Salomé Soulé, Kaiwei Huang, Karine Mulet, Joffrey Mejias, Jérémie Bazin, Nhat My Truong, Junior Lusu Kika, Stéphanie Jaubert, Pierre Abad, Jianlong Zhao, Bruno Favery, Michaël Quentin
{"title":"根结线虫效应子MiEFF12以宿主ER质量控制系统为靶标,抑制免疫反应,实现寄生。","authors":"Salomé Soulé, Kaiwei Huang, Karine Mulet, Joffrey Mejias, Jérémie Bazin, Nhat My Truong, Junior Lusu Kika, Stéphanie Jaubert, Pierre Abad, Jianlong Zhao, Bruno Favery, Michaël Quentin","doi":"10.1111/mpp.13491","DOIUrl":null,"url":null,"abstract":"<p><p>Root-knot nematodes (RKNs) are microscopic parasitic worms able to infest the roots of thousands of plant species, causing massive crop yield losses worldwide. They evade the plant's immune system and manipulate plant cell physiology and metabolism to transform a few root cells into giant cells, which serve as feeding sites for the nematode. RKN parasitism is facilitated by the secretion in planta of effector molecules, mostly proteins that hijack host cellular processes. We describe here a conserved RKN-specific effector, effector 12 (EFF12), that is synthesized exclusively in the oesophageal glands of the nematode, and we demonstrate its function in parasitism. In the plant, MiEFF12 localizes to the endoplasmic reticulum (ER). A combination of RNA-sequencing analysis and immunity-suppression bioassays revealed the contribution of MiEFF12 to the modulation of host immunity. Yeast two-hybrid, split luciferase and co-immunoprecipitation approaches identified an essential component of the ER quality control system, the Solanum lycopersicum plant bap-like (PBL), and basic leucine zipper 60 (BZIP60) proteins as host targets of MiEFF12. Finally, silencing the PBL genes in Nicotiana benthamiana decreased susceptibility to Meloidogyne incognita infection. Our results suggest that EFF12 manipulates PBL function to modify plant immune responses to allow parasitism.</p>","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":"25 7","pages":"e13491"},"PeriodicalIF":4.8000,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11222708/pdf/","citationCount":"0","resultStr":"{\"title\":\"The root-knot nematode effector MiEFF12 targets the host ER quality control system to suppress immune responses and allow parasitism.\",\"authors\":\"Salomé Soulé, Kaiwei Huang, Karine Mulet, Joffrey Mejias, Jérémie Bazin, Nhat My Truong, Junior Lusu Kika, Stéphanie Jaubert, Pierre Abad, Jianlong Zhao, Bruno Favery, Michaël Quentin\",\"doi\":\"10.1111/mpp.13491\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Root-knot nematodes (RKNs) are microscopic parasitic worms able to infest the roots of thousands of plant species, causing massive crop yield losses worldwide. They evade the plant's immune system and manipulate plant cell physiology and metabolism to transform a few root cells into giant cells, which serve as feeding sites for the nematode. RKN parasitism is facilitated by the secretion in planta of effector molecules, mostly proteins that hijack host cellular processes. We describe here a conserved RKN-specific effector, effector 12 (EFF12), that is synthesized exclusively in the oesophageal glands of the nematode, and we demonstrate its function in parasitism. In the plant, MiEFF12 localizes to the endoplasmic reticulum (ER). A combination of RNA-sequencing analysis and immunity-suppression bioassays revealed the contribution of MiEFF12 to the modulation of host immunity. Yeast two-hybrid, split luciferase and co-immunoprecipitation approaches identified an essential component of the ER quality control system, the Solanum lycopersicum plant bap-like (PBL), and basic leucine zipper 60 (BZIP60) proteins as host targets of MiEFF12. Finally, silencing the PBL genes in Nicotiana benthamiana decreased susceptibility to Meloidogyne incognita infection. Our results suggest that EFF12 manipulates PBL function to modify plant immune responses to allow parasitism.</p>\",\"PeriodicalId\":18763,\"journal\":{\"name\":\"Molecular plant pathology\",\"volume\":\"25 7\",\"pages\":\"e13491\"},\"PeriodicalIF\":4.8000,\"publicationDate\":\"2024-07-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11222708/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Molecular plant pathology\",\"FirstCategoryId\":\"97\",\"ListUrlMain\":\"https://doi.org/10.1111/mpp.13491\",\"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.13491","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}
The root-knot nematode effector MiEFF12 targets the host ER quality control system to suppress immune responses and allow parasitism.
Root-knot nematodes (RKNs) are microscopic parasitic worms able to infest the roots of thousands of plant species, causing massive crop yield losses worldwide. They evade the plant's immune system and manipulate plant cell physiology and metabolism to transform a few root cells into giant cells, which serve as feeding sites for the nematode. RKN parasitism is facilitated by the secretion in planta of effector molecules, mostly proteins that hijack host cellular processes. We describe here a conserved RKN-specific effector, effector 12 (EFF12), that is synthesized exclusively in the oesophageal glands of the nematode, and we demonstrate its function in parasitism. In the plant, MiEFF12 localizes to the endoplasmic reticulum (ER). A combination of RNA-sequencing analysis and immunity-suppression bioassays revealed the contribution of MiEFF12 to the modulation of host immunity. Yeast two-hybrid, split luciferase and co-immunoprecipitation approaches identified an essential component of the ER quality control system, the Solanum lycopersicum plant bap-like (PBL), and basic leucine zipper 60 (BZIP60) proteins as host targets of MiEFF12. Finally, silencing the PBL genes in Nicotiana benthamiana decreased susceptibility to Meloidogyne incognita infection. Our results suggest that EFF12 manipulates PBL function to modify plant immune responses to allow 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.