Prevalence of Carbendazin Resistance in Field Populations of the Rice False Smut Pathogen <i>Ustilaginoidea virens</i> from Jiangsu, China, Molecular Mechanisms, and Fitness Stability
Rice false smut (RFS), caused by <i>Ustilaginoidea virens</i>, is an important fungal disease of rice. In China, Methyl Benzimidazole Carbamates (MBCs), including carbendazim, are common fungicides used to control RFS and other rice diseases. In this study, resistance of <i>U. vire...
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MDPI AG
2022-12-01
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| Series: | Journal of Fungi |
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| author | Jiehui Song Zhiying Wang Yan Wang Sijie Zhang Tengyu Lei You Liang Qigen Dai Zhongyang Huo Ke Xu Shuning Chen |
| author_facet | Jiehui Song Zhiying Wang Yan Wang Sijie Zhang Tengyu Lei You Liang Qigen Dai Zhongyang Huo Ke Xu Shuning Chen |
| author_sort | Jiehui Song |
| collection | DOAJ |
| description | Rice false smut (RFS), caused by <i>Ustilaginoidea virens</i>, is an important fungal disease of rice. In China, Methyl Benzimidazole Carbamates (MBCs), including carbendazim, are common fungicides used to control RFS and other rice diseases. In this study, resistance of <i>U. virens</i> to carbendazim was monitored for three consecutive years during 2018 to 2020. A total of 321 <i>U. virens</i> isolates collected from Jiangsu Province of China were tested for their sensitivity to carbendazim on PSA. The concentration at which mycelial growth is inhibited by 50% (EC<sub>50</sub>) of the carbendazim-sensitive isolates was 0.11 to 1.38 µg/mL, with a mean EC<sub>50</sub> value of 0.66 μg/mL. High level of resistance to carbendazim was detected in 14 out of 321 isolates. The resistance was stable but associated with a fitness penalty. There was a statistically significant and moderate negative correlation (r= −0.74, <i>p</i> < 0.001) in sensitivity between carbendazim and diethofencarb. Analysis of the <i>U. virens</i> genome revealed two potential MBC targets, <i>Uvβ1Tub</i> and <i>Uvβ2Tub</i>, that putatively encode β-tubulin gene. The two β-tubulin genes in <i>U. virens</i> share 78% amino acid sequence identity, but their function in MBC sensitivity has been unclear. Both genes were identified and sequenced from <i>U. virens</i> sensitive and resistant isolates. It is known that mutations in the β2-tubulin gene have been shown to confer resistance to carbendazim in other fungi. However, no mutation was found in the <i>Uvβ2Tub</i> gene in either resistant or sensitive isolates. Variations including point mutations, non-sense mutations, codon mutations, and frameshift mutations were found in the <i>Uvβ1Tub</i> gene from the 14 carbendazim-resistant isolates, which have not been reported in other fungi before. Thus, these results indicated that variations of <i>Uvβ1Tub</i> result in the resistance to carbendazim in field isolates of <i>Ustilaginoidea virens</i>. |
| first_indexed | 2024-03-09T16:13:52Z |
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| spelling | doaj.art-61d272d602a248eea21fd668eaa688802023-11-24T16:00:18ZengMDPI AGJournal of Fungi2309-608X2022-12-01812131110.3390/jof8121311Prevalence of Carbendazin Resistance in Field Populations of the Rice False Smut Pathogen <i>Ustilaginoidea virens</i> from Jiangsu, China, Molecular Mechanisms, and Fitness StabilityJiehui Song0Zhiying Wang1Yan Wang2Sijie Zhang3Tengyu Lei4You Liang5Qigen Dai6Zhongyang Huo7Ke Xu8Shuning Chen9Jiangsu Key Laboratory of Crop Genetics and Physiology & Co-Innovation Center for Modern Production Technology of Grain Crops, Agricultural College, Yangzhou University, Yangzhou 225009, ChinaJiangsu Key Laboratory of Crop Genetics and Physiology & Co-Innovation Center for Modern Production Technology of Grain Crops, Agricultural College, Yangzhou University, Yangzhou 225009, ChinaJiangsu Key Laboratory of Crop Genetics and Physiology & Co-Innovation Center for Modern Production Technology of Grain Crops, Agricultural College, Yangzhou University, Yangzhou 225009, ChinaJiangsu Key Laboratory of Crop Genetics and Physiology & Co-Innovation Center for Modern Production Technology of Grain Crops, Agricultural College, Yangzhou University, Yangzhou 225009, ChinaKey Laboratory of Pesticides Evaluation, Ministry of Agriculture, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaJiangsu Key Laboratory of Crop Genetics and Physiology & Co-Innovation Center for Modern Production Technology of Grain Crops, Agricultural College, Yangzhou University, Yangzhou 225009, ChinaJiangsu Key Laboratory of Crop Genetics and Physiology & Co-Innovation Center for Modern Production Technology of Grain Crops, Agricultural College, Yangzhou University, Yangzhou 225009, ChinaJiangsu Key Laboratory of Crop Genetics and Physiology & Co-Innovation Center for Modern Production Technology of Grain Crops, Agricultural College, Yangzhou University, Yangzhou 225009, ChinaJiangsu Key Laboratory of Crop Genetics and Physiology & Co-Innovation Center for Modern Production Technology of Grain Crops, Agricultural College, Yangzhou University, Yangzhou 225009, ChinaKey Laboratory of Pesticides Evaluation, Ministry of Agriculture, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, ChinaRice false smut (RFS), caused by <i>Ustilaginoidea virens</i>, is an important fungal disease of rice. In China, Methyl Benzimidazole Carbamates (MBCs), including carbendazim, are common fungicides used to control RFS and other rice diseases. In this study, resistance of <i>U. virens</i> to carbendazim was monitored for three consecutive years during 2018 to 2020. A total of 321 <i>U. virens</i> isolates collected from Jiangsu Province of China were tested for their sensitivity to carbendazim on PSA. The concentration at which mycelial growth is inhibited by 50% (EC<sub>50</sub>) of the carbendazim-sensitive isolates was 0.11 to 1.38 µg/mL, with a mean EC<sub>50</sub> value of 0.66 μg/mL. High level of resistance to carbendazim was detected in 14 out of 321 isolates. The resistance was stable but associated with a fitness penalty. There was a statistically significant and moderate negative correlation (r= −0.74, <i>p</i> < 0.001) in sensitivity between carbendazim and diethofencarb. Analysis of the <i>U. virens</i> genome revealed two potential MBC targets, <i>Uvβ1Tub</i> and <i>Uvβ2Tub</i>, that putatively encode β-tubulin gene. The two β-tubulin genes in <i>U. virens</i> share 78% amino acid sequence identity, but their function in MBC sensitivity has been unclear. Both genes were identified and sequenced from <i>U. virens</i> sensitive and resistant isolates. It is known that mutations in the β2-tubulin gene have been shown to confer resistance to carbendazim in other fungi. However, no mutation was found in the <i>Uvβ2Tub</i> gene in either resistant or sensitive isolates. Variations including point mutations, non-sense mutations, codon mutations, and frameshift mutations were found in the <i>Uvβ1Tub</i> gene from the 14 carbendazim-resistant isolates, which have not been reported in other fungi before. Thus, these results indicated that variations of <i>Uvβ1Tub</i> result in the resistance to carbendazim in field isolates of <i>Ustilaginoidea virens</i>.https://www.mdpi.com/2309-608X/8/12/1311β-tubulincarbendazim resistancefitnessmolecular mechanism<i>Ustilaginoidea virens</i> |
| spellingShingle | Jiehui Song Zhiying Wang Yan Wang Sijie Zhang Tengyu Lei You Liang Qigen Dai Zhongyang Huo Ke Xu Shuning Chen Prevalence of Carbendazin Resistance in Field Populations of the Rice False Smut Pathogen <i>Ustilaginoidea virens</i> from Jiangsu, China, Molecular Mechanisms, and Fitness Stability Journal of Fungi β-tubulin carbendazim resistance fitness molecular mechanism <i>Ustilaginoidea virens</i> |
| title | Prevalence of Carbendazin Resistance in Field Populations of the Rice False Smut Pathogen <i>Ustilaginoidea virens</i> from Jiangsu, China, Molecular Mechanisms, and Fitness Stability |
| title_full | Prevalence of Carbendazin Resistance in Field Populations of the Rice False Smut Pathogen <i>Ustilaginoidea virens</i> from Jiangsu, China, Molecular Mechanisms, and Fitness Stability |
| title_fullStr | Prevalence of Carbendazin Resistance in Field Populations of the Rice False Smut Pathogen <i>Ustilaginoidea virens</i> from Jiangsu, China, Molecular Mechanisms, and Fitness Stability |
| title_full_unstemmed | Prevalence of Carbendazin Resistance in Field Populations of the Rice False Smut Pathogen <i>Ustilaginoidea virens</i> from Jiangsu, China, Molecular Mechanisms, and Fitness Stability |
| title_short | Prevalence of Carbendazin Resistance in Field Populations of the Rice False Smut Pathogen <i>Ustilaginoidea virens</i> from Jiangsu, China, Molecular Mechanisms, and Fitness Stability |
| title_sort | prevalence of carbendazin resistance in field populations of the rice false smut pathogen i ustilaginoidea virens i from jiangsu china molecular mechanisms and fitness stability |
| topic | β-tubulin carbendazim resistance fitness molecular mechanism <i>Ustilaginoidea virens</i> |
| url | https://www.mdpi.com/2309-608X/8/12/1311 |
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