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Journal of Plant Research

, Volume 124, Issue 4, pp 489–499 | Cite as

The roles of ABA in plant–pathogen interactions

  • Feng Yi Cao
  • Keiko Yoshioka
  • Darrell Desveaux
JPR Symposium Opening a New Era of ABA Research

Abstract

Defence against abiotic and biotic stresses is crucial for the fitness and survival of plants under adverse or suboptimal growth conditions. The phytohormone abscisic acid (ABA) is not only important for mediating abiotic stress responses, but also plays a multifaceted and pivotal role in plant immunity. This review presents examples demonstrating the importance of crosstalk between ABA and the key biotic stress phytohormone salicylic acid in determining the outcome of plant–pathogen interactions. We then provide an overview of how ABA influences plant defence responses against various phytopathogens with particular emphasis on the Arabidopsis–Pseudomonas syringae model pathosystem. Lastly, we discuss future directions for studies of ABA in plant immunity with emphasis on, its role in the crosstalk between biotic and abiotic stress responses, the importance of distinguishing direct and indirect effects of ABA, as well as the prospect of utilizing the recently elucidated core ABA signaling network to gain further insights into the roles of ABA in plant immunity.

Keywords

ABA Plant immunity Pseudomonas syringae/Arabidopsis 

Notes

Acknowledgments

We thank Dr. Peter McCourt and Dr. Shelley Lumba for helpful discussions about ABA signaling. We thank anonymous reviewers for insightful and thorough comments. Work in the Desveaux and Yoshioka labs is supported by the Natural Sciences and Engineering Research Council (NSERC) of Canada. D.D. is a Canada Research Chair in Plant–Microbe Systems Biology.

References

  1. Achuo EA, Prinsen E, Hofte M (2006) Influence of drought, salt stress and abscisic acid on the resistance of tomato to Botrytis cinerea and Oidium neolycopersici. Plant Pathol 55:178–186CrossRefGoogle Scholar
  2. Adie BAT, Perez-Perez J, Perez-Perez MM, Godoy M, Sanchez-Serrano JJ, Schemelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defences in Arabidopsis. Plant Cell 19:1665–1681PubMedCrossRefGoogle Scholar
  3. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate–ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479PubMedCrossRefGoogle Scholar
  4. Armstrong F, Leung J, Grabov A, Brearly J, Giraudat J, Blatt MR (1995) Sensitivity to abscisic acid of guard-cell K+ channel is suppressed by abi1-1, a mutant at Arabidopsis gene encoding a putative protein phosphatase. Proc Natl Acad Sci USA 92:9520–9524PubMedCrossRefGoogle Scholar
  5. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983PubMedCrossRefGoogle Scholar
  6. Assante GL, Merlini L, Nashini G (1977) (+)-Abscisic acid, a metabolite of the fungus Cercospora rosicola. Experientia 33:1556–1557CrossRefGoogle Scholar
  7. Asselbergh B, Achuo AE, Hofte M, Gisegem FV (2008a) Abscisic acid deficiency leads to rapid activation of tomato defence responses upon infection with Erwinia chrysanthemi. Mol Plant Pathol 9:11–24PubMedGoogle Scholar
  8. Asselbergh B, De Vleesschauwer D, Hofte M (2008b) Global switches and fine-tuning-ABA modulates plant pathogen defence. Mol Plant Microbe Interact 6:709–719CrossRefGoogle Scholar
  9. Audenaert K, De Meyer GB, Hofte MM (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol 128:491–501PubMedCrossRefGoogle Scholar
  10. Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BJ (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265:1856–1860PubMedCrossRefGoogle Scholar
  11. Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744PubMedCrossRefGoogle Scholar
  12. Chen H, Xue L, Chintamanani S, Germain H, Lin H, Cui H, Cai R, Zuo J, Tang X, Li X, Guo H, Zhou JM (2009) Ethylene insensitive 3 and ethylene insensitive 3-like1 repress salicylic acid induction deficient 2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell 21:2527–2540PubMedCrossRefGoogle Scholar
  13. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814PubMedCrossRefGoogle Scholar
  14. Conrath U, Pieterse CMJ, Maunch-mani B (2002) Priming in plant–pathogen interactions. Trends Plant Sci 7:210–216PubMedCrossRefGoogle Scholar
  15. Cutler S, Ghassemian M, Bonetta D, Cooney S, McCourt P (1996) A protein farnesyl transferase involved in abscisic acid signal transduction in Arabidopsis. Science 273:1239–1241PubMedCrossRefGoogle Scholar
  16. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679PubMedCrossRefGoogle Scholar
  17. de Torres M, Sanchez P, Fernandez-Delmond I, Grant M (2003) Expression profiling of the host response to bacterial infection: the transition from basal to induced defence responses in RPM1-mediated resistance. Plant J 33:665–676PubMedCrossRefGoogle Scholar
  18. de Torres-Zabala M, Truman W, Bennett MH, Lafforguel G, Mansfield JW, Egea PR, Bogre L, Grant M (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signaling pathway to cause disease. EMBO J 26:1434–1443PubMedCrossRefGoogle Scholar
  19. de Torres-Zabala M, Bennett MH, Truman W, Grant M (2009) Antagonism between salicylic and abscisic acid reflects early host–pathogen conflict and moulds plant defence responses. Plant J 59:375–386PubMedCrossRefGoogle Scholar
  20. DebRoy S, Thilmony R, Kwack YB, Nomura K, He SY (2004) A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc Natl Acad Sci USA 101:9927–9932PubMedCrossRefGoogle Scholar
  21. Dempsey DA, Shah J, Klessig DF (1999) Salicylic acid and disease resistance in plants. Crit Rev Plant Sci 18:547–575CrossRefGoogle Scholar
  22. Dörffling K, Peterson W, Sprecher E, Urbasch I, Hanssen HP (1984) Abscisic acid in phytopathogenic fungi of the genera Botrytis, Ceratocytis, Fusarium, and Rhizoctonia. Z Naturforsch 39:1059–1060Google Scholar
  23. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209PubMedCrossRefGoogle Scholar
  24. Fan LM, Zhao Z, Assmann SM (2004) Guard cells: a dynamic signaling model. Curr Opin Plant Biol 7:537–546PubMedCrossRefGoogle Scholar
  25. Fan J, Hill L, Crooks C, Doerner P, Lamb C (2009) Abscisic acid has a key role in modulating diverse plant–pathogen interactions. Plant Physiol 150:1750–1761PubMedCrossRefGoogle Scholar
  26. Fujii H, Chinnesamy V, Rodrigues A, Rubio S, Antoni R, Park SY, Cutler SR, Sheen J, Rodriguez PL, Zhu JK (2009) In vitro reconstitution of an abscisic acid signaling pathway. Nature 462:660–666PubMedCrossRefGoogle Scholar
  27. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinogaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442PubMedCrossRefGoogle Scholar
  28. Gimenez-Ibanez S, Rathjen JP (2010) The case for defence: plant versus Pseudomonas syringae. Microbes Infect 12:428–437PubMedCrossRefGoogle Scholar
  29. Glazebrook J (2005) Contrasting mechanisms of dense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227PubMedCrossRefGoogle Scholar
  30. Goel AK, Lundberg D, Torres MA, Matthews R, Akimoto-Tomiyama C, Farmer L, Dangl JL, Grant SR (2008) The Pseudomonas syringae type III effector hopAM1 enhances virulence on water-stressed plants. Mol Plant Microbe Interact 21:361–370PubMedCrossRefGoogle Scholar
  31. Goritschnig S, Weihmann T, Zhang Y, Fobert P, McCourt P, Li X (2008) A novel role for protein farnesylation in plant innate immunity. Plant Physiol 148:348–357PubMedCrossRefGoogle Scholar
  32. Grant MR, Jones JD (2009) Hormone (dis)harmony moulds plant heath and disease. Science 324:750–752PubMedCrossRefGoogle Scholar
  33. Gudesblat GE, Torres PS, Vojnov AA (2009) Xanthomonas campestris overcomes Arabidopsis stomatal innate immunity through a DSF cell-to-cell signal-regulated virulence factor. Plant Physiol 149:1017–1027PubMedCrossRefGoogle Scholar
  34. Gupta V, Willits MG, Glazebrook J (2000) Arabidopsis thaliana EDS4 contributes to salicylic acid (SA)-dependent expression of defence responses: evidence for inhibition of jasmonic acid signaling by SA. Mol Plant Microbe Interact 13:503–511PubMedCrossRefGoogle Scholar
  35. Hauck P, Thilmony R, He SY (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci USA 100:8577–8582PubMedCrossRefGoogle Scholar
  36. Jiang CJ, Shimono M, Sugano S, Kojima M, Yazawa K, Yoshida R, Inoue H, Hayashi N, Sakakibara H, Takatsuki H (2010) Abscisic acid interacts antagonistically with salicylic acid signaling pathway in rice–Magnaporthe grisea interaction. Mol Plant Microbe Interact 23:791–798PubMedCrossRefGoogle Scholar
  37. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  38. Kettner J, Dörffling K (1995) Biosynthesis and metabolism of abscisic acid in tomato leaves infected with Botrytis cinerea. Planta 196:627–634CrossRefGoogle Scholar
  39. Koga H, Dohi K, Mori M (2004) Abscisic acid and low temperatures suppress the whole plant-specific resistance reaction of rice plants to the infection of Magnaporthe grisea. Physiol Mol Plant Path 65:3–9CrossRefGoogle Scholar
  40. Laluk K, Mengiste T (2010) Necrotroph attacks on plants: wanton destruction or covert extortion? In: The Arabidopsis book, The American Society of Plant Biologists, Rockville, pp 1–34Google Scholar
  41. Lewis JD, Wu R, Guttman DS, Desveaux D (2010) Allele-specific virulence attenuation of the Pseudomonas syringae HopZ1a type III effector via the Arabidopsis ZAR1 resistance protein. PLoS Genet 6(4):e1000894PubMedCrossRefGoogle Scholar
  42. Li X, Lin H, Zhang W, Zou Y, Zhang J, Tang X, Zhou JM (2005) Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc Natl Acad Sci USA 102:12990–12995PubMedCrossRefGoogle Scholar
  43. Loake G, Grant M (2007) Salicylic acid in plant defence—the players and protangonists. Curr Opin Plant Biol 10:466–472PubMedCrossRefGoogle Scholar
  44. 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 324:1064–1068PubMedGoogle Scholar
  45. Mauch-Mani B, Mauch F (2005) The role of abscisic acid and plant–pathogen interactions. Curr Opin Plant Biol 8:409–414PubMedCrossRefGoogle Scholar
  46. Mayek-Perez N, Garcia-Espinosa R, Lopez-Castaneda C, Acosta-Gallegos J, Simpson J (2002) Water relations, histopathology and growth of common bean (Phaseolus vulgaris L.) during pathogenesis of Macrophomina phaseolina under drought stress. Physiol Mol Plant Path 60:185–195CrossRefGoogle Scholar
  47. McElrone AJ, Sherald JL, Forseth IN (2001) Effects of water stress on symptomatology and growth of Parthenocissus quinquefolia by Xylella fastiosa. Plant Dis 85:1160–1164CrossRefGoogle Scholar
  48. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980PubMedCrossRefGoogle Scholar
  49. Mindrinos M, Katagiri F, Yu GL, Ausubel FM (1994) The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78:1089–1099PubMedCrossRefGoogle Scholar
  50. Moeder W, Yoshioka K (2008) Lesion mimic mutants: a classical, yet still fundamental approach to study programmed cell death. Plant Signal Behav 3:764–767PubMedCrossRefGoogle Scholar
  51. Moeder W, Yoshioka K (2009) Environmental sensitivity in pathogen resistant Arabidopsis mutants. In: Yoshioka K, Shinozaki K (eds) Signal crosstalk in plant stress responses. Wiley, Iowa, pp 113–135CrossRefGoogle Scholar
  52. Moeder W, Ung H, Mosher S, Yoshioka K (2010) SA–ABA antagonism in defense responses. Plant Signal Behav 5:1231–1233PubMedCrossRefGoogle Scholar
  53. Mohr PG, Cahill DM (2003) Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Func Plant Biol 30:461–469CrossRefGoogle Scholar
  54. Mohr PG, Cahill DM (2007) Suppression by ABA of salicylic acid and lignin accumulation and the expression of multiple genes, in Arabidopsis infected with Pseudomonas syringae pv. tomato. Funct Integr Genomics 7:181–191PubMedCrossRefGoogle Scholar
  55. Mosher S, Moeder W, Nishimura N, Jikumaru Y, Joo SH, Urquhart W, Klessig DF, Kim SK, Nambara E, Yoshioka K (2010) The lesion-mimic mutant cpr22 shows alterations in abscisic acid signaling and abscisic acid insensitivity in a salicylic acid-dependent manner. Plant Physiol 152:1901–1913PubMedCrossRefGoogle Scholar
  56. Nambara E, Kawaide H, Kamiya Y, Naito A (1998) Characterization of an Arabidopsis thaliana mutant that has a defect in ABA accumulation: ABA-dependent and ABA-independent accumulation of free amino acids during dehydration. Plant Cell Physiol 39:853–858PubMedGoogle Scholar
  57. Nishimura MT, Dangl JL (2010) Arabidopsis and the plant immune system. Plant J 61:1053–1066PubMedCrossRefGoogle Scholar
  58. Nishimura N, Kitahata N, Seki M, Narusaka Y, Narusaka M, Kuromori T, Asami T, Shinozaki K, Hirayama T (2005) Analysis of ABA hypersensitive germination 2 revealed the pivotal functions of PARN in stress response in Arabidopsis. Plant J 44:972–984PubMedCrossRefGoogle Scholar
  59. Nishimura N, Okamoto M, Narusaka M, Yasuda M, Nakashita H (2009) ABA hypersensitive germination 2–1 causes the activation of both abscisic acid and salicylic acid responses in Arabidopsis. Plant Cell Physiol 50:2112–2122PubMedCrossRefGoogle Scholar
  60. Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TFF, 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 324:1068–1071PubMedGoogle Scholar
  61. Robert-Seilaniantz A, Navarro L, Bari R, Jones JD (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379PubMedCrossRefGoogle Scholar
  62. Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signaling and engineering drought hardiness in plants. Nature 410:317–330CrossRefGoogle Scholar
  63. Seo PJ, Park CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186:471–483PubMedCrossRefGoogle Scholar
  64. Shirano Y, Kachroo P, Shah J, Klessig DF (2002) A gain-of-function mutation in an Arabidopsis toll interleukin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defence responses and results in enhanced disease resistance. Plant Cell 14:3149–3162PubMedCrossRefGoogle Scholar
  65. Siewers V, Kokkelink L, Smedsgaard J, Tudzynski P (2006) Identification of an abscisic acid gene cluster in the grey mold Botrytis cinerea. Appl Environ Microbiol 72:4619–4626PubMedCrossRefGoogle Scholar
  66. Spoel SH, Dong X (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3:348–351PubMedCrossRefGoogle Scholar
  67. Spoel SH, Koorneef A, Claessens SMC, Korzelius JP, Van Pelt JA, Muller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K, Van Loon LC, Dong X, Pieterse CMJ (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defence pathways through a novel function in the cytolsol. Plant Cell 15:760–770PubMedCrossRefGoogle Scholar
  68. Ton J, Mauch-Mani B (2004) β-Amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J 38:119–130PubMedCrossRefGoogle Scholar
  69. Ton J, Jakab G, Toquin V, Flors V, Iavicoli A, Maeder MN, Metraux JP, Mauch-Mani B (2005) Dissecting the β-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell 17:987–999PubMedCrossRefGoogle Scholar
  70. Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci 14:310–317PubMedCrossRefGoogle Scholar
  71. Truman W, de Zabala MT, Grant M (2006) Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J 46:14–33PubMedCrossRefGoogle Scholar
  72. Tuteja N (2007) Abscisic acid and abiotic stress signaling. Plant Signal Behav 2:135–138PubMedCrossRefGoogle Scholar
  73. Vleesschauwer DD, Yang Y, Cruz CV, Hofte M (2010) Abscisic acid-induced resistance against the brown spot pathogen Cochliobolus miyabeanus in rice involves MAP kinase-mediated repression of ethylene signaling. Plant Physiol 152:2036–2052PubMedCrossRefGoogle Scholar
  74. Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206PubMedCrossRefGoogle Scholar
  75. Whalen MC, Innes RW, Bent AF, Staskawicz BJ (1991) Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3:49–59PubMedCrossRefGoogle Scholar
  76. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought and salt stress. Plant Cell 14:S165–S183PubMedCrossRefGoogle Scholar
  77. Yalovsky S, Kukukian A, Rodriguez-Concepcion M, Young CA (2000) Function requirement of plant farnesyltransferase during development in Arabidopsis. Plant Cell 12:1267–1278PubMedCrossRefGoogle Scholar
  78. Yasuda M, Ishikawa A, Jikumaru Y, Umezawa T, Asami T, Maruyama-Nakashita A, Kudo T, Shinozaki K, Yoshida S, Nakashita H (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress responses in Arabidopsis. Plant Cell 20:1678–1692PubMedCrossRefGoogle Scholar
  79. Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker JR, Shinozaki K (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol 43:1473–1483PubMedCrossRefGoogle Scholar
  80. Yoshioka K, Shinozaki K (eds) (2009) Signal crosstalk in plant stress responses. Wiley, IowaGoogle Scholar
  81. Yoshioka K, Moeder W, Kang HG, Kachroo P, Masmoudi K, Berkowtiz G, Klessig DF (2006) The chimeric Arabidopsis cyclic nucleotide channel 11/12 activates multiple pathogen resistance responses. Plant Cell 18:747–763PubMedCrossRefGoogle Scholar
  82. 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 153:1188–1198PubMedCrossRefGoogle Scholar
  83. Zeng W, Melotto M, He SY (2010) Plant stomata: a checkpoint of host immunity and pathogen virulence. Curr Opin Biotechnol 21:599–603PubMedCrossRefGoogle Scholar
  84. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedCrossRefGoogle Scholar
  85. Zimmerli L, Stein M, Lipka V, Schulze-Lefert P, Somerville S (2004) Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis. Plant J 40:633–646PubMedCrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer 2011

Authors and Affiliations

  • Feng Yi Cao
    • 1
  • Keiko Yoshioka
    • 1
    • 2
  • Darrell Desveaux
    • 1
    • 2
  1. 1.Department of Cell and Systems BiologyUniversity of TorontoTorontoCanada
  2. 2.Centre for the Analysis of Genome Evolution and FunctionUniversity of TorontoTorontoCanada

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