The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Characterization of Pseudomonas syringae pv. syringae, Causal Agent of Citrus Blast of Mandarin in Montenegro

  • Ivanovic, Zarko (Institute for Plant Protection and Environment) ;
  • Perovic, Tatjana (Biotechnical Faculty, University of Podgorica) ;
  • Popovic, Tatjana (Institute for Plant Protection and Environment) ;
  • Blagojevic, Jovana (Scholar of Ministry of Education, Science and Technological Development of the Republic of Serbia, Department of Plant Disease, Institute for Plant Protection and Environment) ;
  • Trkulja, Nenad (Institute for Plant Protection and Environment) ;
  • Hrncic, Snjezana (Biotechnical Faculty, University of Podgorica)
  • Received : 2016.08.02
  • Accepted : 2016.11.01
  • Published : 2017.02.01
Download PDF
⟨ Previous Next ⟩

Abstract

Citrus blast caused by bacterium Pseudomonas syringae is a very important disease of citrus occuring in many areas of the world, but with few data about genetic structure of the pathogen involved. Considering the above fact, this study reports genetic characterization of 43 P. syringae isolates obtained from plant tissue displaying citrus blast symptoms on mandarin (Citrus reticulata) in Montenegro, using multilocus sequence analysis of gyrB, rpoD, and gap1 gene sequences. Gene sequences from a collection of 54 reference pathotype strains of P. syringae from the Plant Associated and Environmental Microbes Database (PAMDB) was used to establish a genetic relationship with our isolates obtained from mandarin. Phylogenetic analyses of gyrB, rpoD, and gap1 gene sequences showed that P. syringae pv. syringae causes citrus blast in mandarin in Montenegro, and belongs to genomospecies 1. Genetic homogeneity of isolates suggested that the Montenegrian population might be clonal which indicates a possible common source of infection. These findings may assist in further epidemiological studies of this pathogen and for determining mandarin breeding strategies for P. syringae control.

Keywords

References

  1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. https://doi.org/10.1093/nar/25.17.3389
  2. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. and Struhl, K. 1992. Current protocols in molecular biology. Vol. I. Greene Publishing Associates and Wiley-Interscience, New York, NY, USA.
  3. Berge, O., Monteil, C. L., Bartoli, C., Chandeysson, C., Guilbaud, C., Sands, D. C. and Morris, C. E. 2014. A user's guide to a data base of the diversity of Pseudomonas syringae and its application to classifying strains in this phylogenetic complex. PLoS One 9:e105547. https://doi.org/10.1371/journal.pone.0105547
  4. Bertani, G. 1951. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J. Bacteriol. 62: 293-300.
  5. Bradbury, J. F. 1986. Guide to plant pathogenic bacteria. CAB International, Farnham Royal, Great Britain.
  6. Bryan, M. K. 1928. Lilac blight in the United States. J. Agric. Res. 36:225-235.
  7. Bull, C. T., Clarke, C. R., Cai, R., Vinatzer, B. A., Jardini, T. M. and Koike, S. T. 2011. Multilocus sequence typing of Pseudomonas syringae sensu lato confirms previously described genomospecies and permits rapid identification of P. syringae pv. coriandricola and P. syringae pv. apii causing bacterial leaf spot on parsley. Phytopathology 101:847-858. https://doi.org/10.1094/PHYTO-11-10-0318
  8. Buttner, M. P. and Amy, P. S. 1989. Survival of ice nucleationactive and genetically engineered non-ice-nucleating Pseudomonas syringae strains after freezing. Appl. Environ. Microbiol. 55:1690-1694.
  9. Cambours, M. A., Nejad, P., Granhall, U. and Ramstedt, M. 2005. Frost-related dieback of willows. Comparison of epiphytically and endophytically isolated bacteria from different Salix clones, with emphasis on ice nucleation activity, pathogenic properties and seasonal variation. Biomass Bioenerg. 28:15-27. https://doi.org/10.1016/j.biombioe.2004.06.003
  10. Cao, T., Sayler, R. J., Dejong, T. M., Kirkpatrick, B. C., Bostock, R. M. and Shackel, K. A. 1999. Influence of stem diameter, water content, and freezing-thawing on bacterial canker development in excised stems of dormant stone fruit. Phytopathology 89:962-966. https://doi.org/10.1094/PHYTO.1999.89.10.962
  11. Crosse, J. E. 1966. Epidemiological relations of the pseudomonad pathogens of deciduous fruit trees. Annu. Rev. Phytopathol. 4:291-310. https://doi.org/10.1146/annurev.py.04.090166.001451
  12. de Bruijn, F. J. 1992. Use of repetitive (repetitive extragenic palindromic and enterobacterial repetitive intergeneric consensus) sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti isolates and other soil bacteria. Appl. Environ. Microbiol. 58:2180-2187.
  13. De Cicco, V., Luisi, N. and Salerno, M. 1978. Epidemiology and control of citrus blast. In: Proceedings of third meeting of the International Society of Citriculture, pp. 204-208. August 15-23, 1978, International Society of Citriculture, Sydney, Australia.
  14. Fukuchi, N., Isogai, A., Nakayama, J. and Suzuki, A. 1990. Structure of syringotoxin B, a phytotoxin produced by citrus isolates of Pseudomonas syringae pv. syringae. Agric. Biol. Chem. 54:3377-3379.
  15. Gardan, L., Shafik, H., Belouin, S., Broch, R., Grimont, F. and Grimont, P. A. 1999. DNA relatedness among the pathovars of Pseudomonas syringae and description of Pseudomonas tremae sp. nov. and Pseudomonas cannabina sp. nov. (ex Sutic and Dowson 1959). Int. J. Syst. Evol. Bacteriol. 49:469-478. https://doi.org/10.1099/00207713-49-2-469
  16. Gironde, S. and Manceau, C. 2012. Housekeeping gene sequencing and multilocus variable-number tandem-repeat analysis to identify subpopulations within Pseudomonas syringae pv. maculicola and Pseudomonas syringae pv. tomato that correlate with host specificity. Appl. Environ. Microbiol. 78:3266-3279. https://doi.org/10.1128/AEM.06655-11
  17. Gorlenko, M. V. 1965. Bacterial diseases of plants. 2nd ed. Israel Program for Scientific Translations, Jerusalem, Israel.
  18. Grifoni, A., Bazzicalupo, M., Di Serio, C., Fancelli, S. and Fani, R. 1995. Identification of Azospirillum strains by restriction fragment length polymorphism of the 16S rDNA and of the histidine operon. FEMS Microbiol. Lett. 127:85-91. https://doi.org/10.1111/j.1574-6968.1995.tb07454.x
  19. Gross, D. C. and Cody, Y. S. 1985. Mechanisms of plant pathogenesis by Pseudomonas species. Can. J. Microbiol. 31:403-410. https://doi.org/10.1139/m85-076
  20. Gross, D. C., Cody, Y. S., Proebstring, E. L., Radamaker, G. K. and Spotts, R. A. 1983. Distribution, population dynamics, and characteristics of ice nucleation-active bacteria in deciduous fruit tree orchards. Appl. Environ. Microbiol. 46:1370-1379.
  21. Gross, D. C., Proebstring, E. L. and MacCrindle-Zimmerman, H. 1988. Development, distribution, and characteristics of intrinsic, nonbacterial ice nuclei in Prunus wood. Plant Physiol. 88:915-922. https://doi.org/10.1104/pp.88.3.915
  22. Hilario, E., Buckley, T. R. and Young, J. M. 2004. Improved resolution on the phylogenetic relationships among Pseudomonas by the combined analysis of atpD, carA, recA and 16S rDNA. Antonie van Leeuwenhoek 86:51-64. https://doi.org/10.1023/B:ANTO.0000024910.57117.16
  23. Holding, A. J. and Collee, J. G. 1971. Routine biochemical tests. In: Methods in microbiology, Vol. 6, eds. by J. R. Norris and D. W. Ribbons, pp. 2-30. Academic Press, New York, NY, USA.
  24. Huson, D. H. and Bryant, D. 2006. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23:254-267. https://doi.org/10.1093/molbev/msj030
  25. Isogai, A., Fukuchi, N., Yamashita, S., Suyama, K. and Suzuki, A. 1989. Syringostatins, novel phytotoxins produced by Pseudomonas syringae pv. syringae. Agric. Biol. Chem. 53: 3117-3119.
  26. Kaluzna, M., Janse, J. D. and Young, J. M. 2012. Detection and identification methods and new tests as developed and used in the framework of COST 873 for bacteria pathogenic to stone fruits and nuts. J. Plant Pathol. 94(1 Suppl):S1.117-S1.126.
  27. Kennelly, M. M., Cazorla, F. M., de Vicente, A., Ramos, C. and Sundin, G. W. 2007. Pseudomonas syrinagae diseases of fruit trees: progress toward understanding and control. Plant Dis. 91:4-17. https://doi.org/10.1094/PD-91-0004
  28. King, E. O., Ward, M. K. and Raney, D. E. 1954. Two simple media for the demonstration of pyocyanin and fluorescin. J. Lab. Clin. Med. 44:301-307.
  29. Klement, Z. 1990. Inoculation of plant tissues. Cancer and dieback disease. In: Methods in phytobacteriology, eds. by Z. Klement, K. Rudolph and D. C. Sands, pp. 105-106. Akademiai Kiado, Budapest, Hungary.
  30. Klement, Z., Rozsnyay, D. S., Balo, E., Panczel, M. and Prilesky, G. 1984. The effect of cold on development of bacterial canker in apricot trees infected with Pseudomonas syringae pv. syringae. Physiol. Plant Pathol. 24:237-246. https://doi.org/10.1016/0048-4059(84)90031-6
  31. Kovacs, N. 1956. Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 178:703.
  32. Lelliott, R. A. and Stead, D. E. 1987. Methods for the diagnosis of bacterial diseases of plants. Blackwell Scientific Publications, Oxford, UK.
  33. Lindow, S. E., Arny, D. C. and Upper, C. D. 1982. Bacterial ice nucleation: a factor in frost injury to plants. Plant Physiol. 70:1084-1089. https://doi.org/10.1104/pp.70.4.1084
  34. Lupski, J. R. and Weinstock, G. M. 1992. Short, interspersed repetitive DNA sequences in prokaryotic genomes. J. Bacteriol. 174:4525-4529. https://doi.org/10.1128/jb.174.14.4525-4529.1992
  35. Mirik, M., Baloglu, S., Aysan, Y., Cetinkaya-Yildiz, R., Kusek, M. and Sahin, F. 2005. First outbreak and occurrence of citrus blast disease, caused by Pseudomonas syringae pv. syringae, on orange and mandarin trees in Turkey. Plant Pathol. 54:238. https://doi.org/10.1111/j.1365-3059.2005.01134.x
  36. Mitchell, R. E. 1981. Structure: bacterial. In: Toxins in plant diseases, ed. by R. D. Durbin, pp. 259-291. Academic Press, New York, NY, USA.
  37. Mo, Y. Y. and Gross, D. C. 1991. Plant signal molecules activate the syrB gene, which is required for syringomycin production by Pseudomonas syringae pv. syringae. J. Bacteriol. 173:5784-5792. https://doi.org/10.1128/jb.173.18.5784-5792.1991
  38. Nejad, P., Ramstedt, M. and Granhall, U. 2004. Pathogenic icenucleation active bacteria in willows for short rotation forestry. For. Pathol. 34:369-381. https://doi.org/10.1111/j.1439-0329.2004.00378.x
  39. Panagopoulos, C. G. and Grosse, J. E. 1964. Frost injury as a predisposing factor in blossom blight of pear caused by Pseudomonas syringae van Hall. Nature 202:1352.
  40. Perrot, P. 1998. A to Z of thermodynamics. Oxford University Press, Oxford, UK.
  41. Salerno, M. and Cutuli, G. 1985. Le malattie degli agrumi: batteriosi (blast and black pit). Inf. Fitopatol. 35:27-28.
  42. Sarkar, S. F. and Guttman, D. S. 2004. Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl. Environ. Microbiol. 70:1999-2012. https://doi.org/10.1128/AEM.70.4.1999-2012.2004
  43. Schaad, N. W., Jones, J. B. and Chun, W. 2001. Laboratory guide for identification of plant pathogenic bacteria. 3rd ed. APS Press, St. Paul, MN, USA. 373 pp.
  44. Scortichini, M., Marchesi, U., Dettori, M. T. and Rossi, M. P. 2003. Genetic diversity, presence of the syrB gene, host preference and virulence of Pseudumonas syringae pv. syringae strains from woody and herbaceous host plants. Plant Pathol. 52:277-286. https://doi.org/10.1046/j.1365-3059.2003.00860.x
  45. Scortichini, M., Rossi, M. P., Loreti, S., Bosco, A., Fiori, M., Jackson, W., Stead, D. E., Aspin, A., Marchesi, U., Zini, M. and Janse, J. D. 2005. Pseudomonas syringae pv. coryli, the causal agent of bacterial twig dieback of Corylus avellana. Phytopathology 95:1316-1324. https://doi.org/10.1094/PHYTO-95-1316
  46. Shams-Bakhsh, M. and Rahimian, H. 1997. Comparative study on agents of citrus blast and bacterial canker of stone fruits in Mazandaran. Iran. J. Plant Pathol. 33:132-143.
  47. Shigeta, S. and Nakata, E. 1995. Bacterial brown spot of citrus caused by Pseudomonas syringae pv. syringae van Hall 1902. J. Ann. Phytopathol. Soc. Jpn. 61:150-157. https://doi.org/10.3186/jjphytopath.61.150
  48. Smith, C. O. and Fawcett, H. S. 1930. A comparative study of the citrus blast bacterium and some other allied organisms. J. Agric. Res. 41:233-246.
  49. Sorensen, K. N., Kim, K. H. and Takemoto, J. Y. 1998. PCR detection of cyclic lipodepsinonapeptide-producing Pseudomonas syringae pv. syringae and similarity of strains. Appl. Environ. Microbiol. 61:226-230.
  50. Sule, S. and Seemuller, E. 1987. The role of ice formation in the infection of sour cherry leaves by Pseudomonas syringae pv. syringae. Phytopathology 77:173-177. https://doi.org/10.1094/Phyto-77-173
  51. Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725-2729. https://doi.org/10.1093/molbev/mst197
  52. Thomidis, T., Tsipouridis, C., Exadaktylou, E. and Drogoudi, P. 2005. Comparison of three laboratory methods to evaluate the pathogenicity and virulence of ten Pseudomonas syringae pv. syringae strains on apple, pear, cherry and peach trees. Phytoparasitica 33:137-140. https://doi.org/10.1007/BF03029971
  53. Thornley, M. J. 1960. The differentiation of Pseudomonas from other Gram-negative bacteria on the basis of arginine metabolism. J. Appl. Bacteriol. 23:37-52. https://doi.org/10.1111/j.1365-2672.1960.tb00178.x
  54. Timmer, L. W., Garnsey, S. M. and Graham, J. H. 2000. Compendium of citrus diseases. APS Press, St. Paul, MN, USA.
  55. Vanarelli, S., Rizzo, D., Stefani, L. and Paoli, M. (2010 onwards). Avvizzimento batterico degli agrumi--Piticchia batterica (Citrus blast/black pit). URL http://www.cespevi.it/servfito/pdf/Scheda_Pseudomonas_syringae.pdf [25 January 2014].
  56. Vucinic, Z. 1987. La necrose bacterienne des agrumes sur le littoral montenegrin. In: 50 Years of Agricultural Institute Titograd, ed. by Z. Kalezic, pp. 59-67. Agricultural Institute, Titograd, Yugoslavia (in Serbian).
  57. Whiteside, J. O., Garnsey, S. M. and Timmer, L. W. 1988. Compendium of citrus diseases. APS Press, St. Paul, MN, USA.