Plant growth requires the influx of atmospheric CO 2 through stomatal pores, and this carbon uptake for photosynthesis is inherently associated with a large efflux of water vapor. Under water deficit, plants reduce transpiration and are able to improve carbon for water exchange leading to higher water use efficiency (WUE). Whether increased WUE can be achieved without trade-offs in plant growth is debated. The signals mediating the WUE response under water deficit are not fully elucidated but involve the phytohormone abscisic acid (ABA). ABA is perceived by a family of related receptors known to mediate acclimation responses and to reduce transpiration. We now show that enhanced stimulation of ABA signaling via distinct ABA receptors can result in plants constitutively growing at high WUE in the model species Arabidopsis. WUE was assessed by three independent approaches involving gravimetric analyses, 13 C discrimination studies of shoots and derived cellulose fractions, and by gas exchange measurements of whole plants and individual leaves. Plants expressing the ABA receptors RCAR6/PYL12 combined up to 40% increased WUE with high growth rates, i.e., are water productive. Water productivity was associated with maintenance of net carbon assimilation by compensatory increases of leaf CO 2 gradients, thereby sustaining biomass acquisition. Leaf surface temperatures and growth potentials of plants growing under well-watered conditions were found to be reliable indicators for water productivity. The study shows that ABA receptors can be explored to generate more plant biomass per water transpired, which is a prime goal for a more sustainable water use in agriculture.carbon assimilation | drought resistance | water deficit | water productivity | water use efficiency P lants are ferocious consumers of water, and plant transpiration is the dominant vector for water mobilization from terrestrial surfaces to the atmosphere (1). Plant transpiration is sustained by efficient water uptake through the root systems, which can comprise 500 m 2 of root surface and 500 km in combined length even in a single barley plant. Water is the major factor limiting crop productivity in the field (2). Thus, more than two-thirds of the fresh water resources used globally are channeled into agriculture, thereby contributing to potential social conflicts over water (3).Whereas the gas exchange of CO 2 and water vapor at the stomatal pore is a physical process controlled by both the ratio in partial pressure gradients and gas diffusivities (4, 5), terrestrial plants are able to capture carbon more efficiently under water deficit. Both short-term leaf gas exchange measurements and 13 C isotope discrimination analyses revealed increases of the instantaneous water use efficiency (insWUE) and intrinsic WUE (iWUE), respectively, by a factor of 1.5-2.5 in wheat and other species (6, 7). The underlying mechanisms, however, are not fully elucidated. Gains in WUE have been found to be associated with trade-offs in growth potential (8-10). WUE is control...
The phytohormone abscisic acid (ABA) is induced in response to abiotic stress to mediate plant acclimation to environmental challenge. Key players of the ABA-signaling pathway are the ABA-binding receptors (RCAR/PYR1/PYL), which, together with a plant-specific subclade of protein phosphatase 2C (PP2C), form functional holoreceptors. The Arabidopsis genome encodes nine PP2C coreceptors and 14 different RCARs, which can be divided into three subfamilies. The presence of these gene families in higher plants points to the existence of an intriguing regulatory network and poses questions as to the functional compatibility and specificity of receptor-coreceptor interactions. Here, we analyzed all RCAR-PP2C combinations for their capacity to regulate ABA signaling by transient expression in Arabidopsis protoplasts. Of 126 possible RCAR-PP2C pairings, 113 were found to be functional. The three subfamilies within the RCAR family showed different sensitivities to regulating the ABA response at basal ABA levels when efficiently expressed. At exogenous high ABA levels, the RCARs regulated most PP2Cs and activated the ABA response to a similar extent. The PP2C AHG1 was regulated only by RCAR1/PYL9, RCAR2/ PYL7, and RCAR3/PYL8, which are characterized by a unique tyrosine residue. Site-directed mutagenesis of RCAR1 showed that its tyrosine residue is critical for AHG1 interaction and regulation. Furthermore, the PP2Cs HAI1 to HAI3 were regulated by all RCARs, and the ABA receptor RCAR4/PYL10 showed ABA-dependent PP2C regulation. The findings unravel the interaction network of possible RCAR-PP2C pairings and their different potentials to serve a rheostat function for integrating fluctuating hormone levels into the ABA-response pathway.BA regulates a plethora of responses associated with plant growth and the homeostatic control of water relations. ABA controls root extension and branching, stomatal opening and density, and tolerance to water deficit during seed maturation and drought (1, 2). Core ABA signaling can be considered as a threestep regulatory process involving the receptor complex, protein kinases as intermediate signaling components, and downstream targets such as ion channels and transcription factors (1). The heteromeric receptor complex consists of the ABA-binding RCAR/PYR1/PYL receptor and the PP2C coreceptor. The protein phosphatase activity is regulated by ABA that stabilizes the PP2C-RCAR interaction, which blocks substrate access and thereby inhibits the catalytic activity of the coreceptor (3, 4).The clade A of Arabidopsis PP2Cs comprises nine members and forms a plant-specific subgroup among the large family of PP2Cs, which are Mg 2+ -and Mn 2+-dependent serine-threonine protein phosphatases (5). The ABA-mediated inactivation of PP2C activity releases SNF1-related kinase 2 (SnRK2) from inhibition, and it subsequently targets downstream components such as transcription factors and ion channels (6-12). The 14 different RCARs of Arabidopsis can be divided into three subfamilies according to their sequence hom...
The plant hormone abscisic acid (ABA) acts both as a developmental signal and as an integrator of environmental cues such as drought and cold. ABA perception recruits an ABA-binding regulatory component [regulatory component of ABA receptor (RCAR)/ PYR1/PYL] and an associated protein phosphatase 2C (PP2C). Phytohormone binding inactivates the phosphatase activity of the coreceptor, permitting phosphorelay of the ABA signal via downstream protein kinases. RCARs and PP2C coreceptors are represented by small protein families comprising 14 and 9 members in Arabidopsis, respectively. The specificity of the RCAR-PP2C interaction and the constraints contributing to specific combinations are poorly understood. In this contribution, we analyzed RCAR7/PYL13, which is characterized by three variant amino acid residues in the conserved ABA-binding pocket. RCAR7 regulated the phosphatase activity of the PP2Cs ABI1, ABI2, and PP2CA in vitro at nanomolar ABA levels; however, it was unable to regulate the structurally related hypersensitive to ABA 1 (HAB1). Site-directed mutagenesis of HAB1 established ABA-dependent regulation by RCAR7. Conversion of the noncanonical amino acid residues of RCAR7 into the consensus ABA-binding pocket did not perceptibly change receptor function. Ectopic expression of RCAR7 in Arabidopsis resulted in ABA hypersensitivity affecting gene regulation, seed germination, and stomatal closure. The RCAR7 loss-of-function mutant revealed no changes in ABA responses, similar to the RCAR9 knockout line, whereas the combined deficiency of RCAR7 and RCAR9 resulted in ABA-insensitive seed germination. The study shows a role of RCAR7 in early plant development, proves its ABA receptor function, and identifies structural constraints of RCAR7-PP2C interaction.
The phytohormone abscisic acid (ABA) regulates plant responses to abiotic stress, such as drought and high osmotic conditions. The multitude of functionally redundant components involved in ABA signaling poses a major challenge for elucidating individual contributions to the response selectivity and sensitivity of the pathway. Here, we reconstructed single ABA signaling pathways in yeast for combinatorial analysis of ABA receptors and coreceptors, downstream‐acting SnRK2 protein kinases, and transcription factors. The analysis shows that some ABA receptors stimulate the pathway even in the absence of ABA and that SnRK2s are major determinants of ABA responsiveness by differing in the ligand‐dependent control. Five SnRK2s, including SnRK2.4 known to be active under osmotic stress in plants, activated ABA‐responsive transcription factors and were regulated by ABA receptor complexes in yeast. In the plant tissue, SnRK2.4 and ABA receptors competed for coreceptor interaction in an ABA‐dependent manner consistent with a tight integration of SnRK2.4 into the ABA signaling pathway. The study establishes the suitability of the yeast system for the dissection of core signaling cascades and opens up future avenues of research on ligand‐receptor regulation.
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