Oxytetracycline and Streptomycin Resistance Genes in Xanthomonas arboricola pv. pruni, the Causal Agent of Bacterial Spot in Peach
Xanthomonas arboricola pv. pruni (Xap) causes bacterial spot, a major worldwide disease of Prunus species. Very few chemical management options are available for this disease and frequent applications of oxytetracycline (OTC) in the United States peach orchards have raised concerns about resistance...
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Frontiers Media S.A.
2022-02-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.821808/full |
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| author | Austin Herbert C. Nathan Hancock Brodie Cox Guido Schnabel Daniela Moreno Renato Carvalho Renato Carvalho Jeffrey Jones Matthew Paret Matthew Paret Xueqing Geng Hehe Wang |
| author_facet | Austin Herbert C. Nathan Hancock Brodie Cox Guido Schnabel Daniela Moreno Renato Carvalho Renato Carvalho Jeffrey Jones Matthew Paret Matthew Paret Xueqing Geng Hehe Wang |
| author_sort | Austin Herbert |
| collection | DOAJ |
| description | Xanthomonas arboricola pv. pruni (Xap) causes bacterial spot, a major worldwide disease of Prunus species. Very few chemical management options are available for this disease and frequent applications of oxytetracycline (OTC) in the United States peach orchards have raised concerns about resistance development. During 2017–2020, 430 Xap strains were collected from ten peach orchards in South Carolina. Seven OTC-resistant (OTCR) Xap strains were found in 2017 and 2020 from four orchards about 20–270 km apart. Interestingly, the seven strains were also resistant to streptomycin (STR). Six strains grew on media amended with ≤100 μg/mL OTC, while one strain, R1, grew on ≤250 μg/mL OTC. Genome sequence analysis of four representative OTCR strains revealed a 14–20 kb plasmid carrying tetC, tetR, and strAB in each strain. These three genes were transferable to Xanthomonas perforans via conjugation, and they were PCR confirmed in all seven OTCR Xap strains. When tetC and tetR were cloned and expressed together in a sensitive strain, the transconjugants showed resistance to ≤100 μg/mL OTC. When tetC was cloned and expressed alone in a sensitive strain, the transconjugants showed resistance to ≤250 μg/mL OTC. TetC and tetR expression was inducible by OTC in all six wild-type strains resistant to ≤100 μg/mL OTC. However, in the R1 strain resistant to ≤250 μg/mL OTC, tetR was not expressed, possibly due to the presence of Tn3 in the tetR gene, and in this case tetC was constitutively expressed. These data suggest that tetC confers OTC resistance in Xap strains, and tetR regulates the level of OTC resistance conferred by tetC. To our knowledge, this is the first report of OTC resistance in plant pathogenic xanthomonads. |
| format | Article |
| id | doaj-art-cf05d4e617824ebeafe2250e020bb0b8 |
| institution | DOAJ |
| issn | 1664-302X |
| language | English |
| publishDate | 2022-02-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj-art-cf05d4e617824ebeafe2250e020bb0b82025-08-20T02:57:03ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-02-011310.3389/fmicb.2022.821808821808Oxytetracycline and Streptomycin Resistance Genes in Xanthomonas arboricola pv. pruni, the Causal Agent of Bacterial Spot in PeachAustin Herbert0C. Nathan Hancock1Brodie Cox2Guido Schnabel3Daniela Moreno4Renato Carvalho5Renato Carvalho6Jeffrey Jones7Matthew Paret8Matthew Paret9Xueqing Geng10Hehe Wang11Edisto Research and Education Center, Clemson University, Blackville, SC, United StatesDepartment of Biology and Geology, University of South Carolina Aiken, Aiken, SC, United StatesDepartment of Plant and Environmental Sciences, Clemson University, Clemson, SC, United StatesDepartment of Plant and Environmental Sciences, Clemson University, Clemson, SC, United StatesEdisto Research and Education Center, Clemson University, Blackville, SC, United StatesDepartment of Plant Pathology, University of Florida, Gainesville, FL, United StatesNorth Florida Research and Education Center, University of Florida, Quincy, FL, United StatesDepartment of Plant Pathology, University of Florida, Gainesville, FL, United StatesDepartment of Plant Pathology, University of Florida, Gainesville, FL, United StatesNorth Florida Research and Education Center, University of Florida, Quincy, FL, United StatesSchool of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, ChinaEdisto Research and Education Center, Clemson University, Blackville, SC, United StatesXanthomonas arboricola pv. pruni (Xap) causes bacterial spot, a major worldwide disease of Prunus species. Very few chemical management options are available for this disease and frequent applications of oxytetracycline (OTC) in the United States peach orchards have raised concerns about resistance development. During 2017–2020, 430 Xap strains were collected from ten peach orchards in South Carolina. Seven OTC-resistant (OTCR) Xap strains were found in 2017 and 2020 from four orchards about 20–270 km apart. Interestingly, the seven strains were also resistant to streptomycin (STR). Six strains grew on media amended with ≤100 μg/mL OTC, while one strain, R1, grew on ≤250 μg/mL OTC. Genome sequence analysis of four representative OTCR strains revealed a 14–20 kb plasmid carrying tetC, tetR, and strAB in each strain. These three genes were transferable to Xanthomonas perforans via conjugation, and they were PCR confirmed in all seven OTCR Xap strains. When tetC and tetR were cloned and expressed together in a sensitive strain, the transconjugants showed resistance to ≤100 μg/mL OTC. When tetC was cloned and expressed alone in a sensitive strain, the transconjugants showed resistance to ≤250 μg/mL OTC. TetC and tetR expression was inducible by OTC in all six wild-type strains resistant to ≤100 μg/mL OTC. However, in the R1 strain resistant to ≤250 μg/mL OTC, tetR was not expressed, possibly due to the presence of Tn3 in the tetR gene, and in this case tetC was constitutively expressed. These data suggest that tetC confers OTC resistance in Xap strains, and tetR regulates the level of OTC resistance conferred by tetC. To our knowledge, this is the first report of OTC resistance in plant pathogenic xanthomonads.https://www.frontiersin.org/articles/10.3389/fmicb.2022.821808/fullantibiotic resistanceplant diseasebacterial pathogenstone fruitshorizontal gene transfertransposon |
| spellingShingle | Austin Herbert C. Nathan Hancock Brodie Cox Guido Schnabel Daniela Moreno Renato Carvalho Renato Carvalho Jeffrey Jones Matthew Paret Matthew Paret Xueqing Geng Hehe Wang Oxytetracycline and Streptomycin Resistance Genes in Xanthomonas arboricola pv. pruni, the Causal Agent of Bacterial Spot in Peach Frontiers in Microbiology antibiotic resistance plant disease bacterial pathogen stone fruits horizontal gene transfer transposon |
| title | Oxytetracycline and Streptomycin Resistance Genes in Xanthomonas arboricola pv. pruni, the Causal Agent of Bacterial Spot in Peach |
| title_full | Oxytetracycline and Streptomycin Resistance Genes in Xanthomonas arboricola pv. pruni, the Causal Agent of Bacterial Spot in Peach |
| title_fullStr | Oxytetracycline and Streptomycin Resistance Genes in Xanthomonas arboricola pv. pruni, the Causal Agent of Bacterial Spot in Peach |
| title_full_unstemmed | Oxytetracycline and Streptomycin Resistance Genes in Xanthomonas arboricola pv. pruni, the Causal Agent of Bacterial Spot in Peach |
| title_short | Oxytetracycline and Streptomycin Resistance Genes in Xanthomonas arboricola pv. pruni, the Causal Agent of Bacterial Spot in Peach |
| title_sort | oxytetracycline and streptomycin resistance genes in xanthomonas arboricola pv pruni the causal agent of bacterial spot in peach |
| topic | antibiotic resistance plant disease bacterial pathogen stone fruits horizontal gene transfer transposon |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.821808/full |
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