Genome downsizing drove physiological novelty and the rise of the flowering plants

Background/Question/Methods

The sudden origin and relatively rapid diversification of flowering plants during the mid-Cretaceous, and their rise to dominance globally, has long been considered an ‘abominable mystery’. Flowering plants are a dominate presence in most terrestrial ecosystems and many hypotthesies have been presented to explain this overall success. Common among these is the idea that angiosperms developed a set of physiological traits that allowed them to achieve higher rates of primary productivity in order to outcompete the ferns and gymnosperms that dominated ecosystems previously. Speifically, angiosperms unlike the other major clades of terestrial plants were able to develop leaves with smaller, densley packed stomata and highly brached venation networks which together enable higher rates of transpiraiton, carbon assimilation and growth. Yet, why angiosperms were able to develop these leaf traits is unknown but linked, we predict, to biophysical limitations on cell size. Both theory and empirical data suggest that the upper limit of leaf surface conductance to CO₂ and water vapor is tightly coupled to limitations on minimum cell size. While numerous environmental and physiological factors can influence the final sizes of eukaryotic cells, the minimum size of cells and the rate of their production are strongly constrained by nuclear volume, more commonly measured as genome size. We compiled data for guard cell length (l_g), stomatal density (D_s), vein density (D_v) and genome size from the literature. In total our data set consists of ~1100 species of vascular plants of which 979 are angiosperms, 54 gymnosperms and 54 ferns. For each species in our database that possesed data for l_g, D_s and D_v we calculated maximum potential stomatal conductance (g_{s, max}) and operational stomatal conductance (g_{s, op}).

Results/Conclusions

Our results provide strong evidence that across the major clades of terrestrial plants the ability to develop leaves with high stomatal and vein densities is fundamentally linked to biophysical constraints on minimum cell size. Taken together our data, in combination with analyses of trait evolution, suggest that genome downsizing among the angiosperms was necessary for the development of leaves that permit higher rates of gas exchange and overall higher rates of primary productivity. By reducing minimum cell size, genome downsizing brings g_{s, op} closer to g_{s, max} and thus brings actual primary productivity closer to its maximum potential. If greater competitive ability among the angiosperms drove their ecological dominance, then genome downsizing which reduces minimum cell size is critical to this transformative process.