Decoding stomatal characteristics regulating water use efficiency at leaf and plant scales in rice genotypes.

MAIN CONCLUSION: Stomatal traits in rice genotypes affect water use efficiency. Low-frequency small-size stomata correlate with whole plant efficiency, while low-frequency large-size stomata show intrinsic efficiency and responsiveness to vapour pressure deficit. Leaf surface and the patterning of the epidermal layer play a vital role in determining plant growth. While the surface helps in determining radiation interception, epidermal pattern of stomatal factors strongly regulate gas exchange and water use efficiency (WUE). This study focuses on identifying distinct stomatal traits among rice genotypes to comprehend their influence on WUE. Stomatal frequency ranged from 353 to 687 per mm2 and the size varied between 128.31 and 339.01 µm2 among 150 rice germplasm with significant variability in abaxial and adaxial surfaces. The cumulative water transpired and WUE determined at the outdoor phenomics platform, over the entire crop growth period as well as during specific hours of a 24 h-day did not correlate with stomatal frequency nor size. However, genotypes with low-frequency and large-size stomata recorded higher intrinsic water use efficiency (67.04 µmol CO2 mol-1 H2O) and showed a quicker response to varying vapour pressure deficit that diurnally ranged between 0.03 and 2.17 kPa. The study demonstrated the role of stomatal factors in determining physiological subcomponents of WUE both at single leaf and whole plant levels. Differential expression patterns of stomatal regulatory genes among the contrasting groups explained variations in the epidermal patterning. Increased expression of ERECTA, TMM and YODA genes appear to contribute to decreased stomatal frequency in low stomatal frequency genotypes. These findings underscore the significance of stomatal traits in breeding programs and strongly support the importance of these genes that govern variability in stomatal architecture in future crop improvement programs.

Coping with extremes: Responses of Quercus robur L. and Fagus sylvatica L. to soil drought and elevated vapour pressure deficit.

Climate change, particularly droughts and heat waves, significantly impacts global photosynthesis and forest ecosystem sustainability. To understand how trees respond to and recover from hydrological stress, we investigated the combined effects of soil moisture and atmospheric vapour pressure deficit (VPD) on seedlings of the two major European broadleaved tree species Fagus sylvatica (FS) and Quercus robur (QR). The experiment was conducted under natural forest gap conditions, while soil water availability was strictly manipulated. We monitored gas exchange (net photosynthesis, stomatal conductance and transpiration rates), nonstructural carbohydrates (NSC) concentration in roots and stomatal morphometry (size and density) during a drought period and recovery. Our comparative empirical study allowed us to distinguish and quantify the effects of soil drought and VPD on stomatal behavior, going beyond theoretical models. We found that QR conserved water more conservatively than FS by reducing transpiration and regulating stomatal conductance under drought. FS maintained higher stomatal conductance and transpiration at elevated VPD until soil moisture became critically low. QR showed higher intrinsic water use efficiency than FS. Stomata density and size also likely played a role in photosynthetic rate and speed of recovery, especially since QR with its seasonal adjustments in stomatal traits (smaller, more numerous stomata in summer leaves) responded and recovered faster compared to FS. Our focal species showed different responses in NSC content under drought stress and recovery, suggesting possible different evolutionary pathways in coping with stress. QR mobilized soluble sugars, while FS relied on starch mobilization to resist drought. Although our focal species often co-occur in mixed forests, our study showed that they have evolved different physiological, morphological and biochemical strategies to cope with drought stress. This suggests that ongoing climate change may alter their competitive ability and adaptive potential in favor of one of the species studied.

The multidimensionality of plant drought stress: The relative importance of edaphic and atmospheric drought.

Drought threatens plant growth and related ecosystem services. The emergence of plant drought stress under edaphic drought is well studied, whilst the importance of atmospheric drought only recently gained momentum. Yet, little is known about the interaction and relative contribution of edaphic and atmospheric drought on the emergence of plant drought stress. We conducted a gradient experiment, fully crossing gravimetric water content (GWC: maximum water holding capacity-permanent wilting point) and vapour pressure deficit (VPD: 1-2.25 kPa) using five wheat varieties from three species (Triticum monococcum, T. durum & T. aestivum). We quantified the occurrence of plant drought stress on molecular (abscisic acid), cellular (stomatal conductance), organ (leaf water potential) and stand level (evapotranspiration). Plant drought stress increased with decreasing GWC across all organizational levels. This effect was magnified nonlinearly by VPD after passing a critical threshold of soil water availability. At around 20%GWC (soil matric potential 0.012 MPa), plants lost their ability to regulate leaf water potential via stomata regulation, followed by the emergence of hydraulic dysfunction. The emergence of plant drought stress is characterized by changing relative contributions of soil versus atmosphere and their non-linear interaction. This highly non-linear response is likely to abruptly alter plant-related ecosystem services in a drying world.

Enhanced decreases in rice evapotranspiration in response to elevated atmospheric carbon dioxide under warmer environments.

A short period of exposure to elevated CO2 is known to decrease evapotranspiration via stomatal closure. Based on theoretical evaluation of a canopy transpiration model, we hypothesized that this decrease in the evapotranspiration of rice under elevated CO2 was greater under higher temperature conditions due to an increased sensitivity of transpiration to changes in CO2 induced by the greater vapour pressure deficit. In a temperature gradient chamber-based experiment, a 200 ppm increase in CO2 concentration led to 0.4 mm (-7%) and 1.5 mm (-15%) decreases in 12 h evapotranspiration under ambient temperature and high temperature (+3.7°C) conditions, respectively. Model simulations revealed that the greater vapour pressure deficit under higher temperature conditions explained the variations in the reduction of evapotranspiration observed under elevated CO2 levels between the temperature treatments. Our study suggests the utility of a simple modelling framework for mechanistic understanding of evapotranspiration and crop energy balance system under changing environmental conditions.

Impacts of elevated temperature and vapour pressure deficit on leaf gas exchange and plant growth across six tropical rainforest tree species.

Elevated air temperature (Tair) and vapour pressure deficit (VPDair) significantly influence plant functioning, yet their relative impacts are difficult to disentangle. We examined the effects of elevated Tair (+6°C) and VPDair (+0.7 kPa) on the growth and physiology of six tropical tree species. Saplings were grown under well-watered conditions in climate-controlled glasshouses for 6 months under three treatments: (1) low Tair and low VPDair, (2) high Tair and low VPDair, and (3) high Tair and high VPDair. To assess acclimation, physiological parameters were measured at a set temperature. Warm-grown plants grown under elevated VPDair had significantly reduced stomatal conductance and increased instantaneous water use efficiency compared to plants grown under low VPDair. Photosynthetic biochemistry and thermal tolerance (Tcrit) were unaffected by VPDair, but elevated Tair caused Jmax25 to decrease and Tcrit to increase. Sapling biomass accumulation for all species responded positively to an increase in Tair, but elevated VPDair limited growth. This study shows that stomatal limitation caused by even moderate increases in VPDair can decrease productivity and growth rates in tropical species independently from Tair and has important implications for modelling the impacts of climate change on tropical forests.

Stomatal response to VPD in C4 plants with different biochemical sub-pathways.

C4 NAD-malic enzyme (NAD-ME) species occurs in drier regions and exhibit different drought responses compared to C4 NADP-malic enzyme (NADP-ME) species. However, a physiological mechanism explaining the geographical discrepancies remains uncertain. This study examined gas exchange patterns that might explain different distributions observed between two subtypes of C4 photosynthesis. We measured the response of leaf gas exchange to vapour pressure deficit (VPD) and CO2 in plants from six distinct C4 clades having closely related NAD-ME and NADP-ME species using a Li-Cor 6400 gas exchange system. We found that NAD-ME species exhibited greater relative reductions in stomatal conductance with increases in VPD than NADP-ME species but observed no consistent subtype differences in C4 cycle activity as indicated by the initial slope of the A response to intercellular CO2 concentration. Based on these results, we hypothesise the greater response of gs to increasing VPD may enable NAD-ME plants to outperform NADP-ME plants in hot, dry environments where VPD is normally high.

The poorly-explored stomatal response to temperature at constant evaporative demand.

Changes in leaf temperature are known to drive stomatal responses, because the leaf-to-air water vapour gradient (Δw) increases with temperature if ambient vapour pressure is held constant, and stomata respond to changes in Δw. However, the direct response of stomata to temperature (DRST; the response when Δw is held constant by adjusting ambient humidity) has been examined far less extensively. Though the meagre available data suggest the response is usually positive, results differ widely and defy broad generalisation. As a result, little is known about the DRST. This review discusses the current state of knowledge about the DRST, including numerous hypothesised biophysical mechanisms, potential implications of the response for plant adaptation, and possible impacts of the DRST on plant-atmosphere carbon and water exchange in a changing climate.

Comparing Antoine parameter sources for accurate vapor pressure prediction across a range of temperatures.

Determining the vapor pressure of a substance at the relevant process temperature is a key component in conducting an exposure assessment to ascertain worker exposure. However, vapor pressure data at various temperatures relevant to the work environment is not readily available for many chemicals. The Antoine equation is a mathematical expression that relates temperature and vapor pressure. The objective of this analysis was to compare Antoine parameter data from 3 independent data sources; Hansen, Yaws, and Custom data and identify the source that generates the most accurate vapor pressure values with the least bias, relative to the referent data set from the CRC Handbook of Chemistry and Physics. Temperatures predicted from 3 different Antoine sources across a range of vapor pressures for 59 chemicals are compared to the reference source. The results show that temperatures predicted using Antoine parameters from the 3 sources are not statistically significantly different, indicating that all 3 sources could be useful. However, the Yaws dataset will be used in the SDM 2.0 because the data is readily available and robust.

The impacts of rising vapour pressure deficit in natural and managed ecosystems.

An exponential rise in the atmospheric vapour pressure deficit (VPD) is among the most consequential impacts of climate change in terrestrial ecosystems. Rising VPD has negative and cascading effects on nearly all aspects of plant function including photosynthesis, water status, growth and survival. These responses are exacerbated by land-atmosphere interactions that couple VPD to soil water and govern the evolution of drought, affecting a range of ecosystem services including carbon uptake, biodiversity, the provisioning of water resources and crop yields. However, despite the global nature of this phenomenon, research on how to incorporate these impacts into resilient management regimes is largely in its infancy, due in part to the entanglement of VPD trends with those of other co-evolving climate drivers. Here, we review the mechanistic bases of VPD impacts at a range of spatial scales, paying particular attention to the independent and interactive influence of VPD in the context of other environmental changes. We then evaluate the consequences of these impacts within key management contexts, including water resources, croplands, wildfire risk mitigation and management of natural grasslands and forests. We conclude with recommendations describing how management regimes could be altered to mitigate the otherwise highly deleterious consequences of rising VPD.

Impacts of elevated CO2 levels and temperature on photosynthesis and stomatal closure along an altitudinal gradient are counteracted by the rising atmospheric vapor pressure deficit.

The efficiency of water use in plants, a critical ecophysiological parameter closely related to water and carbon cycles, is essential for understanding the interactions between plants and their environment. This study investigates the effects of ongoing climate change and increasing atmospheric CO2 concentration on intrinsic (stomata-based; iWUE) and evaporative (transpiration-based; eWUE) water use efficiency in oak trees along a naturally small altitudinal gradient (130-630 m a.s.l.) of Vihorlat Mountains (eastern Slovakia, Central Europe). To assess changes in iWUE and eWUE values over the past 60 years (1961-2020), stable carbon isotope ratios in latewood cellulose (δ13Ccell) of annually resolved tree rings were analyzed. Such an approach was sensitive enough to distinguish tree responses to growth environments at different altitudes. Our findings revealed a rising trend in iWUE, particularly in oak trees at low and middle altitudes. However, this increase was negligible at high altitudes. Warmer and drier conditions at lower altitudes likely led to significant stomatal closure and enhanced efficiency in photosynthetic CO2 uptake due to rising CO2 concentration. Conversely, the increasing intracellular-to-ambient CO2 ratio (Ci/Ca) at higher altitudes indicated lower efficiency in photosynthetic CO2 uptake. In contrast to iWUE, eWUE showed no increasing trends over the last 60 years. This suggests that the positive impacts of elevated CO2 concentrations and temperature on photosynthesis and stomatal closure are counteracted by the rising atmospheric vapor pressure deficit (VPD). These differences underscore the importance of the correct interpretation of stomata-based and transpiration-based WUEs and highlight the necessity of atmospheric VPD correction when applying tree-ring δ13C-derived WUE at ecosystem and global levels.

Mechanical advantage makes stomatal opening speed a function of evaporative demand.

Stomatal opening in the light, observed in nearly all vascular land plants, is essential for providing access to atmospheric CO2 for photosynthesis. The speed of stomatal opening in the light is critical for maximizing carbon gain in environments in which light intensity changes, yet we have little understanding of how other environmental signals, particularly evaporative demand driven by vapor pressure deficit (VPD) influences the kinetics of this response. In angiosperms, and some fern species from the family Marsileaceae, a mechanical interaction between the guard cells and the epidermal cells determines the aperture of the pore. Here, we examine whether this mechanical interaction influences the speed of stomatal opening in the light. To test this, we investigated the speed of stomatal opening in response to light across a range of VPDs in seven plant species spanning the evolutionary diversity of guard cell and epidermal cell mechanical interactions. We found that stomatal opening speed is a function of evaporative demand in angiosperm species and Marsilea, which have guard cell and epidermal cell mechanical interactions. Stomatal opening speeds did not change across a range of VPD in species of gymnosperm and fern, which do not have guard cell mechanical interactions with the epidermis. We find that guard cell and epidermal cell mechanical interactions may play a key role in regulating stomatal responsiveness to light. These results provide valuable insight into the adaptive relevance of mechanical advantage.

Characterizing the breakpoint of stomatal response to vapor pressure deficit in an angiosperm.

Vapor pressure difference between the leaf and atmosphere (VPD) is the most important regulator of daytime transpiration, yet the mechanism driving stomatal responses to an increase in VPD in angiosperms remains unresolved. Here, we sought to characterize the mechanism driving stomatal closure at high VPD in an angiosperm species, particularly testing whether abscisic acid (ABA) biosynthesis could explain the observation of a trigger point for stomatal sensitivity to an increase in VPD. We tracked leaf gas exchange and modeled leaf water potential (Ψl) in leaves exposed to a range of step-increases in VPD in the herbaceous species Senecio minimus Poir. (Asteraceae). We found that mild increases in VPD in this species did not induce stomatal closure because modeled Ψl did not decline below a threshold close to turgor loss point (Ψtlp), but when leaves were exposed to a large increase in VPD, stomata closed as modeled Ψl declined below Ψtlp. Leaf ABA levels were higher in leaves exposed to a step-increase in VPD that caused Ψl to transiently decline below Ψtlp and in which stomata closed compared with leaves in which stomata did not close. We conclude that the stomata of S. minimus are insensitive to VPD until Ψl declines to a threshold that triggers the biosynthesis of ABA and that this mechanism might be common to angiosperms.

QSPR predicting the vapor pressure of pesticides into high/low volatility classes.

In this work, the vapor pressure of pesticides is employed as an indicator of their volatility potential. Quantitative Structure-Property Relationship models are established to predict the classification of compounds according to their volatility, into the high and low binary classes separated by the 1-mPa limit. A large dataset of 1005 structurally diverse pesticides with known experimental vapor pressure data at 20 °C is compiled from the publicly available Pesticide Properties DataBase (PPDB) and used for model development. The freely available PaDEL-Descriptor and ISIDA/Fragmentor molecular descriptor programs provide a large number of 19,947 non-conformational molecular descriptors that are analyzed through multivariable linear regressions and the Replacement Method technique. Through the selection of appropriate molecular descriptors of the substructure fragment type and the use of different standard classification metrics of model's quality, the classification of the structure-property relationship achieves acceptable results for discerning between the high and low volatility classes. Finally, an application of the obtained QSPR model is performed to predict the classes for 504 pesticides not having experimentally measured vapor pressures.

Warming-induced vapor pressure deficit suppression of vegetation growth diminished in northern peatlands.

Recent studies have reported worldwide vegetation suppression in response to increasing atmospheric vapor pressure deficit (VPD). Here, we integrate multisource datasets to show that increasing VPD caused by warming alone does not suppress vegetation growth in northern peatlands. A site-level manipulation experiment and a multiple-site synthesis find a neutral impact of rising VPD on vegetation growth; regional analysis manifests a strong declining gradient of VPD suppression impacts from sparsely distributed peatland to densely distributed peatland. The major mechanism adopted by plants in response to rising VPD is the "open" water-use strategy, where stomatal regulation is relaxed to maximize carbon uptake. These unique surface characteristics evolve in the wet soil‒air environment in the northern peatlands. The neutral VPD impacts observed in northern peatlands contrast with the vegetation suppression reported in global nonpeatland areas under rising VPD caused by concurrent warming and decreasing relative humidity, suggesting model improvement for representing VPD impacts in northern peatlands remains necessary.

Vapour pressure deficit modulates hydraulic function and structure of tropical rainforests under nonlimiting soil water supply.

Atmospheric conditions are expected to become warmer and drier in the future, but little is known about how evaporative demand influences forest structure and function independently from soil moisture availability, and how fast-response variables (such as canopy water potential and stomatal conductance) may mediate longer-term changes in forest structure and function in response to climate change. We used two tropical rainforest sites with different temperatures and vapour pressure deficits (VPD), but nonlimiting soil water supply, to assess the impact of evaporative demand on ecophysiological function and forest structure. Common species between sites allowed us to test the extent to which species composition, relative abundance and intraspecific variability contributed to site-level differences. The highest VPD site had lower midday canopy water potentials, canopy conductance (gc ), annual transpiration, forest stature, and biomass, while the transpiration rate was less sensitive to changes in VPD; it also had different height-diameter allometry (accounting for 51% of the difference in biomass between sites) and higher plot-level wood density. Our findings suggest that increases in VPD, even in the absence of soil water limitation, influence fast-response variables, such as canopy water potentials and gc , potentially leading to longer-term changes in forest stature resulting in reductions in biomass.

Vapour pressure deficit was not a primary limiting factor for gas exchange in an irrigated, mature dryland Aleppo pine forest.

Climate change is often associated with increasing vapour pressure deficit (VPD) and changes in soil moisture (SM). While atmospheric and soil drying often co-occur, their differential effects on plant functioning and productivity remain uncertain. We investigated the divergent effects and underlying mechanisms of soil and atmospheric drought based on continuous, in situ measurements of branch gas exchange with automated chambers in a mature semiarid Aleppo pine forest. We investigated the response of control trees exposed to combined soil-atmospheric drought (low SM, high VPD) during the rainless Mediterranean summer and that of trees experimentally unconstrained by soil dryness (high SM; using supplementary dry season water supply) but subjected to atmospheric drought (high VPD). During the seasonal dry period, branch conductance (gbr ), transpiration rate (E) and net photosynthesis (Anet ) decreased in low-SM trees but greatly increased in high-SM trees. The response of E and gbr to the massive rise in VPD (to 7 kPa) was negative in low-SM trees and positive in high-SM trees. These observations were consistent with predictions based on a simple plant hydraulic model showing the importance of plant water potential in the gbr and E response to VPD. These results demonstrate that avoiding drought on the supply side (SM) and relying on plant hydraulic regulation constrains the effects of atmospheric drought (VPD) as a stressor on canopy gas exchange in mature pine trees under field conditions.

Expanding the applicability domain of QSPRs for predicting water solubility and vapor pressure of PFAS.

This work aimed to verify whether it is possible to extend the applicability domain (AD) of existing QSPR (Quantitative Structure-Property Relationship) models by employing a strategy involving additional quantum-chemical calculations. We selected two published QSPR models: for water solubility, logSW, and vapor pressure, logVP of PFAS as case studies. We aimed to enlarge set of compounds used to build the model by applying factorial planning to plan the augmentation of the set of these compounds based on their structural features (descriptors). Next, we used the COSMO-RS model to calculate the logSW and logVP for selected chemicals. This allowed filling gaps in the experimental data for further training QSPR models. We improved the published models by significantly extending number of compounds for which theoretical predictions are reliable (i.e., extending the AD). Additionally, we performed external validation that had not been carried out in original models. To test effectiveness of the AD extension, we screened 4519 PFAS from NORMAN Database. The number of compounds outside the domain was reduced comparing the original model for both properties. Our work shows that combining physics-based methods with data-driven models can significantly improve the performance of predictions of phys-chem properties relevant for the chemical risk assessment.

Disentangling the effects of vapor pressure deficit on northern terrestrial vegetation productivity.

The impact of atmospheric vapor pressure deficit (VPD) on plant photosynthesis has long been acknowledged, but large interactions with air temperature (T) and soil moisture (SM) still hinder a complete understanding of the influence of VPD on vegetation production across various climate zones. Here, we found a diverging response of productivity to VPD in the Northern Hemisphere by excluding interactive effects of VPD with T and SM. The interactions between VPD and T/SM not only offset the potential positive impact of warming on vegetation productivity but also amplifies the negative effect of soil drying. Notably, for high-latitude ecosystems, there occurs a pronounced shift in vegetation productivity's response to VPD during the growing season when VPD surpasses a threshold of 3.5 to 4.0 hectopascals. These results yield previously unknown insights into the role of VPD in terrestrial ecosystems and enhance our comprehension of the terrestrial carbon cycle's response to global warming.

Global water use efficiency saturation due to increased vapor pressure deficit.

The ratio of carbon assimilation to water evapotranspiration (ET) of an ecosystem, referred to as ecosystem water use efficiency (WUEeco), is widely expected to increase because of the rising atmospheric carbon dioxide concentration (Ca). However, little is known about the interactive effects of rising Ca and climate change on WUEeco. On the basis of upscaled estimates from machine learning methods and global FLUXNET observations, we show that global WUEeco has not risen since 2001 because of the asymmetric effects of an increased vapor pressure deficit (VPD), which depressed photosynthesis and enhanced ET. An undiminished ET trend indicates that rising temperature and VPD may play a more important role in regulating ET than declining stomatal conductance. Projected increases in VPD are predicted to affect the future coupling of the terrestrial carbon and water cycles.