The PYL4 A194T Mutant Uncovers a Key Role of PYR1-LIKE4/PROTEIN PHOSPHATASE 2CA Interaction for Abscisic Acid Signaling and Plant Drought Resistance

Pizzio, Gastón A.; Rodríguez, Lesia; Antoni, Regina; González-Guzmán, Miguel; Yunta, Cristina; Merilo, Ebe; Kollist, Hannes; Albert, Armando; Rodrı́guez, Pedro L.

doi:10.1104/pp.113.224162

Cited by 158 publications

(117 citation statements)

References 45 publications

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“…Stomatal size and densities were not different in the RCAR6 line from the wild type, indicating that the observed changes in transpiration reflect ABA signaling-mediated changes in apertures of stomata. This conclusion is in line with other studies in which ectopic ABA receptor expression caused ABAhypersensitive stomatal responses (18,(22)(23)(24).…”

Section: Discussionsupporting

confidence: 82%

“…ABA perception recruits an ABA-binding REGULATORY COMPONENT OF ABA RECEPTOR (RCAR)/PYRABACTIN RESISTANCE 1 (PYR1)/PYR1-LIKE (PYL) and an associated protein phosphatase of type 2C (PP2C) (18, 19). Administration of ABA and ABA agonists (20, 21), ectopic expression of RCARs (17,18,[22][23][24], as well as reduced expression of PP2Cs (25) have been shown to minimize plant transpiration and, in some cases, to enhance survival under water deficit. It is clear that plants with strongly reduced transpiration are limited in CO 2 uptake and, hence, in growth and biomass formation.…”

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confidence: 99%

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Leveraging abscisic acid receptors for efficient water use in Arabidopsis

Yang

Liu

Tischer

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

113

141

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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...

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Section: Discussionsupporting

confidence: 82%

mentioning

confidence: 99%

Leveraging abscisic acid receptors for efficient water use in Arabidopsis

Yang

Liu

Tischer

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

113

141

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“…The crystal structure of RCAR7-PP2CA revealed an additional interaction domain provided by a zinc-finger domain present in PP2CA and HAImember PP2Cs (41), which might provide an explanation for the high affinity of PP2CA in vitro and the high efficiency of RCAR7 to antagonize PP2CA and HAI2 action on ABA signaling. Several studies identified amino acid residues of RCARs (7,14,40,46) that alter interaction with PP2Cs, but none have reported so far on successful alteration of PP2C to establish RCAR binding. For clade A PP2Cs, a number of mutations are known to reduce or obliterate the interaction with RCARs, which results in ABA-insensitive coreceptors such as the classical abi1-1 (ABI1 G180D ) and abi2-1 (ABI2 G168D ) proteins or mutations in the ABA-sensing tryptophan residue (7,8,39).…”

Section: Q386nmentioning

confidence: 99%

Abscisic acid sensor RCAR7/PYL13, specific regulator of protein phosphatase coreceptors

Fuchs

Tischer

Wunschel

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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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.

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“…Subcellular localization studies indicate that PP2Cs are present at the nucleus and cytosol, which is in agreement with their reported interaction with SnRK2s (Fujita et al, 2009 or the slow anion channel 1 (SLAC1) and SLAC1 homolog 3 (SLAH3), and transcriptional regulators, such as bZIP transcription factors and chromatin-remodeling complexes (SWI2/SNF2) (Cherel et al, 2002, Guo et al, 2002, Lee et al, 2007, Saez et al, 2008, Geiger et al, 2009 conformations by contacting the PP2C domain of ABI1. This structural consideration explains that the interaction between ABI1 and RCAR1 (also known as PYL9), which is a member of the ABA Antoni et al, 2012, Brandt et al, 2012, Lynch et al, 2012, Pizzio et al, 2013, Rodrigues et al, 2013.…”

Section: Protein Phosphatases Type 2c Pp2csmentioning

confidence: 99%

“…PP2CA inhibits SLAC1 channel activity in two ways, due to direct interaction with SLAC and by dephosphorylation of the kinase OST1 leading to kinasedependent phosphorylation inhibition (Lee et al, 2009). Another study trying to elucidate implications of PP2CA in ABA signaling pathway came from Pizzio et al (2013). This work generated an allele library composed of 10,000 mutant clones of Arabidopsis PYL4 receptor where mutations that promoted ABA-independent interaction with PP2CA/AHG3 were selected.…”

Section: Aba Controls Kmentioning

confidence: 99%

Fundamental and applied research in ABA signaling: Regulation by ABA of the chromatin remodeling ATPase BRAHMA and biotechnological use of the PP2CA promoter.

Peirats‐Llobet¹

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Optimal response to drought is critical for plant survival and will affect biodiversity and crop performance during climate change. Mitotically heritable epigenetic and dynamic chromatin state changes have been implicated in the plant response to the drought stress hormone abscisic acid (ABA). The Arabidopsis SWI/SNF chromatin-remodeling ATPase BRAHMA (BRM) modulates response to ABA by preventing premature activation of stress response pathways during germination. Here, we show that the core ABA signalosome formed by ABA receptors, PP2Csand SnRK2s physically interact with BRM to regulate BRM activity and post-translationally modify BRM by phosphorylation/dephosphorylation.Genetic evidence suggests that BRM acts downstream of SnRK2.2/2.3 kinases and biochemical studies identified evolutionary conserved SnRK2 phosphorylation sites in the C-terminal region of BRM. Our data suggest that SnRK2-dependent phosphorylation of BRM leads to its inhibition, and PP2CA-mediated dephosphorylation of BRM restores the ability of BRM to repress ABA response.ABA plays a key role to regulate germination and post-germination growth and the AP2-type ABI4 and bZIP-type ABI5 transcription factors RESUMENLa respuesta óptima a la sequía es crítica para la supervivencia de las plantas y afectará a la biodiversidad y al rendimiento de los cultivos durante el cambio climático. Las modificaciones epigenéticas y los cambios dinámicos del estado de la cromatina han sido implicados en la respuesta de la planta al ácido abscísico (ABA), la conocida como la hormona del estrés hídrico. La ATPasa remodeladora de cromatina de tipo SWI/SNF de Arabidopsis, BRAHMA (BRM), modula la respuesta al ABA mediante la prevención de la activación prematura de las vías de respuesta al estrés durante la germinación. Aquí, mostramos que el núcleo del señalosoma de ABA formado por los receptores de ABA, las PP2Cs y las SnRK2s interaccionan físicamente con BRM para regular su actividad y modificarla post-traduccionalmente por mecanismos de fosforilación/desfosforilación. La evidencia genética sugiere que BRM actúa aguas abajo de las quinasas SnRK2.2/2.3 y los estudios bioquímicos identificaron la presencia en la región C-terminal de BRM de sitios de fosforilación de las SnRK2 que estaban conservados evolutivamente. Nuestros datos sugieren que la fosforilación de BRM que depende de las SnRK2 conduce a su inhibición, y que la desfosforilación de BRM mediada por PP2CA restaura la capacidad de BRM para reprimir la respuesta a ABA.El ABA juega un papel clave en la regulación de la germinación y el crecimiento post germinativo y los factores de transcripción de tipo AP2 como ABI4 y de tipo bZIP como ABI5, son necesarios para la inhibición del crecimiento post germinativo mediado por ABA cuando los embriones encuentran estrés hídrico. La detención del crecimiento inducida por ABI4 y ABI5 implica la señalización de ABA y en el caso de ABI5, se ha demostrado que el ABA inhibe la actividad de BRM para ! inducir la transcripción de ABI5. La pérdida de actividad de B...

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The PYL4 A194T Mutant Uncovers a Key Role of PYR1-LIKE4/PROTEIN PHOSPHATASE 2CA Interaction for Abscisic Acid Signaling and Plant Drought Resistance

Cited by 158 publications

References 45 publications

Leveraging abscisic acid receptors for efficient water use in Arabidopsis

Leveraging abscisic acid receptors for efficient water use in Arabidopsis

Abscisic acid sensor RCAR7/PYL13, specific regulator of protein phosphatase coreceptors

Fundamental and applied research in ABA signaling: Regulation by ABA of the chromatin remodeling ATPase BRAHMA and biotechnological use of the PP2CA promoter.

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