Beyond source and sink control - toward an integrated approach to understand the carbon balance in plants.

A conceptual understanding on how the vegetation's carbon (C) balance is determined by source activity and sink demand is important to predict its C uptake and sequestration potential now and in the future. We have gathered trajectories of photosynthesis and growth as a function of environmental conditions described in the literature and compared them with current concepts of source and sink control. There is no clear evidence for pure source or sink control of the C balance, which contradicts recent hypotheses. Using model scenarios, we show how legacy effects via structural and functional traits and antecedent environmental conditions can alter the plant's carbon balance. We, thus, combined the concept of short-term source-sink coordination with long-term environmentally driven legacy effects that dynamically acclimate structural and functional traits over time. These acclimated traits feedback on the sensitivity of source and sink activity and thus change the plant physiological responses to environmental conditions. We postulate a whole plant C-coordination system that is primarily driven by stomatal optimization of growth to avoid a C source-sink mismatch. Therefore, we anticipate that C sequestration of forest ecosystems under future climate conditions will largely follow optimality principles that balance water and carbon resources to maximize growth in the long term.

Do stomata optimize turgor-driven growth? A new framework for integrating stomata response with whole-plant hydraulics and carbon balance.

Every existing optimal stomatal model uses photosynthetic carbon assimilation as a proxy for plant evolutionary fitness. However, assimilation and growth are often decoupled, making assimilation less ideal for representing fitness when optimizing stomatal conductance to water vapor and carbon dioxide. Instead, growth should be considered a closer proxy for fitness. We hypothesize stomata have evolved to maximize turgor-driven growth, instead of assimilation, over entire plants' lifetimes, improving their abilities to compete and reproduce. We develop a stomata model that dynamically maximizes whole-stem growth following principles from turgor-driven growth models. Stomata open to assimilate carbohydrates that supply growth and osmotically generate turgor, while stomata close to prevent losses of turgor and growth due to negative water potentials. In steady state, the growth optimization model captures realistic stomatal, growth, and carbohydrate responses to environmental cues, reconciles conflicting interpretations within existing stomatal optimization theories, and explains patterns of carbohydrate storage and xylem conductance observed during and after drought. Our growth optimization hypothesis introduces a new paradigm for stomatal optimization models, elevates the role of whole-plant carbon use and carbon storage in stomatal functioning, and has the potential to simultaneously predict gross productivity, net productivity, and plant mortality through a single, consistent modeling framework.

Short-term variation in leaf-level water use efficiency in a tropical forest.

The representation of stomatal regulation of transpiration and CO2 assimilation is key to forecasting terrestrial ecosystem responses to global change. Given its importance in determining the relationship between forest productivity and climate, accurate and mechanistic model representation of the relationship between stomatal conductance (gs ) and assimilation is crucial. We assess possible physiological and mechanistic controls on the estimation of the g1 (stomatal slope, inversely proportional to water use efficiency) and g0 (stomatal intercept) parameters, using diurnal gas exchange surveys and leaf-level response curves of six tropical broadleaf evergreen tree species. g1 estimated from ex situ response curves averaged 50% less than g1 estimated from survey data. While g0 and g1 varied between leaves of different phenological stages, the trend was not consistent among species. We identified a diurnal trend associated with g1 and g0 that significantly improved model projections of diurnal trends in transpiration. The accuracy of modeled gs can be improved by accounting for variation in stomatal behavior across diurnal periods, and between measurement approaches, rather than focusing on phenological variation in stomatal behavior. Additional investigation into the primary mechanisms responsible for diurnal variation in g1 will be required to account for this phenomenon in land-surface models.

Maximizing leaf carbon gain in varying saline conditions: An optimization model with dynamic mesophyll conductance.

While the adverse effects of elevated salinity levels on leaf gas exchange in many crops are not in dispute, representing such effects on leaf photosynthetic rates (A) continues to draw research attention. Here, an optimization model for stomatal conductance (gc ) that maximizes A while accounting for mesophyll conductance (gm ) was used to interpret new leaf gas exchange measurements collected for five irrigation water salinity levels. A function between chloroplastic CO2 concentration (cc ) and intercellular CO2 concentration (ci ) modified by salinity stress to estimate gm was proposed. Results showed that with increased salinity, the estimated gm and maximum photosynthetic capacity were both reduced, whereas the marginal water use efficiency λ increased linearly. Adjustments of gm , λ and photosynthetic capacity were shown to be consistent with a large corpus of drought-stress experiments. The inferred model parameters were then used to evaluate the combined effects of elevated salinity and atmospheric CO2 concentration (ca ) on leaf gas exchange. For a given salinity level, increasing ca increased A linearly, but these increases were accompanied by mild reductions in gc and transpiration. The ca level needed to ameliorate A reductions due to increased salinity is also discussed using the aforementioned model calculations.

Stomatal optimization based on xylem hydraulics (SOX) improves land surface model simulation of vegetation responses to climate.

Land surface models (LSMs) typically use empirical functions to represent vegetation responses to soil drought. These functions largely neglect recent advances in plant ecophysiology that link xylem hydraulic functioning with stomatal responses to climate. We developed an analytical stomatal optimization model based on xylem hydraulics (SOX) to predict plant responses to drought. Coupling SOX to the Joint UK Land Environment Simulator (JULES) LSM, we conducted a global evaluation of SOX against leaf- and ecosystem-level observations. SOX simulates leaf stomatal conductance responses to climate for woody plants more accurately and parsimoniously than the existing JULES stomatal conductance model. An ecosystem-level evaluation at 70 eddy flux sites shows that SOX decreases the sensitivity of gross primary productivity (GPP) to soil moisture, which improves the model agreement with observations and increases the predicted annual GPP by 30% in relation to JULES. SOX decreases JULES root-mean-square error in GPP by up to 45% in evergreen tropical forests, and can simulate realistic patterns of canopy water potential and soil water dynamics at the studied sites. SOX provides a parsimonious way to incorporate recent advances in plant hydraulics and optimality theory into LSMs, and an alternative to empirical stress factors.

Optimal stomatal drought response shaped by competition for water and hydraulic risk can explain plant trait covariation.

The classical theory of stomatal optimization stipulates that stomata should act to maximize photosynthesis while minimizing transpiration. This theory, despite its remarkable success in reproducing empirical patterns, does not account for the fact that the available water to plants is dynamically regulated by plants themselves, and that plants compete for water in most locations. Here, we develop an alternative theory in which plants maximize the expected carbon gain under stochastic rainfall in a competitive environment. We further incorporate xylem hydraulic limitation as an additional constraint to transpiration and evaluate its impacts on stomatal optimization by incorporating the direct carbon cost of xylem recovery and the opportunity cost of reduced future photosynthesis as a result of irrecoverable xylem damage. We predict stomatal behaviour to be more conservative with a higher cost induced by xylem damage. By varying the unit carbon cost and extent of xylem recovery, characterizing the direct and opportunity cost of xylem damage, respectively, our model can reproduce several key patterns of stomatal-hydraulic trait covariations. By addressing the key elements of water limitation in plant gas exchange simultaneously, including plants' self-regulation of water availability, competition for water and hydraulic risk, our study provides a comprehensive theoretical basis for understanding stomatal behaviour.

Predicting shifts in the functional composition of tropical forests under increased drought and CO2 from trade-offs among plant hydraulic traits.

Tropical forest responses are an important feedback on global change, but changes in forest composition with projected increases in CO2 and drought are highly uncertain. Here we determine shifts in the most competitive plant hydraulic strategy (the evolutionary stable strategy or ESS) from changes in CO2 and drought frequency and intensity. Hydraulic strategies were defined along a spectrum from drought avoidance to tolerance by physiology traits. Drought impacted competition more than CO2 , with elevated CO2 reducing but not reversing drought-induced shifts in the ESS towards more tolerant strategies. Trait plasticity and/or adaptation intensified these shifts by increasing the competitive ability of the drought tolerant relative to the avoidant strategies. These findings predict losses of drought avoidant evergreens from tropical forests under global change, and point to the importance of changes in precipitation during the dry season and constraints on plasticity and adaptation in xylem traits to forest responses.

Estimating the sensitivity of stomatal conductance to photosynthesis: a review.

A common approach for estimating fluxes of CO2 and water in canopy models is to couple a model of photosynthesis (An ) to a semi-empirical model of stomatal conductance (gs ) such as the widely validated and utilized Ball-Berry (BB) model. This coupling provides an effective way of predicting transpiration at multiple scales. However, the designated value of the slope parameter (m) in the BB model impacts transpiration estimates. There is a lack of consensus regarding how m varies among species or plant functional types (PFTs) or in response to growth conditions. Literature values are highly variable, with inter-species and intra-species variations of >100%, and comparisons are made more difficult because of differences in collection techniques. This paper reviews the various methods used to estimate m and highlights how variations in measurement techniques or the data utilized can influence the resultant m. Additionally, this review summarizes the reported responses of m to [CO2 ] and water stress, collates literature values by PFT and compiles nearly three decades of values into a useful compendium.

Dynamically optimizing stomatal conductance for maximum turgor-driven growth over diel and seasonal cycles.

Stomata have recently been theorized to have evolved strategies that maximize turgor-driven growth over plants' lifetimes, finding support through steady-state solutions in which gas exchange, carbohydrate storage and growth have all reached equilibrium. However, plants do not operate near steady state as plant responses and environmental forcings vary diurnally and seasonally. It remains unclear how gas exchange, carbohydrate storage and growth should be dynamically coordinated for stomata to maximize growth. We simulated the gas exchange, carbohydrate storage and growth that dynamically maximize growth diurnally and annually. Additionally, we test whether the growth-optimization hypothesis explains nocturnal stomatal opening, particularly through diel changes in temperature, carbohydrate storage and demand. Year-long dynamic simulations captured realistic diurnal and seasonal patterns in gas exchange as well as realistic seasonal patterns in carbohydrate storage and growth, improving upon unrealistic carbohydrate responses in steady-state simulations. Diurnal patterns of carbohydrate storage and growth in day-long simulations were hindered by faulty modelling assumptions of cyclic carbohydrate storage over an individual day and synchronization of the expansive and hardening phases of growth, respectively. The growth-optimization hypothesis cannot currently explain nocturnal stomatal opening unless employing corrective 'fitness factors' or reframing the theory in a probabilistic manner, in which stomata adopt an inaccurate statistical 'memory' of night-time temperature. The growth-optimization hypothesis suggests that diurnal and seasonal patterns of stomatal conductance are driven by a dynamic carbon-use strategy that seeks to maintain homeostasis of carbohydrate reserves.

Competition and Drought Alter Optimal Stomatal Strategy in Tree Seedlings.

A better understanding of plant stomatal strategies holds strong promise for improving predictions of vegetation responses to drought because stomata are the primary mechanism through which plants mitigate water stress. It has been assumed that plants regulate stomata to maintain a constant marginal water use efficiency and forego carbon gain when water is scarce. However, recent hypotheses pose that plants maximize carbon assimilation while also accounting for the risk of hydraulic damage via cavitation and hydraulic failure. This "gain-risk" framework incorporates competition in stomatal regulation because it takes into account that neighboring plants can "steal" unused water. This study utilizes stomatal models representing both the water use efficiency and carbon-maximization frameworks, and empirical data from three species in a potted growth chamber experiment, to investigate the effects of drought and competition on seedling stomatal strategy. We found that drought and competition responses in the empirical data were best explained by the carbon-maximization hypothesis and that both drought and competition affected stomatal strategy. Interestingly, stomatal responses differed substantially by species, with seedlings employing a riskier strategy when planted with a high water use competitor, and seedlings employing a more conservative strategy when planted with a low water use competitor. Lower water users in general had less stomatal sensitivity to decreasing Ψ L compared to moderate to high water users. Repeated water stress also resulted in legacy effects on plant stomatal behavior, increasing stomatal sensitivity (i.e., conservative behavior) even when the seedling was returned to well-watered conditions. These results indicate that stomatal strategies are dynamic and change with climate and competition stressors. Therefore, incorporating mechanisms that allow for stomatal behavioral changes in response to water limitation may be an important step to improving carbon cycle projections in coupled climate-Earth system models.

Optimization of leaf morphology in relation to leaf water status: A theory.

The leaf economic traits such as leaf area, maximum carbon assimilation rate, and venation are all correlated and related to water availability. Furthermore, leaves are often broad and large in humid areas and narrower in arid/semiarid and hot and cold areas. We use optimization theory to explain these patterns. We have created a constrained optimization leaf model linking leaf shape to vein structure that is integrated into coupled transpiration and carbon assimilation processes. The model maximizes net leaf carbon gain (NPPleaf) over the loss of xylem water potential. Modeled relations between leaf traits are consistent with empirically observed patterns. As the results of the leaf shape-venation relation, our model further predicts that a broadleaf has overall higher NPPleaf compared to a narrowleaf. In addition, a broadleaf has a lower stomatal resistance compared to a narrowleaf under the same level of constraint. With the same leaf area, a broadleaf will have, on average, larger conduits and lower total leaf xylem resistance and thus be more efficient in water transportation but less resistant to cavitation. By linking venation structure to leaf shape and using water potential as the constraint, our model provides a physical explanation for the general pattern of the covariance of leaf traits through the safety-efficiency trade-off of leaf hydraulic design.

Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms.

• Hydraulic characteristics of pteridophyte (fern and Selaginella) foliage were investigated to determine whether the processes of water conduction and water loss are coordinated in these early vascular plants similarly to angiosperms. • Eight species of pteridophytes and associated woody angiosperms were examined from the sun and shade in a seasonally dry tropical forest. • Maximum leaf hydraulic conductivity (Kleaf ) in the four pteridophytes was within the range of the sampled shade angiosperms but much lower than that of the sun-dwelling angiosperms. Hydraulic conductivity of both angiosperm and pteridophyte leaves showed a similar response to desiccation, with Kleaf becoming rapidly depressed once leaf water potential fell below a threshold. Stomatal closure in angiosperms corresponded closely with the water potential responsible for 50% loss of Kleaf while pteridophytes were found to close stomata before Kleaf depression. • The contrasting behaviour of stomata in this sample of pteridophytes suggest that this may be an intrinsic difference between pteridophytes and angiosperms, with lower safety margins in angiosperms possibly enhancing both optimization of gas exchange and xylem investment.