Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1999 Feb;11(2):191–206. doi: 10.1105/tpc.11.2.191

The Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent.

J Shah 1, P Kachroo 1, D F Klessig 1
PMCID: PMC144168  PMID: 9927638

Abstract

The Arabidopsis NPR1 gene was previously shown to be required for the salicylic acid (SA)- and benzothiadiazole (BTH)-induced expression of pathogenesis-related (PR) genes and systemic acquired resistance. The dominant ssi1 (for suppressor of SA insensitivity) mutation characterized in this study defines a new component of the SA signal transduction pathway that bypasses the requirement of NPR1 for expression of the PR genes and disease resistance. The ssi1 mutation caused PR (PR-1, BGL2 [PR-2], and PR-5) genes to be constitutively expressed and restored resistance to an avirulent strain of Pseudomonas syringae pv tomato in npr1-5 (previously called sai1) mutant plants. In addition, ssi1 plants were small, spontaneously developed hypersensitive response-like lesions, accumulated elevated levels of SA, and constitutively expressed the antimicrobial defensin gene PDF1.2. The phenotypes of the ssi1 mutant are SA dependent. When SA accumulation was prevented in ssi1 npr1-5 plants by expressing the SA-degrading salicylate hydroxylase (nahG) gene, all of the phenotypes associated with the ssi1 mutation were suppressed. However, lesion formation and expression of the PR genes were restored in these plants by the application of BTH. Interestingly, expression of PDF1.2, which previously has been shown to be SA independent but jasmonic acid and ethylene dependent, was also suppressed in ssi1 npr1-5 plants by the nahG gene. Furthermore, exogenous application of BTH restored PDF1.2 expression in these plants. Our results suggest that SSI1 may function as a switch modulating cross-talk between the SA- and jasmonic acid/ethylene-mediated defense signal transduction pathways.

Full Text

The Full Text of this article is available as a PDF (583.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bell C. J., Ecker J. R. Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics. 1994 Jan 1;19(1):137–144. doi: 10.1006/geno.1994.1023. [DOI] [PubMed] [Google Scholar]
  2. Bent A. F., Kunkel B. N., Dahlbeck D., Brown K. L., Schmidt R., Giraudat J., Leung J., Staskawicz B. J. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science. 1994 Sep 23;265(5180):1856–1860. doi: 10.1126/science.8091210. [DOI] [PubMed] [Google Scholar]
  3. Bowling S. A., Clarke J. D., Liu Y., Klessig D. F., Dong X. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell. 1997 Sep;9(9):1573–1584. doi: 10.1105/tpc.9.9.1573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bowling S. A., Guo A., Cao H., Gordon A. S., Klessig D. F., Dong X. A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell. 1994 Dec;6(12):1845–1857. doi: 10.1105/tpc.6.12.1845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cao H., Bowling S. A., Gordon A. S., Dong X. Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance. Plant Cell. 1994 Nov;6(11):1583–1592. doi: 10.1105/tpc.6.11.1583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cao H., Glazebrook J., Clarke J. D., Volko S., Dong X. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell. 1997 Jan 10;88(1):57–63. doi: 10.1016/s0092-8674(00)81858-9. [DOI] [PubMed] [Google Scholar]
  7. Cao H., Li X., Dong X. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc Natl Acad Sci U S A. 1998 May 26;95(11):6531–6536. doi: 10.1073/pnas.95.11.6531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Century K. S., Holub E. B., Staskawicz B. J. NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6597–6601. doi: 10.1073/pnas.92.14.6597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Clarke J. D., Liu Y., Klessig D. F., Dong X. Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell. 1998 Apr;10(4):557–569. doi: 10.1105/tpc.10.4.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dangl J. L., Dietrich R. A., Richberg M. H. Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. Plant Cell. 1996 Oct;8(10):1793–1807. doi: 10.1105/tpc.8.10.1793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Delaney T. P., Friedrich L., Ryals J. A. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6602–6606. doi: 10.1073/pnas.92.14.6602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Delaney T. P., Uknes S., Vernooij B., Friedrich L., Weymann K., Negrotto D., Gaffney T., Gut-Rella M., Kessmann H., Ward E., Ryals J. A central role of salicylic Acid in plant disease resistance. Science. 1994 Nov 18;266(5188):1247–1250. doi: 10.1126/science.266.5188.1247. [DOI] [PubMed] [Google Scholar]
  13. Dempsey D. A., Pathirana M. S., Wobbe K. K., Klessig D. F. Identification of an Arabidopsis locus required for resistance to turnip crinkle virus. Plant J. 1997 Feb;11(2):301–311. doi: 10.1046/j.1365-313x.1997.11020301.x. [DOI] [PubMed] [Google Scholar]
  14. Dietrich R. A., Delaney T. P., Uknes S. J., Ward E. R., Ryals J. A., Dangl J. L. Arabidopsis mutants simulating disease resistance response. Cell. 1994 May 20;77(4):565–577. doi: 10.1016/0092-8674(94)90218-6. [DOI] [PubMed] [Google Scholar]
  15. Doares S. H., Narvaez-Vasquez J., Conconi A., Ryan C. A. Salicylic Acid Inhibits Synthesis of Proteinase Inhibitors in Tomato Leaves Induced by Systemin and Jasmonic Acid. Plant Physiol. 1995 Aug;108(4):1741–1746. doi: 10.1104/pp.108.4.1741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fauth M., Merten A., Hahn M. G., Jeblick W., Kauss H. Competence for Elicitation of H2O2 in Hypocotyls of Cucumber Is Induced by Breaching the Cuticle and Is Enhanced by Salicylic Acid. Plant Physiol. 1996 Feb;110(2):347–354. doi: 10.1104/pp.110.2.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gaffney T., Friedrich L., Vernooij B., Negrotto D., Nye G., Uknes S., Ward E., Kessmann H., Ryals J. Requirement of salicylic Acid for the induction of systemic acquired resistance. Science. 1993 Aug 6;261(5122):754–756. doi: 10.1126/science.261.5122.754. [DOI] [PubMed] [Google Scholar]
  18. Glazebrook J., Rogers E. E., Ausubel F. M. Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics. 1996 Jun;143(2):973–982. doi: 10.1093/genetics/143.2.973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gorina S., Pavletich N. P. Structure of the p53 tumor suppressor bound to the ankyrin and SH3 domains of 53BP2. Science. 1996 Nov 8;274(5289):1001–1005. doi: 10.1126/science.274.5289.1001. [DOI] [PubMed] [Google Scholar]
  20. Greenberg J. T., Guo A., Klessig D. F., Ausubel F. M. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell. 1994 May 20;77(4):551–563. doi: 10.1016/0092-8674(94)90217-8. [DOI] [PubMed] [Google Scholar]
  21. Görlach J., Volrath S., Knauf-Beiter G., Hengy G., Beckhove U., Kogel K. H., Oostendorp M., Staub T., Ward E., Kessmann H. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell. 1996 Apr;8(4):629–643. doi: 10.1105/tpc.8.4.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hammond-Kosack K. E., Jones J. D. Resistance gene-dependent plant defense responses. Plant Cell. 1996 Oct;8(10):1773–1791. doi: 10.1105/tpc.8.10.1773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Jabs T., Dietrich R. A., Dangl J. L. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science. 1996 Sep 27;273(5283):1853–1856. doi: 10.1126/science.273.5283.1853. [DOI] [PubMed] [Google Scholar]
  24. KING E. O., WARD M. K., RANEY D. E. Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med. 1954 Aug;44(2):301–307. [PubMed] [Google Scholar]
  25. Klessig D. F., Malamy J. The salicylic acid signal in plants. Plant Mol Biol. 1994 Dec;26(5):1439–1458. doi: 10.1007/BF00016484. [DOI] [PubMed] [Google Scholar]
  26. Konieczny A., Ausubel F. M. A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 1993 Aug;4(2):403–410. doi: 10.1046/j.1365-313x.1993.04020403.x. [DOI] [PubMed] [Google Scholar]
  27. Krappmann D., Wulczyn F. G., Scheidereit C. Different mechanisms control signal-induced degradation and basal turnover of the NF-kappaB inhibitor IkappaB alpha in vivo. EMBO J. 1996 Dec 2;15(23):6716–6726. [PMC free article] [PubMed] [Google Scholar]
  28. Lawton K. A., Friedrich L., Hunt M., Weymann K., Delaney T., Kessmann H., Staub T., Ryals J. Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J. 1996 Jul;10(1):71–82. doi: 10.1046/j.1365-313x.1996.10010071.x. [DOI] [PubMed] [Google Scholar]
  29. Lawton K., Weymann K., Friedrich L., Vernooij B., Uknes S., Ryals J. Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant Microbe Interact. 1995 Nov-Dec;8(6):863–870. doi: 10.1094/mpmi-8-0863. [DOI] [PubMed] [Google Scholar]
  30. Leslie C. A., Romani R. J. Inhibition of ethylene biosynthesis by salicylic Acid. Plant Physiol. 1988 Nov;88(3):833–837. doi: 10.1104/pp.88.3.833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Levine A., Tenhaken R., Dixon R., Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994 Nov 18;79(4):583–593. doi: 10.1016/0092-8674(94)90544-4. [DOI] [PubMed] [Google Scholar]
  32. Malamy J., Carr J. P., Klessig D. F., Raskin I. Salicylic Acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science. 1990 Nov 16;250(4983):1002–1004. doi: 10.1126/science.250.4983.1002. [DOI] [PubMed] [Google Scholar]
  33. Mauch-Mani B., Slusarenko A. J. Production of Salicylic Acid Precursors Is a Major Function of Phenylalanine Ammonia-Lyase in the Resistance of Arabidopsis to Peronospora parasitica. Plant Cell. 1996 Feb;8(2):203–212. doi: 10.1105/tpc.8.2.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Métraux J. P., Signer H., Ryals J., Ward E., Wyss-Benz M., Gaudin J., Raschdorf K., Schmid E., Blum W., Inverardi B. Increase in salicylic Acid at the onset of systemic acquired resistance in cucumber. Science. 1990 Nov 16;250(4983):1004–1006. doi: 10.1126/science.250.4983.1004. [DOI] [PubMed] [Google Scholar]
  35. Parker J. E., Holub E. B., Frost L. N., Falk A., Gunn N. D., Daniels M. J. Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell. 1996 Nov;8(11):2033–2046. doi: 10.1105/tpc.8.11.2033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Penninckx I. A., Eggermont K., Terras F. R., Thomma B. P., De Samblanx G. W., Buchala A., Métraux J. P., Manners J. M., Broekaert W. F. Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell. 1996 Dec;8(12):2309–2323. doi: 10.1105/tpc.8.12.2309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Pieterse C. M., van Wees S. C., Hoffland E., van Pelt J. A., van Loon L. C. Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell. 1996 Aug;8(8):1225–1237. doi: 10.1105/tpc.8.8.1225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Pieterse C. M., van Wees S. C., van Pelt J. A., Knoester M., Laan R., Gerrits H., Weisbeek P. J., van Loon L. C. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell. 1998 Sep;10(9):1571–1580. doi: 10.1105/tpc.10.9.1571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. ROSS A. F. Systemic acquired resistance induced by localized virus infections in plants. Virology. 1961 Jul;14:340–358. doi: 10.1016/0042-6822(61)90319-1. [DOI] [PubMed] [Google Scholar]
  40. Rogers E. E., Ausubel F. M. Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. Plant Cell. 1997 Mar;9(3):305–316. doi: 10.1105/tpc.9.3.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Ryals J. A., Neuenschwander U. H., Willits M. G., Molina A., Steiner H. Y., Hunt M. D. Systemic Acquired Resistance. Plant Cell. 1996 Oct;8(10):1809–1819. doi: 10.1105/tpc.8.10.1809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Ryals J., Weymann K., Lawton K., Friedrich L., Ellis D., Steiner H. Y., Johnson J., Delaney T. P., Jesse T., Vos P. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B. Plant Cell. 1997 Mar;9(3):425–439. doi: 10.1105/tpc.9.3.425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sano H., Seo S., Orudgev E., Youssefian S., Ishizuka K. Expression of the gene for a small GTP binding protein in transgenic tobacco elevates endogenous cytokinin levels, abnormally induces salicylic acid in response to wounding, and increases resistance to tobacco mosaic virus infection. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10556–10560. doi: 10.1073/pnas.91.22.10556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Schweizer P., Buchala A., Metraux J. P. Gene-Expression Patterns and Levels of Jasmonic Acid in Rice Treated with the Resistance Inducer 2,6-Dichloroisonicotinic Acid. Plant Physiol. 1997 Sep;115(1):61–70. doi: 10.1104/pp.115.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Seo S., Okamoto M., Seto H., Ishizuka K., Sano H., Ohashi Y. Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science. 1995 Dec 22;270(5244):1988–1992. doi: 10.1126/science.270.5244.1988. [DOI] [PubMed] [Google Scholar]
  46. Shah J., Tsui F., Klessig D. F. Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol Plant Microbe Interact. 1997 Jan;10(1):69–78. doi: 10.1094/MPMI.1997.10.1.69. [DOI] [PubMed] [Google Scholar]
  47. Shirasu K., Nakajima H., Rajasekhar V. K., Dixon R. A., Lamb C. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell. 1997 Feb;9(2):261–270. doi: 10.1105/tpc.9.2.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Summermatter K., Sticher L., Metraux J. P. Systemic Responses in Arabidopsis thaliana Infected and Challenged with Pseudomonas syringae pv syringae. Plant Physiol. 1995 Aug;108(4):1379–1385. doi: 10.1104/pp.108.4.1379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Thulke O., Conrath U. Salicylic acid has a dual role in the activation of defence-related genes in parsley. Plant J. 1998 Apr;14(1):35–42. doi: 10.1046/j.1365-313X.1998.00093.x. [DOI] [PubMed] [Google Scholar]
  50. Uknes S., Mauch-Mani B., Moyer M., Potter S., Williams S., Dincher S., Chandler D., Slusarenko A., Ward E., Ryals J. Acquired resistance in Arabidopsis. Plant Cell. 1992 Jun;4(6):645–656. doi: 10.1105/tpc.4.6.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Ward E. R., Uknes S. J., Williams S. C., Dincher S. S., Wiederhold D. L., Alexander D. C., Ahl-Goy P., Metraux J. P., Ryals J. A. Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance. Plant Cell. 1991 Oct;3(10):1085–1094. doi: 10.1105/tpc.3.10.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Weymann K., Hunt M., Uknes S., Neuenschwander U., Lawton K., Steiner H. Y., Ryals J. Suppression and Restoration of Lesion Formation in Arabidopsis lsd Mutants. Plant Cell. 1995 Dec;7(12):2013–2022. doi: 10.1105/tpc.7.12.2013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Xu Y., Chang PFL., Liu D., Narasimhan M. L., Raghothama K. G., Hasegawa P. M., Bressan R. A. Plant Defense Genes Are Synergistically Induced by Ethylene and Methyl Jasmonate. Plant Cell. 1994 Aug;6(8):1077–1085. doi: 10.1105/tpc.6.8.1077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Yang Y., Shah J., Klessig D. F. Signal perception and transduction in plant defense responses. Genes Dev. 1997 Jul 1;11(13):1621–1639. doi: 10.1101/gad.11.13.1621. [DOI] [PubMed] [Google Scholar]
  55. Yu I. C., Parker J., Bent A. F. Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7819–7824. doi: 10.1073/pnas.95.13.7819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Zhang S., Klessig D. F. The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7225–7230. doi: 10.1073/pnas.95.12.7225. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES