). This copious amount of reserve material is why many legume seeds, including many that we use for food, are on the large side (McKey 1994). The 18-cm-long (inedible) seed of tropical legume tree Mora oleifera is the largest eudicot (large group of plants including legumes) seed on the planet (McKey 1994; I mentioned this previously in passing in my post on monocots and seed size).

The legume plant also uses that in-house nitrogen to make a lovely variety of extremely toxic nitrogen-rich alkaloid and lectin defense compounds that suffuse legume tissues along with a suite of other defense chemicals. These poisons are probably the main reason why humans do not use upwards of 99% of legume species for food. The largest single genus of plants on the planet, Astragalus, with over 3000 species, is in the Fabaceae (Frodin 2004). Only the root and resin, respectively from two Astragalus species (A. propinquus and A. brachycalyx), as far as I can tell, are used in any great quantity as people food, and both of those are considered more of a medicinal foodstuff or binder, rather than a main dish. The rest of the Astragalus species and several other legume genera are called “locoweeds” because of the neurological damage caused by their alkaloids. When they occur as weeds in pasture or as natural components of range ecosystems, locoweeds can and often do destroy livestock.

Desert ironwood (Olneya tesota), a beautiful but inedible legume tree from the Sonoran Desert, showing the most common legume banner-and-keel papilionaceous flower type

Reducing the toxicity of legumes has undoubtedly been a focus of legume domestication, especially of those species used as fresh vegetables. The toxic alkaloids can be neutralized by soaking and cooking in the legumes that people regularly consume. Even if considered to be technically somewhat edible by some crazy or desperate people, though, there are several legume species that should only be at most occasionally consumed in small quantities because of the long-term deleterious or immediately nauseating effects of these alkaloids (See essays on neurological damage called lathyrism caused by improper or excessive consumption of wild legume species in the genus Lathyrus by Hank Shaw and Green Deane and in Amy Stewart’s book Wicked Plants). I personally think it is unwise to eat the raw seeds or pods of any wild legumes, but the edible tubers of some of them are very cool and appear to be a lot less toxic than the leaves or reproductive structures).

As Katherine described in her black-eyed pea post, the carbohydrate raffinose in pulses probably isn’t a defense chemical, per se, probably serving a storage role in the seed, but it is what induces flatulence after people eat beans. Unless, that is, you consume Beano before your meal, which contains the enzyme necessary to break down raffinose. People do not make this enzyme, but our gut bacteria that help us digest our food do. When the bacteria tackle raffinose, they produce gas.

Legumes, by the way, are far from the only plants that make toxic alkaloids. Plant-derived alkaloids include some of the most famous and infamous recreational and medical drugs and poisons in humanity’s pharmacopeia, including caffeine, cocaine, and the wide variety of poisons in the nightshade plant family. Non-legumes, however, without that in-house nitrogen supply, can only make alkaloid defenses with nitrogen from the soil, after they’ve satisfied the nitrogen requirement for basic growth, maintenance and reproduction. That’s why the caffeine content of maté and coffee has been shown to vary strongly from farm to farm in concert with soil fertility, as I mentioned in my post on the botany of caffeine.

Thinking phylogenetically: Legumes in an evolutionary context

hyacinth bean (Lablab purpureus), a papilionoid legume

Before the invention of industrial means of chemically fixing nitrogen to produce artificial nitrogen fertilizer, the only way new nitrogen could enter ecosystems was through nitrogen-fixing microorganisms, either free-living in the soil or on the surface of plants, or in root symbioses with nitrogen-fixer plants. Aside from the legumes, some of which do not fix, only a few plant species form nitrogen fixation symbioses with microorganisms. All these other “nitrogen fixers” plant species form symbioses with Frankia actinomycetes that perform the nitrogen fixation, not Rhizobium bacteria as in legumes, and all are found within a large clade within the rosids (a group of plants all evolutionarily derived from a single common ancestor from within the large group of flowering plants named the rosids; Werner et al. 2014).

I mention this bit of evolutionary history not only because its discovery is a triumph of modern ecology. Legumes and other nitrogen fixers are evolutionarily unique. To me this puts in sharp relief how crucial these plants are for supporting human food security. Phylogenetic context (evolutionary relationships among species) in general helps us to better understand the similarities and differences in our food plants, their origins, and why they look, taste, and grow the way they do. For scientists trying to produce better agricultural varieties, phylogenetic context and other genetic and genomic information is essential. And in the case of an enormous plant family like the Fabaceae, the phylogeny is a big, tangled hot mess and is therefore a lot of fun to look at. I’ll do my best to show us where in the legume phylogeny our food comes from.

Legume Phylogenetics: Where are food plants come from in the legume family tree

fossil legume pod, Smithsonian Museum of Natural History, Washington, D. C.

The phylogeny of the legume family is still under construction. Inferring clades (groups of related species arising from a single common ancestor; monophyletic) within the family is complicated by the large number, broad geographic distribution, and genomic complexity of legume species. Before the modern age of using DNA data to infer evolutionary history, the legumes had been split into three major subfamilies: Caesalpinioideae, Mimosoideae, and Faboideae (formerly Papilionoideae). Much recent work, however, has demonstrated that the Faboideae and Mimosoideae arose from within what had previously been called part of the Caesalpinoideae (Legume Phylogeny Working Group 2013), meaning that the old Caesalpinoideae is paraphyletic (includes species from different clades) and therefore not especially useful for classification. Legume systematic biologists are actively replacing the old classification with new names of monophyletic groups within the Fabaceae (LPWG 2013).

red Chinese yardlong bean (Vigna unguiculata) plant

Most legume food plants are papilionoid legumes in the Faboideae. The most widely grown pulses are in four named clades: (1) Phaseoloids (Glycine or soy, beans in Phaseolus, Cajanus and Vigna); (2) Galegoids (lentils in Lens, alfalfa in Medicago, beans and peas in Pisum, Lathyrus, Vicia); (3) Genistoids (Lupinus); and (4) Dalbergoids (peanuts in Arachis)(Lewis et al. 2005, Smykal 2015). Phaseoloids are mostly pan-tropical, whereas galegoids are mostly in the temperate world. The Mimosoideae and Caesalpinoideae are mostly woody trees and shrubs. All major clades, however, include all multiple plant growth forms and may have broad geographical distribution.

My list of edible legume species includes Latin and common names, structures consumed, growth form, taxonomic information, and geographic origin. You can use it to pair up common and Latin names in the Fabaceae phylogenies (Figures 1-3) below. Note, however, that this table only includes a few of the many thousands of variety names for these species. For example, you won’t see separate entries or even an extended list for the numerous varieties of common bean (Phaseolus vulgaris) available from your local grocery or seed catalog. I compiled my list of edible species from a few sources, listed in the References section, as well as personal knowledge. I’d like this list to eventually be exhaustive, but I doubt it is yet. If you think I’ve missed something or got something wrong, please let me know!

Below I’ve depicted the phylogenetic placement of our legume food plants (from my list) within the Fabaceae in three figures, one for the entire family with the Faboideae collapsed to a single branch, another for the Faboideae with a large group of Phaseoloids collapsed to a single branch, and a third for that large group of Phaseoloids. This was actually difficult to figure out, because the Fabaceae phylogeny is in such flux, and the more modern updates don’t include all of the edible species. So, really, this is my best current working guess. In my opinion, future legume systematic efforts, at least within the Faboideae, should make a point to include nutritionally and economically important species. In the phylogenies depicted in Figures 1-3, edible species common names are shown. For Latin names and species information, please see my table of edible legumes. Data for the phylogenies are from papers listed in the References section. If you need a refresher on reading phylogenetic trees, see our primer.

Figure 1: Phylogeny of the legume family (Fabaceae) showing position and relationships among edible legume species outside of the subfamily Faboideae/Papilionoideae, which is collapsed to a single branch (see Figures 2 and 3 for Faboideae phylogenies).

Figure 2. Phylogeny of  Fabaceae subfamily Faboideae, with the exception of the large number of species in the Phaseoloid legume group collapsed here into a single branch called “Phaseoleae-ish” (see figure 3 for phylogeny of these taxa). Position of Faboideae within Fabaceae shown in Figure 1. Some major clades and positions and relationships among edible species are shown.

Figure 3. Phylogeny of a large clade of Phaseoloid legumes, the position of which is shown within the Faboideae in Figure 2 as “Phaseoleae-ish,” because many of these have variously been placed in a tribe Phaseoleae . The phylogenetic relationships among these species is in such a state of flux, it is difficult to ascertain the accurate phylogenetic positions of phaseolioid legumes at this time.

Whirled Peas

Fresh black-eyed peas, on the left and shelled in bowl on the right, with red Chinese long beans in the middle. Two varieties of cow pea (Vigna unguiculata) from our garden three years ago.

It’s no wonder the diverse and cosmopolitan legumes are ubiquitous in myriad winter holiday and traditions or celebrations. Even if the legumes are not the star of the show, they are present, integral. A few weeks ago we had a tamale-making party, a Mexican Christmas tradition. No beans went into the fillings, but everyone ate black beans alongside their tamales, and the coleslaw was dressed with a chickpea miso vinaigrette. Santa brought me a bottle of The Botanist gin, which has the best bottle: the Latin names of the 22 botanical ingredients are etched in raised glass. It includes two clover species (red clover, Trifolium pratense, and white clover, T. repens). We just bought our black-eyed peas to make traditional Hoppin’ John on New Year’s Day. But, mostly, around our house, we’ve been sending out wishes for Whirled Peas. My five-year-old has recently learned to pair her love of frozen green peas with a play on words. The lunchtime blessing in her classroom concludes with: “And may there be peace on Earth and in our hearts.” One recent afternoon I pointed out to her that “whirled” sounds a lot like “world,” and “peas” sounds a lot like “peace.” So she had some whirled peas, and here’s hoping that we all do too. May your 2017 be full of legumes and peace.

References

Cardoso, D., L. P. de Queiroz, R. T. Pennington, H. D. de Lima, E. Fonty, M. R. Wojciechowski, and M. Lavin. 2012. Revisiting the phylogeny of papilionoid legumes: New insights from comprehensively sampled early-branching lineages. American Journal of Botany 99:1991-2013.

Christenhusz, M. J. M., and J. W. Byng. 2016. The number of known plant species in the world and its annual increase. Phytotaxa 261: 201-217.

Delgado-Salinas, A., M. Thulin, R. Pasquet, N. Weeden, and M. Lavin. 2011. Vigna (Leguminosae) sensu lato: The names and identities of the American segregate genera. American Journal of Botany 98:1694-1715.

Frodin, D. G. 2004. History and concepts of big plant genera. Taxon 53:753-774.

Gepts, P. 1998. Origin and evolution of common bean: past events and recent trends. HortScience 33:1124-1130.

Hanson, T. 2015 The triumph of seeds: How grains, nuts, kernels, pulses, and pips conquered the plant kingdom and shaped human history. Basic Books.

Heine, J. 2016. Pulses: a multi-faceted crop. Food outlook: biannual report on global food markets. Food and Agriculture Organization of the United Nations.

LPWG: Legume Phylogeny Working Group. 2013. Legume phylogeny and classification in the 21^st century: progress, prospects and lessons for other species-rich clades. Taxon 62:217-248.

Lewis, G., B. Schrire, B. Mackinder, and M. Lock. 2005. Legumes of the World. Royal Botanic Gardens, Kew. UK.

McKey, D. 1994. Legumes and nitrogen: the evolutionary ecology of a nitrogen-demanding lifestyle. In: Advances in Legume Systematics 5: The nitrogen factor. Edited by Sprent, J. I., and D. McKey. Royal Botanic Gardens, Kew. Pages 211-228.

Pratap, A., and J. Kumar. 2011. Biology and breeding of food legumes. CABI.

Smykal, P., C. J. Coyne, M. J. Ambrose, et al. 2015. Legume crop phylogeny and genetic diversity for science and breeding. Critical Reviews in Plant Science 34:43-104.

Stevens, P. F. 2016. Missouri Botanical Garden’s Angiosperm Phylogeny Website. Version 12, July 2012 (and more or less continuously updated since).

Stewart, Amy. 2009. Wicked plants: The weed that killed Lincoln’s mother and other botanical atrocities. Algonquin Books.

Vaughan, J. G., and C. A. Geissler. 2009. The New Oxford Book of Food Plants. Oxford University Press.

Vitale, A., and R. Bollini. 1995. Legume storage proteins. In: Seed Development and Germination. Edited by J. Kigel. CRC Press. Pages 73-102.

Werner, G. D. A., W. K. Cornwell, J. I. Sprent, J. Kattge, and E. T. Kiers. 2014. A single evolutionary innovation drives the deep evolution of symbiotic N₂-fixation in angiosperms. Nature Communications 5: 4087.

Wojciechowski, M. F., M. Lavin, and M. J. Sanderson. 2004. A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. American Journal of Botany 91:1846-1862.

Wojciechowski, M. F., M. J. Sanderson, K. P. Steele, and A. Liston. 2000. Molecular phylogeny of the “temperate herbaceous tribes” of Papilionoid legumes: A supertree approach. In: P. S. Herendeen and A. Bruneau (editors). Advances in Legume Systematics 9. Pages 277-289. Royal Botanic Gardens, Kew. UK.

Wikipedia’s list of edible legumes

Winter is the season for citrus fruit, and January is the month for breaking out of old routines, so stop staring at your navel and learn about one of the weirder citrus varieties.

I’ll never forget the day one of my general botany students brought to class a Buddha’s hand citron, pulled from a tree right outside our classroom. I had only recently moved to northern California from Indiana, and I’d never seen anything like it: it was a monstrous mass of a dozen pointed twisted fingers splayed irregularly from a stout base. It had the firm heft and girth of a grapefruit and the unmistakable pebbled skin of a citrus fruit, so I wondered whether my student had found a grossly deformed grapefruit; but the oil in the peel smelled heavenly and not at all like a grapefruit. In class we cut through a big finger and found no juicy segments, just white citrus pith all the way through.

Immature Buddha’s hand on the tree

We eventually discovered that this fascinating fruit was a Buddha’s hand citron, Citrus medica variety sarcodactylis, meaning fleshy (sarco-) fingered (-dactyl) citron. Since that day many years ago I’ve become an unapologetic (if surreptitious) collector of the fruits from that same campus tree. The citrons do not drop from the tree on their own, yet I often find one or two lying nearby, probably torn off by a curious tourist or student and then abandoned. Obviously these fruits need a good home, and where better than the window sill in my office?

The first time I left one closed up in my office over a weekend, I opened the door on Monday morning to a waft of fruity floral aroma. It turns out that many people in China and India use the fruit to scent the air, although in west Asia and Europe the fleshy fingers are more often candied or used to flavor alcohol. I do both: the fruits make my office smell nice until they are fully yellow, and then I cook them.

It can be difficult or expensive to get your own hands on a fingered citron, but it’s easy to find a navel orange almost any time of the year. Fortunately, the patterns underlying the morphology of the fingered fruit can also be seen in an everyday navel orange. Between our photos of Buddha’s hands and your own navel orange, you should be able to follow along at home.

Carpels and segments

A Buddha’s hand citron is a fruit, and like all simple fruits, it is the mature ovary of a flower. Citrus fruits – from kumquats to lemons to oranges to grapefruits – are technically berries because they are fleshy throughout and do not have hard pits or tough papery bits inside. More specifically, they are a special type of berry called a hesperidium, derived from the original name Linnaeus bestowed upon the citruses in lovely and colorful reference to the Golden Apples of the Hesperides. (For a lively detailed discussion of orange etymology, see Mabberley 2004).

Frederic Leighton – The Garden of the Hesperides (ca. 1892) via Wikimedia commons

Plant ovaries (and resulting fruits) are made up of the lower parts of one or more carpels, the fundamental units of the “female” part of the flower (the gynoecium). Carpels arise at the tip of a flower extremely early in development, and in many species they gradually fuse together to form a single solid ovary with one or more styles and stigmas.

Orange flowers. The smooth ovary and its thick style and stigma are shown in the center flower, from which petals and stamens have been removed. Click to enlarge.

Under a microscope, the tip of a developing orange flower looks like a tall fluted bundt cake or a French cannelé, each hump a tiny incipient carpel (see images in Lima and Davies 1984). But by the time an orange flower opens, the outside of the ovary is totally smooth.

The carpels that make up a mature orange or grapefruit or lemon are obvious: they are the familiar (and convenient) individual wedge-shaped segments. Among my favorite botany fun facts is that the long pulpy sacs that fill the segments and cushion the seeds are actually individual hollow hairs, filled with juice.

Fingers and the failure to fuse

The gnarled fingers of a Buddha’s hand citron are simply separate carpels that somehow failed to fuse. This is evident when you look closely at the flowers and very young fruits of a Buddha’s hand. Instead of a smooth ovary made of united carpels, the young carpels of a fingered citron are already going off in their own directions.

Click to enlarge

Many non-fingered citron varieties (such as the etrog) contain very little juicy pulp and are valued primarily for their scented zest and their very thick rinds, which are made into jam or candied. Cheap candied citron peel haunts the dreams of fruitcake haters, but homemade versions are amazing. The spongy white part of the rind (albedo) soaks up a lot of sugar syrup, and the zest (flavedo) provides an intense citrusy zing. Fingered citrons are even better suited for candying because they are basically nothing but rind and their fingered shape maximizes the ratio of flavedo to albedo. My recipe for homemade candied Buddha’s hand is below.

Cross section through the base of a Buddha’s hand citron. Click to enlarge.

Fingered citrons also fail to make seeds and must be propagated intentionally by humans, so it was surprising when a recent study (Ramadugu et al., 2015) found a great deal of genetic diversity among eleven distinct varieties of fingered citrons from Yunnan Province in China, the presumed birthplace of fingered citrons. The authors speculate that the fingered mutation may have arisen independently several times from different non-fingered varieties, and that the trait also could have been passed on to hybrid offspring through pollen. Some varieties of the non-fingered types are noticeably ridged (see photos in Ramadugu et al. 2015), so perhaps there is a genetic predisposition towards making fingers. I have not found any studies that have specifically identified the mutation responsible for the fingered trait, but several genes are good candidates. (If you are familiar with research in this area, please leave a comment).

Fingers and navels

Failure to fuse explains the separate fingers of a Buddha’s hand, but it doesn’t explain why there is usually more than one ring of them. To gain insight into this part of the mystery, we need to do a little navel gazing. This kind will be productive, I promise.

Now that’s a pretty navel

Closeup of the navel, showing partially separate carpels, like the fingers of a fingered citron. Click to enlarge

So what is the navel in a navel orange? Navel orange flowers make one normal ring of regular well-behaved carpels (the bundt cake described above) but then they produce a smaller second ring inside of that. The second ring becomes the “navel.” Sometimes the carpels in the second ring fail to fuse, and each is surrounded by rind, contributing to the iconic belly button look. Sometimes the rind around the second ring just gets lumpy and pushes itself into the segments of the first ring. Meanwhile, the tissue surrounding the first ring of carpels grows up around the second ring leaving a small opening through which the navel shows through (Lima and Davies 1984).

A similar developmental pattern happens in fingered citrons, but to a more extreme degree. I’ve seen what look like three rings of carpels, although they are so irregular, it is hard to tell for certain that there are not four.

Even Buddha’s hands from the same tree vary in number of carpels and how many whorled series of carpels develop.

Buddhas aren’t bitter

Citrons (varieties of Citrus medica) represent one of the three original Citrus species from which most of our edible citrus fruits were derived through hybridization. The other two are Citrus maxima (pummelo) and Citrus reticulata (mandarin), and several recent phylogenetic studies have supported the monophyly of these three groups (e.g. Carbonell-Caballero et al. 2015).

Citrons and mandarins are not bitter, whereas pummelos are. The bitterness of a citrus fruit depends on which of two enzymes is acting on a precursor molecule to generate a bitter flavanone or a flavorless one. Some hybrid species, such as grapefruit and bitter orange, express the bitter-flavanone-producing enzyme inherited from their pummelo parent. Interestingly, sweet oranges also have a pummelo parent; however in sweet oranges, a mutation in the bitterness gene disabled the pummelo version of the enzyme, leaving only the sweet mandarin parent’s version to operate in the fruit (Frydman et al. 2013).

Because citrons are not bitter, their zest can be used as an interesting substitute for lemon or orange zest, and it is not necessary to purge the rinds of bitterness before making them into candy garnishes.

Recipes

When my botany class met again after the Buddha’s hand show-and-tell, my student admitted to having served the prize fruit to his friends, sliced into vodka tonics. Well, that was one perfectly good way to use a Buddha’s hand, but below are two of my favorites.

Candied Buddha’s hand citron

1. Wash a large fingered citron to remove any dirt clinging to it. You may have to separate or remove some of the fingers to get it all clean.
2. Chop the solid part of the fruit into chunks or sticks, as you wish. The pieces will shrink only slightly, so cut them to be close to their final size.
3. Cut the fingers into chunks or slice them lengthwise for curls. Very small fingers can be left whole.
4. Make a sugar syrup in the ratio of 2:1 sugar to water. For a large fruit, two cups of sugar in a cup of water should be more than enough. Ordinary table sugar works best in this recipe because it does not burn too quickly and it allows the citron flavors to shine through.
5. Heat the sugar and water gently to dissolve the sugar and add the chopped citron.
6. Continue to simmer the citron in the syrup, stirring frequently, until the pieces appear translucent and the syrup is thick but not caramelized.
7. Let the citron cool in the syrup, then transfer the pieces to a large plate and spread them out.
8. Any leftover syrup can be used as syrup or stirred into the marmalade recipe below.

If you plan to put them in fruit cake or figgy pudding, you can let the pieces dry for a couple of hours and refrigerate them until you are ready to bake. If you want them for candy or garnish, let the pieces dry for a couple of hours and roll them in powdered sugar to coat thoroughly.

They are beautiful strewn on top of an orange soufflé, straight from the oven, or on a scoop of ice cream.

Buddha’s hand marmalade

To be honest, I just use the recipe at the Earthy Delights Recipe Blog. 

My only comment on this recipe (besides that it’s very good!) is that my marmalade sometimes comes out too thick, with too much citrus chunk and not enough gelled matrix. The gelled matrix can also be too thick. Because there is so much pectin in the white (albedo) part of the fruit, this problem might be avoided by using only the pieces that have zest on them and leaving out some of the central mass of the fruit. No matter the texture, though, it tastes wonderful.

References

Carbonell-Caballero, J., Alonso, R., Ibañez, V., Terol, J., Talon, M., & Dopazo, J. (2015). A phylogenetic analysis of 34 chloroplast genomes elucidates the relationships between wild and domestic species within the genus Citrus. Molecular biology and evolution, 32(8).

Frydman, A., Liberman, R., Huhman, D. V., Carmeli‐Weissberg, M., Sapir‐Mir, M., Ophir, R., … & Eyal, Y. (2013). The molecular and enzymatic basis of bitter/non‐bitter flavor of citrus fruit: evolution of branch‐forming rhamnosyltransferases under domestication. The Plant Journal, 73(1), 166-178. http://onlinelibrary.wiley.com/doi/10.1111/tpj.12030/full

Lima, J. E. O., & Davies, F. S. (1984). Secondary-fruit ontogeny in navel orange. American journal of botany, 532-541.

Mabberley, D. J. (2004). Citrus (Rutaceae): a review of recent advances in etymology, systematics and medical applications. Blumea-Biodiversity, Evolution and Biogeography of Plants, 49(2-1), 481-498.

Ramadugu, C., Keremane, M. L., Hu, X., Karp, D., Federici, C. T., Kahn, T., … & Lee, R. F. (2015). Genetic analysis of citron (Citrus medica L.) using simple sequence repeats and single nucleotide polymorphisms. Scientia Horticulturae, 195, 124-137. http://dx.doi.org/10.1016/j.scienta.2015.09.004

For more about the origins of oranges: Wu, G. A., Prochnik, S., Jenkins, J., Salse, J., Hellsten, U., Murat, F., … & Takita, M. A. (2014). Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nature biotechnology, 32(7), 656. http://www.nature.com/nbt/journal/v32/n7/full/nbt.2906.html