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...
Main Authors: | , , , , , |
---|---|
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 |
_version_ | 1797214968042487808 |
---|---|
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. |
first_indexed | 2024-04-24T11:22:36Z |
format | Article |
id | doaj.art-8b9c889684ae43c2bfcd603ef615f28a |
institution | Directory Open Access Journal |
issn | 1664-302X |
language | English |
last_indexed | 2024-04-24T11:22:36Z |
publishDate | 2024-04-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Microbiology |
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 |
work_keys_str_mv | AT ziyewang theendophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT ziyewang theendophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT luxu theendophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT luxu theendophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT xiaoyuelu theendophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT xiaoyuelu theendophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT ruidongwang theendophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT ruidongwang theendophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT jiehan theendophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT jiehan theendophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT aihuayan theendophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT aihuayan theendophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT ziyewang endophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT ziyewang endophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT luxu endophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT luxu endophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT xiaoyuelu endophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT xiaoyuelu endophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT ruidongwang endophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT ruidongwang endophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT jiehan endophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT jiehan endophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT aihuayan endophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi AT aihuayan endophyticmicrobiomeresponsepatternsofjuglansregiatotwopathogenicfungi |