Abstract
The abrupt origin and rapid diversification of the flowering plants during the Cretaceous has long been considered an “abominable mystery.” While the cause of their high diversity has been attributed largely to coevolution with pollinators and herbivores, their ability to outcompete the previously dominant ferns and gymnosperms has been the subject of many hypotheses. Common among these is that the angiosperms alone developed leaves with smaller, more numerous stomata and more highly branching venation networks that enable higher rates of transpiration, photosynthesis, and growth. Yet, how angiosperms pack their leaves with smaller, more abundant stomata and more veins is unknown but linked—we show—to simple biophysical constraints on cell size. Only angiosperm lineages underwent rapid genome downsizing during the early Cretaceous period, which facilitated the reductions in cell size necessary to pack more veins and stomata into their leaves, effectively bringing actual primary productivity closer to its maximum potential. Thus, the angiosperms' heightened competitive abilities are due in no small part to genome downsizing.
Highlights
The flowering plants are highly competitive in almost every terrestrial ecosystem, and their rapid rise during the early Cretaceous period irrevocably altered terrestrial primary productivity and global climate [1,2,3]
Prevailing hypotheses have suggested that the angiosperms rose to dominance through an increase in their maximum potential photosynthesis and whole-plant carbon gain, allowing them to outcompete the ferns and gymnosperms that had previously dominated terrestrial ecosystems
Using a combination of anatomy, cytology, and modelling of liquid water transport and CO2 exchange between leaves and the atmosphere, we provide strong evidence that the success and rapid spread of flowering plants around the world was the result of genome downsizing
Summary
The flowering plants are highly competitive in almost every terrestrial ecosystem, and their rapid rise during the early Cretaceous period irrevocably altered terrestrial primary productivity and global climate [1,2,3]. Terrestrial primary productivity is determined by the photosynthetic capacity of leaves. The primary enzyme in photosynthesis, rubisco, functions poorly when CO2 is limiting, which requires leaf intercellular CO2 concentrations (ci) to be maintained within a narrow range [4] through adjustments in leaf surface conductance to CO2 and water vapor. This surface conductance is one of the greatest biophysical limitations on photosynthetic rates across all terrestrial plants [5,6]. As a consequence, increasing leaf surface conductance to CO2 requires increasing rates of leaf water transport in order to avoid desiccation [7]
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