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


Lai Y.-R., Lin C.-H., Chang C.-P., Ni H.-F., Tsai W.-S., Huang C.-J. (2021): Distribution of copper resistance gene variants of Xanthomonas citri subsp. citri and Xanthomonas euvesicatoria pv. perforans. Plant Protect. Sci., 57: 206–216.

download PDF

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.

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. https://doi.org/10.1094/PHYTO.1999.89.11.1044
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. https://doi.org/10.1128/AEM.71.12.8284-8291.2005
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. https://doi.org/10.1007/s10658-012-9966-8
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 semi-selective medium. European Journal of Plant Pathology, 132: 259–270. https://doi.org/10.1007/s10658-011-9870-7
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. https://doi.org/10.1128/AEM.03043-10
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. https://doi.org/10.1007/s10658-016-1035-2
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. https://doi.org/10.1094/PHYTO-06-12-0134-R
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. https://doi.org/10.1094/PDIS-04-17-0465-RE
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. https://doi.org/10.1094/Phyto-85-1482
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.
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.
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. https://doi.org/10.1111/ppa.12461
Griffin K., Gambley C., Brown P., Li Y. (2017): Copper-tolerance 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. https://doi.org/10.1016/j.cropro.2017.02.008
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.
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.
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
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. https://doi.org/10.1093/molbev/msw054
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 https://doi.org/10.1007/s13593-018-0503-9
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.
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. https://doi.org/10.1111/j.1439-0434.2012.01936.x
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. https://doi.org/10.1111/ppa.13026
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. https://doi.org/10.1016/j.cropro.2007.05.012
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. https://doi.org/10.1094/PD-76-0118
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. https://doi.org/10.1111/mpp.12244
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. https://doi.org/10.1111/mec.14007
Sambrook J., Russel D.W. (2001): Molecular Cloning: A Laboratory Manual. 3rd Ed. Cold Spring Harbor, Cold Spring Harbor Laboratory Press.
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.
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. https://doi.org/10.1111/j.1365-3059.2011.02424.x
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.
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. https://doi.org/10.1016/j.cropro.2017.03.009
download PDF

© 2021 Czech Academy of Agricultural Sciences | Prohlášení o přístupnosti