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Exogenous coronatine, but not coronafacic acid or methyl jasmonate, restores the disease phenotype of a coronatine-defective mutant of Pseudomonas syringae pv. tomato on tomato seedlings

  • Bacterial and Phytoplasma Diseases
  • Published:
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Abstract

Coronatine (COR) functions as a virulence factor in the interaction of Pseudomonas syringae pv. tomato strain DC3000 with tomato and Arabidopsis. COR consists of two moieties, coronafacic acid (CFA) and coronamic acid (CMA). Both COR and CFA function as structural and functional analogues of jasmonic acid (JA) and related signaling compounds such as methyl jasmonate (MeJA) and JA-isoleucine (JA-Ile). The precise function of COR and whether MeJA functions as an analogue of COR in disease development are not known. In this study, we analyzed whether the COR-defective mutant DB29, which is a CFA− CMA− mutant of DC3000, could be complemented for virulence via the exogenous application of COR, CFA, or MeJA. When tomato seedlings were inoculated with DB29 and supplemented with exogenous COR, the DB29 population multiplied in tomato seedlings and induced disease phenotypes similar to wild-type DC3000. Although the addition of exogenous MeJA or CFA enhanced the multiplication of DB29, wild-type disease phenotypes could not be restored with these compounds. Furthermore, inoculation of DB29 along with exogenous COR, but not MeJA or CFA, suppressed the expression of defense-related genes and increased the accumulation of reactive oxygen species, which are associated with severe chlorosis. Taken together, our results suggest that although COR targets the jasmonate pathway by mimicking JA, the function of COR in disease development is distinctly different from MeJA or CFA.

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References

  • Bell KS, Sebaihia M et al (2004) Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci USA 101:11105–11110

    Article  CAS  PubMed  Google Scholar 

  • Bender CL, Alarcón-Chaidez F, Gross DC (1999) Pseudomonas syringae phytotoxins: mode of action, regulation and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev 63:266–292

    CAS  PubMed  Google Scholar 

  • Block A, Schmelz E, Jones JB, Klee HJ (2005) Coronatine and salicylic acid: the battle between Arabidopsis and Pseudomonas for phytohormone control. Mol Plant Pathol 6:79–83

    Article  CAS  Google Scholar 

  • Brooks DM, Hernández-Guzmán G, Kloek AP, Alarcón-Chaidez F, Sreedharan A, Rangaswamy V, Peñaloza-Vázquez A, Bender CL, Kunkel BN (2004) Identification and characterization of a well-defined series of coronatine biosynthetic mutants of Pseudomonas syringae pv. tomato strain DC3000. Mol Plant Microbe Interact 17:162–174

    Article  CAS  PubMed  Google Scholar 

  • Brooks DM, Bender CL, Kunkel BN (2005) The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defences in Arabidopsis thaliana. Mol Plant Pathol 6:629–639

    Article  CAS  Google Scholar 

  • Buell CR, Joardar V et al (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci USA 100:10181–10186

    Article  CAS  PubMed  Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995

    Google Scholar 

  • Daub ME, Ehrenshaft M (2000) The photoactivated Cercospora toxin cercosporin: contributions to plant disease and fundamental biology. Annu Rev Phytopathol 38:461–490

    Article  CAS  PubMed  Google Scholar 

  • Doke N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol Plant Pathol 23:345–357

    Article  CAS  Google Scholar 

  • Elizabeth SV, Bender CL (2007) The phytotoxin coronatine from Pseudomonas syringae pv. tomato DC3000 functions as a virulence factor and influences defence pathways in edible brassicas. Mol Plant Pathol 8:83–92

    Article  CAS  PubMed  Google Scholar 

  • Feys BJF, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751–759

    Article  CAS  PubMed  Google Scholar 

  • Glazebrook J, Chen W, Estes B, Chang HS, Nawrath C, Metraux JP, Zhu T, Katagiri F (2003) Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J 34:217–228

    Article  CAS  PubMed  Google Scholar 

  • He P, Chintamanani S, Chen Z, Zhu L, Kunkel BN, Alfano JR, Tang X, Zhou JM (2004) Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III effectors and coronatine. Plant J 37:589–602

    Article  CAS  PubMed  Google Scholar 

  • Ishiga Y, Uppalapati SR, Ishiga T, Elavarthi S, Martin B, Bender CL (2009a) The phytotoxin coronatine induces light-dependent reactive oxygen species in tomato seedlings. New Phytol 181:147–160

    Article  CAS  PubMed  Google Scholar 

  • Ishiga Y, Uppalapati SR, Ishiga T, Elavarthi S, Martin B, Bender CL (2009b) Involvement of coronatine-inducible reactive oxygen species in bacterial speck disease of tomato. Plant Signal Behav 4:237–239

    Article  CAS  PubMed  Google Scholar 

  • Jones WT, Harvey D, Mitchell RE, Ryan GB, Bender CL, Reynolds PHS (1997) Competitive ELISA employing monoclonal antibodies specific for coronafacoyl amino acid conjugates. Food Agric Immunol 9:67–76

    Article  CAS  Google Scholar 

  • Keane PJ, Kerr A, New PB (1970) Crown gall of stone fruit. II. Identification and nomenclature of Agrobacterium isolates. Aust J Biol Sci 23:585–595

    Google Scholar 

  • Kloek AP, Verbsky ML, Sharma SB, Schoelz JE, Vogel J, Klessig DF, Kunkel BN (2001) Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J 26:509–522

    Article  CAS  PubMed  Google Scholar 

  • Krumm T, Bandemer K, Boland W (1995) Induction of volatile biosynthesis in the Lima bean (Phaseolus lunatus) by leucine- and isoleucine conjugates of 1-oxo- and 1-hydroxyindan-4-carboxylic acid: evidence for amino acid conjugates of jasmonic acid as intermediates in the octadecanoid signalling pathway. FEBS Lett 377:523–529

    Article  CAS  PubMed  Google Scholar 

  • Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331

    Article  CAS  PubMed  Google Scholar 

  • Mittal SM, Davis KR (1995) Role of the phytotoxin coronatine in the infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact 8:165–171

    CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Niki T, Mitsuhara I, Seo S, Ohtsubo N, Ohashi Y (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol 39:500–507

    CAS  Google Scholar 

  • Palmer DA, Bender CL (1995) Ultrastructure of tomato leaf tissue treated with the pseudomonad phytotoxin coronatine and comparison with methyl jasmonate. Mol Plant Microbe Interact 8:683–692

    CAS  Google Scholar 

  • Peñaloza-Vázquez A, Preston GM, Collmer A, Bender CL (2000) Regulatory interactions between the Hrp type III protein secretion system and coronatine biosynthesis in Pseudomonas syringae pv. tomato DC3000. Microbiology 10:2447–2456

    Google Scholar 

  • Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127

    Article  CAS  PubMed  Google Scholar 

  • Thilmony R, Underwood W, He SY (2006) Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J 46:34–53

    Article  CAS  PubMed  Google Scholar 

  • Ueno H, Shibata H, Kihara J, Honda Y, Arase S (2003) Increased tryptophan decarboxylase and monoamine oxidase activities induce Sekiguchi lesion formation in rice infected with Magnaporthe grisea. Plant J 36:215–228

    Article  CAS  PubMed  Google Scholar 

  • Uppalapati SR, Patricia A, Weng H, Palmer DA, Mitchell RE, Jones W, Bender CL (2005) The phytotoxin coronatine and methyl jasmonate impacts multiple phytohormone pathways in tomato. Plant J 42:201–217

    Article  CAS  PubMed  Google Scholar 

  • Uppalapati SR, Ishiga Y, Wangdi T, Kunkel BN, Anand A, Mysore KS, Bender CL (2007) The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Mol Plant Microbe Interact 20:955–965

    Article  CAS  PubMed  Google Scholar 

  • Uppalapati SR, Ishiga Y, Wangdi T, Urbanczyk-Wochniak E, Ishiga T, Mysore KS, Bender CL (2008) Pathogenicity of Pseudomonas syringae pv. tomato on tomato seedlings: phenotypic and gene expression analyses of the virulence function of coronatine. Mol Plant Microbe Interact 21:383–395

    Article  CAS  PubMed  Google Scholar 

  • Weiler EW, Kutchan TM, Gorba T, Brodschelm W, Neisel U, Bublitz F (1994) The Pseudomonas phytotoxin coronatine mimics octadecanoid signaling molecules of higher plants. FEBS Lett 345:9–13

    Article  CAS  PubMed  Google Scholar 

  • Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what’s in a name? Annu Rev Phytopathol 40:251–285

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Thilmony R, Bender CL, Schaller A, He SY, Howe GA (2003) Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 36:485–499

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded in part by National Science Foundation grant IBN-0620469 and the Oklahoma Agricultural Experiment Station (C. L. Bender). Y. Ishiga was supported by a postdoctoral fellowship from the Japan Society for the Promotion of Science (JSPS). The OSU Microarray Facility was supported by grants from NSF (EOS-0132534) and NIH (1P20RR16478-02 and 5P20RR15564-03). The authors also thank Dr. Kiran Mysore for providing some of the resources required to complete this work.

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Authors and Affiliations

  1. Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, OK, 74078, USA

    Yasuhiro Ishiga, Takako Ishiga & Carol L. Bender

  2. Plant Biology Division, The Samuel Roberts Noble Foundation, 2510 Sam Noble Parkway, Ardmore, OK, 73401, USA

    Yasuhiro Ishiga & Srinivasa Rao Uppalapati

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  1. Yasuhiro Ishiga
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  2. Srinivasa Rao Uppalapati
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  3. Takako Ishiga
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  4. Carol L. Bender
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Correspondence to Srinivasa Rao Uppalapati or Carol L. Bender.

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Ishiga, Y., Uppalapati, S.R., Ishiga, T. et al. Exogenous coronatine, but not coronafacic acid or methyl jasmonate, restores the disease phenotype of a coronatine-defective mutant of Pseudomonas syringae pv. tomato on tomato seedlings. J Gen Plant Pathol 76, 188–195 (2010). https://doi.org/10.1007/s10327-010-0228-3

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  • DOI: https://doi.org/10.1007/s10327-010-0228-3

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