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Plant Cell. 1998 Sep; 10(9): 1571–1580.
doi: 10.1105/tpc.10.9.1571
PMCID: PMC144073
PMID: 9724702

A novel signaling pathway controlling induced systemic resistance in Arabidopsis.

C M Pieterse, S C van Wees, J A van Pelt, M Knoester, R Laan, H Gerrits, P J Weisbeek, and L C van Loon
Author information Copyright and License information PMC Disclaimer

Abstract

Plants have the ability to acquire an enhanced level of resistance to pathogen attack after being exposed to specific biotic stimuli. In Arabidopsis, nonpathogenic, root-colonizing Pseudomonas fluorescens bacteria trigger an induced systemic resistance (ISR) response against infection by the bacterial leaf pathogen P. syringae pv tomato. In contrast to classic, pathogen-induced systemic acquired resistance (SAR), this rhizobacteria-mediated ISR response is independent of salicylic acid accumulation and pathogenesis-related gene activation. Using the jasmonate response mutant jar1, the ethylene response mutant etr1, and the SAR regulatory mutant npr1, we demonstrate that signal transduction leading to P. fluorescens WCS417r-mediated ISR requires responsiveness to jasmonate and ethylene and is dependent on NPR1. Similar to P. fluorescens WCS417r, methyl jasmonate and the ethylene precursor 1-aminocyclopropane-1-carboxylate were effective in inducing resistance against P. s. tomato in salicylic acid-nonaccumulating NahG plants. Moreover, methyl jasmonate-induced protection was blocked in jar1, etr1, and npr1 plants, whereas 1-aminocyclopropane-1-carboxylate-induced protection was affected in etr1 and npr1 plants but not in jar1 plants. Hence, we postulate that rhizobacteria-mediated ISR follows a novel signaling pathway in which components from the jasmonate and ethylene response are engaged successively to trigger a defense reaction that, like SAR, is regulated by NPR1. We provide evidence that the processes downstream of NPR1 in the ISR pathway are divergent from those in the SAR pathway, indicating that NPR1 differentially regulates defense responses, depending on the signals that are elicited during induction of resistance.

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Selected References

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  • Berger S, Bell E, Sadka A, Mullet JE. Arabidopsis thaliana Atvsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases, and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate. Plant Mol Biol. 1995 Mar;27(5):933–942. [PubMed] [Google Scholar]
  • Bleecker AB, Estelle MA, Somerville C, Kende H. Insensitivity to Ethylene Conferred by a Dominant Mutation in Arabidopsis thaliana. Science. 1988 Aug 26;241(4869):1086–1089. [PubMed] [Google Scholar]
  • Bowling SA, Clarke JD, Liu Y, Klessig DF, Dong X. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell. 1997 Sep;9(9):1573–1584. [PMC free article] [PubMed] [Google Scholar]
  • Brederode FT, Linthorst HJ, Bol JF. Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Mol Biol. 1991 Dec;17(6):1117–1125. [PubMed] [Google Scholar]
  • Cao H, Bowling SA, Gordon AS, Dong X. Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance. Plant Cell. 1994 Nov;6(11):1583–1592. [PMC free article] [PubMed] [Google Scholar]
  • Cao H, Glazebrook J, Clarke JD, 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. [PubMed] [Google Scholar]
  • Chang C, Kwok SF, Bleecker AB, Meyerowitz EM. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science. 1993 Oct 22;262(5133):539–544. [PubMed] [Google Scholar]
  • de Laat AM, van Loon LC. Regulation of Ethylene Biosynthesis in Virus-Infected Tobacco Leaves : II. TIME COURSE OF LEVELS OF INTERMEDIATES AND IN VIVO CONVERSION RATES. Plant Physiol. 1982 Jan;69(1):240–245. [PMC free article] [PubMed] [Google Scholar]
  • Delaney TP, 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. [PubMed] [Google Scholar]
  • Delaney TP, Friedrich L, Ryals JA. 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. [PMC free article] [PubMed] [Google Scholar]
  • Ecker JR, Davis RW. Plant defense genes are regulated by ethylene. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5202–5206. [PMC free article] [PubMed] [Google Scholar]
  • Epple P, Apel K, Bohlmann H. An Arabidopsis thaliana thionin gene is inducible via a signal transduction pathway different from that for pathogenesis-related proteins. Plant Physiol. 1995 Nov;109(3):813–820. [PMC free article] [PubMed] [Google Scholar]
  • Farmer EE, Ryan CA. Octadecanoid Precursors of Jasmonic Acid Activate the Synthesis of Wound-Inducible Proteinase Inhibitors. Plant Cell. 1992 Feb;4(2):129–134. [PMC free article] [PubMed] [Google Scholar]
  • Farmer EE, Johnson RR, Ryan CA. Regulation of expression of proteinase inhibitor genes by methyl jasmonate and jasmonic Acid. Plant Physiol. 1992 Mar;98(3):995–1002. [PMC free article] [PubMed] [Google Scholar]
  • Feinberg AP, Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. [PubMed] [Google Scholar]
  • 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. [PubMed] [Google Scholar]
  • Gundlach H, Müller MJ, Kutchan TM, Zenk MH. Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2389–2393. [PMC free article] [PubMed] [Google Scholar]
  • KING EO, WARD MK, RANEY DE. Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med. 1954 Aug;44(2):301–307. [PubMed] [Google Scholar]
  • Knoester M, van Loon LC, van den Heuvel J, Hennig J, Bol JF, Linthorst HJ. Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi. Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1933–1937. [PMC free article] [PubMed] [Google Scholar]
  • 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. [PubMed] [Google Scholar]
  • Lawton KA, 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. [PubMed] [Google Scholar]
  • Logemann J, Schell J, Willmitzer L. Improved method for the isolation of RNA from plant tissues. Anal Biochem. 1987 May 15;163(1):16–20. [PubMed] [Google Scholar]
  • Malamy J, Carr JP, Klessig DF, 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. [PubMed] [Google Scholar]
  • Métraux JP, 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. [PubMed] [Google Scholar]
  • Penninckx IA, Eggermont K, Terras FR, Thomma BP, De Samblanx GW, Buchala A, Métraux JP, Manners JM, Broekaert WF. 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. [PMC free article] [PubMed] [Google Scholar]
  • Pieterse CM, Derksen AM, Folders J, Govers F. Expression of the Phytophthora infestans ipiB and ipiO genes in planta and in vitro. Mol Gen Genet. 1994 Aug 2;244(3):269–277. [PubMed] [Google Scholar]
  • Pieterse CM, van Wees SC, Hoffland E, van Pelt JA, van Loon LC. 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. [PMC free article] [PubMed] [Google Scholar]
  • Potter S, Uknes S, Lawton K, Winter AM, Chandler D, DiMaio J, Novitzky R, Ward E, Ryals J. Regulation of a hevein-like gene in Arabidopsis. Mol Plant Microbe Interact. 1993 Nov-Dec;6(6):680–685. [PubMed] [Google Scholar]
  • Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD. Systemic Acquired Resistance. Plant Cell. 1996 Oct;8(10):1809–1819. [PMC free article] [PubMed] [Google Scholar]
  • Ryals J, Weymann K, Lawton K, Friedrich L, Ellis D, Steiner HY, Johnson J, Delaney TP, Jesse T, Vos P, et al. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B. Plant Cell. 1997 Mar;9(3):425–439. [PMC free article] [PubMed] [Google Scholar]
  • Schaller GE, Bleecker AB. Ethylene-binding sites generated in yeast expressing the Arabidopsis ETR1 gene. Science. 1995 Dec 15;270(5243):1809–1811. [PubMed] [Google Scholar]
  • Schweizer P, Buchala A, Silverman P, Seskar M, Raskin I, Metraux JP. Jasmonate-Inducible Genes Are Activated in Rice by Pathogen Attack without a Concomitant Increase in Endogenous Jasmonic Acid Levels. Plant Physiol. 1997 May;114(1):79–88. [PMC free article] [PubMed] [Google Scholar]
  • Shah J, Tsui F, Klessig DF. 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. [PubMed] [Google Scholar]
  • Siebert PD, Larrick JW. Competitive PCR. Nature. 1992 Oct 8;359(6395):557–558. [PubMed] [Google Scholar]
  • Staswick PE, Su W, Howell SH. Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6837–6840. [PMC free article] [PubMed] [Google Scholar]
  • 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. [PMC free article] [PubMed] [Google Scholar]
  • van Loon LC. Induction by 2-chloroethylophosphonic acid of viral-like lesions, associated proteins, and systemic resistance in tobacco. Virology. 1977 Jul 15;80(2):417–420. [PubMed] [Google Scholar]
  • van Loon LC, Bakker PA, Pieterse CM. Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol. 1998;36:453–483. [PubMed] [Google Scholar]
  • Van Wees SC, Pieterse CM, Trijssenaar A, Van 't Westende YA, Hartog F, Van Loon LC. Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol Plant Microbe Interact. 1997 Aug;10(6):716–724. [PubMed] [Google Scholar]
  • Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Metraux JP, Ryals JA. Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance. Plant Cell. 1991 Oct;3(10):1085–1094. [PMC free article] [PubMed] [Google Scholar]
  • Whalen MC, Innes RW, Bent AF, Staskawicz BJ. Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell. 1991 Jan;3(1):49–59. [PMC free article] [PubMed] [Google Scholar]
  • Xu Y, Chang PFL, Liu D, Narasimhan ML, Raghothama KG, Hasegawa PM, Bressan RA. Plant Defense Genes Are Synergistically Induced by Ethylene and Methyl Jasmonate. Plant Cell. 1994 Aug;6(8):1077–1085. [PMC free article] [PubMed] [Google Scholar]
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