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For Plants, Polyploidy Is Not a Four-Letter Word

This article was published in Scientific American’s former blog network and reflects the views of the author, not necessarily those of Scientific American


The sacred Asian water lotus, Nelumbo nucifera -- the pedestal of choice for a variety of Egyptian and Indian deities. It's easy to see why. Public Domain. Click image for link.

Creative Commons ehamburg. Click image for license and source.

For animals, inheriting more than the usual two copies of DNA is usually a very bad thing. It can happen when two sperm fertilize one egg, or when sexual cell division errs, leaving a sperm or an egg with double the approved payload. But for animal embryos, the result is usually the same: death.

This is particularly true in mammals and birds, where more than two copies -- a condition termed polyploidy -- produces something euphemistically termed "general developmental disruption". Practically speaking, this means system meltdown, and it happens very quickly. In humans, three or more whole genome copies occurs in about 5% of human miscarriages.


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Only two cases of successful polyploidy are known among birds, and only one among mammals: the South American red viscacha rat (which is much cuter than it sounds). It has four copies of its genome, which makes it tetraploid.

Polyploidy is slightly more common among other animals. A few hundred cases of polyploidy are known in insects, reptiles, amphibians, crustaceans, fish, and other "lower" animals. Polyploidy can often be induced in these creatures; something called "triploid trout" is making waves among anglers in the Pacific Northwest. The fish's three sets of chromosomes can't pair properly during sexual cell division, rendering them sterile but thereby enabling them to grow bigger than their diploid kin, since they don't waste energy on such frivolities as eggs, sperm, and hooking up. You know how fishermen feel about big fish, so "triploids" have already inspired the requisite epic fishing videos.

Though polyploidy is not common in animals, it is suspected that it might have played a role in the evolution, eons ago, of vertebrates, ray-finned fish, and the salmon family (of which trout are members). But on the whole, polyploidy is a dicey and often dangerous affair for animals.

Not so for plants, who seem to have a more laissez-faire attitude toward the whole business.

In my post earlier this week about a mutant diploid moss, I mentioned that it was capable of making functional eggs and sperm with two copies of the genome instead of the usual one. In other words, the offspring of this mutant would be tetraploid. The fact these plants seem to be capable of producing viable polyploid offspring suggests polyploidy can be an instrument of evolution in mosses, as it is for many other plants, suggested the authors of the paper that I wrote about.

For in plants, unlike animals, polyploidy is common, seemingly innocuous, and often acted upon by natural selection as an instrument of speciation. Perhaps plants tolerate genome duplication better than animals because they have inherently more flexible body plans than animals, and can more easily cope with any gross anatomical changes that might accompany it.

Whatever the reason, plant polyploidy is rampant. Scientists have estimated that half to two-thirds of flowering plants are polyploid, including more than 99% of ferns and 80% of the species in the grass family -- the source of rice, wheat, barley, oats, and corn. So are a huge proportion of our other crops, including sugarcane, potatoes, sweet potatoes, bananas, strawberries, and apples. We may well have artificially selected for this. In plants, genome duplication often seems to help make more stuff, which is good if you're looking to eat the stuff.

Though genome duplication can happen on its own in plants through the same mechanisms I mentioned above for animals, that is not the most common way. It more frequently follows accidental interbreeding of two closely related species. This usually produces sterile offspring, since the the mismatched chromosomes have nothing to pair with during sexual cell division. But if, by chance, this chimera duplicates its genome, fertility is restored by pairing the assorted lot. Simultaneously, a tetraploid organism and a new species have been created.

For example, two of the major varieties of wheat grown today are the result of sequential hybrid doubling and quadrupling of the genomes of its wild grass ancestors. The original ancestral species had 14 chromosomes. Today, farmers plant both tetraploid 28-chromosome durum wheat and hexaploid 42-chromosome bread wheat. Durum wheat makes more toothsome pasta, while the gluten-y hexaploid flour forms protein networks that stretch into loftier, lighter bread.

Two other polyploid plants made waves last week: the carnivorous bladderwort and the sacred lotus. The bladderwort's time in the spotlight was thanks to the discovery that it is nearly free of non-protein coding "junk" DNA, a material nearly every other complex organism is awash in, including you.

But the tiny, insect-eating plant has managed to achieve this parsimony in spite of three rounds of genome duplication. In theory, it's got eight copies of each gene, with respect to the two-copy ancestor of nearly all true or "eudicots", a massive group of flowering plants. That makes it octoploid. (It may be even ploidier than that when you take into account that the eudicots seem to have tripled their genomes shortly after evolving.) But in practice, and for reasons scientists don't entirely understand, the bladderwort has somehow deleted all but one copy of most of its duplicated genes, along with the vast majority of its non-protein coding DNA. Now *that's* efficiency.

The sacred lotus's full genetic sequence was published May 10. Lotus seems be the first plant to have split off from the rest of the eudicots, even prior to the early genome triplication I alluded to above. But it separately doubled its own genome sometime after. Suspiciously, the authors of the paper revealing its sequence report, the doubling seems to have taken place about 65 million years ago.

That is notable, of course, because it's right around the time our planet got the snot knocked out of it by the asteroid that bid sayonara to the dinosaurs -- but also to about 60% of plant species. During times of environmental stress, the authors note, plants that have duplicated their genomes seem to adapt and survive better. One might speculate that is thanks to the raw material that a second, superfluous set of genes provides natural selection for creating proteins with new functions.

Many other plant species seem to have doubled their genomes around the time of the K-T asteroid impact, the authors write, suggesting that whatever the conditions at the time were, polyploidy seems to have been a good survival strategy for plants. It was also an option far less available to animals, who, for this and probably many other reasons (they lack some plants' ability to make fortified resting structures and go dormant, for instance) suffered heavier losses. It's thought that perhaps 80% of Earth's animal species went extinct in the catastrophic aftermath of the impact.

References:

Otto S. & Whitton J. (2000). Polyploid Incidence and Evolution, Annual Review of Genetics, 34 401-437. DOI: 10.1146/annurev.genet.34.1.401

Ming R., VanBuren R., Liu Y., Yang M., Han Y., Li L.T., Zhang Q., Kim M.J., Schatz M.C. & Campbell M. & (2013). Genome of the long-living sacred lotus (Nelumbo nucifera Gaertn.), Genome Biology, 14 (5) R41. DOI: 10.1186/gb-2013-14-5-r41

Ibarra-Laclette E., Lyons E., Hernández-Guzmán G., Pérez-Torres C.A., Carretero-Paulet L., Chang T.H., Lan T., Welch A.J., Juárez M.J.A. & Simpson J. & (2013). Architecture and evolution of a minute plant genome, Nature, DOI: 10.1038/nature12132

Many other plant species seem to have doubled their genomes around the time of the K-T asteroid impact, suggesting that whatever the conditions at the time were, polyploidy seems to have been a good strategy.