ABI1 and PP2CA Phosphatases Are Negative Regulators of Snf1-Related Protein Kinase1 Signaling in <i>Arabidopsis</i>

Rodrigues, Américo; Adamo, Mattia; Crozet, Pierre; Margalha, Leonor; Confraria, Ana; Martinho, Cláudia; Elias, Alexandre; Rabissi, Agnese; Lumbreras, Victoria; González-Guzmán, Miguel; Antoni, Regina; Rodrı́guez, Pedro L.; Baena-González, Elena

doi:10.1105/tpc.113.114066

Cited by 259 publications

(258 citation statements)

References 92 publications

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“…Here, the limitations of mutant approaches become obvious, as indirect effects are difficult to evaluate. Observations such as phosphorylation of SnRK1 by SnRK2, which has been found in phosphoproteomic studies (Umezawa et al, 2013), or crosstalk via PP2C phosphatases (Rodrigues et al, 2013) might explain these findings.…”

Section: Bzip1 and Bzip53 Reprogram Primary Carbohydrate And Amino Acmentioning

confidence: 92%

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Crosstalk between Two bZIP Signaling Pathways Orchestrates Salt-Induced Metabolic Reprogramming in Arabidopsis Roots

et al. 2015

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ORCID IDs: 0000-0003-3058-7570 (A.F.); 0000-0002-7910-9118 (J.S.); 0000-0001-8122-5460 (M.J.M.); 0000-0002-6332-1712 (J.V.-C.); 0000-0002-5605-7984 (J.H.)Soil salinity increasingly causes crop losses worldwide. Although roots are the primary targets of salt stress, the signaling networks that facilitate metabolic reprogramming to induce stress tolerance are less understood than those in leaves. Here, a combination of transcriptomic and metabolic approaches was performed in salt-treated Arabidopsis thaliana roots, which revealed that the group S1 basic leucine zipper transcription factors bZIP1 and bZIP53 reprogram primary C-and N-metabolism. In particular, gluconeogenesis and amino acid catabolism are affected by these transcription factors. Importantly, bZIP1 expression reflects cellular stress and energy status in roots. In addition to the well-described abiotic stress response pathway initiated by the hormone abscisic acid (ABA) and executed by SnRK2 (Snf1-RELATED-PROTEIN-KINASE2) and AREB-like bZIP factors, we identify a structurally related ABA-independent signaling module consisting of SnRK1s and S1 bZIPs. Crosstalk between these signaling pathways recruits particular bZIP factor combinations to establish at least four distinct gene expression patterns. Understanding this signaling network provides a framework for securing future crop productivity.

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Section: Bzip1 and Bzip53 Reprogram Primary Carbohydrate And Amino Acmentioning

confidence: 92%

“…Class 4 genes depend on group C, and S1 bZIPs and are independent of AREB-like TFs. A potential interaction between SnRK1 and SnRK2 kinases is proposed by Umezawa et al (2013) and Rodrigues et al (2013).…”

Section: Bzip1 and Bzip53 Reprogram Primary Carbohydrate And Amino Acmentioning

confidence: 99%

Crosstalk between Two bZIP Signaling Pathways Orchestrates Salt-Induced Metabolic Reprogramming in Arabidopsis Roots

et al. 2015

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“…This response seems essential in low R:FR light and short photoperiods, conditions associated with reduced photosynthesis, energy deprivation, and stress in which ABA is required (30). The molecular mechanisms by which this hormone controls bud growth are yet to be determined.…”

Section: Discussionmentioning

confidence: 99%

Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds

González-Grandío

Pajoro

Franco-Zorrilla

et al. 2016

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

243

239

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Shoot-branching patterns determine key aspects of plant life and are important targets for crop breeding. However, we are still largely ignorant of the genetic networks controlling locally the most important decision during branch development: whether the axillary bud, or branch primordium, grows out to give a lateral shoot or remains dormant. Here we show that, inside the buds, the TEOSINTE BRANCHED1, CYCLOIDEA, PCF (TCP) transcription factor BRANCHED1 (BRC1) binds to and positively regulates the transcription of three related Homeodomain leucine zipper protein (HD-ZIP)-encoding genes: HOMEOBOX PROTEIN 21 (HB21), HOMEOBOX PROTEIN 40 (HB40), and HOMEOBOX PROTEIN 53 (HB53). These three genes, together with BRC1, enhance 9-CIS-EPOXICAROTENOID DIOXIGENASE 3 (NCED3) expression, lead to abscisic acid accumulation, and trigger hormone response, thus causing suppression of bud development. This TCP/HD-ZIP genetic module seems to be conserved in dicot and monocotyledonous species to prevent branching under light-limiting conditions.

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“…Conserved amino acid residues in the RCAR molecule and a conserved tryptophan residue found in clade A PP2Cs coordinate the phytohormone by direct ionic interaction and/or water-mediated hydrogen bonds. ABA coreceptors present in the cytosol and nucleus (8,20,21) target protein kinases, transcription factors, and ion channels for ABAdependent regulation (22)(23)(24)(25)(26). The PP2Cs negatively regulate SNF1-related kinases such as OST1/SnrK2.6/SnrK2E, SnrK2.2/ SnrK2D, and SnRK2.3/SnrK2I (27,28).…”

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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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ABI1 and PP2CA Phosphatases Are Negative Regulators of Snf1-Related Protein Kinase1 Signaling in Arabidopsis

Cited by 259 publications

References 92 publications

Crosstalk between Two bZIP Signaling Pathways Orchestrates Salt-Induced Metabolic Reprogramming in Arabidopsis Roots

Crosstalk between Two bZIP Signaling Pathways Orchestrates Salt-Induced Metabolic Reprogramming in Arabidopsis Roots

Abscisic acid signaling is controlled by a BRANCHED1/HD-ZIP I cascade in Arabidopsis axillary buds

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

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