The Role of ABA in Plant Immunity is Mediated through the PYR1 Receptor

[EN] ABA is involved in plant responses to a broad range of pathogens and exhibits complex antagonistic and synergistic relationships with salicylic acid (SA) and ethylene (ET) signaling pathways, respectively. However, the specific receptor of ABA that triggers the positive and negative responses of ABA during immune responses remains unknown. Through a reverse genetic analysis, we identified that PYR1, a member of the family of PYR/PYL/RCAR ABA receptors, is transcriptionally upregulated and specifically perceives ABA during biotic stress, initiating downstream signaling mediated by ABA-activated SnRK2 protein kinases. This exerts a damping effect on SA-mediated signaling, required for resistance to biotrophic pathogens, and simultaneously a positive control over the resistance to necrotrophic pathogens controlled by ET. We demonstrated that PYR1-mediated signaling exerted control on a priori established hormonal cross-talk between SA and ET, thereby redirecting defense outputs. Defects in ABA/PYR1 signaling activated SA biosynthesis and sensitized plants for immune priming by poising SA-responsive genes for enhanced expression. As a trade-off effect,pyr1-mediated activation of the SA pathway blunted ET perception, which is pivotal for the activation of resistance towards fungal necrotrophs. The specific perception of ABA by PYR1 represented a regulatory node, modulating different outcomes in disease resistance.This research was founded by the Spanish AEI agency by grant BIO2017-82503-R to P.L.R. and by grant RTI2018-098501-B-I00 to P.V.García-Andrade, J.; González, B.; Gonzalez-Guzman, M.; Rodríguez Egea, PL.; Vera Vera, P. (2020). The Role of ABA in Plant Immunity is Mediated through the PYR1 Receptor. International Journal of Molecular Sciences. 21(16):1-21. https://doi.org/10.3390/ijms211658521212116Malamy, J., Carr, J. P., Klessig, D. F., & Raskin, I. (1990). Salicylic Acid: A Likely Endogenous Signal in the Resistance Response of Tobacco to Viral Infection. Science, 250(4983), 1002-1004. doi:10.1126/science.250.4983.1002Métraux, J. P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., … Inverardi, B. (1990). Increase in Salicylic Acid at the Onset of Systemic Acquired Resistance in Cucumber. Science, 250(4983), 1004-1006. doi:10.1126/science.250.4983.1004Glazebrook, J. (2005). Contrasting Mechanisms of Defense Against Biotrophic and Necrotrophic Pathogens. Annual Review of Phytopathology, 43(1), 205-227. doi:10.1146/annurev.phyto.43.040204.135923Verhage, A., van Wees, S. C. M., & Pieterse, C. M. J. (2010). Plant Immunity: It’s the Hormones Talking, But What Do They Say?: Figure 1. Plant Physiology, 154(2), 536-540. doi:10.1104/pp.110.161570Broekaert, W. F., Delauré, S. L., De Bolle, M. F. C., & Cammue, B. P. A. (2006). The Role of Ethylene in Host-Pathogen Interactions. Annual Review of Phytopathology, 44(1), 393-416. doi:10.1146/annurev.phyto.44.070505.143440Grant, M. R., & Jones, J. D. G. (2009). Hormone (Dis)harmony Moulds Plant Health and Disease. Science, 324(5928), 750-752. doi:10.1126/science.1173771Pieterse, C. M. J., Van der Does, D., Zamioudis, C., Leon-Reyes, A., & Van Wees, S. C. M. (2012). Hormonal Modulation of Plant Immunity. Annual Review of Cell and Developmental Biology, 28(1), 489-521. doi:10.1146/annurev-cellbio-092910-154055Thaler, J. S., & Bostock, R. M. (2004). INTERACTIONS BETWEEN ABSCISIC-ACID-MEDIATED RESPONSES AND PLANT RESISTANCE TO PATHOGENS AND INSECTS. Ecology, 85(1), 48-58. doi:10.1890/02-0710Spoel, S. H., Koornneef, A., Claessens, S. M. C., Korzelius, J. P., Van Pelt, J. A., Mueller, M. J., … Pieterse, C. M. J. (2003). NPR1 Modulates Cross-Talk between Salicylate- and Jasmonate-Dependent Defense Pathways through a Novel Function in the Cytosol. The Plant Cell, 15(3), 760-770. doi:10.1105/tpc.009159Thomma, B. P. H. J., Eggermont, K., Tierens, K. F. M.-J., & Broekaert, W. F. (1999). Requirement of Functional Ethylene-Insensitive 2Gene for Efficient Resistance of Arabidopsis to Infection by Botrytis cinerea . Plant Physiology, 121(4), 1093-1101. doi:10.1104/pp.121.4.1093Gu, Y.-Q., Yang, C., Thara, V. K., Zhou, J., & Martin, G. B. (2000). Pti4 Is Induced by Ethylene and Salicylic Acid, and Its Product Is Phosphorylated by the Pto Kinase. The Plant Cell, 12(5), 771-785. doi:10.1105/tpc.12.5.771Berrocal-Lobo, M., Molina, A., & Solano, R. (2002). Constitutive expression ofETHYLENE-RESPONSE-FACTOR1inArabidopsisconfers resistance to several necrotrophic fungi. The Plant Journal, 29(1), 23-32. doi:10.1046/j.1365-313x.2002.01191.xDı́az, J., ten Have, A., & van Kan, J. A. L. (2002). The Role of Ethylene and Wound Signaling in Resistance of Tomato to Botrytis cinerea . Plant Physiology, 129(3), 1341-1351. doi:10.1104/pp.001453Leslie, C. A., & Romani, R. J. (1988). Inhibition of Ethylene Biosynthesis by Salicylic Acid. Plant Physiology, 88(3), 833-837. doi:10.1104/pp.88.3.833Chen, H., Xue, L., Chintamanani, S., Germain, H., Lin, H., Cui, H., … Zhou, J.-M. (2009). ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 Repress SALICYLIC ACID INDUCTION DEFICIENT2 Expression to Negatively Regulate Plant Innate Immunity in Arabidopsis . The Plant Cell, 21(8), 2527-2540. doi:10.1105/tpc.108.065193Huang, P., Dong, Z., Guo, P., Zhang, X., Qiu, Y., Li, B., … Guo, H. (2019). Salicylic Acid Suppresses Apical Hook Formation via NPR1-Mediated Repression of EIN3 and EIL1 in Arabidopsis. The Plant Cell, 32(3), 612-629. doi:10.1105/tpc.19.00658Spoel, S. H., Johnson, J. S., & Dong, X. (2007). Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proceedings of the National Academy of Sciences, 104(47), 18842-18847. doi:10.1073/pnas.0708139104Cutler, S. R., Rodriguez, P. L., Finkelstein, R. R., & Abrams, S. R. (2010). Abscisic Acid: Emergence of a Core Signaling Network. Annual Review of Plant Biology, 61(1), 651-679. doi:10.1146/annurev-arplant-042809-112122Mauch-Mani, B., & Mauch, F. (2005). The role of abscisic acid in plant–pathogen interactions. Current Opinion in Plant Biology, 8(4), 409-414. doi:10.1016/j.pbi.2005.05.015Asselbergh, B., De Vleesschauwer, D., & Höfte, M. (2008). Global Switches and Fine-Tuning—ABA Modulates Plant Pathogen Defense. Molecular Plant-Microbe Interactions®, 21(6), 709-719. doi:10.1094/mpmi-21-6-0709Fan, J., Hill, L., Crooks, C., Doerner, P., & Lamb, C. (2009). Abscisic Acid Has a Key Role in Modulating Diverse Plant-Pathogen Interactions . Plant Physiology, 150(4), 1750-1761. doi:10.1104/pp.109.137943Sánchez-Vallet, A., López, G., Ramos, B., Delgado-Cerezo, M., Riviere, M.-P., Llorente, F., … Molina, A. (2012). Disruption of Abscisic Acid Signaling Constitutively Activates Arabidopsis Resistance to the Necrotrophic Fungus Plectosphaerella cucumerina . Plant Physiology, 160(4), 2109-2124. doi:10.1104/pp.112.200154Adie, B. A. T., Pérez-Pérez, J., Pérez-Pérez, M. M., Godoy, M., Sánchez-Serrano, J.-J., Schmelz, E. A., & Solano, R. (2007). ABA Is an Essential Signal for Plant Resistance to Pathogens Affecting JA Biosynthesis and the Activation of Defenses in Arabidopsis. The Plant Cell, 19(5), 1665-1681. doi:10.1105/tpc.106.048041García-Andrade, J., Ramírez, V., Flors, V., & Vera, P. (2011). Arabidopsis ocp3 mutant reveals a mechanism linking ABA and JA to pathogen-induced callose deposition. The Plant Journal, 67(5), 783-794. doi:10.1111/j.1365-313x.2011.04633.xJensen, M. K., Hagedorn, P. H., de Torres-Zabala, M., Grant, M. R., Rung, J. H., Collinge, D. B., & Lyngkjaer, M. F. (2008). Transcriptional regulation by an NAC (NAM-ATAF1,2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towardsBlumeria graminisf. sp.hordeiin Arabidopsis. The Plant Journal, 56(6), 867-880. doi:10.1111/j.1365-313x.2008.03646.xDe Torres-Zabala, M., Truman, W., Bennett, M. H., Lafforgue, G., Mansfield, J. W., Rodriguez Egea, P., … Grant, M. (2007). Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. The EMBO Journal, 26(5), 1434-1443. doi:10.1038/sj.emboj.7601575Mine, A., Berens, M. L., Nobori, T., Anver, S., Fukumoto, K., Winkelmüller, T. M., … Tsuda, K. (2017). Pathogen exploitation of an abscisic acid- and jasmonate-inducible MAPK phosphatase and its interception by Arabidopsis immunity. Proceedings of the National Academy of Sciences, 114(28), 7456-7461. doi:10.1073/pnas.1702613114Peng, Z., Hu, Y., Zhang, J., Huguet-Tapia, J. C., Block, A. K., Park, S., … White, F. F. (2019). Xanthomonas translucens commandeers the host rate-limiting step in ABA biosynthesis for disease susceptibility. Proceedings of the National Academy of Sciences, 116(42), 20938-20946. doi:10.1073/pnas.1911660116Chen, W., Provart, N. J., Glazebrook, J., Katagiri, F., Chang, H.-S., Eulgem, T., … Zhu, T. (2002). Expression Profile Matrix of Arabidopsis Transcription Factor Genes Suggests Their Putative Functions in Response to Environmental Stresses[W]. The Plant Cell, 14(3), 559-574. doi:10.1105/tpc.010410Anderson, J. P., Badruzsaufari, E., Schenk, P. M., Manners, J. M., Desmond, O. J., Ehlert, C., … Kazan, K. (2004). Antagonistic Interaction between Abscisic Acid and Jasmonate-Ethylene Signaling Pathways Modulates Defense Gene Expression and Disease Resistance in Arabidopsis. The Plant Cell, 16(12), 3460-3479. doi:10.1105/tpc.104.025833Yang, Z., Tian, L., Latoszek-Green, M., Brown, D., & Wu, K. (2005). Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Molecular Biology, 58(4), 585-596. doi:10.1007/s11103-005-7294-5Dittrich, M., Mueller, H. M., Bauer, H., Peirats-Llobet, M., Rodriguez, P. L., Geilfus, C.-M., … Hedrich, R. (2019). The role of Arabidopsis ABA receptors from the PYR/PYL/RCAR family in stomatal acclimation and closure signal integration. Nature Plants, 5(9), 1002-1011. doi:10.1038/s41477-019-0490-0Hubbard, K. E., Nishimura, N., Hitomi, K., Getzoff, E. D., & Schroeder, J. I. (2010). Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes & Development, 24(16), 1695-1708. doi:10.1101/gad.1953910Klingler, J. P., Batelli, G., & Zhu, J.-K. (2010). ABA receptors: the START of a new paradigm in phytohormone signalling. Journal of Experimental Botany, 61(12), 3199-3210. doi:10.1093/jxb/erq151Raghavendra, A. S., Gonugunta, V. K., Christmann, A., & Grill, E. (2010). ABA perception and signalling. Trends in Plant Science, 15(7), 395-401. doi:10.1016/j.tplants.2010.04.006Umezawa, T., Sugiyama, N., Mizoguchi, M., Hayashi, S., Myouga, F., Yamaguchi-Shinozaki, K., … Shinozaki, K. (2009). Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proceedings of the National Academy of Sciences, 106(41), 17588-17593. doi:10.1073/pnas.0907095106Vlad, F., Rubio, S., Rodrigues, A., Sirichandra, C., Belin, C., Robert, N., … Merlot, S. (2009). Protein Phosphatases 2C Regulate the Activation of the Snf1-Related Kinase OST1 by Abscisic Acid inArabidopsis . The Plant Cell, 21(10), 3170-3184. doi:10.1105/tpc.109.069179Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S.-Y., … Zhu, J.-K. (2009). In vitro reconstitution of an abscisic acid signalling pathway. Nature, 462(7273), 660-664. doi:10.1038/nature08599Ma, Y., Szostkiewicz, I., Korte, A., Moes, D., Yang, Y., Christmann, A., & Grill, E. (2009). Regulators of PP2C Phosphatase Activity Function as Abscisic Acid Sensors. Science, 324(5930), 1064-1068. doi:10.1126/science.1172408Park, S.-Y., Fung, P., Nishimura, N., Jensen, D. R., Fujii, H., Zhao, Y., … Cutler, S. R. (2009). Abscisic Acid Inhibits Type 2C Protein Phosphatases via the PYR/PYL Family of START Proteins. Science, 324(5930), 1068-1071. doi:10.1126/science.1173041Umezawa, T., Sugiyama, N., Takahashi, F., Anderson, J. C., Ishihama, Y., Peck, S. C., & Shinozaki, K. (2013). Genetics and Phosphoproteomics Reveal a Protein Phosphorylation Network in the Abscisic Acid Signaling Pathway in Arabidopsis thaliana. Science Signaling, 6(270). doi:10.1126/scisignal.2003509Gonzalez-Guzman, M., Pizzio, G. A., Antoni, R., Vera-Sirera, F., Merilo, E., Bassel, G. W., … Rodriguez, P. L. (2012). Arabidopsis PYR/PYL/RCAR Receptors Play a Major Role in Quantitative Regulation of Stomatal Aperture and Transcriptional Response to Abscisic Acid. The Plant Cell, 24(6), 2483-2496. doi:10.1105/tpc.112.098574González-Guzmán, M., Rodríguez, L., Lorenzo-Orts, L., Pons, C., Sarrión-Perdigones, A., Fernández, M. A., … Rodríguez, P. L. (2014). Tomato PYR/PYL/RCAR abscisic acid receptors show high expression in root, differential sensitivity to the abscisic acid agonist quinabactin, and the capability to enhance plant drought resistance. Journal of Experimental Botany, 65(15), 4451-4464. doi:10.1093/jxb/eru219Helander, J. D. M., Vaidya, A. S., & Cutler, S. R. (2016). Chemical manipulation of plant water use. Bioorganic & Medicinal Chemistry, 24(3), 493-500. doi:10.1016/j.bmc.2015.11.010Antoni, R., Gonzalez-Guzman, M., Rodriguez, L., Rodrigues, A., Pizzio, G. A., & Rodriguez, P. L. (2011). Selective Inhibition of Clade A Phosphatases Type 2C by PYR/PYL/RCAR Abscisic Acid Receptors . Plant Physiology, 158(2), 970-980. doi:10.1104/pp.111.188623Tischer, S. V., Wunschel, C., Papacek, M., Kleigrewe, K., Hofmann, T., Christmann, A., & Grill, E. (2017). Combinatorial interaction network of abscisic acid receptors and coreceptors fromArabidopsis thaliana. Proceedings of the National Academy of Sciences, 114(38), 10280-10285. doi:10.1073/pnas.1706593114Antoni, R., Gonzalez-Guzman, M., Rodriguez, L., Peirats-Llobet, M., Pizzio, G. A., Fernandez, M. A., … Rodriguez, P. L. (2012). PYRABACTIN RESISTANCE1-LIKE8 Plays an Important Role for the Regulation of Abscisic Acid Signaling in Root . Plant Physiology, 161(2), 931-941. doi:10.1104/pp.112.208678Fujii, H., Verslues, P. E., & Zhu, J.-K. (2007). Identification of Two Protein Kinases Required for Abscisic Acid Regulation of Seed Germination, Root Growth, and Gene Expression in Arabidopsis. The Plant Cell, 19(2), 485-494. doi:10.1105/tpc.106.048538García-Andrade, J., Ramírez, V., López, A., & Vera, P. (2013). Mediated Plastid RNA Editing in Plant Immunity. PLoS Pathogens, 9(10), e1003713. doi:10.1371/journal.ppat.1003713Rubio, S., Rodrigues, A., Saez, A., Dizon, M. B., Galle, A., Kim, T.-H., … Rodriguez, P. L. (2009). Triple Loss of Function of Protein Phosphatases Type 2C Leads to Partial Constitutive Response to Endogenous Abscisic Acid . Plant Physiology, 150(3), 1345-1355. doi:10.1104/pp.109.137174Schweighofer, A., Hirt, H., & Meskiene, I. (2004). Plant PP2C phosphatases: emerging functions in stress signaling. Trends in Plant Science, 9(5), 236-243. doi:10.1016/j.tplants.2004.03.007Carrasco, J. L. (2003). A novel transcription factor involved in plant defense endowed with protein phosphatase activity. The EMBO Journal, 22(13), 3376-3384. doi:10.1093/emboj/cdg323Carrasco, J. L., Castelló, M. J., Naumann, K., Lassowskat, I., Navarrete-Gómez, M., Scheel, D., & Vera, P. (2014). Arabidopsis Protein Phosphatase DBP1 Nucleates a Protein Network with a Role in Regulating Plant Defense. PLoS ONE, 9(3), e90734. doi:10.1371/journal.pone.0090734Clarke, J. D., Volko, S. M., Ledford, H., Ausubel, F. M., & Dong, X. (2000). Roles of Salicylic Acid, Jasmonic Acid, and Ethylene in cpr-Induced Resistance in Arabidopsis. The Plant Cell, 12(11), 2175-2190. doi:10.1105/tpc.12.11.2175Wildermuth, M. C., Dewdney, J., Wu, G., & Ausubel, F. M. (2001). Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414(6863), 562-565. doi:10.1038/35107108Garcion, C., Lohmann, A., Lamodière, E., Catinot, J., Buchala, A., Doermann, P., & Métraux, J.-P. (2008). Characterization and Biological Function of the ISOCHORISMATE SYNTHASE2 Gene of Arabidopsis. Plant Physiology, 147(3), 1279-1287. doi:10.1104/pp.108.119420Mauch-Mani, B., Baccelli, I., Luna, E., & Flors, V. (2017). Defense Priming: An Adaptive Part of Induced Resistance. Annual Review of Plant Biology, 68(1), 485-512. doi:10.1146/annurev-arplant-042916-041132Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., … Ryals, J. (1993). Requirement of Salicylic Acid for the Induction of Systemic Acquired Resistance. Science, 261(5122), 754-756. doi:10.1126/science.261.5122.754Cheng, W.-H., Endo, A., Zhou, L., Penney, J., Chen, H.-C., Arroyo, A., … Sheen, J. (2002). A Unique Short-Chain Dehydrogenase/Reductase in Arabidopsis Glucose Signaling and Abscisic Acid Biosynthesis and Functions. The Plant Cell, 14(11), 2723-2743. doi:10.1105/tpc.006494Koiwai, H., Nakaminami, K., Seo, M., Mitsuhashi, W., Toyomasu, T., & Koshiba, T. (2004). Tissue-Specific Localization of an Abscisic Acid Biosynthetic Enzyme, AAO3, in Arabidopsis. Plant Physiology, 134(4), 1697-1707. doi:10.1104/pp.103.036970Endo, A., Koshiba, T., Kamiya, Y., & Nambara, E. (2008). Vascular system is a node of systemic stress responses. Plant Signaling & Behavior, 3(12), 1138-1140. doi:10.4161/psb.3.12.7145Endo, A., Sawada, Y., Takahashi, H., Okamoto, M., Ikegami, K., Koiwai, H., … Nambara, E. (2008). Drought Induction of Arabidopsis 9-cis-Epoxycarotenoid Dioxygenase Occurs in Vascular Parenchyma Cells . Plant Physiology, 147(4), 1984-1993. doi:10.1104/pp.108.116632Alvarez, M. E., Pennell, R. I., Meijer, P.-J., Ishikawa, A., Dixon, R. A., & Lamb, C. (1998). Reactive Oxygen Intermediates Mediate a Systemic Signal Network in the Establishment of Plant Immunity. Cell, 92(6), 773-784. doi:10.1016/s0092-8674(00)81405-1Yu, A., Lepere, G., Jay, F., Wang, J., Bapaume, L., Wang, Y., … Navarro, L. (2013). Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proceedings of the National Academy of Sciences, 110(6), 2389-2394. doi:10.1073/pnas.1211757110Flors, V., Ton, J., Van Doorn, R., Jakab, G., García-Agustín, P., & Mauch-Mani, B. (2007). Interplay between JA, SA and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. The Plant Journal, 54(1), 81-92. doi:10.1111/j.1365-313x.2007.03397.xPétriacq, P., Stassen, J. H. M., & Ton, J. (2016). Spore Density Determines Infection Strategy by the Plant Pathogenic Fungus Plectosphaerella cucumerina. Plant Physiology, 170(4), 2325-2339. doi:10.1104/pp.15.00551Koornneef, A., & Pieterse, C. M. J. (2008). Cross Talk in Defense Signaling. Plant Physiology, 146(3), 839-844. doi:10.1104/pp.107.112029Ton, J., Flors, V., & Mauch-Mani, B. (2009). The multifaceted role of ABA in disease resistance. Trends in Plant Science, 14(6), 310-317. doi:10.1016/j.tplants.2009.03.006De Vleesschauwer, D., Yang, Y., Vera Cruz, C., & Höfte, M. (2010). Abscisic Acid-Induced Resistance against the Brown Spot Pathogen Cochliobolus miyabeanus in Rice Involves MAP Kinase-Mediated Repression of Ethylene Signaling . Plant Physiology, 152(4), 2036-2052. doi:10.1104/pp.109.152702De Torres Zabala, M., Bennett, M. H., Truman, W. H., & Grant, M. R. (2009). Antagonism between salicylic and abscisic acid reflects early host-pathogen conflict and moulds plant defence responses. The Plant Journal, 59(3), 375-386. doi:10.1111/j.1365-313x.2009.03875.xBelin, C., de Franco, P.-O., Bourbousse, C., Chaignepain, S., Schmitter, J.-M., Vavasseur, A., … Thomine, S. (2006). Identification of Features Regulating OST1 Kinase Activity and OST1 Function in Guard Cells . Plant Physiology, 141(4), 1316-1327. doi:10.1104/pp.106.079327Planes, M. D., Niñoles, R., Rubio, L., Bissoli, G., Bueso, E., García-Sánchez, M. J., … Serrano, R. (2014). A mechanism of growth inhibition by abscisic acid in germinating seeds of Arabidopsis thaliana based on inhibition of plasma membrane H+-ATPase and decreased cytosolic pH, K+, and anions. Journal of Experimental Botany, 66(3), 813-825. doi:10.1093/jxb/eru44