Fangyan Wang, Haoqing Zhang, Hongwei Liu, Chuanfa Wu, Yi Wan, Lifei Zhu, Jian Yang, Peng Cai, Jianping Chen, Tida Ge
{"title":"通过微生物相互作用和激素途径调节抗击小麦黄曲霉病毒。","authors":"Fangyan Wang, Haoqing Zhang, Hongwei Liu, Chuanfa Wu, Yi Wan, Lifei Zhu, Jian Yang, Peng Cai, Jianping Chen, Tida Ge","doi":"10.1186/s40168-024-01911-z","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>The rhizosphere microbiome is critical for promoting plant growth and mitigating soil-borne pathogens. However, its role in fighting soil-borne virus-induced diseases, such as wheat yellow mosaic virus (WYMV) transmitted by Polymyxa graminis zoospores, remains largely underexplored. In this study, we hypothesized that during viral infections, plant microbiomes engage in critical interactions with plants, with key microbes playing vital roles in maintaining plant health. Our research aimed to identify microbial taxa that not only suppress the disease but also boost wheat yield by using a blend of techniques, including field surveys, yield assessments, high-throughput sequencing of plant and soil microbiomes, microbial isolation, hydroponic experiments, and transcriptome sequencing.</p><p><strong>Results: </strong>We found that, compared with roots and leaves, the rhizosphere microbiome showed a better performance in predicting wheat yield and the prevalence of P. graminis and WYMV across the three WYMV-impacted regions in China. Using machine learning, we found that healthy rhizospheres were marked with potentially beneficial microorganisms, such as Sphingomonas and Allorhizobium-Neorhizobium-Parararhizobium-Rhizobium, whereas diseased rhizospheres were associated with a higher prevalence of potential pathogens, such as Bipolaris and Fusicolla. Structural equation modeling showed that these biomarkers both directly and indirectly impacted wheat yield by modulating the rhizosphere microbiome and P. graminis abundance. Upon re-introduction of two key healthy rhizosphere biomarkers, Sphingomonas azotifigens and Rhizobium deserti, into the rhizosphere, wheat growth and health were enhanced. This was attributed to the up-regulation of auxin and cytokinin signaling pathways and the regulation of jasmonic acid and salicylic acid pathways during infections.</p><p><strong>Conclusions: </strong>Overall, our study revealed the critical role of the rhizosphere microbiome in combating soil-borne viral diseases, with specific rhizosphere microbes playing key roles in this process. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"200"},"PeriodicalIF":13.8000,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11481568/pdf/","citationCount":"0","resultStr":"{\"title\":\"Combating wheat yellow mosaic virus through microbial interactions and hormone pathway modulations.\",\"authors\":\"Fangyan Wang, Haoqing Zhang, Hongwei Liu, Chuanfa Wu, Yi Wan, Lifei Zhu, Jian Yang, Peng Cai, Jianping Chen, Tida Ge\",\"doi\":\"10.1186/s40168-024-01911-z\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Background: </strong>The rhizosphere microbiome is critical for promoting plant growth and mitigating soil-borne pathogens. However, its role in fighting soil-borne virus-induced diseases, such as wheat yellow mosaic virus (WYMV) transmitted by Polymyxa graminis zoospores, remains largely underexplored. In this study, we hypothesized that during viral infections, plant microbiomes engage in critical interactions with plants, with key microbes playing vital roles in maintaining plant health. Our research aimed to identify microbial taxa that not only suppress the disease but also boost wheat yield by using a blend of techniques, including field surveys, yield assessments, high-throughput sequencing of plant and soil microbiomes, microbial isolation, hydroponic experiments, and transcriptome sequencing.</p><p><strong>Results: </strong>We found that, compared with roots and leaves, the rhizosphere microbiome showed a better performance in predicting wheat yield and the prevalence of P. graminis and WYMV across the three WYMV-impacted regions in China. Using machine learning, we found that healthy rhizospheres were marked with potentially beneficial microorganisms, such as Sphingomonas and Allorhizobium-Neorhizobium-Parararhizobium-Rhizobium, whereas diseased rhizospheres were associated with a higher prevalence of potential pathogens, such as Bipolaris and Fusicolla. Structural equation modeling showed that these biomarkers both directly and indirectly impacted wheat yield by modulating the rhizosphere microbiome and P. graminis abundance. Upon re-introduction of two key healthy rhizosphere biomarkers, Sphingomonas azotifigens and Rhizobium deserti, into the rhizosphere, wheat growth and health were enhanced. This was attributed to the up-regulation of auxin and cytokinin signaling pathways and the regulation of jasmonic acid and salicylic acid pathways during infections.</p><p><strong>Conclusions: </strong>Overall, our study revealed the critical role of the rhizosphere microbiome in combating soil-borne viral diseases, with specific rhizosphere microbes playing key roles in this process. Video Abstract.</p>\",\"PeriodicalId\":18447,\"journal\":{\"name\":\"Microbiome\",\"volume\":\"12 1\",\"pages\":\"200\"},\"PeriodicalIF\":13.8000,\"publicationDate\":\"2024-10-15\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11481568/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Microbiome\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1186/s40168-024-01911-z\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Microbiome","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1186/s40168-024-01911-z","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
Combating wheat yellow mosaic virus through microbial interactions and hormone pathway modulations.
Background: The rhizosphere microbiome is critical for promoting plant growth and mitigating soil-borne pathogens. However, its role in fighting soil-borne virus-induced diseases, such as wheat yellow mosaic virus (WYMV) transmitted by Polymyxa graminis zoospores, remains largely underexplored. In this study, we hypothesized that during viral infections, plant microbiomes engage in critical interactions with plants, with key microbes playing vital roles in maintaining plant health. Our research aimed to identify microbial taxa that not only suppress the disease but also boost wheat yield by using a blend of techniques, including field surveys, yield assessments, high-throughput sequencing of plant and soil microbiomes, microbial isolation, hydroponic experiments, and transcriptome sequencing.
Results: We found that, compared with roots and leaves, the rhizosphere microbiome showed a better performance in predicting wheat yield and the prevalence of P. graminis and WYMV across the three WYMV-impacted regions in China. Using machine learning, we found that healthy rhizospheres were marked with potentially beneficial microorganisms, such as Sphingomonas and Allorhizobium-Neorhizobium-Parararhizobium-Rhizobium, whereas diseased rhizospheres were associated with a higher prevalence of potential pathogens, such as Bipolaris and Fusicolla. Structural equation modeling showed that these biomarkers both directly and indirectly impacted wheat yield by modulating the rhizosphere microbiome and P. graminis abundance. Upon re-introduction of two key healthy rhizosphere biomarkers, Sphingomonas azotifigens and Rhizobium deserti, into the rhizosphere, wheat growth and health were enhanced. This was attributed to the up-regulation of auxin and cytokinin signaling pathways and the regulation of jasmonic acid and salicylic acid pathways during infections.
Conclusions: Overall, our study revealed the critical role of the rhizosphere microbiome in combating soil-borne viral diseases, with specific rhizosphere microbes playing key roles in this process. Video Abstract.
期刊介绍:
Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.