Summary Both photosynthesis (A) and stomatal conductance (g s) respond to changing irradiance, yet stomatal responses are an order of magnitude slower than photosynthesis, resulting in noncoordination between A and g s in dynamic light environments.Infrared gas exchange analysis was used to examine the temporal responses and coordination of A and g s to a step increase and decrease in light in a range of different species, and the impact on intrinsic water use efficiency was evaluated.The temporal responses revealed a large range of strategies to save water or maximize photosynthesis in the different species used in this study but also displayed an uncoupling of A and g s in most of the species. The shape of the guard cells influenced the rapidity of response and the overall g s values achieved, with different impacts on A and W i. The rapidity of g s in dumbbell‐shaped guard cells could be attributed to size, whilst in elliptical‐shaped guard cells features other than anatomy were more important for kinetics.Our findings suggest significant variation in the rapidity of stomatal responses amongst species, providing a novel target for improving photosynthesis and water use.

Contents Summary93I.Introduction93II.Influence of the speed of gs responses on A and Wi93III.Determinants of the rapidity of gs responses95IV.Conclusion97Acknowledgements97References97 Summary Stomatal movements control CO2 uptake for photosynthesis and water loss through transpiration, and therefore play a key role in plant productivity and water use efficiency. The predicted doubling of global water usage by 2030 mean that stomatal behaviour is central to current efforts to increase photosynthesis and crop yields, particularly under conditions of reduced water availability. In the field, slow stomatal responses to dynamic environmental conditions add a temporal dimension to gaseous fluxes between the leaf and atmosphere. Here, we review recent work on the rapidity of stomatal responses and present some of the possible anatomical and biochemical mechanisms that influence the rapidity of stomatal movements.

The acclimation of plants to light has been studied extensively, yet little is known about the effect of dynamic fluctuations in light on plant phenotype and acclimatory responses. We mimicked natural fluctuations in light over a diurnal period to examine the effect on the photosynthetic processes and growth of Arabidopsis (Arabidopsis thaliana). High and low light intensities, delivered via a realistic dynamic fluctuating or square wave pattern, were used to grow and assess plants. Plants subjected to square wave light had thicker leaves and greater photosynthetic capacity compared with fluctuating light-grown plants. This, together with elevated levels of proteins associated with electron transport, indicates greater investment in leaf structural components and photosynthetic processes. In contrast, plants grown under fluctuating light had thinner leaves, lower leaf light absorption, but maintained similar photosynthetic rates per unit leaf area to square wave-grown plants. Despite high light use efficiency, plants grown under fluctuating light had a slow growth rate early in development, likely due to the fact that plants grown under fluctuating conditions were not able to fully utilize the light energy absorbed for carbon fixation. Diurnal leaf-level measurements revealed a negative feedback control of photosynthesis, resulting in a decrease in total diurnal carbon assimilated of at least 20%. These findings highlight that growing plants under square wave growth conditions ultimately fails to predict plant performance under realistic light regimes and stress the importance of considering fluctuations in incident light in future experiments that aim to infer plant productivity under natural conditions in the field.In the natural environment, plants experience a range of light intensities and spectral properties due to changes in sun angle and cloud cover in addition to shading from overlapping leaves and neighboring plants. Therefore, leaves are subjected to spatial and temporal gradients in incident light, which has major consequences for photosynthetic carbon assimilation (Pearcy, 1990;Chazdon and Pearcy, 1991;Pearcy and Way, 2012). As light is the key resource for photosynthesis, plants acclimate to the light environment under which they are grown to maintain performance and fitness. Acclimation involves altering metabolic processes (including light harvesting and CO 2 capture) brought about by a range of mechanisms, from adjustments to leaf morphology to changes in photosynthetic apparatus stoichiometry (Terashima et al., 2006;Athanasiou et al., 2010;Kono and Terashima, 2014), all of which impact on photosynthesis. The primary determinant of crop yield is the cumulative rate of photosynthesis over the growing season, which is regulated by the amount of light captured by the plant and the ability of the plant to efficiently use this energy to convert CO 2 into biomass and harvestable yield (Sinclair and Muchow, 1999). Currently, considerable research efforts in plant biology focus on improving performance,...

In Arabidopsis thaliana, changes in metabolism and gene expression drive increased drought tolerance and initiate diverse drought avoidance and escape responses. To address regulatory processes that link these responses, we set out to identify genes that govern early responses to drought. To do this, a high-resolution time series transcriptomics data set was produced, coupled with detailed physiological and metabolic analyses of plants subjected to a slow transition from well-watered to drought conditions. A total of 1815 drought-responsive differentially expressed genes were identified. The early changes in gene expression coincided with a drop in carbon assimilation, and only in the late stages with an increase in foliar abscisic acid content. To identify gene regulatory networks (GRNs) mediating the transition between the early and late stages of drought, we used Bayesian network modeling of differentially expressed transcription factor (TF) genes. This approach identified AGAMOUS-LIKE22 (AGL22), as key hub gene in a TF GRN. It has previously been shown that AGL22 is involved in the transition from vegetative state to flowering but here we show that AGL22 expression influences steady state photosynthetic rates and lifetime water use. This suggests that AGL22 uniquely regulates a transcriptional network during drought stress, linking changes in primary metabolism and the initiation of stress responses.

Stomatal movements depend on the transport and metabolism of osmotic solutes that drive reversible changes in guard cell volume and turgor. These processes are defined by a deep knowledge of the identities of the key transporters and of their biophysical and regulatory properties, and have been modeled successfully with quantitative kinetic detail at the cellular level. Transpiration of the leaf and canopy, by contrast, is described by quasilinear, empirical relations for the inputs of atmospheric humidity, CO 2 , and light, but without connection to guard cell mechanics. Until now, no framework has been available to bridge this gap and provide an understanding of their connections. Here, we introduce OnGuard2, a quantitative systems platform that utilizes the molecular mechanics of ion transport, metabolism, and signaling of the guard cell to define the water relations and transpiration of the leaf. We show that OnGuard2 faithfully reproduces the kinetics of stomatal conductance in Arabidopsis thaliana and its dependence on vapor pressure difference (VPD) and on water feed to the leaf. OnGuard2 also predicted with VPD unexpected alterations in K + channel activities and changes in stomatal conductance of the slac1 Cl 2 channel and ost2 H + -ATPase mutants, which we verified experimentally. OnGuard2 thus bridges the micro-macro divide, offering a powerful tool with which to explore the links between guard cell homeostasis, stomatal dynamics, and foliar transpiration. INTRODUCTIONStomata provide the main pathway for CO 2 entry for photosynthesis and for transpirational water loss across the leaf epidermis. Pairs of guard cells surround each stoma, regulating the aperture to balance the often conflicting demands for CO 2 and for water conservation. Guard cells open and close the pore, driven by osmotic solute uptake and loss, notably of K + and Cl 2 , and by the synthesis and metabolism of organic solutes, especially sucrose (Suc) and malate (Mal) (Willmer and Fricker, 1996;Kim et al., 2010;Roelfsema and Hedrich, 2010;Lawson and Blatt, 2014;Jezek and Blatt, 2017). A number of well-defined signals, including light, CO 2 , and the water stress hormone abscisic acid (ABA), modulate transport and solute accumulation to alter cell volume, turgor, and stomatal aperture. Much research at the cellular level has focused on these inputs and their connection to stomatal movements, especially stomatal closing. Studies have highlighted both Ca 2+ -independent and Ca 2+ -dependent signaling, including elevated free cytosolic Ca 2+ concentration ([Ca 2+ ] i ), cytosolic pH (pH i ), protein kinases, and phosphatases, that inactivate inward-rectifying K + channels and activate Cl 2 channels and outward-rectifying K + channels to bias the membrane for solute loss (Blatt et al., 1990;Lemtiri-Chlieh and MacRobbie, 1994; Blatt, 1998, 1999;Marten et al., 2007;Assmann and Jegla, 2016;Jezek and Blatt, 2017).At the tissue and whole-plant levels, by contrast, attention has been drawn to inputs closely tied to photosynthesis, including tra...

Starch in Arabidopsis (Arabidopsis thaliana) guard cells is rapidly degraded at the start of the day by the glucan hydrolases a-AMYLASE3 (AMY3) and b-AMYLASE1 (BAM1) to promote stomatal opening. This process is activated via phototropinmediated blue light signaling downstream of the plasma membrane H 1-ATPase. It remains unknown how guard cell starch degradation integrates with light-regulated membrane transport processes in the fine control of stomatal opening kinetics. We report that H 1 , K 1 , and Cl 2 transport across the guard cell plasma membrane is unaltered in the amy3 bam1 mutant, suggesting that starch degradation products do not directly affect the capacity to transport ions. Enzymatic quantification revealed that after 30 min of blue light illumination, amy3 bam1 guard cells had similar malate levels as the wild type, but had dramatically altered sugar homeostasis, with almost undetectable amounts of Glc. Thus, Glc, not malate, is the major starchderived metabolite in Arabidopsis guard cells. We further show that impaired starch degradation in the amy3 bam1 mutant resulted in an increase in the time constant for opening of 40 min. We conclude that rapid starch degradation at dawn is required to maintain the cytoplasmic sugar pool, clearly needed for fast stomatal opening. The conversion and exchange of metabolites between subcellular compartments therefore coordinates the energetic and metabolic status of the cell with membrane ion transport.

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Plants experience changes in light intensity and quality due to variations in solar angle and shading from clouds and overlapping leaves. Stomatal opening to increasing irradiance is often an order of magnitude slower than photosynthetic responses, which can result in CO2 diffusional limitations on leaf photosynthesis, as well as unnecessary water loss when stomata continue to open after photosynthesis has reached saturation. Stomatal opening to light is driven by two distinct pathways; the ‘red’ or photosynthetic response that occurs at high fluence rates and saturates with photosynthesis, and is thought to be the main mechanism that coordinates stomatal behaviour with photosynthesis; and the guard cell-specific ‘blue’ light response that saturates at low fluence rates, and is often considered independent of photosynthesis, and important for early morning stomatal opening. Here we review the literature on these complicated signal transduction pathways and osmoregulatory processes in guard cells that are influenced by the light environment. We discuss the possibility of tuning the sensitivity and magnitude of stomatal response to blue light which potentially represents a novel target to develop ideotypes with the ‘ideal’ balance between carbon gain, evaporative cooling, and maintenance of hydraulic status that is crucial for maximizing crop performance and productivity.