Plant Protect. Sci., 2021, 57(3):206-216 | DOI: 10.17221/160/2020-PPS

Distribution of copper resistance gene variants of Xanthomonas citri subsp. citri and Xanthomonas euvesicatoria pv. perforansOriginal Paper

Yi-Ru Lai1, Chih-Hung Lin1, Chun-Pi Chang1, Hui-Fang Ni2, Wen-Shi Tsai1, Chien-Jui Huang ORCID...*,1
1 Department of Plant Medicine, Faculty of Agriculture, National Chiayi University, Chiayi, Taiwan
2 Department of Plant Protection, Chiayi Agricultural Experiment Station, Taiwan Agricultural Research Institute, Chiayi, Taiwan

In Taiwan, numerous crops are threatened by Xanthomonas diseases such as citrus bacterial canker caused by X. citri subsp. citri and tomato bacterial spot mainly caused by X. euvesicatoria pv. perforans. Foliar sprays of copper-based bactericides have been frequently used for control of plant bacterial diseases. However, in Taiwan not much attention was paid on copper-resistant (CuR) Xanthomonas spp. and their impact on disease control efficacy of copper-based bactericides. In this study, CuR Xanthomonas isolates were collected from citrus and tomato in Taiwan. Compared with the pronounced effect on the copper sensitive isolate, spraying of copper hydroxide at the recommended rate of 0.5 kg/ha could not protect tomato plants against bacterial spot caused by the CuR isolate. Phylogenetic analysis of concatenated copper resistance genes, copL, copA, and copB, indicate that the Taiwanese CuR isolates belong to the worldwide clade. In addition to the three previously reported variants of the copB gene, analysis of complete copB sequences from xanthomonads associated with citrus and solanaceous hosts revealed the other three variants of copB and their global distribution. Copper-resistant Xanthomonas isolates from Taiwan have the two unreported variants of copB genes which differ from the other three previously reported types in the sizes and structures. The information provided here reveals the necessity to develop and include alternative measures rather than relying on foliar sprays of copper bactericides for sustainable control of tomato bacterial spot in Taiwan.

Keywords: citrus; efficacy; polymorphism; tomato; xanthomonad

Published: June 10, 2021  Show citation

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Lai Y, Lin C, Chang C, Ni H, Tsai W, Huang C. Distribution of copper resistance gene variants of Xanthomonas citri subsp. citri and Xanthomonas euvesicatoria pv. perforans. Plant Protect. Sci.. 2021;57(3):206-216. doi: 10.17221/160/2020-PPS.
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References

  1. Basim H., Stall R.E., Minsavage G.V., Jones J.B. (1999): Chromosomal gene transfer by conjugation in the plant pathogen Xanthomonas axonopodis pv. vesicatoria. Phytopathology, 89: 1044-1049. Go to original source... Go to PubMed...
  2. Basim H., Minsavage G.V., Stall R.E., Wang J.F., Shanker S., Jones J.B. (2005): Characterization of a unique chromosomal copper resistance gene cluster from Xanthomonas campestris pv. vesicatoria. Applied and Environmental Microbiology, 71: 8284-8291. Go to original source... Go to PubMed...
  3. Behlau F., Canteros B.I., Jones J.B., Graham J.H. (2012a): Copper resistance genes from different xanthomonads and citrus epiphytic bacteria confer resistance to Xanthomonas citri subsp. citri. European Journal of Plant Pathology, 133: 949-963. Go to original source...
  4. Behlau F., Jones J.B., Myers M.E., Graham J.H. (2012b): Monitoring for resistant populations of Xanthomonas citri subsp. citri and epiphytic bacteria on citrus trees treated with copper or streptomycin using a new semiselective medium. European Journal of Plant Pathology, 132: 259-270. Go to original source...
  5. Behlau F., Canteros B.I., Minsavage G.V., Jones J.B., Graham J.H. (2011): Molecular characterization of copper resistance genes from Xanthomonas citri subsp. citri and Xanthomonas alfalfae subsp. citrumelonis. Applied and Environmental Microbiology, 77: 4089-4096. Go to original source... Go to PubMed...
  6. Behlau F., Gochez A.M., Lugo A.J., Elibox W., Minsavage G.V., Potnis N., White F.F., Ebrahim M., Jones J.B., Ramsubhag A. (2017): Characterization of a unique copper resistance gene cluster in Xanthomonas campestris pv. campestris isolated in Trinidad, West Indies. European Journal of Plant Pathology, 147: 671-681. Go to original source...
  7. Behlau F., Hong J.C., Jones J.B., Graham J.H. (2013): Evidence for acquisition of copper resistance genes from different sources in citrus-associated xanthomonads. Phytopathology, 103: 409-418. Go to original source... Go to PubMed...
  8. Burlakoti R.R., Hsu C.F., Chen J.R., Wang J.F. (2018): Population dynamics of xanthomonads associated with bacterial spot of tomato and pepper during 27 years across Taiwan. Plant Disease, 102: 1348-1356. Go to original source... Go to PubMed...
  9. Canteros B.I., Minsavage G.V., Jones J.B., Stall R.E. (1995): Diversity of plasmids in Xanthomonas campestris pv. vesicatoria. Phytopathology, 85: 1482-1486. Go to original source...
  10. Canteros B.I., Rybak M., Gochez A., Velazquez P., Rivadeneira M., Mitidieri M., Garren S., Zequeira L. (2008): Occurrence of copper resistance in Xanthomonas axonopodis pv. citri in Argentina. Phytopathology, 98: S30-S31.
  11. Conover R.A., Gerhold R.A. (1981): Mixtures of copper and maneb or mancozeb for control of bacterial spot of tomato and their compatibility for control of fungus diseases [Phytophthora infestans, Stemphylium solani, Xanthomonas campestris pv. vesicatoria, Florida]. Proceedings of Annual Meeting of the Florida State Horticultural Society, 94: 154-156.
  12. Constantin E.C., Cleenwerck I., Maes M., Baeyen S., van Malderghem C., De Vos P., Cottyn B. (2016): Genetic characterization of strains named as Xanthomonas axonopodis pv. dieffenbachiae leads to a taxonomic revision of the X. axonopodis species complex. Plant Pathology, 65: 792-806. Go to original source...
  13. Griffin K., Gambley C., Brown P., Li Y. (2017): Coppertolerance in Pseudomonas syringae pv. tomato and Xanthomonas spp. and the control of diseases associated with these pathogens in tomato and pepper. A systematic literature review. Crop Protection, 96: 144-150. Go to original source...
  14. Hammer O., Harper D.A.T., Ryan P.D. (2001): PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4: 1-9.
  15. Hseu S.H., Hsu S.T. (1991): Sensitivity of strains of Xanthomonas campestris pv. vesicatoria from Taiwan to copper and other agrochemicals. Plant Protection Bulletin, 33: 410-419.
  16. Huang C.J., Ni H.F. (2017): First report of Citrus depressa as a new natural host of Xanthomonas citri subsp. citri pathotype A in Taiwan. Journal of Plant Pathology, 99: 289. doi: 10.4454/jpp.v99i1.3803
  17. Kumar S., Stecher G., Tamura K. (2016): MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33: 1870-1874. Go to original source... Go to PubMed...
  18. Lamichhane J.R., Osdaghi E., Behlau F., Köhl J., Jones J.B., Aubertot J.-N. (2018): Thirteen decades of antimicrobial copper compounds applied in agriculture. A review. Agronomy for Sustainable Development, 38: 28. doi: 10.1007/s13593-018-0503-9 Go to original source...
  19. Leu Y.S., Deng W.L., Wu Y.F., Cheng A.S., Hsu S.T., Tzeng K.C. (2010): Characterization of Xanthomonas associated with bacterial spot of tomato and pepper in Taiwan. Plant Pathology Bulletin, 19: 181-190.
  20. Lin H.-C., Feng C.-Y., Chang Y.-A., Chang H. (2012): Molecular typing and genetic characterization of pathogenic variants of Xanthomonas axonopodis pv. citri in Taiwan. Journal of Phytopathology, 160: 475-483. Go to original source...
  21. Marin T.G.S., Galvanin A.L., Lanza F.E., Behlau F. (2019): Description of copper tolerant Xanthomonas citri subsp. citri and genotypic comparison with sensitive and resistant strains. Plant Pathology, 68: 1088-1098. Go to original source...
  22. Pernezny K., Nagata R., Havranek N., Sanch.ez J. (2008): Comparison of two culture media for determination of the copper resistance of Xanthomonas strains and their usefulness for prediction of control with copper bactericides. Crop Protection, 27: 256-262. Go to original source...
  23. Pohronezny K., Stall R.E., Canteros B.I., Kegley M., Datnoff L.E., Subramanya R. (1992): Sudden shift in the prevalent race of Xanthomonas campestris pv. vesicatoria in pepper fields in southern Florida. Plant Disease, 76: 118-120. Go to original source...
  24. Potnis N., Timilsina S., Strayer A., Shantharaj D., Barak J.D., Paret M.L., Vallad G.E., Jones J.B. (2015): Bacterial spot of tomato and pepper: Diverse Xanthomonas species with a wide variety of virulence factors posing a worldwide challenge. Molecular Plant Pathology, 16: 907-920. Go to original source... Go to PubMed...
  25. Richard D., Ravigne V., Rieux A., Facon B., Boyer C., Boyer K., Grygiel P., Javegny S., Terville M., Canteros B.I., Robene I., Verniere C., Chabirand A., Pruvost O., Lefeuvre P. (2017): Adaptation of genetically monomorphic bacteria: Evolution of copper resistance through multiple horizontal gene transfers of complex and versatile mobile genetic elements. Molecular Ecology, 26: 2131-2149. Go to original source... Go to PubMed...
  26. Sambrook J., Russel D.W. (2001): Molecular Cloning: A Laboratory Manual. 3rd Ed. Cold Spring Harbor, Cold Spring Harbor Laboratory Press.
  27. Stall R.E., Miller J.W., Marco G.M., de Echenique B.I.C. (1980): Population dynamics of Xanthomonas citri causing cancrosis of citrus in Argentina. Proceedings of the Florida State Horticultural Society, 93: 10-14.
  28. Tsai W.S., Shih S.L., Kenyon L., Green S.K., Jan F.J. (2011): Temporal distribution and pathogenicity of the predominant tomato-infecting begomoviruses in Taiwan. Plant Pathology, 60: 787-799. Go to original source...
  29. Wu Y.F., Hsu S.T., Tzeng K.C. (1995): Association of plasmid with copper resistance in strains of Xanthomonas campestris pv. vesicatoria from Taiwan. Plant Protection Bulletin, 37: 209-218.
  30. Zhang S., Fu Y., Mersha Z., Pernezny K. (2017): Assessment of copper resistance in Pseudomonas syringae pv. phaseolicola, the pathogen of halo blight on snap bean. Crop Protection, 98: 8-15. Go to original source...

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