Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms

Abstract

Summary• Hydraulic dysfunction in leaves determines key aspects of whole-plant responses to water stress; however, our understanding of the physiology of hydraulic dysfunction and its relationships to leaf structure and ecological strategy remains incomplete.• Here, we studied a morphologically and ecologically diverse sample of angiosperms to test whether the water potential inducing a 50% loss in leaf hydraulic conductance (P50 leaf ) is predicted by properties of leaf xylem relating to water tension-induced conduit collapse. We also assessed the relationships between P50 leaf and other traits considered to reflect drought resistance and ecological strategy.• Across species, P50 leaf was strongly correlated with a theoretical predictor of vulnerability to cell collapse in minor veins (the cubed ratio of the conduit wall thickness to the conduit lumen breadth). P50 leaf was also correlated with mesophyll traits known to be related to drought resistance, but unrelated to traits associated with carbon economy.• Our data indicate a link between the structural mechanics of leaf xylem and hydraulic function under water stress. Although it is possible that collapse may contribute directly to dysfunction, this relationship may also be a secondary product of vascular economics, suggesting that leaf xylem is dimensioned to avoid wall collapse.

Reversible Leaf Xylem Collapse: A Potential “Circuit Breaker” against Cavitation

“…Conduit deformation has been observed in tracheids of conifer leaves, most notably in transfusion tracheids, which supply water laterally from the vein to the photosynthetic cells (Cochard et al, 2004a;Brodribb and Holbrook, 2005;Zhang et al, 2014). In angiosperms, leaf xylem conduit thickness-to-span ratios (thought to be predictive of collapse) have been shown to correlate with resistance to the loss of hydraulic conductance as xylem tensions increase (Blackman et al, 2010), but no previous study has addressed whether xylem conduits in angiosperm leaves collapse as leaf water potentials (C L ) decline.Plants avoid negative pressures that cause cavitation by closing their stomata. But in angiosperms, the regulation of transpiration is complicated by a stomatal mechanism in which the achievement of large apertures, and thus high surface conductances, involves not just the swelling of guard cells but also the shrinkage of subsidiary cells (Franks and Farquhar, 2007).…”

Partitioning hydraulic resistance in Sorghum bicolor leaves reveals unique correlations with stomatal conductance during drought

“…The hydraulic resistance of the whole leaf (r * Leaf ) is tightly correlated with maximum rates of gas exchange across a broad range of species (Brodribb et al 2007), but also changes temporally in response to leaf hydration status (Brodribb and Holbrook 2003;Kim and Steudle 2007;Heinen et al 2009) and incident light Scoffoni et al 2008). These temporal responses of r * Leaf can be mediated through cavitation events within the leaf xylem Trifilò et al 2003;Johnson et al 2012), cell collapse of the xylem elements (Cochard et al 2004a;Brodribb and Holbrook 2005;Blackman et al 2010) or changes in aquaporin regulation after water leaves the vasculature (Cochard et al 2007). Taken together, these results illustrate the varying function of individual components of r * Leaf on the rates of leaf gas exchange.…”

“…Under this scenario, high r * OLV in leaves may facilitate whole-plant water conservation despite the hydraulic architecture of the remainder of the plant. The ability to tolerate low soil moisture and low leaf water potentials would be more important in xeric systems, and likely reflects characteristics of the individual vessel elements that limit cavitation (Wheeler et al 2005;Hacke et al 2006;Blackman et al 2010) and major vein density (Scoffoni et al 2011). Investigating how leaf resistances are partitioned in a widely distributed group of grasses would provide new insights into how leaf resistances contribute to plant distributions across the landscape.…”

Sap flow in response to rainfall pulses for two shrub species in the semiarid Chinese Loess Plateau

“…Therefore, the planted shrubs will be forced to endure repetitive cycles of water scarcity followed by rainfall response (Burgess, 2006;Eberbach and Burrows, 2006). Understanding the mechanisms that underlie the responses of the planted shrubs to rainfall is a key problem in studies of the responses of semi-arid ecosystems with vegetation restoration to global climate change (Blackman and Brodribb, 2011;Blackman et al, 2010;Fravolini et al, 2005;Ivans et al, 2006;Potts et al, 2006;Sponseller, 2007).…”