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Reprogramming of phytopathogen transcriptome by a non-bactericidal pesticide residue alleviates its virulence in rice

Haruna MatsumotoKey Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, ChinaYuan QianState Key Laboratory of Rice Biology & Ministry of Agricultural and Rural Affairs Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Pesticide and Environmental Toxicology, Zhejiang University, Hangzhou 310058, ChinaXiaoyan FanInstitute of Environmental Biotechnology, Graz University of Technology, Petersgasse 12, 8010 Graz, AustriaSunlu ChenState Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing 210095, ChinaYanxia NieEcology and Environmental Sciences Center, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, ChinaKun QiaoState Key Laboratory of Rice Biology & Ministry of Agricultural and Rural Affairs Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Pesticide and Environmental Toxicology, Zhejiang University, Hangzhou 310058, ChinaDandan XiangKey laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization (MOA), Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, ChinaXinzhong ZhangTea Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou 310008, ChinaMeng LiState Key Laboratory of Rice Biology & Ministry of Agricultural and Rural Affairs Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Pesticide and Environmental Toxicology, Zhejiang University, Hangzhou 310058, ChinaBo GuoShanghai International Studies University, Shanghai 200083, ChinaPeilin ShenState Key Laboratory of Rice Biology & Ministry of Agricultural and Rural Affairs Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Pesticide and Environmental Toxicology, Zhejiang University, Hangzhou 310058, ChinaQiangwei WangKey Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, ChinaYunlong YuKey Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, ChinaTomislav CernavaInstitute of Environmental Biotechnology, Graz University of Technology, Petersgasse 12, 8010 Graz, AustriaMengcen WangGlobal Education Program for AgriScience Frontiers, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan
2022en
ABI

Аннотация

Bacteria equipped with virulence systems based on highly bioactive small molecules can circumvent their host's defense mechanisms. Pathogens employing this strategy are currently threatening global rice production. In the present study, variations in the virulence of the highly destructive Burkholderia plantarii were observed in different rice-producing regions. The environment-linked variation was not attributable to any known host-related or external factors. Co-occurrence analyses indicated a connection between reduced virulence and 5-Amino-1,3,4-thiadiazole-2-thiol (ATT), a non-bactericidal organic compound. ATT, which accumulates in rice plants during metabolization of specific agrochemicals, was found to reduce virulence factor secretion by B. plantarii up to 88.8% and inhibit pathogen virulence by hijacking an upstream signaling cascade. Detailed assessment of the newly discovered virulence inhibitor resulted in mechanistic insights into positive effects of ATT accumulation in plant tissues. Mechanisms of virulence alleviation were deciphered by integrating high-throughput data, gene knockout mutants, and molecular interaction assays. TroK, a histidine protein kinase in a two-component system that regulates virulence factor secretion, is likely the molecular target antagonized by ATT. Our findings provide novel insights into virulence modulation in an important plant-pathogen system that relies on the host's metabolic activity and subsequent signaling interference.

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