Download PDF
Plant Biol (Stuttg) 2002; 4(5): 535-544
DOI: 10.1055/s-2002-35441
Review Article
Georg Thieme Verlag Stuttgart ·New York

Signalling in Rhizobacteria-Induced Systemic Resistance in Arabidopsis thaliana

C. M. J. Pieterse 1 , S. C. M. Van Wees 1,2 , J. Ton 1,3 , J. A. Van Pelt 1 , L. C. Van Loon 1
  • 1 Graduate School Experimental Plant Sciences, Section Phytopathology, Faculty of Biology, Utrecht University, Utrecht, The Netherlands
  • 2 Present address: Torrey Mesa Research Institute, Syngenta, 3115 Merryfield Row, San Diego, CA 92121, USA
  • 3 Present address: Laboratory of Biochemistry, NCCR, University of Neuchâtel, Rue Emile-Argand 9, CH-2007 Neuchâtel 7, Switzerland
Further Information

Publication History

Received: July 9, 2002

Accepted: September 2, 2002

Publication Date:
15 November 2002 (online)

   Permissions and Reprints

Abstract

To protect themselves from disease, plants have evolved sophisticated defence mechanisms in which the signal molecules salicylic acid, jasmonic acid and ethylene often play crucial roles. Elucidation of signalling pathways controlling disease resistance is a major objective in research on plant-pathogen interactions. The capacity of a plant to develop a broad spectrum, systemic acquired resistance (SAR) after primary infection with a necrotizing pathogen is well-known and its signal transduction pathway extensively studied. Plants of which the roots have been colonized by specific strains of non-pathogenic fluorescent Pseudomonas spp. develop a phenotypically similar form of protection that is called rhizobacteria-mediated induced systemic resistance (ISR). In contrast to pathogen-induced SAR, which is regulated by salicylic acid, rhizobacteria-mediated ISR is controlled by a signalling pathway in which jasmonic acid and ethylene play key roles. In the past eight years, the model plant species Arabidopsis thaliana was explored to study the molecular basis of rhizobacteria-mediated ISR. Here we review current knowledge of the signal transduction steps involved in the ISR pathway that leads from recognition of the rhizobacteria in the roots to systemic expression of broad-spectrum disease resistance in aboveground foliar tissues.

Key words

Arabidopsis - disease resistance - ethylene - induced systemic resistance - jasmonic acid - plant defence - Pseudomonas fluorescens - systemic acquired resistance

References

  • 01 Bakker,  P. A. H. M.,, Van Peer,  R.,, and Schippers,  B.. (1991) Suppression of soil-borne plant pathogens by fluorescent Pseudomonas: mechanisms and prospects. Biotic Interactions and Soil-Borne Diseases, Developments in Agricultural and Managed-Forest Ecology. Beemster, A. B. R., Bollen, G. J., Gerlagh, M., Ruissen, M. A., Schippers, B., and Tempel, A., eds. Amsterdam, The Netherlands; Elsevier Scientific Publishers pp. 217-230
    Google Scholar
  • 02 Bell,  E.,, Creelman,  R. A.,, and Mullet,  J. E.. (1995);  A chloroplast lipoxygenase is required for wound-induced accumulation of jasmonic acid in Arabidopsis.  Proc. Natl. Acad. Sci. USA. 92 8675-8679
    Google Scholar
  • 03 Bent,  A. F.,, Innes,  R. W.,, Ecker,  J. R.,, and Staskawicz,  B. J.. (1992);  Disease development in ethylene-insensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas pathogens.  Mol. Plant-Microbe Interact.. 5 372-378
    Google Scholar
  • 04 Bigirimana,  J., and Höfte,  M.. (2002);  Induction of systemic resistance to Colletotrichum lindemuthianum in bean by a benzothiadiazole derivative and rhizobacteria.  Phytoparasitica. 30 159-168
    Google Scholar
  • 05 Bork,  P.. (1993);  Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally?.  Proteins . 17 363-374
    Google Scholar
  • 06 Bowling,  S. A.,, Guo,  A.,, Cao,  H.,, Gordon,  A. S.,, Klessig,  D. F.,, and Dong,  X.. (1994);  A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance.  Plant Cell. 6 1845-1857
    Google Scholar
  • 07 Cameron,  R. K.,, Dixon,  R. A.,, and Lamb,  C. J.. (1994);  Biologically induced systemic acquired resistance in Arabidopsis thaliana. .  Plant J.. 5 715-725
    Google Scholar
  • 08 Cao,  H., Bowling,  S. A.,, Gordon,  A. S.,, and Dong,  X.. (1994);  Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance.  Plant Cell. 6 1583-1592
    Google Scholar
  • 09 Cao,  H.,, Glazebrook,  J.,, Clarke,  J. D.,, Volko,  S.,, and Dong,  X.. (1997);  The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats.  Cell. 88 57-63
    Google Scholar
  • 10 Conrath,  U.,, Pieterse,  C. M. J.,, and Mauch-Mani,  B.. (2002);  Priming in plant-pathogen interactions.  Trends Plant Sci.. 7 210-216
    CrossrefPubMedGoogle Scholar
  • 11 De Boer,  M.,, Van der Sluis,  I.,, Van Loon,  L. C.,, and Bakker,  P. A. H. M.. (1999);  Combining fluorescent Pseudomonas spp. strains to enhance suppression of fusarium wilt of radish.  Eur. J. Plant Pathol.. 105 201-210
    CrossrefPubMedGoogle Scholar
  • 12 De Meyer,  G., and Höfte,  M.. (1997);  Salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 induces resistance to leaf infection by Botrytis cinerea on bean.  Phytopathology. 87 588-593
    PubMedGoogle Scholar
  • 13 Delaney,  T. P.,, Uknes,  S.,, Vernooij,  B.,, Friedrich,  L.,, Weymann,  K.,, Negrotto,  D.,, Gaffney,  T.,, Gur-Rella,  M.,, Kessmann,  H.,, Ward,  E.,, and Ryals,  J.. (1994);  A central role of salicylic acid in plant disease resistance.  Science. 266 1247-1250
    PubMedGoogle Scholar
  • 14 Delaney,  T. P.,, Friedrich,  L.,, and Ryals,  J. A.. (1995);  Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance.  Proc. Natl. Acad. Sci. USA. 92 6602-6606
    PubMedGoogle Scholar
  • 15 Delaney,  T. P.. (1997);  Genetic dissection of acquired resistance to disease.  Plant Physiol.. 113 5-12
    CrossrefPubMedGoogle Scholar
  • 16 Dempsey,  D. A.,, Shah,  J.,, and Klessig,  D. F.. (1999);  Salicylic acid and disease resistance in plants.  Crit. Rev. Plant Sci.. 18 547-575
    PubMedGoogle Scholar
  • 17 Després,  C.,, DeLong,  C.,, Glaze,  S.,, Liu,  E.,, and Fobert,  P. R.. (2000);  The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors.  Plant Cell. 12 279-290
    CrossrefPubMedGoogle Scholar
  • 18 Dong,  X.. (1998);  SA, JA, ethylene, and disease resistance in plants.  Curr. Opinion Plant Biol.. 1 316-323
    PubMedGoogle Scholar
  • 19 Dong,  X.. (2001);  Genetic dissection of systemic acquired resistance.  Curr. Opinion Plant Biol.. 4 309-314
    PubMedGoogle Scholar
  • 20 Duijff,  B. J.,, Pouhair,  D.,, Olivain,  C.,, Alabouvette,  C.,, and Lemanceau,  P.. (1998);  Implication of systemic induced resistance in the suppression of fusarium wilt of tomato by Pseudomonas fluorescens WCS417r and by nonpathogenic Fusarium oxysporum Fo47.  Eur. J. Plant Pathol.. 104 903-910
    CrossrefPubMedGoogle Scholar
  • 21 Fan,  W., and Dong,  X.. (2002);  In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. .  Plant Cell. 14 1377-1389
    CrossrefPubMedGoogle Scholar
  • 22 Gaffney,  T.,, Friedrich,  L.,, Vernooij,  B.,, Negrotto,  D.,, Nye,  G.,, Uknes,  S.,, Ward,  E.,, Kessmann,  H.,, and Ryals,  J.. (1993);  Requirement of salicylic acid for the induction of systemic acquired resistance.  Science. 261 754-756
    PubMedGoogle Scholar
  • 23 Glazebrook,  J.,, Rogers,  E. E.,, and Ausubel,  F. M.. (1996);  Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening.  Genetics. 143 973-982
    PubMedGoogle Scholar
  • 24 Glazebrook,  J.. (2001);  Genes controlling expression of defense responses in Arabidopsis - 2001 status.  Curr. Opinion Plant Biol.. 4 301-308
    PubMedGoogle Scholar
  • 25 Gupta,  V.,, Willits,  M. G.,, and Glazebrook,  J.. (2000);  Arabidopsis thaliana EDS4 contributes to salicylic acid (SA)-dependent expression of defense responses: evidence for inhibition of jasmonic acid signaling by SA.  Mol. Plant-Microbe Interact.. 13 503-511
    PubMedGoogle Scholar
  • 26 Hammerschmidt,  R.. (1999);  Induced disease resistance: how do induced plants stop pathogens?.  Physiol. Mol. Plant Pathol.. 55 77-84
    CrossrefPubMedGoogle Scholar
  • 27 Hammerschmidt,  R.,, Métraux,  J.-P.,, and Van Loon,  L. C.. (2001);  Inducing resistance: a summary of papers presented at the First International Symposium on Induced Resistance to Plant Diseases, Corfu, May 2000.  Eur. J. Plant Pathol.. 107 1-6
    PubMedGoogle Scholar
  • 28 Hoffland,  E.,, and Pieterse,  C. M. J.,, Bik,  L.,, and Van Pelt,  J. A.. (1995);  Induced systemic resistance in radish is not associated with accumulation of pathogenesis-related proteins.  Physiol. Mol. Plant Pathol.. 46 309-320
    CrossrefPubMedGoogle Scholar
  • 29 Kachroo,  P.,, Yoshioka,  K.,, Shah,  J.,, Dooner,  K. D.,, and Klessig,  D. F.. (2000);  Resistance to turnip crinkle virus in Arabidopsis is regulated by two host genes and is salicylic acid dependent but NPR1, ethylene, and jasmonate independent.  Plant Cell. 12 677-690
    CrossrefPubMedGoogle Scholar
  • 30 Kinkema,  M.,, Fan,  W.,, and Dong,  X.. (2000);  Nuclear localization of NPR1 is required for activation of PR gene expression.  Plant Cell. 12 2339-2350
    CrossrefPubMedGoogle Scholar
  • 31 Kloepper,  J. W.,, Leong,  J.,, Teintze,  M.,, and Schroth,  M. N.. (1980);  Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria.  Nature. 286 885-886
    CrossrefPubMedGoogle Scholar
  • 32 Knoester,  M.,, Pieterse,  C. M. J.,, Bol,  J. F.,, and Van Loon,  L. C.. (1999);  Systemic resistance in Arabidopsis induced by rhizobacteria requires ethylene-dependent signaling at the site of application.  Mol. Plant-Microbe Interact.. 12 720-727
    PubMedGoogle Scholar
  • 33 Kuc,  J.. (1982);  Induced immunity to plant disease.  Bioscience. 32 854-860
    PubMedGoogle Scholar
  • 34 Kunkel,  B. N.. (1996);  A useful weed put to work: genetic analysis of disease resistance in Arabidopsis thaliana. .  Trends Genet.. 12 62-69
    PubMedGoogle Scholar
  • 35 Kus,  J. V.,, Zaton,  K.,, Sarkar,  R.,, and Cameron,  R. K.. (2002);  Age-related resistance in Arabidopsis is a developmentally regulated defense response to Pseudomonas syringae. .  Plant Cell. 14 479-490
    CrossrefPubMedGoogle Scholar
  • 36 Lawton,  K.,, Weymann,  K.,, Friedrich,  L.,, Vernooij,  B.,, Uknes,  S.,, and Ryals,  J.. (1995);  Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene.  Mol. Plant-Microbe Interact.. 8 863-870
    PubMedGoogle Scholar
  • 37 Leeman,  M.,, Van Pelt,  J. A.,, Den Ouden,  F. M.,, Heinsbroek,  M.,, Bakker,  P. A. H. M.,, and Schippers,  B.. (1995 a);  Induction of systemic resistance by Pseudomonas fluorescens in radish cultivars differing in susceptibility to fusarium wilt, using a novel bioassay.  Eur. J. Plant Pathol.. 101 655-664
    CrossrefPubMedGoogle Scholar
  • 38 Leeman,  M.,, Van Pelt,  J. A.,, Den Ouden,  F. M.,, Heinsbroek,  M.,, Bakker,  P. A. H. M.,, and Schippers,  B.. (1995 b);  Induction of systemic resistance against fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens. .  Phytopathology . 85 1021-1027
    PubMedGoogle Scholar
  • 39 Leeman,  M.,, Van Pelt,  J. A.,, Hendrickx,  M. J.,, Scheffer,  R. J.,, Bakker,  P. A. H. M.,, and Schippers,  B.. (1995 c);  Biocontrol of fusarium wilt of radish in commercial greenhouse trials by seed treatment with Pseudomonas fluorescens WCS374.  Phytopathology. 85 1301-1305
    PubMedGoogle Scholar
  • 40 Lynch,  J. M.. (1976);  Products of soil microorganisms in relation to plant growth.  Crit. Rev. Microbiol.. 5 67-107
    PubMedGoogle Scholar
  • 41 Lynch,  J. M., and Whipps,  J. M.. (1991) Substrate flow in the rhizosphere. The Rhizosphere and Plant Growth. Keister, D. L. and Cregan, P. B., eds Dordrecht, The Netherlands; Kluwer pp. 15-24
    Google Scholar
  • 42 Malamy,  J.,, Carr,  J. P.,, Klessig,  D. F.,, and Raskin,  I.. (1990);  Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection.  Science. 250 1002-1004
    PubMedGoogle Scholar
  • 43 Mauch-Mani,  B., and Slusarenko,  A. J.. (1993);  Arabidopsis as a model host for studying plant-pathogen interactions.  Trends Microbiol.. 1 265-270
    CrossrefPubMedGoogle Scholar
  • 44 Mauch-Mani,  B., and Slusarenko,  A. J.. (1994);  Systemic acquired resistance in Arabidopsis thaliana induced by a predisposing infection with a pathogenic isolate of Fusarium oxysporum. .  Mol. Plant-Microbe Interact.. 7 378-383
    PubMedGoogle Scholar
  • 45 Maurhofer,  M.,, Reimann,  C.,, Schmidli-Sacherer,  P.,, Heeb,  S. D.,, and Défago,  G.. (1998);  Salicylic acid biosynthesis genes expressed in Pseudomonas fluorescens strain P3 improve the induction of systemic resistance in tobacco against tobacco necrosis virus.  Phytopathology. 88 678-684
    PubMedGoogle Scholar
  • 46 Métraux,  J.-P.,, Signer,  H.,, Ryals,  J.,, Ward,  E.,, Wyss-Benz,  M.,, Gaudin,  J.,, Raschdorf,  K.,, Schmid,  E.,, Blum,  W.,, and Inverardi,  B.. (1990);  Increase in salicylic acid at the onset of systemic acquired resistance in cucumber.  Science. 250 1004-1006
    PubMedGoogle Scholar
  • 47 Métraux,  J.-P.. (2001);  Systemic acquired resistance and salicylic acid: current state of knowledge.  Eur. J. Plant Pathol.. 107 13-18
    CrossrefPubMedGoogle Scholar
  • 48 Nawrath,  C., and Métraux,  J.-P.. (1999);  Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation.  Plant Cell. 11 1393-1404
    CrossrefPubMedGoogle Scholar
  • 49 Pieterse,  C. M. J.,, Van Wees,  S. C. M.,, Hoffland,  E.,, Van Pelt,  J. A.,, and Van Loon,  L. C.. (1996);  Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression.  Plant Cell. 8 1225-1237
    CrossrefPubMedGoogle Scholar
  • 50 Pieterse,  C. M. J.,, Van Wees,  S. C. M.,, Van Pelt,  J. A.,, Knoester,  M.,, Laan,  R.,, Gerrits,  H.,, Weisbeek,  P. J.,, and Van Loon,  L. C.. (1998);  A novel signaling pathway controlling induced systemic resistance in Arabidopsis. .  Plant Cell. 10 1571-1580
    CrossrefPubMedGoogle Scholar
  • 51 Pieterse,  C. M. J., and Van Loon,  L. C.. (1999);  Salicylic acid-independent plant defence pathways.  Trends Plant Sci.. 4 52-58
    CrossrefPubMedGoogle Scholar
  • 52 Pieterse,  C. M. J.,, Van Pelt,  J. A.,, Ton,  J.,, Parchmann,  S.,, Mueller,  M. J.,, Buchala,  A. J.,, Métraux,  J..P.,, and Van Loon,  L. C.. (2000);  Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis requires sensitivity to jasmonate and ethylene but is not accompanied by an increase in their production.  Physiol. Mol. Plant Pathol.. 57 123-134
    CrossrefPubMedGoogle Scholar
  • 53 Pieterse,  C. M. J.,, Ton,  J.,, and Van Loon,  L. C.. (2001 a);  Cross-talk between plant defence signalling pathways: boost or burden?.  AgBiotechNet. 3 ABN 068
    PubMedGoogle Scholar
  • 54 Pieterse,  C. M. J.,, Van Pelt,  J. A.,, Van Wees,  S. C. M.,, Ton,  J.,, Léon-Kloosterziel,  K. M.,, Keurentjes,  J. J. B.,, Verhagen,  B. W. M.,, Knoester,  M.,, Van der Sluis,  I.,, Bakker,  P. A. H. M.,, and Van Loon,  L. C.. (2001 b);  Rhizobacteria-mediated induced systemic resistance: triggering, signalling and expression.  Eur. J. Plant Pathol.. 107 51-61
    CrossrefPubMedGoogle Scholar
  • 55 Press,  C. M.,, Wilson,  M.,, Tuzun,  S.,, and Kloepper,  J. W.. (1997);  Salicylic acid produced by Serratia marcescens 91-166 is not the primary determinant of induced systemic resistance in cucumber or tobacco.  Mol. Plant-Microbe Interact.. 10 761-768
    PubMedGoogle Scholar
  • 56 Raaijmakers,  J. M., and Weller,  D. M.. (1998);  Natural plant protection by 2,4-diacetylphloroglucinol-producing Pseudomonas spp. in take-all decline soils.  Mol. Plant-Microbe Interact.. 11 144-152
    PubMedGoogle Scholar
  • 57 Rogers,  E. E., and Ausubel,  F. M.. (1997);  Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression.  Plant Cell. 9 305-316
    CrossrefPubMedGoogle Scholar
  • 58 Ross,  A. F.. (1961);  Systemic acquired resistance induced by localized virus infections in plants.  Virology. 14 340-358
    CrossrefPubMedGoogle Scholar
  • 59 Ryals,  J.,, Weymann,  K.,, Lawton,  K.,, Friedrich,  L.,, Ellis,  D.,, Steiner,  H. Y.,, Johnson,  J.,, Delaney,  T. P.,, Jesse,  T.,, Vos,  P.,, and Uknes,  S.. (1997);  The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IkB.  Plant Cell. 9 425-439
    CrossrefPubMedGoogle Scholar
  • 60 Ryals,  J. A.,, Neuenschwander,  U. H.,, Willits,  M. G.,, Molina,  A.,, Steiner,  H.-Y.,, and Hunt,  M. D.. (1996);  Systemic acquired resistance.  Plant Cell. 8 1808-1819
    PubMedGoogle Scholar
  • 61 Schippers,  B.,, Bakker,  A. W.,, and Bakker,  P. A. H. M.. (1987);  Interactions of deleterious and beneficial rhizosphere micoorganisms and the effect of cropping practices.  Annu. Rev. Phytopathol.. 115 339-358
    PubMedGoogle Scholar
  • 62 Shah,  J.,, Tsui,  F.,, and Klessig,  D. F.. (1997);  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.. 10 69-78
    PubMedGoogle Scholar
  • 63 Sticher,  L.,, Mauch-Mani,  B.,, and Métraux,  J.-P.. (1997);  Systemic acquired resistance.  Annu. Rev. Phytopathol.. 35 235-270
    CrossrefPubMedGoogle Scholar
  • 64 Subramaniam,  R.,, Desveaux,  D.,, Spickler,  C.,, Michnick,  S. W.,, and Brisson,  N.. (2001);  Direct visualization of protein interactions in plant cells.  Nat. Biotechnol.. 19 769-772
    PubMedGoogle Scholar
  • 65 Thomma,  B. P. H. J.,, Eggermont,  K.,, Penninckx,  I. A. M. A.,, Mauch-Mani,  B.,, Vogelsang,  R.,, Cammue,  B. P. A.,, and Broekaert,  W. F.. (1998);  Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens.  Proc. Natl. Acad. Sci. USA. 95 15107-15111
    CrossrefPubMedGoogle Scholar
  • 66 Thomma,  B. P. H. J.,, Eggermont,  K.,, Tierens,  K. F. M.,, and Broekaert,  W. F.. (1999);  Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. .  Plant Physiol.. 121 1093-1102
    CrossrefPubMedGoogle Scholar
  • 67 Ton,  J.,, Pieterse,  C. M. J.,, and Van Loon,  L. C.. (1999);  Identification of a locus in Arabidopsis controlling both the expression of rhizobacteria-mediated induced systemic resistance (ISR) and basal resistance against Pseudomonas syringae pv. tomato. .  Mol. Plant-Microbe Interact.. 12 911-918
    PubMedGoogle Scholar
  • 68 Ton,  J.. (2001) Rhizobacteria-mediated induced systemic resistance in Arabidopsis: molecular-genetic basis of induced resistance in relation to basal resistance. Utrecht University, The Netherlands; Ph. D. Thesis 136 pages
    Google Scholar
  • 69 Ton,  J.,, Davison,  S.,, Van Wees,  S. C. M.,, Van Loon,  L. C.,, and Pieterse,  C. M. J.. (2001);  The Arabidopsis ISR1 locus controlling rhizobacteria-mediated induced systemic resistance is involved in ethylene signaling.  Plant Physiol.. 125 652-661
    CrossrefPubMedGoogle Scholar
  • 70 Ton,  J.,, De Vos,  M.,, Robben,  C.,, Buchala,  A. J.,, Métraux,  J.-P.,, Van Loon,  L. C.,, and Pieterse,  C. M. J.. (2002 a);  Characterization of Arabidopsis enhanced disease susceptibility mutants that are affected in systemically induced resistance.  Plant J.. 29 11-21
    CrossrefPubMedGoogle Scholar
  • 71 Ton,  J.,, Van Pelt,  J. A.,, Van Loon,  L. C.,, and Pieterse,  C. M. J.. (2002 b);  Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. .  Mol. Plant-Microbe Interact.. 15 27-34
    PubMedGoogle Scholar
  • 72 Ton,  J.,, Van Pelt,  J. A.,, Van Loon,  L. C.,, and Pieterse,  C. M. J.. (2002 c);  The Arabidopsis ISR1 locus is required for rhizobacteria-mediated induced systemic resistance against different pathogens.  Plant Biol.. 4 224-227
    Article in Thieme ConnectPubMedGoogle Scholar
  • 73 Tuzun,  S., and Kloepper,  J.. (1995) Practical application and implementation of induced resistance. Induced Resistance to Diseases in Plants. Hammerschmidt, R. and Kuc, J., eds. Dordrecht, The Netherlands; Kluwer Academic Press pp. 152-168
    Google Scholar
  • 74 Uknes,  S.,, Mauch-Mani,  B.,, Moyer,  M.,, Potter,  S.,, Williams,  S.,, Dincher,  S.,, Chandler,  D.,, Slusarenko,  A.,, Ward,  E.,, and Ryals,  J.. (1992);  Acquired resistance in Arabidopsis. .  Plant Cell. 4 645-656
    CrossrefPubMedGoogle Scholar
  • 75 Van Loon,  L. C.. (1997);  Induced resistance and the role of pathogenesis-related proteins.  Eur. J. Plant Pathol.. 103 753-765
    CrossrefPubMedGoogle Scholar
  • 76 Van Loon,  L. C.,, Bakker,  P. A. H. M.,, and Pieterse,  C. M. J.. (1998);  Systemic resistance induced by rhizosphere bacteria.  Annu. Rev. Phytopathol.. 36 453-483
    CrossrefPubMedGoogle Scholar
  • 77 Van Loon,  L. C., and Van Strien,  E. A.. (1999);  The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins.  Physiol. Mol. Plant Pathol.. 55 85-97
    CrossrefPubMedGoogle Scholar
  • 78 Van Peer,  R., and Schippers,  B.. (1989);  Plant growth responses to bacterization and rhizosphere microbial development in hydroponic cultures.  Can. J. Microbiol.. 35 456-463
    PubMedGoogle Scholar
  • 79 Van Peer,  R.,, Niemann,  G. J.,, and Schippers,  B.. (1991);  Induced resistance and phytoalexin accumulation in biological control of fusarium wilt of carnation by Pseudomonas sp. strain WCS417r.  Phytopathology. 91 728-734
    PubMedGoogle Scholar
  • 80 Van Peer,  R., and Schippers,  B.. (1992);  Lipopolysaccharides of plant growth-promoting Pseudomonas sp.strain WCS417r induce resistance in carnation to fusarium wilt.  Neth. J. Plant Pathol.. 98 129-139
    PubMedGoogle Scholar
  • 81 Van Wees,  S. C. M.,, Pieterse,  C. M. J.,, Trijssenaar,  A.,, Van't Westende,  Y. A. M.,, Hartog,  F.,, and Van Loon,  L. C.. (1997);  Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria.  Mol. Plant-Microbe Interact.. 10 716-724
    PubMedGoogle Scholar
  • 82 Van Wees,  S. C. M.. (1999) Rhizobacteria-mediated induced systemic resistance in Arabidopsis: signal transduction and expression. Utrecht University, The Netherlands; Ph. D. Thesis 137 pages
    Google Scholar
  • 83 Van Wees,  S. C. M.,, Luijendijk,  M.,, Smoorenburg,  I.,, Van Loon,  L. C.,, and Pieterse,  C. M. J.. (1999);  Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene Atvsp upon challenge.  Plant Mol. Biol.. 41 537-549
    CrossrefPubMedGoogle Scholar
  • 84 Van Wees,  S. C. M.,, De Swart,  E. A. M.,, Van Pelt,  J. A.,, Van Loon,  L. C.,, and Pieterse,  C. M. J.. (2000);  Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. .  Proc. Natl. Acad. Sci. USA. 97 8711-8716
    CrossrefPubMedGoogle Scholar
  • 85 Verhagen,  B. W. M.,, Glazebrook,  J.,, Chang,  H.-S.,, Zou,  G.,, Zhu,  T.,, Van Loon,  L. C.,, and Pieterse,  C. M. J.. (2001) Expression profiling of Arabidopsis genes during rhizobacteria-mediated induced systemic resistance (ISR). Madison, USA; 10th International Congress on Molecular Plant-Microbe Interactions, Book of Abstracts p. 281
    Google Scholar
  • 86 Ward,  E. R.,, Uknes,  S J.,, Williams,  S. C.,, Dincher,  S. S.,, Wiederhold,  D. L.,, Alexander,  D. C.,, Ahl-Goy,  P.,, Métraux,  J.-P.,, and Ryals,  J. A.. (1991);  Coordinate gene activity in response to agents that induce systemic acquired resistance.  Plant Cell. 3 1085-1094
    CrossrefPubMedGoogle Scholar
  • 87 Wei,  G.,, Kloepper,  J. W.,, and Tuzun,  S.. (1991);  Induction of systemic resistance of cucumber to Colletrotichum orbiculare by select strains of plant-growth promoting rhizobacteria.  Phytopathology. 81 1508-1512
    PubMedGoogle Scholar
  • 88 Wei,  G.,, Kloepper,  J. W.,, and Tuzun,  S.. (1996);  Induced systemic resistance to cucumber diseases and increased plant growth by plant growth-promoting rhizobacteria under field conditions.  Phytopathology. 86 221-224
    PubMedGoogle Scholar
  • 89 Zhang,  Y.,, Fan,  W.,, Kinkema,  M.,, Li,  X.,, and Dong,  X.. (1999);  Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene.  Proc. Natl. Acad. Sci. USA. 96 6523-6528
    CrossrefPubMedGoogle Scholar
  • 90 Zhou,  J. M.,, Trifa,  Y.,, Silva,  H.,, Pontier,  D.,, Lam,  E.,, Shah,  J.,, and Klessig,  D. F.. (2000);  NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid.  Mol. Plant-Microbe Interact.. 13 191-202
    PubMedGoogle Scholar

C. M. J. Pieterse

Phytopathology
Faculty of Biology
Utrecht University

P.O. Box 800.84
3508 TB Utrecht
The Netherlands

Email: c.m.j.pieterse@bio.uu.nl

URL: http://www.bio.uu.nl/~fytopath

Section Editor: L. A. C. J. Voesenek

      >