Microbe-mediated stress resistance in plants: the roles played by core and stress-specific microbiota.

IF 13.8 1区 生物学 Q1 MICROBIOLOGY
Sijia Liu, Jiadong Wu, Zhen Cheng, Haofei Wang, Zhelun Jin, Xiang Zhang, Deqiang Zhang, Jianbo Xie
{"title":"Microbe-mediated stress resistance in plants: the roles played by core and stress-specific microbiota.","authors":"Sijia Liu, Jiadong Wu, Zhen Cheng, Haofei Wang, Zhelun Jin, Xiang Zhang, Deqiang Zhang, Jianbo Xie","doi":"10.1186/s40168-025-02103-z","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Plants in natural surroundings frequently encounter diverse forms of stress, and microbes are known to play a crucial role in assisting plants to withstand these challenges. However, the mining and utilization of plant-associated stress-resistant microbial sub-communities from the complex microbiome remains largely elusive.</p><p><strong>Results: </strong>This study was based on the microbial communities over 13 weeks under four treatments (control, drought, salt, and disease) to define the shared core microbiota and stress-specific microbiota. Through co-occurrence network analysis, the dynamic change networks of microbial communities under the four treatments were constructed, revealing distinct change trajectories corresponding to different treatments. Moreover, by simulating species extinction, the impact of the selective removal of microbes on network robustness was quantitatively assessed. It was found that under varying environmental conditions, core microbiota made significant potential contributions to the maintenance of network stability. Our assessment utilizing null and neutral models indicated that the assembly of stress-specific microbiota was predominantly driven by deterministic processes, whereas the assembly of core microbiota was governed by stochastic processes. We also identified the microbiome features from functional perspectives: the shared microbiota tended to enhance the ability of organisms to withstand multiple types of environmental stresses and stress-specific microbial communities were associated with the diverse mechanisms of mitigating specific stresses. Using a culturomic approach, 781 bacterial strains were isolated, and nine strains were selected to construct different SynComs. These experiments confirmed that communities containing stress-specific microbes effectively assist plants in coping with environmental stresses.</p><p><strong>Conclusions: </strong>Collectively, we not only systematically revealed the dynamics variation patterns of rhizosphere microbiome under various stresses, but also sought constancy from the changes, identified the potential contributions of core microbiota and stress-specific microbiota to plant stress tolerance, and ultimately aimed at the beneficial microbial inoculation strategies for plants. Our research provides novel insights into understanding the microbe-mediated stress resistance process in plants. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"13 1","pages":"111"},"PeriodicalIF":13.8000,"publicationDate":"2025-05-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12051278/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Microbiome","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1186/s40168-025-02103-z","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Background: Plants in natural surroundings frequently encounter diverse forms of stress, and microbes are known to play a crucial role in assisting plants to withstand these challenges. However, the mining and utilization of plant-associated stress-resistant microbial sub-communities from the complex microbiome remains largely elusive.

Results: This study was based on the microbial communities over 13 weeks under four treatments (control, drought, salt, and disease) to define the shared core microbiota and stress-specific microbiota. Through co-occurrence network analysis, the dynamic change networks of microbial communities under the four treatments were constructed, revealing distinct change trajectories corresponding to different treatments. Moreover, by simulating species extinction, the impact of the selective removal of microbes on network robustness was quantitatively assessed. It was found that under varying environmental conditions, core microbiota made significant potential contributions to the maintenance of network stability. Our assessment utilizing null and neutral models indicated that the assembly of stress-specific microbiota was predominantly driven by deterministic processes, whereas the assembly of core microbiota was governed by stochastic processes. We also identified the microbiome features from functional perspectives: the shared microbiota tended to enhance the ability of organisms to withstand multiple types of environmental stresses and stress-specific microbial communities were associated with the diverse mechanisms of mitigating specific stresses. Using a culturomic approach, 781 bacterial strains were isolated, and nine strains were selected to construct different SynComs. These experiments confirmed that communities containing stress-specific microbes effectively assist plants in coping with environmental stresses.

Conclusions: Collectively, we not only systematically revealed the dynamics variation patterns of rhizosphere microbiome under various stresses, but also sought constancy from the changes, identified the potential contributions of core microbiota and stress-specific microbiota to plant stress tolerance, and ultimately aimed at the beneficial microbial inoculation strategies for plants. Our research provides novel insights into understanding the microbe-mediated stress resistance process in plants. Video Abstract.

植物微生物介导的抗逆性:核心和胁迫特异性微生物群的作用。
背景:植物在自然环境中经常遇到各种形式的胁迫,而微生物在帮助植物抵御这些挑战方面起着至关重要的作用。然而,从复杂的微生物组中挖掘和利用与植物相关的抗逆性微生物亚群落在很大程度上仍然难以捉摸。结果:本研究基于四种处理(对照、干旱、盐和疾病)下13周的微生物群落,以确定共享的核心微生物群和应激特异性微生物群。通过共现网络分析,构建了4种处理下微生物群落的动态变化网络,揭示了不同处理对应的不同变化轨迹。此外,通过模拟物种灭绝,定量评估了选择性去除微生物对网络鲁棒性的影响。研究发现,在不同的环境条件下,核心微生物群对网络稳定性的维持有着重要的潜在贡献。我们利用零模型和中性模型进行的评估表明,应力特异性微生物群的组装主要由确定性过程驱动,而核心微生物群的组装则由随机过程控制。我们还从功能角度确定了微生物组的特征:共享的微生物群倾向于增强生物体承受多种类型环境胁迫的能力,而应激特异性微生物群落与减轻特定胁迫的多种机制有关。采用培养法分离781株细菌,选择9株构建不同的syncom。这些实验证实,含有胁迫特异性微生物的群落能有效地帮助植物应对环境胁迫。结论:本研究不仅系统揭示了不同胁迫条件下根际微生物群的动态变化规律,而且从变化中寻求一致性,确定了核心微生物群和胁迫特异性微生物群对植物抗逆性的潜在贡献,并最终针对植物的有益微生物接种策略。我们的研究为理解微生物介导的植物抗逆性过程提供了新的见解。视频摘要。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Microbiome
Microbiome MICROBIOLOGY-
CiteScore
21.90
自引率
2.60%
发文量
198
审稿时长
4 weeks
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.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:604180095
Book学术官方微信