Stomatal responses to humidity, soil moisture and other factors that influence plant water status are critical drivers of photosynthesis, productivity, water yield, ecohydrology and climate forcing, ...yet we still lack a thorough mechanistic understanding of these responses. Here I review historical and recent advances in stomatal water relations. Clear evidence now implicates a metabolically mediated response to leaf water status (‘hydroactive feedback’) in stomatal responses to evaporative demand and soil drought, possibly involving abscisic acid production in leaves. Other hypothetical mechanisms involving vapor and heat transport within leaves may contribute to humidity, light and temperature responses, but require further theoretical clarification and experimental validation. Variation and dynamics in hydraulic conductance, particularly within leaves, may contribute to water status responses. Continuing research to fully resolve mechanisms of stomatal responses to water status should focus on several areas: validating and quantifying the mechanism of leaf-based hydroactive feedback, identifying where in leaves water status is actively sensed, clarifying the role of leaf vapor and energy transport in humidity and temperature responses, and verifying foundational but minimally replicated results of stomatal hydromechanics across species. Clarity on these matters promises to deliver modelers with a tractable and reliable mechanistic model of stomatal responses to water status.
Water movement from the xylem to stomata is poorly understood. There is still no consensus about whether apoplastic or symplastic pathways are more important, and recent work suggests vapour ...diffusion may also play a role. The objective of this study was to estimate the proportions of hydraulic conductance outside the bundle sheath contributed by apoplastic, symplastic and gas phase pathways, using a novel analytical framework based on measurable anatomical and biophysical parameters. The calculations presented here suggest that apoplastic pathways provide the majority of conductance outside the bundle sheath under most conditions, whereas symplastic pathways contribute only a small proportion. The contributions of apoplastic and gas phase pathways vary depending on several critical but poorly known or highly variable parameters namely, the effective Poiseuille radius for apoplastic bulk flow, the thickness of cell walls and vertical temperature gradients within the leaf. The gas phase conductance should increase strongly as the leaf centre becomes warmer than the epidermis – providing up to 44% of vertical water transport for a temperature gradient of 0.2 K. These results may help to explain how leaf water transport is influenced by light absorption, temperature and differences in leaf anatomy among species.
It is clear that stomata play a critical role in regulating water loss from terrestrial vegetation. What is not clear is how this regulation is achieved. Stomata appear to respond to perturbations of ...many aspects of the soil-plant-atmosphere hydraulic continuum, but there is little agreement regarding the mechanism (or mechanisms) by which stomata sense such perturbations. This review discusses feedback and feedforward mechanisms by which hydraulic perturbations are putatively transduced into stomatal movements, in relation to generic empirical features of those responses. It is argued that a metabolically mediated feedback response of stomatal guard cells to the water status in their immediate vicinity ('hydro-active local feed-back') remains the best explanation for many well-known features of hydraulically related stomatal behaviour, such as transient 'wrong-way' responses and the equivalence of hydraulic supply and demand as stomatal effectors. Furthermore, many curious phenomena that appear inconsistent with feedback, such as 'apparent feedforward' humidity responses and 'isohydric' behaviour (water potential homeostasis), are in fact expected to emerge from the juxtaposition of hydro-active local feedback and the well-known hysteretic and threshold-like effect of water potential on xylem hydraulic resistance.
Recent decades have been characterized by increasing temperatures worldwide, resulting in an exponential climb in vapor pressure deficit (VPD). VPD has been identified as an increasingly important ...driver of plant functioning in terrestrial biomes and has been established as a major contributor in recent drought-induced plant mortality independent of other drivers associated with climate change. Despite this, few studies have isolated the physiological response of plant functioning to high VPD, thus limiting our understanding and ability to predict future impacts on terrestrial ecosystems. An abundance of evidence suggests that stomatal conductance declines under high VPD and transpiration increases in most species up until a given VPD threshold, leading to a cascade of subsequent impacts including reduced photosynthesis and growth, and higher risks of carbon starvation and hydraulic failure. Incorporation of photosynthetic and hydraulic traits in ‘next-generation’ land-surface models has the greatest potential for improved prediction of VPD responses at the plant- and global-scale, and will yield more mechanistic simulations of plant responses to a changing climate. By providing a fully integrated framework and evaluation of the impacts of high VPD on plant function, improvements in forecasting and long-term projections of climate impacts can be made.
Summary
A surge of papers have reported low leaf vulnerability to xylem embolism during drought. Here, we focus on the less studied, and more sensitive, outside‐xylem leaf hydraulic responses to ...multiple internal and external conditions. Studies of 34 species have resolved substantial vulnerability to dehydration of the outside‐xylem pathways, and studies of leaf hydraulic responses to light also implicate dynamic outside‐xylem responses. Detailed experiments suggest these dynamic responses arise at least in part from strong control of radial water movement across the vein bundle sheath. While leaf xylem vulnerability may influence leaf and plant survival during extreme drought, outside‐xylem dynamic responses are important for the control and resilience of water transport and leaf water status for gas exchange and growth.
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) Koxis strongly enhanced by the proximity of veins to lower epidermis; and (8) Koxis strongly influenced by spongy mesophyll anatomy, decreasing with protoplast size and increasing with airspace fraction and cell wall thickness. Correlations between anatomy and Koxacross species sometimes diverged from predicted causal effects, demonstrating the need for integrative models to resolve causation. For example, (9) Koxwas 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.
Leaf dry mass per unit leaf area (LMA) is a central trait in ecology, but its anatomical and compositional basis has been unclear. An explicit mathematical and physical framework for quantifying the ...cell and tissue determinants of LMA will enable tests of their influence on species, communities and ecosystems. We present an approach to explaining LMA from the numbers, dimensions and mass densities of leaf cells and tissues, which provided unprecedented explanatory power for 11 broadleaved woody angiosperm species diverse in LMA (33–262 g m−2; R2 = 0.94; P < 0.001). Across these diverse species, and in a larger comparison of evergreen vs. deciduous angiosperms, high LMA resulted principally from larger cell sizes, greater major vein allocation, greater numbers of mesophyll cell layers and higher cell mass densities. This explicit approach enables relating leaf anatomy and composition to a wide range of processes in physiological, evolutionary, community and macroecology.
Abstract
Crop photosynthesis and yield are limited by slow photosynthetic induction in sunflecks. We quantified variation in induction kinetics across diverse genotypes of wheat for the first time. ...Following a preliminary study that hinted at wide variation in induction kinetics across 58 genotypes, we grew 10 genotypes with contrasting responses in a controlled environment and quantified induction kinetics of carboxylation capacity (Vcmax) from dynamic A versus ci curves after a shift from low to high light (from 50 µmol m-2 s-1 to 1500 µmol m-2 s-1), in five flag leaves per genotype. Within-genotype median time for 95% induction (t95) of Vcmax varied 1.8-fold, from 5.2 min to 9.5 min. Our simulations suggest that non-instantaneous induction reduces daily net carbon gain by up to 15%, and that breeding to speed up Vcmax induction in the slowest of our 10 genotypes to match that in the fastest genotype could increase daily net carbon gain by up to 3.4%, particularly for leaves in mid-canopy positions (cumulative leaf area index ≤1.5 m2 m-2), those that experience predominantly short-duration sunflecks, and those with high photosynthetic capacities.
Significant variation exists in the induction time of photosynthesis following near-darkness to light transitions across wheat genotypes. Slow induction reduced daily carbon assimilation by up to 15%.
Abstract
Reduced stomatal conductance is a common plant response to rising atmospheric CO
2
and increases water use efficiency (
W
). At the leaf-scale,
W
depends on water and nitrogen availability ...in addition to atmospheric CO
2
. In hydroclimate models
W
is a key driver of rainfall, droughts, and streamflow extremes. We used global climate data to derive Aridity Indices (AI) for forests over the period 1965–2015 and synthesised those with data for nitrogen deposition and
W
derived from stable isotopes in tree rings. AI and atmospheric CO
2
account for most of the variance in
W
of trees across the globe, while cumulative nitrogen deposition has a significant effect only in regions without strong legacies of atmospheric pollution. The relation of aridity and
W
displays a clear discontinuity.
W
and AI are strongly related below a threshold value of AI ≈ 1 but are not related where AI > 1. Tree ring data emphasise that effective demarcation of water-limited from non-water-limited behaviour of stomata is critical to improving hydrological models that operate at regional to global scales.
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