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Stomata serve dual and often conflicting roles, facilitating carbon dioxide influx into the plant leaf for photosynthesis and restricting water efflux via transpiration. Strategies for reducing transpiration without incurring a cost for photosynthesis must circumvent this inherent coupling of carbon dioxide and water vapor diffusion. We expressed the synthetic, light-gated K⁺ channel BLINK1 in guard cells surrounding stomatal pores in Arabidopsis to enhance the solute fluxes that drive stomatal aperture. BLINK1 introduced a K⁺ conductance and accelerated both stomatal opening under light exposure and closing after irradiation. Integrated over the growth period, BLINK1 drove a 2.2-fold increase in biomass in fluctuating light without cost in water use by the plant. Thus, we demonstrate the potential of enhancing stomatal kinetics to improve water use efficiency without penalty in carbon fixation.

The basic requirements for plant growth are light, CO2, water, and minerals. However, the absorption and utilization of each of these requires investment on the part of the plant. The primary products of plants are sugars, and the hexose sugars glucose and fructose are the raw material for most of the metabolic pathways and organic matter in plants. To be metabolized, hexose sugars must first be phosphorylated. Only two families of enzymes capable of catalysing the essential irreversible phosphorylation of glucose and fructose have been identified in plants, hexokinases (HXKs) and fructokinases (FRKs). These hexose-phosphorylating enzymes appear to coordinate sugar production with the abilities to absorb light, CO2, water, and minerals. This review describes the long- and short-term effects mediated by HXK and FRK in various tissues, as well as the role of these enzymes in the coordination of sugar production with the absorption of light, CO2, water, and minerals.

Stomatal movements in response to environmental stimuli critically control the plant water status. Although these movements are governed by osmotically driven changes in guard cell volume, the role of membrane water channels (aquaporins) has remained hypothetical. Assays in epidermal peels showed that knockout Arabidopsis thaliana plants lacking the Plasma membrane Intrinsic Protein 2;1 (PIP2;1) aquaporin have a defect in stomatal closure, specifically in response to abscisic acid (ABA). ABA induced a 2-fold increase in osmotic water permeability (Pf) of guard cell protoplasts and an accumulation of reactive oxygen species in guard cells, which were both abrogated in pip2;1 plants. Open stomata 1 (OST1)/Snf1-related protein kinase 2.6 (SnRK2.6), a protein kinase involved in guard cell ABA signaling, was able to phosphorylate a cytosolic PIP2;1 peptide at Ser-121. OST1 enhanced PIP2;1 water transport activity when coexpressed in Xenopus laevis oocytes. Upon expression in pip2;1 plants, a phosphomimetic form (Ser121Asp) but not a phosphodeficient form (Ser121Ala) of PIP2;1 constitutively enhanced the Pf of guard cell protoplasts while suppressing its ABA-dependent activation and was able to restore ABA-dependent stomatal closure in pip2;1. This work supports a model whereby ABA-triggered stomatal closure requires an increase in guard cell permeability to water and possibly hydrogen peroxide, through OST1-dependent phosphorylation of PIP2;1 at Ser-121.

Maximum and minimum stomatal conductance, as well as stomatal size and rate of response, are known to vary widely across plant species, but the functional relationship between these static and dynamic stomatal properties is unknown. The objective of this study was to test three hypotheses: (i) operating stomatal conductance under standard conditions (g op) correlates with minimum stomatal conductance prior to morning light [g min(dawn)]; (ii) stomatal size (S) is negatively correlated with g op and the maximum rate of stomatal opening in response to light, (dg/dt)max; and (iii) g op correlates negatively with instantaneous water-use efficiency (WUE) despite positive correlations with maximum rate of carboxylation (Vc max) and light-saturated rate of electron transport (J max). Using five closely related species of the genus Banksia, the above variables were measured, and it was found that all three hypotheses were supported by the results. Overall, this indicates that leaves built for higher rates of gas exchange have smaller stomata and faster dynamic characteristics. With the aid of a stomatal control model, it is demonstrated that higher g op can potentially expose plants to larger tissue water potential gradients, and that faster stomatal response times can help offset this risk.

Coronatine (COR) facilitates entry of bacteria into the plant apoplast by stimulating stomata opening. COR-induced signaling events at stomata remain unclear. We found that the COR and jasmonate isoleucine (JA-Ile) co-receptor JAZ2 is constitutively expressed in guard cells and modulates stomatal dynamics during bacterial invasion We analyzed tissue expression patterns of AtJAZ genes and measured stomata opening and pathogen resistance in loss- and gain-of-function mutants. Arabidopsis jaz2 mutants are partially impaired in pathogen-induced stomatal closing and more susceptible to Pseudomonas. Gain-of-function mutations in JAZ2 prevent stomatal reopening by COR and are highly resistant to bacterial penetration. The JAZ2 targets MYC2, MYC3 and MYC4 directly regulate the expression of ANAC19, ANAC55 and ANAC72 to modulate stomata aperture. Due to the antagonistic interactions between the salicylic acid (SA) and JA defense pathways, efforts to increase resistance to biotrophs result in enhanced susceptibility to necrotrophs, and vice versa. Remarkably, dominant jaz2Djas mutants are resistant to Pseudomonas syringae but retain unaltered resistance against necrotrophs. Our results demonstrate the existence of a COI1-JAZ2-MYC2,3,4-ANAC19,55,72 module responsible for the regulation of stomatal aperture that is hijacked by bacterial COR to promote infection. They also provide novel strategies for crop protection against biotrophs without compromising resistance to necrotrophs.

Stomatal movements are crucial for the control of plant water status and protection against pathogens. Assays on epidermal peels revealed that, similar to abscisic acid (ABA), pathogen-associated molecular pattern (PAMP) flg22 requires the AtPIP2;1 aquaporin to induce stomatal closure. Flg22 also induced an increase in osmotic water permeability (Pf) of guard cell protoplasts through activation of AtPIP2;1. The use of HyPer, a genetic probe for intracellular hydrogen peroxide (H2O2), revealed that both ABA and flg22 triggered an accumulation of H2O2 in wild-type but not pip2;1 guard cells. Pretreatment of guard cells with flg22 or ABA facilitated the influx of exogenous H2O2 Brassinosteroid insensitive 1-associated receptor kinase 1 (BAK1) and open stomata 1 (OST1)/Snf1-related protein kinase 2.6 (SnRK2.6) were both necessary to flg22-induced Pf and both phosphorylated AtPIP2;1 on Ser121 in vitro. Accumulation of H2O2 and stomatal closure as induced by flg22 was restored in pip2;1 guard cells by a phosphomimetic form (Ser121Asp) but not by a phosphodeficient form (Ser121Ala) of AtPIP2;1. We propose a mechanism whereby phosphorylation of AtPIP2;1 Ser121 by BAK1 and/or OST1 is triggered in response to flg22 to activate its water and H2O2 transport activities. This work establishes a signaling role of plasma membrane aquaporins in guard cells and potentially in other cellular context involving H2O2 signaling.

The non-protein amino acid γ-aminobutyric acid (GABA) has been proposed to be an ancient messenger for cellular communication conserved across biological kingdoms. GABA has well-defined signalling roles in animals; however, whilst GABA accumulates in plants under stress it has not been determined if, how, where and when GABA acts as an endogenous plant signalling molecule. Here, we establish endogenous GABA as a bona fide plant signal, acting via a mechanism not found in animals. Using Arabidopsis thaliana , we show guard cell GABA production is necessary and sufficient to reduce stomatal opening and transpirational water loss, which improves water use efficiency and drought tolerance, via negative regulation of a stomatal guard cell tonoplast-localised anion transporter. We find GABA modulation of stomata occurs in multiple plants, including dicot and monocot crops. This study highlights a role for GABA metabolism in fine tuning physiology and opens alternative avenues for improving plant stress resilience. GABA accumulates during stress in plants but how, where and when GABA acts is not clear. Here the authors show that GABA production in Arabidopsis guard cells reduces stomatal opening and transpirational water loss, thereby improving water use efficiency.

Stomatal movements rely on alterations in guard cell turgor. This requires massive K ⁺ bidirectional fluxes across the plasma and tonoplast membranes. Surprisingly, given their physiological importance, the transporters mediating the energetically uphill transport of K ⁺ into the vacuole remain to be identified. Here, we report that, in Arabidopsis guard cells, the tonoplast-localized K ⁺/H ⁺ exchangers NHX1 and NHX2 are pivotal in the vacuolar accumulation of K ⁺ and that nhx1 nhx2 mutant lines are dysfunctional in stomatal regulation. Hypomorphic and complete-loss-of-function double mutants exhibited significantly impaired stomatal opening and closure responses. Disruption of K ⁺ accumulation in guard cells correlated with more acidic vacuoles and the disappearance of the highly dynamic remodelling of vacuolar structure associated with stomatal movements. Our results show that guard cell vacuolar accumulation of K ⁺ is a requirement for stomatal opening and a critical component in the overall K ⁺ homeostasis essential for stomatal closure, and suggest that vacuolar K ⁺ fluxes are also of decisive importance in the regulation of vacuolar dynamics and luminal pH that underlie stomatal movements.

Summary Stomata are epidermal pores that control the exchange of gaseous CO2 and H2O between plants and their environment. Modulating stomatal density can alter this exchange and thus presents a viable target for engineering improved crop productivity and climate resilience. Here, we show that stomatal density in Arabidopsis thaliana can be decreased by the expression of a water‐forming NAD(P)H oxidase targeted to stomatal precursor cells. We demonstrate that this reduction in stomatal density occurs irrespective of whether the expressed enzyme is localized to the cytosol, chloroplast stroma or chloroplast intermembrane space of these cells. We also reveal that this decrease in stomatal density occurs in the absence of any measurable impact on the efficiency and thermal sensitivity of photosynthesis, or on stomatal dynamics. Consequently, overexpression plants exhibit a higher intrinsic water‐use efficiency due to an increase in CO2 fixed per unit water transpired. Finally, we demonstrate that this enhanced water‐use efficiency translates to an improvement in vegetative growth and biomass accumulation under water‐deficit conditions. Together, these results thus provide a novel approach for enhancing plant productivity through metabolic engineering of stomatal density.

Plant responses to abiotic stresses are coordinated by arrays of growth and developmental programs. Phytohormones such as abscisic acid (ABA) and indole-3-acetic acid (IAA) play critical roles in developmental progresses and environmental responses through complex signalling networks. However, crosstalk between the two hormones at the biosynthesis level remains largely unknown. Here, we report that carotenoid-deficient mutants ( phs1 , phs2 , phs3 - 1 , phs4 , and PDS -RNAi transgenic rice) were impaired in the biosynthesis of ABA and IAA. Under drought conditions, phs3 - 1 and PDS -RNAi transgenic rice showed larger stomata aperture and earlier wilting compared to the wild type at both seedling and panicle developmental stage. Interestingly, these carotenoid-deficient lines showed increased cold resistance, which was likely due to the combined effects of reduced IAA content, alleviated oxidative damage and decreased membrane penetrability. Furthermore, we found that IAA content was significantly declined in rice treated with fluridone (a carotenoid and ABA biosynthesis inhibitor), and expression of auxin synthesis and metabolism-related genes were altered in the fluridone-treated rice similar to that in the carotenoid-deficient mutants. In addition, exogenous IAA, but not ABA, could restore the dwarf phenotype of phs3 - 1 and PDS -RNAi transgenic rice. These results support a crosstalk between ABA and IAA at the biosynthesis level, and this crosstalk is involved in development and differentially affects drought and cold tolerance in rice.