Characteristics of soil microbial community assembly patterns in fields with serious occurrence of tobacco Fusarium wilt disease

IntroductionFusarium wilt disease (FWD) of tobacco is a destructive disease caused by Fusarium spp. in tobacco-growing regions worldwide. The Fusarium spp. infection may alter the composition and structure of the tobacco root microbial community; however, the relationship between these factors under...

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Main Authors: Huidi Liu, Yongfeng Zhang, Hongchen Li, Shilu Chen, Jingze Zhang, Wei Ding
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-11-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1482952/full
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author Huidi Liu
Yongfeng Zhang
Hongchen Li
Shilu Chen
Jingze Zhang
Wei Ding
author_facet Huidi Liu
Yongfeng Zhang
Hongchen Li
Shilu Chen
Jingze Zhang
Wei Ding
author_sort Huidi Liu
collection DOAJ
description IntroductionFusarium wilt disease (FWD) of tobacco is a destructive disease caused by Fusarium spp. in tobacco-growing regions worldwide. The Fusarium spp. infection may alter the composition and structure of the tobacco root microbial community; however, the relationship between these factors under large-scale geographical conditions in China remains underexplored.MethodsIn the context of this investigation, soil samples from the rhizosphere of tobacco plants were procured from fields afflicted with FWD and those devoid of the disease in the Hanzhong region of Shaanxi province, as well as in the Sanmenxia and Nanyang regions of Henan province. These regions are recognized for the commercial cultivation of tobacco. The examination focused on discerning the influence of tobacco FWD on the composition and configuration of the rhizosphere microbial community, along with their co-occurrence patterns. This scrutiny was underpinned by targeted PCR amplification and high-throughput sequencing (amplicon sequencing) of the 16S rRNA gene and the ITS1 region.ResultsThe amplicon data analyses showed that FWD influenced the microbial structure and composition of the tobacco rhizosphere soil. FWD had a greater impact on the microbiome of the tobacco fungal community than on the microbiome of the bacterial community. Healthy plants had the ability to recruit potential beneficial bacteria. Diseased plants were more susceptible to colonization by other pathogenic fungi, but they still had the capacity to recruit potential beneficial bacteria. The analysis of microbial intra- and inter-kingdom networks further indicated that FWD destabilized microbial networks. In the overall microbial interaction, microorganisms primarily interacted within their boundaries, but FWD increased the proportion of interactions occurring across boundaries. In addition, FWD could disrupt the interactions within microbial network modules.DiscussionThis study provides evidence that FWD can cause changes in the composition and network of microbial communities, affecting the interactions among various microorganisms, including bacteria and fungi. These findings contribute to our understanding of how plant microbiomes change due to disease. Furthermore, they add to our knowledge of the mechanisms that govern the assembly and interactions of microbial communities under the influence of FWD.
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spelling doaj-art-473d1e45d112440da79442e451ab46912024-11-13T14:42:47ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-11-011510.3389/fmicb.2024.14829521482952Characteristics of soil microbial community assembly patterns in fields with serious occurrence of tobacco Fusarium wilt diseaseHuidi Liu0Yongfeng Zhang1Hongchen Li2Shilu Chen3Jingze Zhang4Wei Ding5College of Plant Protection, Southwest University, Chongqing, ChinaShangluo Prefecture Branch of Shaanxi Tobacco Corporation, Shangluo, ChinaSanmenxia Tobacco Corporation of Henan Province, Sanmenxia, ChinaCollege of Plant Protection, Southwest University, Chongqing, ChinaInstitute of Biotechnology, Zhejiang University, Hangzhou, ChinaCollege of Plant Protection, Southwest University, Chongqing, ChinaIntroductionFusarium wilt disease (FWD) of tobacco is a destructive disease caused by Fusarium spp. in tobacco-growing regions worldwide. The Fusarium spp. infection may alter the composition and structure of the tobacco root microbial community; however, the relationship between these factors under large-scale geographical conditions in China remains underexplored.MethodsIn the context of this investigation, soil samples from the rhizosphere of tobacco plants were procured from fields afflicted with FWD and those devoid of the disease in the Hanzhong region of Shaanxi province, as well as in the Sanmenxia and Nanyang regions of Henan province. These regions are recognized for the commercial cultivation of tobacco. The examination focused on discerning the influence of tobacco FWD on the composition and configuration of the rhizosphere microbial community, along with their co-occurrence patterns. This scrutiny was underpinned by targeted PCR amplification and high-throughput sequencing (amplicon sequencing) of the 16S rRNA gene and the ITS1 region.ResultsThe amplicon data analyses showed that FWD influenced the microbial structure and composition of the tobacco rhizosphere soil. FWD had a greater impact on the microbiome of the tobacco fungal community than on the microbiome of the bacterial community. Healthy plants had the ability to recruit potential beneficial bacteria. Diseased plants were more susceptible to colonization by other pathogenic fungi, but they still had the capacity to recruit potential beneficial bacteria. The analysis of microbial intra- and inter-kingdom networks further indicated that FWD destabilized microbial networks. In the overall microbial interaction, microorganisms primarily interacted within their boundaries, but FWD increased the proportion of interactions occurring across boundaries. In addition, FWD could disrupt the interactions within microbial network modules.DiscussionThis study provides evidence that FWD can cause changes in the composition and network of microbial communities, affecting the interactions among various microorganisms, including bacteria and fungi. These findings contribute to our understanding of how plant microbiomes change due to disease. Furthermore, they add to our knowledge of the mechanisms that govern the assembly and interactions of microbial communities under the influence of FWD.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1482952/fullFusarium wilt diseasemicrobiomemicrobiome assemblymicrobial networkmicrobial interaction
spellingShingle Huidi Liu
Yongfeng Zhang
Hongchen Li
Shilu Chen
Jingze Zhang
Wei Ding
Characteristics of soil microbial community assembly patterns in fields with serious occurrence of tobacco Fusarium wilt disease
Frontiers in Microbiology
Fusarium wilt disease
microbiome
microbiome assembly
microbial network
microbial interaction
title Characteristics of soil microbial community assembly patterns in fields with serious occurrence of tobacco Fusarium wilt disease
title_full Characteristics of soil microbial community assembly patterns in fields with serious occurrence of tobacco Fusarium wilt disease
title_fullStr Characteristics of soil microbial community assembly patterns in fields with serious occurrence of tobacco Fusarium wilt disease
title_full_unstemmed Characteristics of soil microbial community assembly patterns in fields with serious occurrence of tobacco Fusarium wilt disease
title_short Characteristics of soil microbial community assembly patterns in fields with serious occurrence of tobacco Fusarium wilt disease
title_sort characteristics of soil microbial community assembly patterns in fields with serious occurrence of tobacco fusarium wilt disease
topic Fusarium wilt disease
microbiome
microbiome assembly
microbial network
microbial interaction
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1482952/full
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