Shengping Shang, Xiaofei Liang, Guangli Liu, Youwei Du, Song Zhang, Yanan Meng, Junming Zhu, Jeffrey A. Rollins, Rong Zhang, Guangyu Sun
{"title":"一种真菌效应物通过操纵叶绿体中由 DAHPS 介导的代谢通量来抑制植物免疫。","authors":"Shengping Shang, Xiaofei Liang, Guangli Liu, Youwei Du, Song Zhang, Yanan Meng, Junming Zhu, Jeffrey A. Rollins, Rong Zhang, Guangyu Sun","doi":"10.1111/nph.20117","DOIUrl":null,"url":null,"abstract":"<div>\n \n <p>\n \n </p><ul>\n \n \n <li>Plant secondary metabolism represents an important and ancient form of defense against pathogens. Phytopathogens secrete effectors to suppress plant defenses and promote infection. However, it is largely unknown, how fungal effectors directly manipulate plant secondary metabolism.</li>\n \n \n <li>Here, we characterized a fungal defense-suppressing effector CfEC28 from <i>Colletotrichum fructicola</i>. Gene deletion assays showed that ∆<i>CfEC28</i>-mutants differentiated appressoria normally on plant surface but were almost nonpathogenic due to increased number of plant papilla accumulation at attempted penetration sites. CfEC28 interacted with a family of chloroplast-localized 3-deoxy-<span>d</span>-arabinose-heptulonic acid-7-phosphate synthases (DAHPSs) in apple. CfEC28 inhibited the enzymatic activity of an apple DAHPS (MdDAHPS1) and suppressed DAHPS-mediated secondary metabolite accumulation through blocking the manganese ion binding region of DAHPS. Dramatically, transgene analysis revealed that overexpression of MdDAHPS1 provided apple with a complete resistance to <i>C. fructicola</i>.</li>\n \n \n <li>We showed that a novel effector CfEC28 can be delivered into plant chloroplasts and contributes to the full virulence of <i>C. fructicola</i> by targeting the DAHPS to disrupt the pathway linking the metabolism of primary carbohydrates with the biosynthesis of aromatic defense compounds.</li>\n \n \n <li>Our study provides important insights for understanding plant–microbe interactions and a valuable gene for improving plant disease resistance.</li>\n </ul>\n \n </div>","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"244 4","pages":"1552-1569"},"PeriodicalIF":8.3000,"publicationDate":"2024-09-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"A fungal effector suppresses plant immunity by manipulating DAHPS-mediated metabolic flux in chloroplasts\",\"authors\":\"Shengping Shang, Xiaofei Liang, Guangli Liu, Youwei Du, Song Zhang, Yanan Meng, Junming Zhu, Jeffrey A. Rollins, Rong Zhang, Guangyu Sun\",\"doi\":\"10.1111/nph.20117\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div>\\n \\n <p>\\n \\n </p><ul>\\n \\n \\n <li>Plant secondary metabolism represents an important and ancient form of defense against pathogens. Phytopathogens secrete effectors to suppress plant defenses and promote infection. However, it is largely unknown, how fungal effectors directly manipulate plant secondary metabolism.</li>\\n \\n \\n <li>Here, we characterized a fungal defense-suppressing effector CfEC28 from <i>Colletotrichum fructicola</i>. Gene deletion assays showed that ∆<i>CfEC28</i>-mutants differentiated appressoria normally on plant surface but were almost nonpathogenic due to increased number of plant papilla accumulation at attempted penetration sites. CfEC28 interacted with a family of chloroplast-localized 3-deoxy-<span>d</span>-arabinose-heptulonic acid-7-phosphate synthases (DAHPSs) in apple. CfEC28 inhibited the enzymatic activity of an apple DAHPS (MdDAHPS1) and suppressed DAHPS-mediated secondary metabolite accumulation through blocking the manganese ion binding region of DAHPS. Dramatically, transgene analysis revealed that overexpression of MdDAHPS1 provided apple with a complete resistance to <i>C. fructicola</i>.</li>\\n \\n \\n <li>We showed that a novel effector CfEC28 can be delivered into plant chloroplasts and contributes to the full virulence of <i>C. fructicola</i> by targeting the DAHPS to disrupt the pathway linking the metabolism of primary carbohydrates with the biosynthesis of aromatic defense compounds.</li>\\n \\n \\n <li>Our study provides important insights for understanding plant–microbe interactions and a valuable gene for improving plant disease resistance.</li>\\n </ul>\\n \\n </div>\",\"PeriodicalId\":214,\"journal\":{\"name\":\"New Phytologist\",\"volume\":\"244 4\",\"pages\":\"1552-1569\"},\"PeriodicalIF\":8.3000,\"publicationDate\":\"2024-09-26\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"New Phytologist\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://onlinelibrary.wiley.com/doi/10.1111/nph.20117\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"PLANT SCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"New Phytologist","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/nph.20117","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
A fungal effector suppresses plant immunity by manipulating DAHPS-mediated metabolic flux in chloroplasts
Plant secondary metabolism represents an important and ancient form of defense against pathogens. Phytopathogens secrete effectors to suppress plant defenses and promote infection. However, it is largely unknown, how fungal effectors directly manipulate plant secondary metabolism.
Here, we characterized a fungal defense-suppressing effector CfEC28 from Colletotrichum fructicola. Gene deletion assays showed that ∆CfEC28-mutants differentiated appressoria normally on plant surface but were almost nonpathogenic due to increased number of plant papilla accumulation at attempted penetration sites. CfEC28 interacted with a family of chloroplast-localized 3-deoxy-d-arabinose-heptulonic acid-7-phosphate synthases (DAHPSs) in apple. CfEC28 inhibited the enzymatic activity of an apple DAHPS (MdDAHPS1) and suppressed DAHPS-mediated secondary metabolite accumulation through blocking the manganese ion binding region of DAHPS. Dramatically, transgene analysis revealed that overexpression of MdDAHPS1 provided apple with a complete resistance to C. fructicola.
We showed that a novel effector CfEC28 can be delivered into plant chloroplasts and contributes to the full virulence of C. fructicola by targeting the DAHPS to disrupt the pathway linking the metabolism of primary carbohydrates with the biosynthesis of aromatic defense compounds.
Our study provides important insights for understanding plant–microbe interactions and a valuable gene for improving plant disease resistance.
期刊介绍:
New Phytologist is an international electronic journal published 24 times a year. It is owned by the New Phytologist Foundation, a non-profit-making charitable organization dedicated to promoting plant science. The journal publishes excellent, novel, rigorous, and timely research and scholarship in plant science and its applications. The articles cover topics in five sections: Physiology & Development, Environment, Interaction, Evolution, and Transformative Plant Biotechnology. These sections encompass intracellular processes, global environmental change, and encourage cross-disciplinary approaches. The journal recognizes the use of techniques from molecular and cell biology, functional genomics, modeling, and system-based approaches in plant science. Abstracting and Indexing Information for New Phytologist includes Academic Search, AgBiotech News & Information, Agroforestry Abstracts, Biochemistry & Biophysics Citation Index, Botanical Pesticides, CAB Abstracts®, Environment Index, Global Health, and Plant Breeding Abstracts, and others.