Biophysical constraints on the origin of leaves inferred from the fossil record

Abstract

The molecular tool kit for producing flat-bladed photosynthetic structures evolved in marine and terrestrial plants during the middle Paleozoic, but it took a further 20 million years before leaves suddenly spread throughout land floras. This delay has long been difficult to explain, given the apparent advantage of leaves for photosynthetic primary production. Theory and experiments predict that exceptionally high atmospheric CO 2 levels in the middle Paleozoic delayed the origin of leaves by restricting stomatal development. This would have limited evaporative cooling, leading to lethal overheating of leaves absorbing large quantities of solar energy. Here we test the central prediction of this argument with a morphometric analysis of 300 plant fossils from major European collections. We show a 25-fold enlargement of leaf blades in two phylogenetically independent clades as atmospheric CO 2 levels fell during the late Paleozoic. Furthermore, preliminary data suggest that the first abrupt increase in leaf size was accompanied by an 8-fold rise in stomatal density. These evolutionary patterns support the relaxation of biophysical constraints on leaf area predicted by theory and point to a significant role for CO 2 in plant evolution.

Developmentally based scaling of leaf venation architecture explains global ecological patterns

“…The developmental algorithm and scaling relationships we have shown makes this possible for dicotyledons, providing a strong ecological advantage. Dicotyledons can produce large leaves with both large major veins for mechanical support and high vein densities that enable transpirational cooling and high photosynthetic rates 1,[47][48][49] . Large simple leaves with high vein density are an angiosperm innovation, because the ongoing production of minor veins in expanding leaves depends on the plate meristem that is typically found only in angiosperms 18 .…”

Evolution of C 4 plants: a new hypothesis for an interaction of CO 2 and water relations mediated by plant hydraulics

“…Previously hypothesized modifications of the water transport system and associated plant features driven by low CO 2 include the evolution of xylem vessels and stomata [108], and the planate leaf [109,110] with high vein density [78]. These innovations permitted more rapid growth and diversification, leading to the succession of dominance from pteridophytes to gymnosperms to angiosperms [78,80,111,112].…”

Evolutionary context for understanding and manipulating plant responses to past, present and future atmospheric [CO 2 ]

“…The development of megaphyll leaves in multiple independent lineages was coincident with the transition from high to low [CO 2 ] during the Devonian and Carboniferous 400 -350 Ma [25,28]. As [CO 2 ] dropped, rates of A would have become increasingly limited by the resistance to diffusion of CO 2 from the atmosphere to the site of fixation by Rubisco.…”