Stomatal pores form a crucial interface between the leaf mesophyll and the atmosphere, controlling water and carbon balance in plants [1]. Major advances have been made in understanding the regulatory networks and ion fluxes in the guard cells surrounding the stomatal pore [2]. However, our knowledge on the role of carbon metabolism in these cells is still fragmentary [3-5]. In particular, the contribution of starch in stomatal opening remains elusive [6]. Here, we used Arabidopsis thaliana as a model plant to provide the first quantitative analysis of starch turnover in guard cells of intact leaves during the diurnal cycle. Starch is present in guard cells at the end of night, unlike in the rest of the leaf, but is rapidly degraded within 30 min of light. This process is critical for the rapidity of stomatal opening and biomass production. We exploited Arabidopsis molecular genetics to define the mechanism and regulation of guard cell starch metabolism, showing it to be mediated by a previously uncharacterized pathway. This involves the synergistic action of β-amylase 1 (BAM1) and α-amylase 3 (AMY3)-enzymes that are normally not required for nighttime starch degradation in other leaf tissues. This pathway is under the control of the phototropin-dependent blue-light signaling cascade and correlated with the activity of the plasma membrane H(+)-ATPase. Our results show that guard cell starch degradation has an important role in plant growth by driving stomatal responses to light.

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,...

The control of gaseous exchange between the leaf and external atmosphere is governed by stomatal conductance ( gs); therefore, stomata play a critical role in photosynthesis and transpiration and overall plant productivity. Stomatal conductance is determined by both anatomical features and behavioral characteristics. Here we review some of the osmoregulatory pathways in guard cell metabolism, genes and signals that determine stomatal function and patterning, and the recent work that explores coordination between gs and carbon assimilation ( A) and the influence of spatial distribution of functional stomata on underlying mesophyll anatomy. We also evaluate the current literature on mesophyll-driven signals that may coordinate stomatal behavior with mesophyll carbon assimilation and explore stomatal kinetics as a possible target to improve A and water use efficiency. By understanding these processes, we can start to provide insight into manipulation of these regulatory pathways to improve stomatal behavior and identify novel unexploited targets for altering stomatal behavior and improving crop plant productivity.

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.

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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.

Highlights Stomatal conductance is a major determinant of crop yield. The speed of stomatal response to changing environmental conditions greatly impacts photosynthesis and water use. Existing natural variation in the magnitude and rapidity of stomatal conductance is a potential target for future breeding. Genetic manipulation of stomatal conductance has the potential to improve crop performance.

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