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Pathogen-Mediated Assembly of Plant-Beneficial Bacteria to Alleviate Fusarium Wilt in Pseudostellaria heterophylla

Fusarium wilt (FW) is a primary replant disease that affects Pseudostellaria heterophylla (Taizishen) and is caused by Fusarium oxysporum, which occurs widely in China under the continuous monocropping regime. However, the ternary interactions among the soil microbiota, P. heterophylla, and F. oxysp...

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Autores principales: Yuan, Qing-Song, Wang, Lu, Wang, Hui, Wang, Xiaoai, Jiang, Weike, Ou, Xiaohong, Xiao, Chenghong, Gao, Yanping, Xu, Jiao, Yang, Ye, Cui, Xiuming, Guo, Lanping, Huang, Luqi, Zhou, Tao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9005978/
https://www.ncbi.nlm.nih.gov/pubmed/35432244
http://dx.doi.org/10.3389/fmicb.2022.842372
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author Yuan, Qing-Song
Wang, Lu
Wang, Hui
Wang, Xiaoai
Jiang, Weike
Ou, Xiaohong
Xiao, Chenghong
Gao, Yanping
Xu, Jiao
Yang, Ye
Cui, Xiuming
Guo, Lanping
Huang, Luqi
Zhou, Tao
author_facet Yuan, Qing-Song
Wang, Lu
Wang, Hui
Wang, Xiaoai
Jiang, Weike
Ou, Xiaohong
Xiao, Chenghong
Gao, Yanping
Xu, Jiao
Yang, Ye
Cui, Xiuming
Guo, Lanping
Huang, Luqi
Zhou, Tao
author_sort Yuan, Qing-Song
collection PubMed
description Fusarium wilt (FW) is a primary replant disease that affects Pseudostellaria heterophylla (Taizishen) and is caused by Fusarium oxysporum, which occurs widely in China under the continuous monocropping regime. However, the ternary interactions among the soil microbiota, P. heterophylla, and F. oxysporum remain unknown. We investigated the potential interaction relationship by which the pathogen-mediated P. heterophylla regulates the soil and the tuberous root microbiota via high-throughput sequencing. Plant–pathogen interaction assays were conducted to measure the arrival of F. oxysporum and Pseudomonas poae at the tuberous root via qPCR and subsequent seedling disease incidence. A growth assay was used to determine the effect of the tuberous root crude exudate inoculated with the pathogen on P. poae. We observed that pathogen-mediated P. heterophylla altered the diversity and the composition of the microbial communities in its rhizosphere soil and tuberous root. Beneficial microbe P. poae and pathogen F. oxysporum were significantly enriched in rhizosphere soil and within the tuberous root in the FW group with high severity. Correlation analysis showed that, accompanied with FW incidence, P. poae co-occurred with F. oxysporum. The aqueous extract of P. heterophylla tuberous root infected by F. oxysporum substantially promoted the growth of P. poae isolates (H1-3-A7, H2-3-B7, H4-3-C1, and N3-3-C4). These results indicated that the extracts from the tuberous root of P. heterophylla inoculated with F. oxysporum might attract P. poae and promote its growth. Furthermore, the colonization assay found that the gene copies of sucD in the P. poae and F. oxysporum treatment (up to 6.57 × 10(10)) group was significantly higher than those in the P. poae treatment group (3.29 × 10(10)), and a pathogen-induced attraction assay found that the relative copies of sucD of P. poae in the F. oxysporum treatment were significantly higher than in the H(2)O treatment. These results showed that F. oxysporum promoted the colonization of P. poae on the tuberous root via F. oxysporum mediation. In addition, the colonization assay found that the disease severity index in the P. poae and F. oxysporum treatment group was significantly lower than that in the F. oxysporum treatment group, and a pathogen-induced attraction assay found that the disease severity index in the F. oxysporum treatment group was significantly higher than that in the H(2)O treatment group. Together, these results suggest that pathogen-mediated P. heterophylla promoted and assembled plant-beneficial microbes against plant disease. Therefore, deciphering the beneficial associations between pathogen-mediated P. heterophylla and microbes can provide novel insights into the implementation and design of disease management strategies.
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spelling pubmed-90059782022-04-14 Pathogen-Mediated Assembly of Plant-Beneficial Bacteria to Alleviate Fusarium Wilt in Pseudostellaria heterophylla Yuan, Qing-Song Wang, Lu Wang, Hui Wang, Xiaoai Jiang, Weike Ou, Xiaohong Xiao, Chenghong Gao, Yanping Xu, Jiao Yang, Ye Cui, Xiuming Guo, Lanping Huang, Luqi Zhou, Tao Front Microbiol Microbiology Fusarium wilt (FW) is a primary replant disease that affects Pseudostellaria heterophylla (Taizishen) and is caused by Fusarium oxysporum, which occurs widely in China under the continuous monocropping regime. However, the ternary interactions among the soil microbiota, P. heterophylla, and F. oxysporum remain unknown. We investigated the potential interaction relationship by which the pathogen-mediated P. heterophylla regulates the soil and the tuberous root microbiota via high-throughput sequencing. Plant–pathogen interaction assays were conducted to measure the arrival of F. oxysporum and Pseudomonas poae at the tuberous root via qPCR and subsequent seedling disease incidence. A growth assay was used to determine the effect of the tuberous root crude exudate inoculated with the pathogen on P. poae. We observed that pathogen-mediated P. heterophylla altered the diversity and the composition of the microbial communities in its rhizosphere soil and tuberous root. Beneficial microbe P. poae and pathogen F. oxysporum were significantly enriched in rhizosphere soil and within the tuberous root in the FW group with high severity. Correlation analysis showed that, accompanied with FW incidence, P. poae co-occurred with F. oxysporum. The aqueous extract of P. heterophylla tuberous root infected by F. oxysporum substantially promoted the growth of P. poae isolates (H1-3-A7, H2-3-B7, H4-3-C1, and N3-3-C4). These results indicated that the extracts from the tuberous root of P. heterophylla inoculated with F. oxysporum might attract P. poae and promote its growth. Furthermore, the colonization assay found that the gene copies of sucD in the P. poae and F. oxysporum treatment (up to 6.57 × 10(10)) group was significantly higher than those in the P. poae treatment group (3.29 × 10(10)), and a pathogen-induced attraction assay found that the relative copies of sucD of P. poae in the F. oxysporum treatment were significantly higher than in the H(2)O treatment. These results showed that F. oxysporum promoted the colonization of P. poae on the tuberous root via F. oxysporum mediation. In addition, the colonization assay found that the disease severity index in the P. poae and F. oxysporum treatment group was significantly lower than that in the F. oxysporum treatment group, and a pathogen-induced attraction assay found that the disease severity index in the F. oxysporum treatment group was significantly higher than that in the H(2)O treatment group. Together, these results suggest that pathogen-mediated P. heterophylla promoted and assembled plant-beneficial microbes against plant disease. Therefore, deciphering the beneficial associations between pathogen-mediated P. heterophylla and microbes can provide novel insights into the implementation and design of disease management strategies. Frontiers Media S.A. 2022-03-30 /pmc/articles/PMC9005978/ /pubmed/35432244 http://dx.doi.org/10.3389/fmicb.2022.842372 Text en Copyright © 2022 Yuan, Wang, Wang, Wang, Jiang, Ou, Xiao, Gao, Xu, Yang, Cui, Guo, Huang and Zhou. 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
Yuan, Qing-Song
Wang, Lu
Wang, Hui
Wang, Xiaoai
Jiang, Weike
Ou, Xiaohong
Xiao, Chenghong
Gao, Yanping
Xu, Jiao
Yang, Ye
Cui, Xiuming
Guo, Lanping
Huang, Luqi
Zhou, Tao
Pathogen-Mediated Assembly of Plant-Beneficial Bacteria to Alleviate Fusarium Wilt in Pseudostellaria heterophylla
title Pathogen-Mediated Assembly of Plant-Beneficial Bacteria to Alleviate Fusarium Wilt in Pseudostellaria heterophylla
title_full Pathogen-Mediated Assembly of Plant-Beneficial Bacteria to Alleviate Fusarium Wilt in Pseudostellaria heterophylla
title_fullStr Pathogen-Mediated Assembly of Plant-Beneficial Bacteria to Alleviate Fusarium Wilt in Pseudostellaria heterophylla
title_full_unstemmed Pathogen-Mediated Assembly of Plant-Beneficial Bacteria to Alleviate Fusarium Wilt in Pseudostellaria heterophylla
title_short Pathogen-Mediated Assembly of Plant-Beneficial Bacteria to Alleviate Fusarium Wilt in Pseudostellaria heterophylla
title_sort pathogen-mediated assembly of plant-beneficial bacteria to alleviate fusarium wilt in pseudostellaria heterophylla
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9005978/
https://www.ncbi.nlm.nih.gov/pubmed/35432244
http://dx.doi.org/10.3389/fmicb.2022.842372
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