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Depletion of abscisic acid levels in roots of flooded Carrizo citrange (Poncirus trifoliata L. Raf. × Citrus sinensis L. Osb.) plants is a stress-specific response associated to the differential expression of PYR/PYL/RCAR receptors

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Abstract

Soil flooding reduces root abscisic acid (ABA) levels in citrus, conversely to what happens under drought. Despite this reduction, microarray analyses suggested the existence of a residual ABA signaling in roots of flooded Carrizo citrange seedlings. The comparison of ABA metabolism and signaling in roots of flooded and water stressed plants of Carrizo citrange revealed that the hormone depletion was linked to the upregulation of CsAOG, involved in ABA glycosyl ester (ABAGE) synthesis, and to a moderate induction of catabolism (CsCYP707A, an ABA 8′-hydroxylase) and buildup of dehydrophaseic acid (DPA). Drought strongly induced both ABA biosynthesis and catabolism (CsNCED1, 9-cis-neoxanthin epoxycarotenoid dioxygenase 1, and CsCYP707A) rendering a significant hormone accumulation. In roots of flooded plants, restoration of control ABA levels after stress release was associated to the upregulation of CsBGLU18 (an ABA β-glycosidase) that cleaves ABAGE. Transcriptional profile of ABA receptor genes revealed a different induction in response to soil flooding (CsPYL5) or drought (CsPYL8). These two receptor genes along with CsPYL1 were cloned and expressed in a heterologous system. Recombinant CsPYL5 inhibited ΔNHAB1 activity in vitro at lower ABA concentrations than CsPYL8 or CsPYL1, suggesting its better performance under soil flooding conditions. Both stress conditions induced ABA-responsive genes CsABI5 and CsDREB2A similarly, suggesting the occurrence of ABA signaling in roots of flooded citrus seedlings. The impact of reduced ABA levels in flooded roots on CsPYL5 expression along with its higher hormone affinity reinforce the role of this ABA receptor under soil-flooding conditions and explain the expression of certain ABA-responsive genes.

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Acknowledgements

This work was supported by Ministerio de Economía y Competitividad (MINECO), Fondo Europeo de Desarrollo Regional (FEDER) and Universitat Jaume I through grants No. AGL201676574-R, UJI-B2016-23/UJI-B2016-24 to A.G-C. and V.A. and MINECO, FEDER and Consejo Superior de Investigaciones Cientificas (CSIC) through grant BIO2014-52537-R to P.L.R. S.I.Z. and M.M. were supported by predoctoral grants from Universitat Jaume I and Generalitat Valenciana, respectively. M.G.G. was recipient of a “JAE-DOC” contract from the CSIC. Mass spectrometry analyses were performed at the central facilities (Servei Central d’Instrumentació Científica, SCIC) of Universitat Jaume I.

Author contributions

V.A. and A.G.C. planned and designed the experiments and analyzed microarray data, M.M. and S.I.Z. performed experiments and analyzed citrus samples, P.R. and M.G.G. planned and designed PYR/PYL receptor cloning, V.A. and M.G.G. performed cloning of selected genes and in vitro analyses, V.A., M.G.G., M.M. and S.I.Z. analyzed data and prepared figures and tables and V.A. wrote first draft of the manuscript. V.A., A.G.C., P.R., M.G.G., M.M. and S.I.Z. participated in the discussion of results and manuscript writing. All authors have read and approved the final version of the manuscript and declare that they have no conflicts of interest.

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  1. Miguel González-Guzmán

    Present address: Departamento de Biología Medioambiental, Centro de Investigaciones Biológicas, CSIC, 28040, Madrid, Spain

Authors and Affiliations

  1. Ecofisiologia i Biotecnologia Department Ciències Agràries i del Medi Natural, Universitat Jaume I, 12071, Castelló de la Plana, Spain

    Vicent Arbona, Sara I. Zandalinas, Matías Manzi & Aurelio Gómez-Cadenas

  2. Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas-Universidad Politécnica de Valencia, 46022, Valencia, Spain

    Miguel González-Guzmán & Pedro L. Rodriguez

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  1. Vicent Arbona
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Correspondence to Vicent Arbona.

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Arbona, V., Zandalinas, S.I., Manzi, M. et al. Depletion of abscisic acid levels in roots of flooded Carrizo citrange (Poncirus trifoliata L. Raf. × Citrus sinensis L. Osb.) plants is a stress-specific response associated to the differential expression of PYR/PYL/RCAR receptors. Plant Mol Biol 93, 623–640 (2017). https://doi.org/10.1007/s11103-017-0587-7

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