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Effects of single- and mixed-bacterial inoculation on the colonization and assembly of endophytic communities in plant roots

The introduction and inoculation of beneficial bacteria in plants have consistently been considered as one of the most important ways to improve plant health and production. However, the effects of bacterial inoculation on the community assembly and composition of the root endophytic microbiome rema...

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Autores principales: Zhang, Ting, Xiong, Juan, Tian, Rongchuan, Li, Ye, Zhang, Qinyi, Li, Ke, Xu, Xiaohong, Liang, Lianming, Zheng, Yi, Tian, Baoyu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9464981/
https://www.ncbi.nlm.nih.gov/pubmed/36105708
http://dx.doi.org/10.3389/fpls.2022.928367
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author Zhang, Ting
Xiong, Juan
Tian, Rongchuan
Li, Ye
Zhang, Qinyi
Li, Ke
Xu, Xiaohong
Liang, Lianming
Zheng, Yi
Tian, Baoyu
author_facet Zhang, Ting
Xiong, Juan
Tian, Rongchuan
Li, Ye
Zhang, Qinyi
Li, Ke
Xu, Xiaohong
Liang, Lianming
Zheng, Yi
Tian, Baoyu
author_sort Zhang, Ting
collection PubMed
description The introduction and inoculation of beneficial bacteria in plants have consistently been considered as one of the most important ways to improve plant health and production. However, the effects of bacterial inoculation on the community assembly and composition of the root endophytic microbiome remain largely unknown. In this study, 55 strains were randomly isolated from tomato roots and then inoculated into wheat seeds singly or in combination. Most of the isolated bacterial strains showed an ability to produce lignocellulose-decomposing enzymes and promote plant growth. The results demonstrated that bacterial inoculation had a significant effect on the wheat root endophytic microbiome. The wheat root samples inoculated with single-bacterial species were significantly separated into two groups (A and B) that had different community structures and compositions. Among these, root endophytic communities for most wheat samples inoculated with a single-bacterial strain (Group A) were predominated by one or several bacterial species, mainly belonging to Enterobacterales. In contrast, only a few of the root samples inoculated with a single-bacterial strain (Group B) harbored a rich bacterial flora with relatively high bacterial diversity. However, wheat roots inoculated with a mixed bacterial complex were colonized by a more diverse and abundant bacterial flora, which was mainly composed of Enterobacterales, Actinomycetales, Bacillales, Pseudomonadales, and Rhizobiales. The results demonstrated that inoculation with bacterial complexes could help plants establish more balanced and beneficial endophytic communities. In most cases, bacterial inoculation does not result in successful colonization by the target bacterium in wheat roots. However, bacterial inoculation consistently had a significant effect on the root microbiome in plants. CAP analysis demonstrated that the variation in wheat root endophytic communities was significantly related to the taxonomic status and lignocellulose decomposition ability of the inoculated bacterial strain (p < 0.05). To reveal the role of lignocellulose degradation in shaping the root endophytic microbiome in wheat, four bacterial strains with different colonization abilities were selected for further transcriptome sequencing analysis. The results showed that, compared with that in the dominant bacterial species Ent_181 and Ent_189 of Group A, the expression of lignocellulose-decomposing enzymes was significantly downregulated in Bac_133 and Bac_71 (p < 0.05). In addition, we found that the dominant bacterial species of the tomato endophytic microbiome were more likely to become dominant populations in the wheat root microbiome. In general, our results demonstrated that lignocellulose-decomposing enzymes played a vital role in the formation of endophytes and their successful colonization of root tissues. This finding establishes a theoretical foundation for the development of broad-spectrum probiotics.
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spelling pubmed-94649812022-09-13 Effects of single- and mixed-bacterial inoculation on the colonization and assembly of endophytic communities in plant roots Zhang, Ting Xiong, Juan Tian, Rongchuan Li, Ye Zhang, Qinyi Li, Ke Xu, Xiaohong Liang, Lianming Zheng, Yi Tian, Baoyu Front Plant Sci Plant Science The introduction and inoculation of beneficial bacteria in plants have consistently been considered as one of the most important ways to improve plant health and production. However, the effects of bacterial inoculation on the community assembly and composition of the root endophytic microbiome remain largely unknown. In this study, 55 strains were randomly isolated from tomato roots and then inoculated into wheat seeds singly or in combination. Most of the isolated bacterial strains showed an ability to produce lignocellulose-decomposing enzymes and promote plant growth. The results demonstrated that bacterial inoculation had a significant effect on the wheat root endophytic microbiome. The wheat root samples inoculated with single-bacterial species were significantly separated into two groups (A and B) that had different community structures and compositions. Among these, root endophytic communities for most wheat samples inoculated with a single-bacterial strain (Group A) were predominated by one or several bacterial species, mainly belonging to Enterobacterales. In contrast, only a few of the root samples inoculated with a single-bacterial strain (Group B) harbored a rich bacterial flora with relatively high bacterial diversity. However, wheat roots inoculated with a mixed bacterial complex were colonized by a more diverse and abundant bacterial flora, which was mainly composed of Enterobacterales, Actinomycetales, Bacillales, Pseudomonadales, and Rhizobiales. The results demonstrated that inoculation with bacterial complexes could help plants establish more balanced and beneficial endophytic communities. In most cases, bacterial inoculation does not result in successful colonization by the target bacterium in wheat roots. However, bacterial inoculation consistently had a significant effect on the root microbiome in plants. CAP analysis demonstrated that the variation in wheat root endophytic communities was significantly related to the taxonomic status and lignocellulose decomposition ability of the inoculated bacterial strain (p < 0.05). To reveal the role of lignocellulose degradation in shaping the root endophytic microbiome in wheat, four bacterial strains with different colonization abilities were selected for further transcriptome sequencing analysis. The results showed that, compared with that in the dominant bacterial species Ent_181 and Ent_189 of Group A, the expression of lignocellulose-decomposing enzymes was significantly downregulated in Bac_133 and Bac_71 (p < 0.05). In addition, we found that the dominant bacterial species of the tomato endophytic microbiome were more likely to become dominant populations in the wheat root microbiome. In general, our results demonstrated that lignocellulose-decomposing enzymes played a vital role in the formation of endophytes and their successful colonization of root tissues. This finding establishes a theoretical foundation for the development of broad-spectrum probiotics. Frontiers Media S.A. 2022-08-29 /pmc/articles/PMC9464981/ /pubmed/36105708 http://dx.doi.org/10.3389/fpls.2022.928367 Text en Copyright © 2022 Zhang, Xiong, Tian, Li, Zhang, Li, Xu, Liang, Zheng and Tian. 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 Plant Science
Zhang, Ting
Xiong, Juan
Tian, Rongchuan
Li, Ye
Zhang, Qinyi
Li, Ke
Xu, Xiaohong
Liang, Lianming
Zheng, Yi
Tian, Baoyu
Effects of single- and mixed-bacterial inoculation on the colonization and assembly of endophytic communities in plant roots
title Effects of single- and mixed-bacterial inoculation on the colonization and assembly of endophytic communities in plant roots
title_full Effects of single- and mixed-bacterial inoculation on the colonization and assembly of endophytic communities in plant roots
title_fullStr Effects of single- and mixed-bacterial inoculation on the colonization and assembly of endophytic communities in plant roots
title_full_unstemmed Effects of single- and mixed-bacterial inoculation on the colonization and assembly of endophytic communities in plant roots
title_short Effects of single- and mixed-bacterial inoculation on the colonization and assembly of endophytic communities in plant roots
title_sort effects of single- and mixed-bacterial inoculation on the colonization and assembly of endophytic communities in plant roots
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9464981/
https://www.ncbi.nlm.nih.gov/pubmed/36105708
http://dx.doi.org/10.3389/fpls.2022.928367
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