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Arabidopsis abscisic acid receptors play an important role in disease resistance

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Abstract

Stomata are natural pores of plants and constitute the entry points for water during transpiration. However, they also facilitate the ingress of potentially harmful bacterial pathogens. The phytohormone abscisic acid (ABA) plays a pivotal role in protecting plants against biotic stress, by regulating stomatal closure. In the present study, we investigated the mechanism whereby ABA influences plant defense responses to Pseudomonas syringae pv. tomato (Pst) DC3000, which is a virulent bacterial pathogen of Arabidopsis, at the pre-invasive stage. We found that overexpression of two ABA receptors, namely, RCAR4/PYL10-OX and RCAR5/PYL11-OX (hereafter referred to as RCARs), resulted in ABA-hypersensitive phenotypes being exhibited during the seed germination and seedling growth stages. Sensitivity to ABA enhanced the resistance of RCAR4-OX and RCAR5-OX plants to Pst DC3000, through promoting stomatal closure leading to the development of resistance to this bacterial pathogen. Protein phosphatase HAB1 is an important component that is responsible for ABA signaling and which interacts with ABA receptors. We found that hab1 mutants exhibited enhanced resistance to Pst DC3000; moreover, similar to RCAR4-OX and RCAR5-OX plants, this enhanced resistance was correlated with stomatal closure. Taken together, our findings demonstrate that alteration of RCAR4- or RCAR5-HAB1 mediated ABA signaling influences resistance to bacterial pathogens via stomatal regulation.

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Abbreviations

ABA:

Abscisic acid

ABI:

ABA-insensitive

AHG:

ABA-hypersensitive germination

AIP:

AKT1 interacting protein phosphatase

AIPH:

AIP1 homologue

BiFC:

Bimolecular fluorescence complementation

cfu:

Colony forming units

HAB:

Hypersensitive to ABA

hpi:

Hours post-inoculation

PAMPs:

Pathogen-associated molecular patterns

PP2C:

Protein phosphatase type 2 C

PRR:

Pattern recognition receptors

Pst :

Pseudomonas syringae pv. tomato

PYL:

PYR-like

PYR:

Pyrabactin resistance

qRT-PCR:

Quantitative reverse transcription-polymerase chain reaction

RCAR:

Regulatory component of ABA receptor

SOS:

Stomatal opening solution

WT:

Wild-type

References

  • Amborabe BE, Bonmort J, Fleurat-Lessard P, Roblin G (2008) Early events induced by chitosan on plant cells. J Exp Bot 59:2317–2324

    Article  CAS  PubMed  Google Scholar 

  • Antoni R, Gonzalez-Guzman M, Rodriguez L, Rodrigues A, Pizzio GA, Rodriguez PL (2012) Selective inhibition of clade A phosphatases type 2C by PYR/PYL/RCAR abscisic acid receptors. Plant Physiol 158:970–980

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aubert Y, Vile D, Pervent M, Aldon D, Ranty B, Simonneau T, Vavasseur A, Galaud JP (2010) RD20, a stress-inducible caleosin, participates in stomatal control, transpiration and drought tolerance in Arabidopsis thaliana. Plant Cell Physiol 51:1975–1987

    Article  CAS  PubMed  Google Scholar 

  • Cao FY, Yoshioka K, Desveaux D (2011) The roles of ABA in plant–pathogen interactions. J Plant Res 124:489–499

    Article  CAS  PubMed  Google Scholar 

  • Cho SM, Kang BR, Han SH, Anderson AJ, Park JY, Lee YH, Cho BH, Yang KY, Ryu CM, Kim YC (2008) 2R,3R-butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol Plant Microbe Interact 21:1067–1075

    Article  CAS  PubMed  Google Scholar 

  • Christmann A, Grill E (2009) Are GTGs ABA’s biggest fans? Cell 136:21–23

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • de Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW, Egea PR, Bogre L, Grant M (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J 26:1434–1443

    Article  PubMed Central  PubMed  Google Scholar 

  • Desclos-Theveniau M, Arnaud D, Huang TY, Lin GJC, Chen WY, Lin YC, Zimmerli L (2012) The Arabidopsis lectin receptor kinase LecRK-V.5 represses stomatal immunity induced by Pseudomonas syringae pv. tomato DC3000. PLoS Pathog 8:e1002513

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Feng DX, Tasset C, Hanemian M, Barlet X, Hu J, Trémousaygue D, Deslandes L, Marco Y (2012) Biological control of bacterial wilt in Arabidopsis thaliana involves abscissic acid signalling. New Phytol 194:1035–1045

    Article  CAS  PubMed  Google Scholar 

  • Fujii H, Verslues PE, Zhu JK (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19:485–494

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hao Q, Yin P, Li W, Wang L, Yan C, Lin Z, Wu JZ, Wang J, Yan SF, Yan N (2011) The molecular basis of ABA-independent inhibition of PP2Cs by a subclass of PYL proteins. Mol Cell 42:662–672

    Article  PubMed  Google Scholar 

  • Ito H, Fukuda Y, Murata K, Kimura A (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153:163–168

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Karimi M, Inze D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Pant Sci 7:193–195

    Article  CAS  Google Scholar 

  • Katagiri F, Thilmony R, He SY (2002) The Arabidopsis thalianaPseudomonas syringae interaction. Arabidopsis Book 1:e0039

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ 35:53–60

    Article  CAS  PubMed  Google Scholar 

  • Lee SC, Lan WZ, Kim BG, Li L, Cheong YH, Pandey GK, Lu G, Buchanan BB, Luan S (2007) A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc Natl Acad Sci USA 104:15959–15964

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lee SC, Lan W, Buchanan BB, Luan S (2009) A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc Natl Acad Sci USA 106:21419–21424

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lee SC, Lim CW, Lan W, He K, Luan S (2013) ABA signaling in guard cells entails a dynamic protein–protein interaction relay from the PYL–RCAR family receptors to ion channels. Mol Plant 6:528–538

    Article  CAS  PubMed  Google Scholar 

  • Lim CW, Baek W, Han SW, Lee SC (2013) Arabidopsis PYL8 plays an important role for ABA signaling and drought stress responses. Plant Pathol J 29:471–476

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lim CW, Luan S, Lee SC (2014) A prominent role for RCAR3-mediated ABA signaling in response to Pseudomonas syringae pv. tomato DC3000 infection in Arabidopsis. Plant Cell Physiol 55:1691–1703

    Article  PubMed  Google Scholar 

  • Liu SH, Fu BY, Xu HX, Zhu LH, Zhai HQ, Li ZK (2007) Cell death in response to osmotic and salt stresses in two rice (Oryza sativa L.) ecotypes. Plant Sci 172:897–902

    Article  CAS  Google Scholar 

  • Ma 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 324:1064–1068  

  • Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980

    Article  CAS  PubMed  Google Scholar 

  • Melotto M, Underwood W, He SY (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 46:101–122

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001) The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J 25:295–303

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rubio S, Rodrigues A, Saez A, Dizon MB, Galle A, Kim TH, Santiago J, Flexas J, Schroeder JI, Rodriguez PL (2009) Triple loss of function of protein phosphatases type 2C leads to partial constitutive response to endogenous abscisic acid. Plant Physiol 150:1345–1355

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Saez A, Apostolova N, Gonzalez-Guzman M, Gonzalez-Garcia MP, Nicolas C, Lorenzo O, Rodriguez PL (2004) Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J 37:354–369

    Article  CAS  PubMed  Google Scholar 

  • Saez A, Robert N, Maktabi MH, Schroeder JI, Serrano R, Rodriguez PL (2006) Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases type 2C ABI1 and HAB1. Plant Physiol 141:1389–1399

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park SY, Marquez JA, Cutler SR, Rodriguez PL (2009) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J 60:575–588

    Article  CAS  PubMed  Google Scholar 

  • Szostkiewicz I, Richter K, Kepka M, Demmel S, Ma Y, Korte A, Assaad FF, Christmann A, Grill E (2010) Closely related receptor complexes differ in their ABA selectivity and sensitivity. Plant J 61:25–35

    Article  CAS  PubMed  Google Scholar 

  • Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci 14:310–317

    Article  CAS  PubMed  Google Scholar 

  • Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci USA 106:17588–17593

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Waadt R, Schmidt LK, Lohse M, Hashimoto K, Bock R, Kudla J (2008) Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J 56:505–516

    Article  CAS  PubMed  Google Scholar 

  • Zeng W, He SY (2010) A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv. tomato DC3000 in Arabidopsis. Plant Physiol 153:1188–1198

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from “the Next-Generation BioGreen 21 Program for Agriculture and Technology Development (No. PJ01101001)” Rural Development Administration, Republic of Korea.

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Correspondence to Sung Chul Lee.

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Supplementary Fig. 1

ABA-induced inhibition of seedling growth in RCAR4-OX (left) and RCAR5-OX (right) mutants and the WT. The seeds of each plant were germinated and grown in vertical plate containing 0.5 μM ABA. After 9-10 days, the representative images were taken. (PPTX 160 kb)

Supplementary Fig. 2

Interactions of RCAR4 and RCAR5 proteins with the group A type 2C protein phosphatases. A yeast two-hybrid assay of interactions between RCAR4 and RCAR5 with the group A type PP2Cs. Yeast strain AH109 was transformed with RCAR4 and RCAR5 (as bait) cloned into pGBKT7 and 9 PP2Cs (as prey) cloned into a pGADGH vector. Interaction was indicated by growth on selection medium (SC-ALTH) including 0 (top) or 10 μM ABA (middle). Growth on SC-LT was used as a control (bottom). (PPTX 544 kb)

Supplementary Fig. 3

RT-PCR analysis of RCAR4, RCAR5, and HAB1 gene expression from the leaves of wild-type (Col-0) and transgenic lines (T2). Actin8 gene served as an internal control. The number in parentheses indicates the cycles of PCR. (PPTX 69 kb)

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Lim, C.W., Lee, S.C. Arabidopsis abscisic acid receptors play an important role in disease resistance. Plant Mol Biol 88, 313–324 (2015). https://doi.org/10.1007/s11103-015-0330-1

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