Integrated Analysis of GC-MS-Based Metabolomics and Proteomics Reveals the Importance of Volatile Metabolite Stigmasterol in the Defence Response of Panax notoginseng Against Root Rot.
{"title":"Integrated Analysis of GC-MS-Based Metabolomics and Proteomics Reveals the Importance of Volatile Metabolite Stigmasterol in the Defence Response of Panax notoginseng Against Root Rot.","authors":"Xiao-Min Li, Han-Lin Wang, Long-Yi Wei, Gui Li, Yuan Qu, Di-Qiu Liu","doi":"10.1111/mpp.70144","DOIUrl":null,"url":null,"abstract":"<p><p>Root rot disease in Panax notoginseng, primarily caused by the pathogenic fungus Fusarium solani, significantly impacts the growth and production of this medicinal herb. To elucidate the defence mechanisms of P. notoginseng against root rot, we employed proteomics and gas chromatography-mass spectrometry (GC-MS)-based metabolomics analyses. These analyses revealed significant accumulations of metabolites involved in phenylpropanoid, terpenoid and steroid biosynthesis pathways in F. solani-infected P. notoginseng roots. This accumulation correlated with the up-regulation of synthetases in these pathways as indicated by proteomics data. Focusing on stigmasterol, a representative steroid with differential accumulation levels, and its biosynthesis gene PnCYP710A, we investigated the role of stigmasterol metabolism in the defence response against root rot. Stigmasterol exhibited significant inhibitory effects on spore germination and hyphal growth of F. solani. Furthermore, PnCYP710A was up-regulated upon F. solani infection and induced by hormonal signals such as methyl jasmonate (MeJA). Overexpression of PnCYP710A in tobacco enhanced resistance to F. solani, up-regulated expression of JA biosynthesis/signalling pathway-related genes, increased accumulation of stigmasterol/lignin/callus, and maintained reactive oxygen species homeostasis during F. solani infection. Conversely, RNA interference (RNAi) of PnCYP710A in P. notoginseng yielded opposite effects. Additionally, PnWRKY4 positively regulated the transcription level of PnCYP710A by binding to its promoter. In summary, this study not only identifies volatile metabolites and proteins involved in the defence response of P. notoginseng against root rot but also discovers that PnWRKY4 activates stigmasterol biosynthesis to resist root rot pathogen infection.</p>","PeriodicalId":18763,"journal":{"name":"Molecular plant pathology","volume":"26 9","pages":"e70144"},"PeriodicalIF":4.9000,"publicationDate":"2025-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12405599/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular plant pathology","FirstCategoryId":"97","ListUrlMain":"https://doi.org/10.1111/mpp.70144","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}
引用次数: 0
Abstract
Root rot disease in Panax notoginseng, primarily caused by the pathogenic fungus Fusarium solani, significantly impacts the growth and production of this medicinal herb. To elucidate the defence mechanisms of P. notoginseng against root rot, we employed proteomics and gas chromatography-mass spectrometry (GC-MS)-based metabolomics analyses. These analyses revealed significant accumulations of metabolites involved in phenylpropanoid, terpenoid and steroid biosynthesis pathways in F. solani-infected P. notoginseng roots. This accumulation correlated with the up-regulation of synthetases in these pathways as indicated by proteomics data. Focusing on stigmasterol, a representative steroid with differential accumulation levels, and its biosynthesis gene PnCYP710A, we investigated the role of stigmasterol metabolism in the defence response against root rot. Stigmasterol exhibited significant inhibitory effects on spore germination and hyphal growth of F. solani. Furthermore, PnCYP710A was up-regulated upon F. solani infection and induced by hormonal signals such as methyl jasmonate (MeJA). Overexpression of PnCYP710A in tobacco enhanced resistance to F. solani, up-regulated expression of JA biosynthesis/signalling pathway-related genes, increased accumulation of stigmasterol/lignin/callus, and maintained reactive oxygen species homeostasis during F. solani infection. Conversely, RNA interference (RNAi) of PnCYP710A in P. notoginseng yielded opposite effects. Additionally, PnWRKY4 positively regulated the transcription level of PnCYP710A by binding to its promoter. In summary, this study not only identifies volatile metabolites and proteins involved in the defence response of P. notoginseng against root rot but also discovers that PnWRKY4 activates stigmasterol biosynthesis to resist root rot pathogen infection.
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.