{"title":"马铃薯包囊线虫的一种由根际微生物转化为孵化因子的根分泌分子。","authors":"Ryota Akiyama,Yui Kawano,Kosuke Shimizu,Soichiro Makino,Karen Akanuma,Haru Nagatomo,Masami Yokota Hirai,Yukihiro Sugimoto,Atsuhiko Kushida,Keiji Tanino,Masaharu Mizutani","doi":"10.1111/nph.70252","DOIUrl":null,"url":null,"abstract":"Eclepins are root-secreted compounds that induce the hatching of cyst nematodes. Solanoeclepin A (SEA) and B (SEB) have been isolated as potent hatching factors for potato cyst nematodes (PCNs). SEB is biosynthesized in roots, released into the rhizosphere, and converted into SEA by soil microorganisms. However, given that SEB and SEA exhibit comparable hatching-inducing activity toward PCNs, the ecological significance of microbial solanoeclepin metabolism in eclepin-mediated communication remains unclear. In this study, we identified solanoeclepin C (SEC), a previously unrecognized solanoeclepin secreted by tomato and potato roots. Structural analysis revealed that SEC is an acetylated derivative of SEB. Soil incubation experiments demonstrated that SEC is converted into SEB and subsequently into SEA. SEC exhibits 10 000-fold lower hatching-inducing activity than SEA. Gene expression analysis in hydroponically grown tomatoes showed that solanoeclepin biosynthesis is upregulated under nitrogen and phosphorus deficiencies, with nitrogen starvation having the strongest effect. Our results demonstrate that although SEC itself exhibits low hatching-inducing activity, it is converted by soil microorganisms into SEB and SEA, which are then exploited by PCNs to trigger their hatching. These findings reveal a previously unrecognized three-way interaction among plants, soil microbes, and nematodes mediated by solanoeclepins.","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"34 1","pages":""},"PeriodicalIF":8.3000,"publicationDate":"2025-05-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Solanoeclepin C, a root-secreted molecule converted by rhizosphere microbes to hatching factors for potato cyst nematodes.\",\"authors\":\"Ryota Akiyama,Yui Kawano,Kosuke Shimizu,Soichiro Makino,Karen Akanuma,Haru Nagatomo,Masami Yokota Hirai,Yukihiro Sugimoto,Atsuhiko Kushida,Keiji Tanino,Masaharu Mizutani\",\"doi\":\"10.1111/nph.70252\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"Eclepins are root-secreted compounds that induce the hatching of cyst nematodes. Solanoeclepin A (SEA) and B (SEB) have been isolated as potent hatching factors for potato cyst nematodes (PCNs). SEB is biosynthesized in roots, released into the rhizosphere, and converted into SEA by soil microorganisms. However, given that SEB and SEA exhibit comparable hatching-inducing activity toward PCNs, the ecological significance of microbial solanoeclepin metabolism in eclepin-mediated communication remains unclear. In this study, we identified solanoeclepin C (SEC), a previously unrecognized solanoeclepin secreted by tomato and potato roots. Structural analysis revealed that SEC is an acetylated derivative of SEB. Soil incubation experiments demonstrated that SEC is converted into SEB and subsequently into SEA. SEC exhibits 10 000-fold lower hatching-inducing activity than SEA. Gene expression analysis in hydroponically grown tomatoes showed that solanoeclepin biosynthesis is upregulated under nitrogen and phosphorus deficiencies, with nitrogen starvation having the strongest effect. Our results demonstrate that although SEC itself exhibits low hatching-inducing activity, it is converted by soil microorganisms into SEB and SEA, which are then exploited by PCNs to trigger their hatching. These findings reveal a previously unrecognized three-way interaction among plants, soil microbes, and nematodes mediated by solanoeclepins.\",\"PeriodicalId\":214,\"journal\":{\"name\":\"New Phytologist\",\"volume\":\"34 1\",\"pages\":\"\"},\"PeriodicalIF\":8.3000,\"publicationDate\":\"2025-05-26\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"New Phytologist\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1111/nph.70252\",\"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://doi.org/10.1111/nph.70252","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0
摘要
eclepin是根分泌的化合物,可诱导囊肿线虫的孵化。已分离出Solanoeclepin A (SEA)和B (SEB)作为马铃薯囊肿线虫(PCNs)的有效孵化因子。SEB在根内生物合成,释放到根际,并通过土壤微生物转化为SEA。然而,鉴于SEB和SEA对pcn的孵化诱导活性相当,微生物solanoecepin代谢在ecepin介导的通讯中的生态意义尚不清楚。在这项研究中,我们发现了一种以前未被发现的茄茄素C (SEC),它由番茄和马铃薯的根分泌。结构分析表明,SEC是SEB的乙酰化衍生物。土壤培养实验表明,SEC转化为SEB,随后转化为SEA。SEC的诱导孵化活性比SEA低10000倍。水培番茄的基因表达分析表明,缺氮和缺磷条件下,茄茄素的生物合成上调,其中氮饥饿的影响最大。我们的研究结果表明,尽管SEC本身表现出较低的诱导孵化活性,但它可以被土壤微生物转化为SEB和SEA,然后被pcn利用来触发它们的孵化。这些发现揭示了植物、土壤微生物和线虫之间由solanoeclepins介导的一种以前未被认识到的三方相互作用。
Solanoeclepin C, a root-secreted molecule converted by rhizosphere microbes to hatching factors for potato cyst nematodes.
Eclepins are root-secreted compounds that induce the hatching of cyst nematodes. Solanoeclepin A (SEA) and B (SEB) have been isolated as potent hatching factors for potato cyst nematodes (PCNs). SEB is biosynthesized in roots, released into the rhizosphere, and converted into SEA by soil microorganisms. However, given that SEB and SEA exhibit comparable hatching-inducing activity toward PCNs, the ecological significance of microbial solanoeclepin metabolism in eclepin-mediated communication remains unclear. In this study, we identified solanoeclepin C (SEC), a previously unrecognized solanoeclepin secreted by tomato and potato roots. Structural analysis revealed that SEC is an acetylated derivative of SEB. Soil incubation experiments demonstrated that SEC is converted into SEB and subsequently into SEA. SEC exhibits 10 000-fold lower hatching-inducing activity than SEA. Gene expression analysis in hydroponically grown tomatoes showed that solanoeclepin biosynthesis is upregulated under nitrogen and phosphorus deficiencies, with nitrogen starvation having the strongest effect. Our results demonstrate that although SEC itself exhibits low hatching-inducing activity, it is converted by soil microorganisms into SEB and SEA, which are then exploited by PCNs to trigger their hatching. These findings reveal a previously unrecognized three-way interaction among plants, soil microbes, and nematodes mediated by solanoeclepins.
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.