{"title":"根结线虫利用类似过氧化氢酶的效应器,通过直接降解 H2O2 来操纵植物活性氧水平","authors":"Zhaolu Zhu, Dadong Dai, Mengzhuo Zheng, Yiling Shi, Shahid Siddique, Feifan Wang, Shurong Zhang, Chuanshuai Xie, Dexin Bo, Boyan Hu, Yangyang Chen, Donghai Peng, Ming Sun, Jinshui Zheng","doi":"10.1111/mpp.70000","DOIUrl":null,"url":null,"abstract":"Plants produce reactive oxygen species (ROS) upon infection, which typically trigger defence mechanisms and impede pathogen proliferation. Root‐knot nematodes (RKNs, <jats:italic>Meloidogyne</jats:italic> spp.) represent highly detrimental pathogens capable of parasitizing a broad spectrum of crops, resulting in substantial annual agricultural losses. The involvement of ROS in RKN parasitism is well acknowledged. In this study, we identified a novel effector from <jats:italic>Meloidogyne incognita</jats:italic>, named CATLe, that contains a conserved catalase domain, exhibiting potential functions in regulating host ROS levels. Phylogenetic analysis revealed that CATLe is conserved across RKNs. Temporal and spatial expression assays showed that the <jats:italic>CATLe</jats:italic> gene was specifically up‐regulated at the early infection stages and accumulated in the subventral oesophageal gland cells of <jats:italic>M. incognita</jats:italic>. Immunolocalization demonstrated that CATLe was secreted into the giant cells of the host plant during <jats:italic>M. incognita</jats:italic> parasitism. Transient expression of CATLe significantly dampened the flg22‐induced ROS production in <jats:italic>Nicotiana benthamiana</jats:italic>. In planta assays confirmed that <jats:italic>M. incognita</jats:italic> can exploit CATLe to manipulate host ROS levels by directly degrading H<jats:sub>2</jats:sub>O<jats:sub>2</jats:sub>. Additionally, interfering with expression of the <jats:italic>CATLe</jats:italic> gene through double‐stranded RNA soaking and host‐induced gene silencing significantly attenuated <jats:italic>M. incognita</jats:italic> parasitism, highlighting the important role of CATLe. Taken together, our results suggest that RKNs can directly degrade ROS products using a functional catalase, thereby manipulating host ROS levels and facilitating parasitism.","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":"10 1","pages":"e70000"},"PeriodicalIF":4.8000,"publicationDate":"2024-09-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Root‐knot nematodes exploit the catalase‐like effector to manipulate plant reactive oxygen species levels by directly degrading H2O2\",\"authors\":\"Zhaolu Zhu, Dadong Dai, Mengzhuo Zheng, Yiling Shi, Shahid Siddique, Feifan Wang, Shurong Zhang, Chuanshuai Xie, Dexin Bo, Boyan Hu, Yangyang Chen, Donghai Peng, Ming Sun, Jinshui Zheng\",\"doi\":\"10.1111/mpp.70000\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"Plants produce reactive oxygen species (ROS) upon infection, which typically trigger defence mechanisms and impede pathogen proliferation. Root‐knot nematodes (RKNs, <jats:italic>Meloidogyne</jats:italic> spp.) represent highly detrimental pathogens capable of parasitizing a broad spectrum of crops, resulting in substantial annual agricultural losses. The involvement of ROS in RKN parasitism is well acknowledged. In this study, we identified a novel effector from <jats:italic>Meloidogyne incognita</jats:italic>, named CATLe, that contains a conserved catalase domain, exhibiting potential functions in regulating host ROS levels. Phylogenetic analysis revealed that CATLe is conserved across RKNs. Temporal and spatial expression assays showed that the <jats:italic>CATLe</jats:italic> gene was specifically up‐regulated at the early infection stages and accumulated in the subventral oesophageal gland cells of <jats:italic>M. incognita</jats:italic>. Immunolocalization demonstrated that CATLe was secreted into the giant cells of the host plant during <jats:italic>M. incognita</jats:italic> parasitism. Transient expression of CATLe significantly dampened the flg22‐induced ROS production in <jats:italic>Nicotiana benthamiana</jats:italic>. In planta assays confirmed that <jats:italic>M. incognita</jats:italic> can exploit CATLe to manipulate host ROS levels by directly degrading H<jats:sub>2</jats:sub>O<jats:sub>2</jats:sub>. Additionally, interfering with expression of the <jats:italic>CATLe</jats:italic> gene through double‐stranded RNA soaking and host‐induced gene silencing significantly attenuated <jats:italic>M. incognita</jats:italic> parasitism, highlighting the important role of CATLe. Taken together, our results suggest that RKNs can directly degrade ROS products using a functional catalase, thereby manipulating host ROS levels and facilitating parasitism.\",\"PeriodicalId\":18763,\"journal\":{\"name\":\"Molecular plant pathology\",\"volume\":\"10 1\",\"pages\":\"e70000\"},\"PeriodicalIF\":4.8000,\"publicationDate\":\"2024-09-10\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Molecular plant pathology\",\"FirstCategoryId\":\"97\",\"ListUrlMain\":\"https://doi.org/10.1111/mpp.70000\",\"RegionNum\":1,\"RegionCategory\":\"农林科学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"PLANT SCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular plant pathology","FirstCategoryId":"97","ListUrlMain":"https://doi.org/10.1111/mpp.70000","RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
Root‐knot nematodes exploit the catalase‐like effector to manipulate plant reactive oxygen species levels by directly degrading H2O2
Plants produce reactive oxygen species (ROS) upon infection, which typically trigger defence mechanisms and impede pathogen proliferation. Root‐knot nematodes (RKNs, Meloidogyne spp.) represent highly detrimental pathogens capable of parasitizing a broad spectrum of crops, resulting in substantial annual agricultural losses. The involvement of ROS in RKN parasitism is well acknowledged. In this study, we identified a novel effector from Meloidogyne incognita, named CATLe, that contains a conserved catalase domain, exhibiting potential functions in regulating host ROS levels. Phylogenetic analysis revealed that CATLe is conserved across RKNs. Temporal and spatial expression assays showed that the CATLe gene was specifically up‐regulated at the early infection stages and accumulated in the subventral oesophageal gland cells of M. incognita. Immunolocalization demonstrated that CATLe was secreted into the giant cells of the host plant during M. incognita parasitism. Transient expression of CATLe significantly dampened the flg22‐induced ROS production in Nicotiana benthamiana. In planta assays confirmed that M. incognita can exploit CATLe to manipulate host ROS levels by directly degrading H2O2. Additionally, interfering with expression of the CATLe gene through double‐stranded RNA soaking and host‐induced gene silencing significantly attenuated M. incognita parasitism, highlighting the important role of CATLe. Taken together, our results suggest that RKNs can directly degrade ROS products using a functional catalase, thereby manipulating host ROS levels and facilitating parasitism.
期刊介绍:
Molecular Plant Pathology is now an open access journal. Authors pay an article processing charge to publish in the journal and all articles will be freely available to anyone. BSPP members will be granted a 20% discount on article charges. The Editorial focus and policy of the journal has not be changed and the editorial team will continue to apply the same rigorous standards of peer review and acceptance criteria.