Functional & Integrative Genomics

, Volume 7, Issue 3, pp 181–191 | Cite as

Suppression by ABA of salicylic acid and lignin accumulation and the expression of multiple genes, in Arabidopsis infected with Pseudomonas syringae pv. tomato

Original Paper

Abstract

Abscisic acid (ABA) has been implicated in determining the outcome of interactions between many plants and their pathogens. We had previously shown that increased concentrations of ABA within leaves of Arabidopsis induced susceptibility towards an avirulent strain of Pseudomonas syringae pathovar (pv.) tomato. We now show that ABA induces susceptibility via suppression of the accumulation of components crucial for a resistance response. Lignin and salicylic acid concentrations in leaves were increased during a resistant interaction but reduced when plants were treated with ABA. The reduction in lignin and salicylic acid production was independent of the development of the hypersensitive response (HR), indicating that, in this host-pathogen system, HR is not required for resistance. Genome-wide gene expression analysis using microarrays showed that treatment with ABA suppressed the expression of many defence-related genes, including those important for phenylpropanoid biosynthesis and those encoding resistance-related proteins. Together, these results show that resistance induction in Arabidopsis to an avirulent strain of P. syringae pv. tomato is regulated by ABA.

Keywords

ABA Microarray Disease resistance Arabidopsis thaliana Salicylic acid Lignin 

Supplementary material

10142_2006_41_MOESM1_ESM.xls (7.1 mb)
ESM 1(xls 7 465 kb)

References

  1. 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 signalling pathways modulates defence gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479PubMedCrossRefGoogle Scholar
  2. Audenaert K, Meyer GD, Hofte M (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signalling mechanisms. Plant Physiol 128:1–11CrossRefGoogle Scholar
  3. Cahill DM, Ward EWB (1989) Rapid localized changes in abscisic acid concentrations in soybean in interactions with Phytophthora megasperma f.sp. glycinea or after treatment with elicitors. Physiol Mol Plant Pathol 35:483–493CrossRefGoogle Scholar
  4. Datta SK, Muthukrishnan S (1999) Pathogenesis-related proteins in plants. CRC Press, FloridaGoogle Scholar
  5. Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E, Ryals J (1994) A central role for salicylic acid in plant disease resistance. Science 266:1247–1250CrossRefPubMedGoogle Scholar
  6. Edwards HH (1983) Effect of kinetin, abscisic acid, and cations on host-parasite relations of barley inoculated with Erysiphe graminis f.sp. hordei. Phytopathol Z 107:22–30Google Scholar
  7. Finkelstein RR, Rock CD (2002) Abscisic acid biosynthesis and response. In: CR Somerville, EM Meyerowitz (eds) The Arabidopsis book. American Society of Plant Biologists, Rockville, DOI 10.1199/tab.0058, http://www.aspb.org/publications/arabidopsis/ Google Scholar
  8. Foster R, Chua N-H (1999) An Arabidopsis mutant with deregulated ABA gene expression: implications for negative regulator function. Plant J 17:363–372PubMedCrossRefGoogle Scholar
  9. Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756CrossRefPubMedGoogle Scholar
  10. Graham MY, Graham TL (1991) Rapid accumulation of anionic peroxidases and phenolic polymers in soybean cotyledon tissues following treatment with Phytophthora megasperma f.sp. glycinea wall glucan. Plant Physiol 97:1445–1455PubMedGoogle Scholar
  11. He CY, Wolyn DJ (2005) Potential role for salicylic acid in induced resistance of asparagus roots to Fusarium oxysporum f.sp. asparagi. Plant Pathol 54:227–232CrossRefGoogle Scholar
  12. Katagiri F, Thilmony R, He SY (2002) The Arabidopsis thalianaPseudomonas syringae interaction. In: Somerville CR, Meyerowitz EM (eds) The Arabidopsis book. American Society of Plant Biologists, Rockville, DOI 10.1199/tab.0039, http://www.aspb.org/publications/arabidopsis/ Google Scholar
  13. Kettner J, Dorffling K (1995) Biosynthesis and metabolism of abscisic acid in tomato leaves infected with Botrytis cinerea. Planta 196:627–634CrossRefGoogle Scholar
  14. Koch E, Slusarenko A (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2:437–445PubMedCrossRefGoogle Scholar
  15. Lee S, Sharma Y, Lee TK, Chang M, Davis KR (2001) Lignification induced by Pseudomonads harbouring avirulent genes on Arabidopsis. Mol Cells 12:25–31PubMedGoogle Scholar
  16. Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222PubMedCrossRefGoogle Scholar
  17. Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant-pathogen interactions. Curr Opin Plant Biol 8:409–414PubMedCrossRefGoogle Scholar
  18. McDonald KL, Cahill DM (1999) Influence of abscisic acid and the abscisic acid biosynthesis inhibitor, norflurazon, on interactions between Phytophthora sojae and soybean (Glycine max). Eur J Plant Pathol 105:651–658CrossRefGoogle Scholar
  19. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834PubMedCrossRefGoogle Scholar
  20. Mohr PG, Cahill DM (2001) Relative roles of glyceollin, lignin and the hypersensitive response and the influence of ABA in compatible and incompatible interactions of soybeans with Phytophthora sojae. Physiol Mol Plant Pathol 58:31–41CrossRefGoogle Scholar
  21. 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
  22. Raes J, Rohde A, Christensen JH, Van De Peer Y, Boerjan W (2003) Genome-wide characterisation of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071PubMedCrossRefGoogle Scholar
  23. Rairdan GJ, Delaney TP (2002) Role of salicylic acid and NIM1/NPR1 in race-specific resistance in Arabidopsis. Genetics 161:803–811PubMedGoogle Scholar
  24. Raskin I, Turner IM, Melander WR (1989) Regulation of heat production in the inflorescences of Arum lily by endogenous salicylic acid. Proc Natl Acad Sci USA 86:2214–2218PubMedCrossRefGoogle Scholar
  25. Reuber TL, Ausubel FM (1996) Isolation of Arabidopsis genes that differentiate between resistance mediated by the RPS2 and RPM1 disease resistance genes. Plant Cell 8:241–249PubMedCrossRefGoogle Scholar
  26. Thomma BPHJ, Tierens KFM, Penninckx IAMA, Mauch-Mani B, Broekaert WF, Cammue BPA (2001) Different micro-organisms differentially induce Arabidopsis disease response pathways. Plant Physiol Biochem 39:673–680CrossRefGoogle Scholar
  27. Thomma BPHJ, Cammue BPA, Thevissen K (2002) Plant defensins. Planta 216:193–202PubMedCrossRefGoogle Scholar
  28. Tierens KFM-J, Thomma BPHJ, Bari RP, Garmier M, Eggermont K, Brouwer M, Penninckx IAMA, Broekaert WF, Cammue BPA (2002) Esa1, an Arabidopsis mutant with enhanced susceptibility to a range of necrotrophic fungal pathogens, shows a distorted induction of defence responses by reactive oxygen generating compounds. Plant J 29:131–140PubMedCrossRefGoogle Scholar
  29. 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
  30. Wang R, Okamoto M, Xing X, Crawford NM (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron and sulfate metabolism. Plant Physiol 132:556–567PubMedCrossRefGoogle Scholar
  31. Ward EWB, Cahill DM, Bhattacharyya MK (1989) Abscisic acid suppression of phenylalanine ammonia-lyase activity and mRNA, and resistance of soybeans of Phytophthora megasperma f. sp. glycinea. Plant Physiol 91:23–27PubMedCrossRefGoogle Scholar
  32. 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
  33. Whenham RJ, Fraser RSS, Brown LP, Payne JA (1986) Tobacco-mosaic-virus-induced increase in abscisic-acid concentration in tobacco leaves: Intracellular location in light and dark-green areas, and relationship to symptom development. Planta 168:592–598CrossRefGoogle Scholar
  34. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565PubMedCrossRefGoogle Scholar
  35. Xie Z, Fan B, Chen Z (1998) Induction of PR-1 proteins and potentiation of pathogen signals by salicylic acid exhibit the same dose response and structural specificity in plant cell cultures. Mol Plant–Microb Interact 11:568–571Google Scholar
  36. Zhu T, Budworth P, Han B, Brown D, Chang H-S, Zou G, Wang X (2001) Toward elucidating the global gene expression patterns of developing Arabidopsis: parallel analysis of 8300 genes by a high density oligonucleotide probe array. Plant Physiol Biochem 39:221–242CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.School of Life and Environmental SciencesDeakin UniversityGeelongAustralia
  2. 2.Department of Plant SciencesUniversity of ArizonaTucsonUSA

Personalised recommendations