A critical transition in leaf evolution facilitated the Cretaceous angiosperm revolution

Abstract

The revolutionary rise of broad-leaved (flowering) angiosperm plant species during the Cretaceous initiated a global ecological transformation towards modern biodiversity. Still, the mechanisms involved in this angiosperm radiation remain enigmatic. Here we show that the period of rapid angiosperm evolution initiated after the leaf interior (post venous) transport path length for water was reduced beyond the leaf interior transport path length for CO2 at a critical leaf vein density of 2.5–5 mm mm−2. Data and our modelling approaches indicate that surpassing this critical vein density was a pivotal moment in leaf evolution that enabled evolving angiosperms to profit from developing leaves with more and smaller stomata in terms of higher carbon returns from equal water loss. Surpassing the critical vein density may therefore have facilitated evolving angiosperms to develop leaves with higher gas exchange capacities required to adapt to the Cretaceous CO2 decline and outcompete previously dominant coniferous species in the upper canopy.

Apparent Overinvestment in Leaf Venation Relaxes Leaf Morphological Constraints on Photosynthesis in Arid Habitats

“…Hypostomatous leaves are more common at mesic locations in our study, where leaves also are thinner. The shorter pathways for water and CO 2 transport in thin leaves of mesic environments may favor the presence of stomata solely on the abaxial surface (de Boer et al, 2012). The close relationship between aridity and stomatal distribution challenges our ability to disentangle the effect of leaf type versus the specific adaption of leaf morphology to aridity as an underlying cause for the negative relationship between d x and d y .…”

“…Zwieniecki and Boyce (2014) observed that derived angiosperms achieve an optimal vein architecture (with d x :d y % 1) by combining high vein densities with relatively thin leaves. This specific leaf morphology is unique to angiosperms (Feild et al, 2011;de Boer et al, 2012) and allows high rates of transpiration and photosynthesis, owing to the short distances for postvenous water transport and subsequent high k leaf (Brodribb et al, 2007). Some gymnosperms also achieve optimal vein placement with a contrasting morphology that combines thick leaves with low vein densities, resulting in relatively long postvenous water transport distances and subsequently low k leaf .…”

Tectonic-driven climate change and the diversification of angiosperms

“…We favor an abiotic first-order context allowing angiosperm radiation by a global climate change driven by both a breakup of Pangea in Gondwana and Laurasia and the drift of the smaller land masses. It is in this new Cretaceous global context that novel functional traits, such as biological innovation with interaction with pollinating insects (7), ecological adaptation (15), morphological novelties with the symmetry of the flower (8), and ecophysiological innovations with evolution of densely veined leaves (10,35), have combined and collectively explain the evolutionary success of the angiosperms. Still, none of the local or global scale is exclusive, and both act in a pluralistic way because these biotic interactions may have driven a local-scale success of several radiations.…”

“…Their radiation was characterized by high and rapid diversification (3,4), high rates of speciation throughout the Cretaceous (5), and unprecedented ecological dominance. Most hypotheses to explain angiosperm radiation invoke biotic (instrinsic) factors, such as pollinating insects (6), coevolution with herbivorous insects (7), morphological novelties (8), or ecophysiological innovations (9)(10)(11) as well as macroevolutionary patterns (1). However, recent studies have shown that extrinsic influences combined with biotic factors may drive species diversity at the multimillion-year time scale (6,12), reviving the potential role of global climate change (13,14) on angiosperm radiation.…”

Mimicking how plants control CO2 influx: CO2 activation of ion current rectification in nanochannels

“…As shown in Figure 1a, during the photosynthesis of plants, CO 2 causes the reversible activation of anion channels. 25 The reaction of CO 2 , H 2 O and transmembrane proteins forms protons and bicarbonate under the catalysis of carbonic anhydrase, which causes a conformational change in transmembrane proteins. Hence, CO 2 is sensed by the plants to adjust the opening of these pores and induce anion transport from one side of the membrane to the other.…”