The endophytic microbiome response patterns of Juglans regia to two pathogenic fungi

The endophytic microbial community reassembles to participate in plant immune balance when the host plants are stressed by pathogens. However, it remains unclear whether this assembly is pathogen-specific and how regulatory pathways are coordinated in multi-pathogens. In order to investigate the eff...

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Main Authors: Ziye Wang, Lu Xu, Xiaoyue Lu, Ruidong Wang, Jie Han, Aihua Yan
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1378273/full
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author Ziye Wang
Ziye Wang
Lu Xu
Lu Xu
Xiaoyue Lu
Xiaoyue Lu
Ruidong Wang
Ruidong Wang
Jie Han
Jie Han
Aihua Yan
Aihua Yan
author_facet Ziye Wang
Ziye Wang
Lu Xu
Lu Xu
Xiaoyue Lu
Xiaoyue Lu
Ruidong Wang
Ruidong Wang
Jie Han
Jie Han
Aihua Yan
Aihua Yan
author_sort Ziye Wang
collection DOAJ
description The endophytic microbial community reassembles to participate in plant immune balance when the host plants are stressed by pathogens. However, it remains unclear whether this assembly is pathogen-specific and how regulatory pathways are coordinated in multi-pathogens. In order to investigate the effects of infection with Colletotrichum gloeosporioides (Cg treatment) and Fusarium proliferatum (Fp treatment) on walnut leaf endophytic microbiome in their assembly, co-occurrence pattern, and on comprehensive chemical function of the internal environment of leaf, an interaction system of the walnut–pathogenic fungi was constructed using seed embryo tissue culture technology. The study showed differences in the assembly of endophytic microbial communities in walnut trees across three groups (control group, Ck; Cg; Fp) after Cg and Fp treatments. Despite changes in relative abundances, the dominant communities in phyla and genera remained comparable during the infection of the two pathogens. Endophyte fungi were more sensitive to the pathogen challenge than endophyte bacteria. Both promoted the enrichment of beneficial bacteria such as Bacillus and Pseudomonas, changed the modularity of the community, and reduced the stability and complexity of the endophyte community. Pathogenic fungi infection mainly affects the metabolism of porphyrin and chlorophyll, purine metabolism, phenylpropane metabolism, and amino acid metabolism. However, there was no significant difference in the secondary metabolites for the different susceptible plants. By screening endogenous antagonistic bacteria, we further verified that Pseudomonas psychrotolerans and Bacillus subtilis had inhibitory effects on the two pathogenic fungi and participated in the interaction between the leaves and pathogenic fungi. The antibacterial substances may be 1-methylnaphthalene, 1,3-butadiene, 2,3-butanediol, and toluene aldehyde.
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spelling doaj.art-8b9c889684ae43c2bfcd603ef615f28a2024-04-11T04:22:38ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-04-011510.3389/fmicb.2024.13782731378273The endophytic microbiome response patterns of Juglans regia to two pathogenic fungiZiye Wang0Ziye Wang1Lu Xu2Lu Xu3Xiaoyue Lu4Xiaoyue Lu5Ruidong Wang6Ruidong Wang7Jie Han8Jie Han9Aihua Yan10Aihua Yan11Key Laboratory of Forest Protection of National Forestry and Grassland Administration, Chinese Academy of Forestry, Ecology and Nature Conservation Institute, Beijing, ChinaCollege of Forestry, Hebei Agricultural University, Baoding, Hebei, ChinaCollege of Forestry, Hebei Agricultural University, Baoding, Hebei, ChinaHebei Province Key Laboratory of Forest Trees Germplasm Resources and Forest Protection, Baoding, Hebei, ChinaCollege of Forestry, Hebei Agricultural University, Baoding, Hebei, ChinaHebei Province Key Laboratory of Forest Trees Germplasm Resources and Forest Protection, Baoding, Hebei, ChinaCollege of Forestry, Hebei Agricultural University, Baoding, Hebei, ChinaHebei Province Key Laboratory of Forest Trees Germplasm Resources and Forest Protection, Baoding, Hebei, ChinaCollege of Forestry, Hebei Agricultural University, Baoding, Hebei, ChinaHebei Province Key Laboratory of Forest Trees Germplasm Resources and Forest Protection, Baoding, Hebei, ChinaCollege of Forestry, Hebei Agricultural University, Baoding, Hebei, ChinaHebei Urban Forest Health Technology Innovation Center, Baoding, Hebei, ChinaThe endophytic microbial community reassembles to participate in plant immune balance when the host plants are stressed by pathogens. However, it remains unclear whether this assembly is pathogen-specific and how regulatory pathways are coordinated in multi-pathogens. In order to investigate the effects of infection with Colletotrichum gloeosporioides (Cg treatment) and Fusarium proliferatum (Fp treatment) on walnut leaf endophytic microbiome in their assembly, co-occurrence pattern, and on comprehensive chemical function of the internal environment of leaf, an interaction system of the walnut–pathogenic fungi was constructed using seed embryo tissue culture technology. The study showed differences in the assembly of endophytic microbial communities in walnut trees across three groups (control group, Ck; Cg; Fp) after Cg and Fp treatments. Despite changes in relative abundances, the dominant communities in phyla and genera remained comparable during the infection of the two pathogens. Endophyte fungi were more sensitive to the pathogen challenge than endophyte bacteria. Both promoted the enrichment of beneficial bacteria such as Bacillus and Pseudomonas, changed the modularity of the community, and reduced the stability and complexity of the endophyte community. Pathogenic fungi infection mainly affects the metabolism of porphyrin and chlorophyll, purine metabolism, phenylpropane metabolism, and amino acid metabolism. However, there was no significant difference in the secondary metabolites for the different susceptible plants. By screening endogenous antagonistic bacteria, we further verified that Pseudomonas psychrotolerans and Bacillus subtilis had inhibitory effects on the two pathogenic fungi and participated in the interaction between the leaves and pathogenic fungi. The antibacterial substances may be 1-methylnaphthalene, 1,3-butadiene, 2,3-butanediol, and toluene aldehyde.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1378273/fullendophytic microbiomepathogenic fungimetabolomeendogenous antagonistic bacteriaexpression mode
spellingShingle Ziye Wang
Ziye Wang
Lu Xu
Lu Xu
Xiaoyue Lu
Xiaoyue Lu
Ruidong Wang
Ruidong Wang
Jie Han
Jie Han
Aihua Yan
Aihua Yan
The endophytic microbiome response patterns of Juglans regia to two pathogenic fungi
Frontiers in Microbiology
endophytic microbiome
pathogenic fungi
metabolome
endogenous antagonistic bacteria
expression mode
title The endophytic microbiome response patterns of Juglans regia to two pathogenic fungi
title_full The endophytic microbiome response patterns of Juglans regia to two pathogenic fungi
title_fullStr The endophytic microbiome response patterns of Juglans regia to two pathogenic fungi
title_full_unstemmed The endophytic microbiome response patterns of Juglans regia to two pathogenic fungi
title_short The endophytic microbiome response patterns of Juglans regia to two pathogenic fungi
title_sort endophytic microbiome response patterns of juglans regia to two pathogenic fungi
topic endophytic microbiome
pathogenic fungi
metabolome
endogenous antagonistic bacteria
expression mode
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1378273/full
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