Leaf shrinkage with dehydration: coordination with hydraulic vulnerability and drought tolerance.

Christine Scoffoni,Steven Diep,Lawren Sack,Hervé Cochard,Christine Vuong

doi:10.1104/pp.113.221424

Abstract

Leaf shrinkage with dehydration has attracted attention for over 100 years, especially as it becomes visibly extreme during drought. However, little has been known of its correlation with physiology. Computer simulations of the leaf hydraulic system showed that a reduction of hydraulic conductance of the mesophyll pathways outside the xylem would cause a strong decline of leaf hydraulic conductance (K(leaf)). For 14 diverse species, we tested the hypothesis that shrinkage during dehydration (i.e. in whole leaf, cell and airspace thickness, and leaf area) is associated with reduction in K(leaf) at declining leaf water potential (Ψ(leaf)). We tested hypotheses for the linkage of leaf shrinkage with structural and physiological water relations parameters, including modulus of elasticity, osmotic pressure at full turgor, turgor loss point (TLP), and cuticular conductance. Species originating from moist habitats showed substantial shrinkage during dehydration before reaching TLP, in contrast with species originating from dry habitats. Across species, the decline of K(leaf) with mild dehydration (i.e. the initial slope of the K(leaf) versus Ψ(leaf) curve) correlated with the decline of leaf thickness (the slope of the leaf thickness versus Ψ(leaf) curve), as expected based on predictions from computer simulations. Leaf thickness shrinkage before TLP correlated across species with lower modulus of elasticity and with less negative osmotic pressure at full turgor, as did leaf area shrinkage between full turgor and oven desiccation. These findings point to a role for leaf shrinkage in hydraulic decline during mild dehydration, with potential impacts on drought adaptation for cells and leaves, influencing plant ecological distributions.

Highlights

Leaf shrinkage with dehydration has attracted attention for over 100 years, especially as it becomes visibly extreme during drought
2001; Cochard et al, 2004a; Johnson et al, 2009), and computer modeling and experimental work showed that species with high major vein length per leaf area (VLA; i.e. for the first three vein-branching orders) were more resistant to hydraulic decline, providing more pathways around embolisms (Scoffoni et al, 2011)
There was less difference across simulations in the P50 values (Table I). These findings indicated a strong impact of reduction in mesophyll hydraulic conductance on Kleaf vulnerability, especially at high water potentials, with more pronounced effects of xylem embolism on Kleaf vulnerability under stronger dehydration (Fig. 2; Table I)

Summary

Introduction

Leaf shrinkage with dehydration has attracted attention for over 100 years, especially as it becomes visibly extreme during drought. Leaf thickness shrinkage before TLP correlated across species with lower modulus of elasticity and with less negative osmotic pressure at full turgor, as did leaf area shrinkage between full turgor and oven desiccation These findings point to a role for leaf shrinkage in hydraulic decline during mild dehydration, with potential impacts on drought adaptation for cells and leaves, influencing plant ecological distributions. Before the bulk leaf turgor loss point (TLP; leaf water potential [Cleaf] at TLP) is reached, the slope of leaf thickness versus Cleaf or relative water content (RWC) is shallower than past TLP for most species (Meidner, 1955, Kennedy and Booth, 1958, Burquez, 1987, McBurney, 1992, Sancho-Knapik et al, 2010, 2011) This is because before TLP, declining Cleaf is strongly driven by declines in turgor pressure, which have a relatively low impact on cell and airspace volume, whereas past the TLP, declining Cleaf depends only on solute concentration, which increases in inverse proportion as cell water volume declines while airspaces may shrink or expand (Tyree and Hammel, 1972, Sancho-Knapik et al, 2011). Such an association would arise if, across species, shrinkage occurred simultaneously with vein xylem embolism or if tissue shrinkage led to declines in the extraxylem hydraulic conductance

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