With ‘Downsized’ DNA, Flowering Plants Took Over the World

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When people consider evolutionary events related to the origin and diversification of new species and groups, they tend to emphasize novel adaptations — specific genes giving rise to new, beneficial traits. But a growing body of research suggests that in some cases, that deciding factor may be something much more fundamental: size. In a paper published today in PLOS Biology, a pair of researchers studying the angiosperms, or flowering plants, has named genome size as the limiting constraint in their evolution.

The success of flowering plants, a group that includes everything from orchids and tulips to grasses and wheat, represents a long-standing puzzle for biologists. (In an 1879 letter to the renowned botanist Joseph Dalton Hooker, Charles Darwin called it an “abominable mystery.”) Terrestrial plants first appeared nearly half a billion years ago, but flowering plants arose only in the past 100 million years, beginning in the Cretaceous period. Yet, once angiosperms emerged, their structural and functional diversity exploded — far outpacing the diversification and spread of the other major plant groups, the gymnosperms (including conifers) and ferns.

Today, the 350,000 flowering-plant species, which have flourished in the vast majority of environments on Earth, constitute 90 percent of all plants on land. Since Darwin’s time, biologists pursuing the answer to that abominable mystery have sought to explain how the flowering plants could possibly have achieved this level of dominance in such a relatively short time.

Perhaps the answer has been so elusive because those scientists have usually focused on the physiological traits that set the angiosperms apart from their relatives. In the PLOS Biology paper, however, Kevin Simonin, a plant biologist at San Francisco State University, and Adam Roddy, a postdoctoral fellow at Yale University, argue that it’s the genome sizes underlying those individual adaptations that really matter.

The Advantages of Genome Downsizing

Species diverge hugely in genome size, without respect to the organisms’ complexity; in an oft-cited example, the onion has five times as much DNA as humans do. In the new study, Simonin and Roddy demonstrated what that variability in genome size means for large-scale biodiversity. They compiled vast amounts of data on genome size, cell size, cell density and photosynthetic rate for hundreds of angiosperms, ferns and gymnosperms, then traced the correlations among those traits back through time to weave a cohesive evolutionary narrative.

The emergence of angiosperms was marked by many events in which lineages of plants duplicated their whole genome. This process opened a door for greater diversification because the extra copies of genes could evolve and take on new functions. But because carrying so much genetic material can also be physiologically taxing, natural selection typically followed up these duplication events by aggressively pruning unneeded sequences. This “genome downsizing” often left flowering plants with less DNA than their parent species had. In fact, by following the family trees of the flowering plants back to their base, researchers have determined that the very first angiosperms had small genomes. “We now know that this not only contributed to their diversity, but may have given angiosperms the metabolic advantage to outcompete the other plant groups,” Simonin said.

He and Roddy posited that angiosperms’ small genomes set off a cascade of effects that over time flowed from their physiology into their structure and ultimately into their ecological role. Less DNA made it possible for the flowering plants to build their leaves from smaller cells, which in turn allowed them to pack more of certain cell types into the same volume. They could therefore have a higher density of stomata — the pores that facilitate the intake of carbon dioxide from the air and the release of water vapor — and a higher density of veins to provide enough water to keep those pores open. And the flowering plants did not have to sacrifice a high density of photosynthetic cells to achieve these benefits.

As a result, flowering plants could turn sunlight into sugars through photosynthesis much more efficiently. The rise of their superior capacity for hydration and gas exchange also coincided with falling levels of atmospheric carbon dioxide during the Cretaceous period, which contributed further to the angiosperms’ competitive edge over their green-plant peers. According to Simonin and Roddy, phylogenetic evidence shows that changes in genome size and the relevant physiological traits occurred together.



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