Leaf Maximum Photosynthetic Rate and Venation Are Linked by Hydraulics

Abstract

Leaf veins are almost ubiquitous across the range of terrestrial plant diversity, yet their influence on leaf photosynthetic performance remains uncertain. We show here that specific physical attributes of the vascular plumbing network are key limiters of the hydraulic and photosynthetic proficiency of any leaf. Following the logic that leaf veins evolved to bypass inefficient water transport through living mesophyll tissue, we examined the hydraulic pathway beyond the distal ends of the vein system as a possible limiter of water transport in leaves. We tested a mechanistic hypothesis that the length of this final traverse, as water moves from veins across the mesophyll to where it evaporates from the leaf, governs the hydraulic efficiency and photosynthetic carbon assimilation of any leaf. Sampling 43 species across the breadth of plant diversity from mosses to flowering plants, we found that the post-vein traverse as determined by characters such as vein density, leaf thickness, and cell shape, was strongly correlated with the hydraulic conductivity and maximum photosynthetic rate of foliage. The shape of this correlation provided clear support for the a priori hypothesis that vein positioning limits photosynthesis via its influence on leaf hydraulic efficiency.Leaves have sustained virtually all terrestrial ecosystems over the last 400 million years (Kenrick and Crane, 1991;Boyce et al., 2002;Boyce, 2005). Over this period land plants have evolved an enormous diversity of leaf structure; diversity that marks phylogenetic relations among clades and constrains the functional performance and climatic associations of plant species

Developmentally based scaling of leaf venation architecture explains global ecological patterns

“…Finally, Price et al 14 proposed that vein density should be independent from leaf size, because a constrained distance between the minor veins and thus a high vein density is needed for water and sugar transport. This idea comes from physiological studies that showed such an importance of high vein density but also adaptive variation across species 4,43,[51][52][53] . Indeed, we found here a considerably higher and more variable range of values for total vein density (Fig.…”

Weak coordination among petiole, leaf, vein, and gas‐exchange traits across Australian angiosperm species and its possible implications

“…2007; Brodribb and Jordan 2008). So why should these relationships break down within the subset of evergreen angiosperms examined here?…”

“…2004; Brodribb et al. 2007; Brodribb and Jordan 2008, 2011). It is also possible that gas exchange measurements made in the field may not align with maximal hydraulic capacity if the water potential of the xylem at the time of measurement was sufficiently low to engender significant loss of conductance.…”

“…It is also supported by strong correlations between hydraulic conductance measured within the leaf and rates of gas exchange across diverse taxa (Brodribb et al. 2007; Brodribb and Jordan 2008), but also within a single species (Brodribb and Jordan 2011). In contrast, other studies have found poor coordination between these traits (angiosperms in Brodribb and Holbrook 2006; Maherali et al.…”

“…This is because more numerous and efficient leaf veins reduce the distance liquid water must travel from vein endings to the points of evaporation within the leaf lamina, wherever that is presumed to be (Brodribb et al. 2007; Noblin et al. 2008; Zwieniecki and Boyce 2014), although this relationship is likely shifted by leaf thickness (Noblin et al.…”