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Diseased-induced multifaceted variations in community assembly and functions of plant-associated microbiomes

Plant-associated microorganisms are believed to be part of the so-called extended plant phenotypes, affecting plant growth and health. Understanding how plant-associated microorganisms respond to pathogen invasion is crucial to controlling plant diseases through microbiome manipulation. In this stud...

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Autores principales: Kuang, Lu, Li, Ting, Wang, Baozhan, Peng, Junwei, Li, Jiangang, Li, Pengfa, Jiang, Jiandong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10060855/
https://www.ncbi.nlm.nih.gov/pubmed/37007500
http://dx.doi.org/10.3389/fmicb.2023.1141585
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author Kuang, Lu
Li, Ting
Wang, Baozhan
Peng, Junwei
Li, Jiangang
Li, Pengfa
Jiang, Jiandong
author_facet Kuang, Lu
Li, Ting
Wang, Baozhan
Peng, Junwei
Li, Jiangang
Li, Pengfa
Jiang, Jiandong
author_sort Kuang, Lu
collection PubMed
description Plant-associated microorganisms are believed to be part of the so-called extended plant phenotypes, affecting plant growth and health. Understanding how plant-associated microorganisms respond to pathogen invasion is crucial to controlling plant diseases through microbiome manipulation. In this study, healthy and diseased (bacterial wilt disease, BWD) tomato (Solanum lycopersicum L.) plants were harvested, and variations in the rhizosphere and root endosphere microbial communities were subsequently investigated using amplicon and shotgun metagenome sequencing. BWD led to a significant increase in rhizosphere bacterial diversity in the rhizosphere but reduced bacterial diversity in the root endosphere. The ecological null model indicated that BWD enhanced the bacterial deterministic processes in both the rhizosphere and root endosphere. Network analysis showed that microbial co-occurrence complexity was increased in BWD-infected plants. Moreover, higher universal ecological dynamics of microbial communities were observed in the diseased rhizosphere. Metagenomic analysis revealed the enrichment of more functional gene pathways in the infected rhizosphere. More importantly, when tomato plants were infected with BWD, some plant-harmful pathways such as quorum sensing were significantly enriched, while some plant-beneficial pathways such as streptomycin biosynthesis were depleted. These findings broaden the understanding of plant–microbiome interactions and provide new clues to the underlying mechanism behind the interaction between the plant microbiome and BWD.
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spelling pubmed-100608552023-03-31 Diseased-induced multifaceted variations in community assembly and functions of plant-associated microbiomes Kuang, Lu Li, Ting Wang, Baozhan Peng, Junwei Li, Jiangang Li, Pengfa Jiang, Jiandong Front Microbiol Microbiology Plant-associated microorganisms are believed to be part of the so-called extended plant phenotypes, affecting plant growth and health. Understanding how plant-associated microorganisms respond to pathogen invasion is crucial to controlling plant diseases through microbiome manipulation. In this study, healthy and diseased (bacterial wilt disease, BWD) tomato (Solanum lycopersicum L.) plants were harvested, and variations in the rhizosphere and root endosphere microbial communities were subsequently investigated using amplicon and shotgun metagenome sequencing. BWD led to a significant increase in rhizosphere bacterial diversity in the rhizosphere but reduced bacterial diversity in the root endosphere. The ecological null model indicated that BWD enhanced the bacterial deterministic processes in both the rhizosphere and root endosphere. Network analysis showed that microbial co-occurrence complexity was increased in BWD-infected plants. Moreover, higher universal ecological dynamics of microbial communities were observed in the diseased rhizosphere. Metagenomic analysis revealed the enrichment of more functional gene pathways in the infected rhizosphere. More importantly, when tomato plants were infected with BWD, some plant-harmful pathways such as quorum sensing were significantly enriched, while some plant-beneficial pathways such as streptomycin biosynthesis were depleted. These findings broaden the understanding of plant–microbiome interactions and provide new clues to the underlying mechanism behind the interaction between the plant microbiome and BWD. Frontiers Media S.A. 2023-03-16 /pmc/articles/PMC10060855/ /pubmed/37007500 http://dx.doi.org/10.3389/fmicb.2023.1141585 Text en Copyright © 2023 Kuang, Li, Wang, Peng, Li, Li and Jiang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Kuang, Lu
Li, Ting
Wang, Baozhan
Peng, Junwei
Li, Jiangang
Li, Pengfa
Jiang, Jiandong
Diseased-induced multifaceted variations in community assembly and functions of plant-associated microbiomes
title Diseased-induced multifaceted variations in community assembly and functions of plant-associated microbiomes
title_full Diseased-induced multifaceted variations in community assembly and functions of plant-associated microbiomes
title_fullStr Diseased-induced multifaceted variations in community assembly and functions of plant-associated microbiomes
title_full_unstemmed Diseased-induced multifaceted variations in community assembly and functions of plant-associated microbiomes
title_short Diseased-induced multifaceted variations in community assembly and functions of plant-associated microbiomes
title_sort diseased-induced multifaceted variations in community assembly and functions of plant-associated microbiomes
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10060855/
https://www.ncbi.nlm.nih.gov/pubmed/37007500
http://dx.doi.org/10.3389/fmicb.2023.1141585
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