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Infection by a coronatine-producing strain of Pectobacterium cacticidum isolated from sunflower plants in Mexico is characterized by soft rot and chlorosis

  • Bacterial and Phytoplasma Diseases
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Abstract

A novel strain of Pectobacterium, isolated from infected sunflower plants (Helianthus annuus L.) in Mexico was characterized. Inoculated sunflower plants developed both tissue chlorosis and soft-rot on leaves. The broad host range shown by this pathogen, which included members of the Agavaceae, Asteraceae, Brassicaceae and Solanaceae, was characteristic of the genus Pectobacterium. The metabolic profile and molecular data, in addition to the secretion of plant-cell-wall-degrading enzymes, confirmed its identification as a member of the Pectobacterium genus. A phylogenetic tree constructed on the basis of its 16S rDNA sequence revealed a high identity (98 %) with P. cacticidum. Amplification and restriction-fragment-length-polymorphism analysis of internal transcribed sequences further confirmed its classification as P. cacticidum. Similar to strains of P. atrosepticum, P. carotovorum and Dickeya spp., the new P. cacticidum strain FHLGJ22 has a coronafacic ligase gene and produces coronatine, a virulence factor usually associated with phytopathogenic strains of Pseudomonas syringae. Our results suggest that this strain may utilize a dual infection process involving cell maceration and plant toxins, which is synchronized via an unknown mechanism, might confer an adaptive advantage to colonize different plant hosts.

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References

  • Alcorn SM, Orum TV, Steigerwalt AG, Foster JLM, Fogleman JC, Brenner DJ (1991) Taxonomy and pathogenicity of Erwinia cacticida sp. nov. Int J Sys Bacteriol 41:197–212

    Article  CAS  Google Scholar 

  • Andro T, Chambost JP, Kotoujansky A, Cattaneo J, Bertheau Y, Barras F, Van Gijsegem F, Coleno A (1984) Mutants of Erwinia chrysanthemi defective in secretion of pectinase and cellulose. J Bacteriol 160:1199–1203

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bell KS, Sebaihia M, Pritchard L, Holden MTG, Hyman LJ, Holeva MC, Thomson NR, Bentley SD, Churcher LJC, Mungall K, Atkin R, Bason N, Brooks K, Chillingworth T, Clark K, Doggett J, Fraser A, Hance Z, Hauser H, Jagels K, Moule S, Norbertczak H, Ormond D, Price C, Quail MA, Sanders M, Walker D, Whitehead S, Salmond GPC, Birch PRJ, Parkhill J, Toth IK (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  PubMed Central  CAS  PubMed  Google Scholar 

  • Bender CL, Young SA, Mitchell RE (1991) Conservation of plasmid DNA sequences in coronatine-producing pathovars of Pseudomonas syringae. Appl Environ Microbiol 57:993–999

    PubMed Central  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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bereswill S, Bugert P, Völksch B, Ullrich M, Bender CL, Geider K (1994) Identification and relatedness of coronatine-producing Pseudomonas syringae pathovars by PCR analysis and sequence determination of the amplification products. App Environ Microbiol 60:2924–2930

    CAS  Google Scholar 

  • Burkholder WH, MacFadden LA, Dimock EW (1953) A bacterial blight of chrysanthemums. Phytopathology 43:522–526

    Google Scholar 

  • Cole JR, Wang Q, Cárdenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2008) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucl Acids Res 37:D141–D145

    Article  PubMed Central  PubMed  Google Scholar 

  • Davis KR, Schott E, Ausubel FM (1991) Virulence of selected phytopathogenic pseudomonads in Arabidopsis thaliana. Mol Plant Microbe Interact 4:477–488

    Article  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74:2461–2470

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fucikovsky L (1997) Review of plant bacterial diseases caused by fluorescent Pseudomonas species in México. In: Rudolph K (ed) Pseudomonas syringae pathovar and related pathogens. Developments in Plant Pathology, 9th edn. Springer, Berlin, pp 435–439

    Google Scholar 

  • Gardan L, Gouy C, Christen R, Samson R (2003) Elevation of three subspecies of Pectobacterium carotovorum to species level: pectobacterium atrosepticum sp. nov., Pectobacterium betavasculorum sp. nov. and Pectobacterium wasabiae sp. nov. Int J Syst Evol Microbiol 53:381–391

    Article  CAS  PubMed  Google Scholar 

  • Hauben L, Moore EB, Vauterin L, Steenackers M, Mergaert J, Verdonck L, Swings J (1998) Phylogenetic position of phytopathogens within the Enterobacteriaceae. Syst Appl Microbiol 21:384–397

    Article  CAS  PubMed  Google Scholar 

  • Holt JG, Krieg NR, Sneath PH, Staley JT, Williams ST (1994) Bergey’s manual of determinative bacteriology, 9th edn. Williams and Wilkins, Baltimore, pp 175–184

    Google Scholar 

  • Hugouvieux-Cotte-Pattat N, Condemine G, Nasser W, Reverchon S (1996) Regulation of pectinolysis in Erwinia chrysanthemi. Annu Rev Microbiol 50:213–257

    Article  CAS  PubMed  Google Scholar 

  • Ishiga Y, Uppalapati SR, Ishiga T, Elavarthi S, Martin B, Bender CL (2009) 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, Bender CL (2010) 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

    Article  CAS  Google Scholar 

  • Jiménez-Hidalgo I, Virgen-Calleros G, Martínez de la Vega O, Vandemark G, Olalde-Portugal V (2004) Identification and characterization of bacteria causing soft-rot in Agave tequilana. Eur J Plant Pathol 110:317–331

    Article  Google Scholar 

  • Jones LR (1900) A soft rot of carrot and other vegetables caused by Bacillus carotovorus Jones. Vermont Agric Exp Stn Rep 13:299–332

    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 

  • King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44:301–307

    CAS  PubMed  Google Scholar 

  • Koda Y, Takahashi K, Kikuta Y, Greulich F, Toshima H, Ichihara A (1996) Similarities of the biological activities of coronatine and coronafacic acid to those of jasmonic acid. Phytochemistry 41:93–96

    Article  CAS  Google Scholar 

  • Liu H, Coulthurst SJ, Pritchard L, Hedley PE, Ravensdale M, Humphris S, Burr T, Takle G, Brurberg MB, Birch PRJ, Salmond GPC, Toth IK (2008) Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog 4:e1000093

    Article  PubMed Central  PubMed  Google Scholar 

  • Liyanage H, Penfold C, Turner J, Bender CL (1995) Sequence, expression and transcriptional analysis of the coronafacate ligase-encoding gene required for coronatine biosynthesis by Pseudomonas syringae. Gene 153:17–23

    Article  CAS  PubMed  Google Scholar 

  • Ma B, Hibbing ME, Kim HS, Reedy RM, Yedidia I, Breuer J, Breuer J, Glasner JD, Perna NT, Kelman A, Charkowski AO (2007) Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology 97:1150–1163

    Article  PubMed  Google Scholar 

  • Melotto M, Underwood W, Koczan J, Nomura K, Yang-He S (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980

    Article  CAS  PubMed  Google Scholar 

  • Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, p 431

    Google Scholar 

  • Munkvold KR, Russell AB, Kvitko BH, Collmer A (2009) Pseudomonas syringae pv. tomato DC3000 type III effector HopAA1-1 functions redundantly with chlorosis-promoting factor PSPTO4723 to produce bacterial speck lesions in host tomato. Mol Plant Microbe Interact 22:1341–1355

    Article  CAS  PubMed  Google Scholar 

  • Palmer DA, Bender CL (1993) Effects of environmental and nutritional factors on production of the polyketide phytotoxin coronatine by Pseudomonas syringae pv. glycinea. Appl Environ Microbiol 59:1619–1626

    PubMed Central  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Samson R, Legendre JB, Christen R, Fisher-Le Saux M, Achouak W, Gardan L (2005) Transfer of Pectobacterium dadantii (Burkholder et al. 1965) Brenner et al. 1973 and Brenneria paradisiaca to the genus Dickeya gen. nov. as Dickeya chrysanthemi comb. nov. and delineation of four novel species, Dickeya chrysanthemi sp. nov., Dickeya dianthicola sp. nov., Dickeya dieffenbachiae sp. nov. and Dickeya zeae sp. nov. Int J Syst Evol Microbiol 55: 1415–1427

  • Sanger F, Air GM, Barrell BG, Brown NL, Coulson AR, Fiddes JC, Hutchison CA, Slocombe PM, Smith M (1977) Nucleotide sequence of bacteriophage φX174 DNA. Nature 265:687–695

    Article  CAS  PubMed  Google Scholar 

  • Slawiak M, Lojkowska E (2009) Genes responsible for coronatine synthesis in Pseudomonas syringae present in the genome of soft rot bacteria. Eur J Plant Pathol 124:353–361

    Article  CAS  Google Scholar 

  • Sreedharan A, Peñaloza-Vázquez A, Kunkel BN, Bender CL (2006) CorR regulates multiple components of virulence in Pseudomonas syringae pv. tomato DC3000. Mol Plant Microbe Interact 19:768–779

    Article  CAS  PubMed  Google Scholar 

  • Takahashi K, Fujino K, Kikuta Y, Koda Y (1994) Expansion of potato cells in response to jasmonic acid. Plant Sci 100:3–8

    Article  CAS  Google Scholar 

  • Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Toth IK, Avrova AO, Hyman LJ (2001) Rapid identification and differentiation of the soft rot erwinias by 16S-23S intergenic transcribed spacer-PCR and restriction fragment length polymorphic analysis. Appl Environ Microbiol 67:4070–4076

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Toth IK, Bell KS, Holeva MC, Birch PRJ (2003) Soft rot erwiniae: from genes to genomes. Mol Plant Pathol 4:17–30

    Article  CAS  PubMed  Google Scholar 

  • Toth IK, Pritchard L, Birch PRJ (2006) Comparative genomics reveals what makes an enterobacterial plant pathogen. Annu Rev Phytopathol 44:305–336

    Article  CAS  PubMed  Google Scholar 

  • Völksch B, Bublitz F, Fritsche W (1989) Coronatine production by Pseudomonas syringae pathovars: screening method and capacity of product formation. J Basic Microbiol 29:463–468

    Article  Google Scholar 

  • Waleron M, Waleron K, Lojkowska E (2014) Characterization of Pectobacterium carotovorum subsp. odoriferum causing soft rot of stored vegetables. Eur J Plant Pathol 139:457–469

    Article  Google Scholar 

  • Wang X, Alarcón-Chaidez F, Peñaloza-Vázquez A, Bender CL (2002) Differential regulation of coronatine biosynthesis in Pseudomonas syringae pv. tomato DC3000 and P. syringae pv. glycinea PG4180. Physiol Mol Plant Pathol 60:111–120

    Article  CAS  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 

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Acknowledgments

We thank the late Dr. Leopold Fucikovsky (Colegio de Postgraduados en Ciencias Agrícolas, Estado de México, México) and Dr. Miguel Gómez Lim (Cinvestav, Unidad Irapuato, México) for providing the isolates of Pectobacterium. We also thank Dr. Jorge Molina Torres (Cinvestav, Unidad Irapuato, México) for technical support during the coronatine detection and identification by GC–MS assay.

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Correspondence to John Paul Délano-Frier.

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Valenzuela-Soto, J.H., Maldonado-Bonilla, L.D., Hernández-Guzmán, G. et al. Infection by a coronatine-producing strain of Pectobacterium cacticidum isolated from sunflower plants in Mexico is characterized by soft rot and chlorosis. J Gen Plant Pathol 81, 368–381 (2015). https://doi.org/10.1007/s10327-015-0606-y

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