Christine Scoffoni

The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta‐analysis

Increasing drought is one of the most critical challenges facing species and ecosystems worldwide, and improved theory and practices are needed for quantification of species tolerances. Leaf water potential at turgor loss, or wilting (π(tlp) ), is classically recognised as a major physiological determinant of plant water stress response. However, the cellular basis of π(tlp) and its importance for predicting ecological drought tolerance have been controversial. A meta-analysis of 317 species from 72 studies showed that π(tlp) was strongly correlated with water availability within and across biomes, indicating power for anticipating drought responses. We derived new equations giving both π(tlp) and relative water content at turgor loss point (RWC(tlp) ) as explicit functions of osmotic potential at full turgor (π(o) ) and bulk modulus of elasticity (ε). Sensitivity analyses and meta-analyses showed that π(o) is the major driver of π(tlp) . In contrast, ε plays no direct role in driving drought tolerance within or across species, but sclerophylly and elastic adjustments act to maintain RWC(tlp,) preventing cell dehydration, and additionally protect against nutrient, mechanical and herbivory stresses independent of drought tolerance. These findings clarify biogeographic trends and the underlying basis of drought tolerance parameters with applications in comparative assessments of species and ecosystems worldwide.

Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future

The design and function of leaf venation are important to plant performance, with key implications for the distribution and productivity of ecosystems, and applications in paleobiology, agriculture and technology. We synthesize classical concepts and the recent literature on a wide range of aspects of leaf venation. We describe 10 major structural features that contribute to multiple key functions, and scale up to leaf and plant performance. We describe the development and plasticity of leaf venation and its adaptation across environments globally, and a new global data compilation indicating trends relating vein length per unit area to climate, growth form and habitat worldwide. We synthesize the evolution of vein traits in the major plant lineages throughout paleohistory, highlighting the multiple origins of individual traits. We summarize the strikingly diverse current applications of leaf vein research in multiple fields of science and industry. A unified core understanding will enable an increasing range of plant biologists to incorporate leaf venation into their research.

Decline of Leaf Hydraulic Conductance with Dehydration: Relationship to Leaf Size and Venation Architecture

Across plant species, leaves vary enormously in their size and their venation architecture, of which one major function is to replace water lost to transpiration. The leaf hydraulic conductance (Kleaf) represents the capacity of the transport system to deliver water, allowing stomata to remain open for photosynthesis. Previous studies showed that Kleaf relates to vein density (vein length per area). Additionally, venation architecture determines the sensitivity of Kleaf to damage; severing the midrib caused Kleaf and gas exchange to decline, with lesser impacts in leaves with higher major vein density that provided more numerous water flow pathways around the damaged vein. Because xylem embolism during dehydration also reduces Kleaf, we hypothesized that higher major vein density would also reduce hydraulic vulnerability. Smaller leaves, which generally have higher major vein density, would thus have lower hydraulic vulnerability. Tests using simulations with a spatially explicit model confirmed that smaller leaves with higher major vein density were more tolerant of major vein embolism. Additionally, for 10 species ranging strongly in drought tolerance, hydraulic vulnerability, determined as the leaf water potential at 50% and 80% loss of Kleaf, was lower with greater major vein density and smaller leaf size (|r| = 0.85–0.90; P < 0.01). These relationships were independent of other aspects of physiological and morphological drought tolerance. These findings point to a new functional role of venation architecture and small leaf size in drought tolerance, potentially contributing to well-known biogeographic trends in leaf size.

Developmentally based scaling of leaf venation architecture explains global ecological patterns

Leaf size and venation show remarkable diversity across dicotyledons, and are key determinants of plant adaptation in ecosystems past and present. Here we present global scaling relationships of venation traits with leaf size. Across a new database for 485 globally distributed species, larger leaves had major veins of larger diameter, but lower length per leaf area, whereas minor vein traits were independent of leaf size. These scaling relationships allow estimation of intact leaf size from fragments, to improve hindcasting of past climate and biodiversity from fossil remains. The vein scaling relationships can be explained by a uniquely synthetic model for leaf anatomy and development derived from published data for numerous species. Vein scaling relationships can explain the global biogeographical trend for smaller leaves in drier areas, the greater construction cost of larger leaves and the ability of angiosperms to develop larger and more densely vascularised lamina to outcompete earlier-evolved plant lineages.

The rapid light response of leaf hydraulic conductance: new evidence from two experimental methods

Previous studies have shown a rapid enhancement in leaf hydraulic conductance (K(leaf)) from low to high irradiance (from <10 to >1000 micromol photons m(-2) s(-1)), using the high-pressure flow meter (HPFM), for 7 of 14 tested woody species. However, theoretical suggestions have been made that this response might arise as an artifact of the HPFM. We tested the K(leaf) light response for six evergreen species using refined versions of the rehydration kinetics method (RKM) and the evaporative flux method (EFM). We found new evidence for a rapid, 60% to 100% increase in K(leaf) from low to high irradiance for three species. In the RKM, the leaf rehydration time constant declined by up to 70% under high irradiance relative to darkness. In the EFM, under higher irradiance, the flow rate increased disproportionately to the water potential gradient. Combining our data with those of previous studies, we found that heterobaric species, i.e. those with bundle sheath extensions (BSEs) showed a twofold greater K(leaf) light response on average than homobaric species, i.e. those without BSEs. We suggest further research to characterize this substantial dynamic at the nexus of plant light- and water-relations.

Leaf Shrinkage with Dehydration: Coordination with Hydraulic Vulnerability and Drought Tolerance

Leaf shrinkage is a potential driver of leaf hydraulic vulnerability, especially under mild stress, and carries strong ecological implications. 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 (Kleaf). 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 Kleaf at declining leaf water potential (Ψleaf). 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 Kleaf with mild dehydration (i.e. the initial slope of the Kleaf versus Ψleaf curve) correlated with the decline of leaf thickness (the slope of the leaf thickness versus Ψleaf 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.

Combined impacts of irradiance and dehydration on leaf hydraulic conductance: insights into vulnerability and stomatal control

The leaf is a hydraulic bottleneck, accounting for a large part of plant resistance. Thus, the leaf hydraulic conductance (K(leaf) ) is of key importance in determining stomatal conductance (g(s) ) and rates of gas exchange. Previous studies showed that K(leaf) is dynamic with leaf water status and irradiance. For four species, we tested the combined impacts of these factors on K(leaf) and on g(s) . We determined responses of K(leaf) and g(s) to declining leaf water potential (Ψ(leaf) ) under low and high irradiance (<6 and >900 µmol photons m(-2) s(-1) photosynthetically active radiation, respectively). We hypothesized greater K(leaf) vulnerability under high irradiance. We also hypothesized that K(leaf) and g(s) would be similar in their responses to either light or dehydration: similar light-responses of K(leaf) and g(s) would stabilize Ψ(leaf) across irradiances for leaves transpiring at a given vapour pressure deficit, and similar dehydration responses would arise from the control of stomata by Ψ(leaf) or a correlated signal. For all four species, the K(leaf) light response declined from full hydration to turgor loss point. The K(leaf) and g(s) differed strongly in their light- and dehydration responses, supporting optimization of hydraulic transport across irradiances, and semi-independent, flexible regulation of liquid and vapour phase water transport with leaf water status.

Dynamics of leaf hydraulic conductance with water status: quantification and analysis of species differences under steady state

Leaf hydraulic conductance (Kleaf) is a major determinant of photosynthetic rate in well-watered and drought-stressed plants. Previous work assessed the decline of Kleaf with decreasing leaf water potential (Ψleaf), most typically using rehydration kinetics methods, and found that species varied in the shape of their vulnerability curve, and that hydraulic vulnerability correlated with other leaf functional traits and with drought sensitivity. These findings were tested and extended, using a new steady-state evaporative flux method under high irradiance, and the function for the vulnerability curve of each species was determined individually using maximum likelihood for 10 species varying strongly in drought tolerance. Additionally, the ability of excised leaves to recover in Kleaf with rehydration was assessed, and a new theoretical framework was developed to estimate how rehydration of measured leaves may affect estimation of hydraulic parameters. As hypothesized, species differed in their vulnerability function. Drought-tolerant species showed shallow linear declines and more negative Ψleaf at 80% loss of Kleaf (P80), whereas drought-sensitive species showed steeper, non-linear declines, and less negative P80. Across species, the maximum Kleaf was independent of hydraulic vulnerability. Recovery of Kleaf after 1 h rehydration of leaves dehydrated below their turgor loss point occurred only for four of 10 species. Across species without recovery, a more negative P80 correlated with the ability to maintain Kleaf through both dehydration and rehydration. These findings indicate that resistance to Kleaf decline is important not only in maintaining open stomata during the onset of drought, but also in enabling sustained function during drought recovery.

Leaf mesophyll conductance and leaf hydraulic conductance: an introduction to their measurement and coordination

Two highly contrasting variables summarizing the efficiency of transport of materials within the leaf are recognized as playing central roles in determining gas exchange and plant performance. This paper summarizes current approaches for the measurement of mesophyll conductance to CO2 (g m) and leaf hydraulic conductance (K leaf) and addresses the physiological integration of these parameters. First, the most common methods to determine g m and K leaf are summarized. Next, novel data compilation is analysed, which indicates that, across diverse species, g m is strongly linked with gas exchange parameters such as net CO2 assimilation (A area) and stomatal conductance (g s), and with K leaf, independently of leaf vein length per leaf area. Based on their parallel responses to a number of environmental variables, this review proposes that g m is linked to the outside-xylem but not to the xylem component of K leaf. Further, a mechanistic hypothesis is proposed to explain the interactions among all these and other physiological parameters. Finally, the possibility of estimating g m based on this hypothesis was tested using a regression analysis and a neurofuzzy logic approach. These approaches enabled the estimation of g m of given species from K leaf and leaf mass per area, providing a higher predictive power than from either parameter alone. The possibility of estimating g m from measured K leaf or vice-versa would result in a rapid increase in available data. Studies in which g m, K leaf, and leaf mass per area are simultaneously determined are needed in order to confirm and strengthen predictive and explanatory models for these parameters and importantly improve resolution of the integrated hydraulic-stomatal-photosynthetic system.

How Does Leaf Anatomy Influence Water Transport outside the Xylem

Anatomical data from diverse species, applied to a novel integrative model, elucidate the mechanistic basis of differences in water transport outside the xylem in leaves. Leaves are arguably the most complex and important physicobiological systems in the ecosphere. Yet, water transport outside the leaf xylem remains poorly understood, despite its impacts on stomatal function and photosynthesis. We applied anatomical measurements from 14 diverse species to a novel model of water flow in an areole (the smallest region bounded by minor veins) to predict the impact of anatomical variation across species on outside-xylem hydraulic conductance (Kox). Several predictions verified previous correlational studies: (1) vein length per unit area is the strongest anatomical determinant of Kox, due to effects on hydraulic pathlength and bundle sheath (BS) surface area; (2) palisade mesophyll remains well hydrated in hypostomatous species, which may benefit photosynthesis, (3) BS extensions enhance Kox; and (4) the upper and lower epidermis are hydraulically sequestered from one another despite their proximity. Our findings also provided novel insights: (5) the BS contributes a minority of outside-xylem resistance; (6) vapor transport contributes up to two-thirds of Kox; (7) Kox is strongly enhanced by the proximity of veins to lower epidermis; and (8) Kox is strongly influenced by spongy mesophyll anatomy, decreasing with protoplast size and increasing with airspace fraction and cell wall thickness. Correlations between anatomy and Kox across species sometimes diverged from predicted causal effects, demonstrating the need for integrative models to resolve causation. For example, (9) Kox was enhanced far more in heterobaric species than predicted by their having BS extensions. Our approach provides detailed insights into the role of anatomical variation in leaf function.