The Endophytic Root Microbiome Is Different in Healthy and Ralstonia solanacearum-Infected Plants and Is Regulated by a Consortium Containing Beneficial Endophytic Bacteria
ABSTRACT Plant bacterial wilt disease caused by Ralstonia solanacearum leads to huge economic losses worldwide. Endophytes play vital roles in promoting plant growth and health. It is hypothesized that the endophytic root microbiome and network structure are different in healthy and diseased plants....
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-02-01
|
| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02031-22 |
| _version_ | 1811164352624984064 |
|---|---|
| author | Yiting Li Gaofu Qi Ziqiong Xie Baolong Li Rui Wang Jun Tan Heli Shi Bikun Xiang Xiuyun Zhao |
| author_facet | Yiting Li Gaofu Qi Ziqiong Xie Baolong Li Rui Wang Jun Tan Heli Shi Bikun Xiang Xiuyun Zhao |
| author_sort | Yiting Li |
| collection | DOAJ |
| description | ABSTRACT Plant bacterial wilt disease caused by Ralstonia solanacearum leads to huge economic losses worldwide. Endophytes play vital roles in promoting plant growth and health. It is hypothesized that the endophytic root microbiome and network structure are different in healthy and diseased plants. Here, the endophytic root microbiomes and network structures of healthy and diseased tobacco plants were investigated. Composition and network structures of endophytic root microbiomes were distinct between healthy and diseased plants. Healthy plants were enriched with more beneficial bacteria and bacteria with antagonistic activity against R. solanacearum. R. solanacearum was most abundant in diseased plants. Microbial networks in diseased plants had fewer modules and edges, lower connectivity, and fewer keystone microorganisms than those in healthy plants. Almost half of the nodes were unique in the two networks. Ralstonia was identified as a key microorganism of the diseased-plant network. In healthy plants, abundant bacteria and biomarkers (Pseudomonas and Streptomyces) and keystone microorganisms (Bacillus, Lysobacter, and Paenibacillus) were plant-beneficial bacteria and showed antibacterial and plant growth-promoting activities. The endophytic strain Bacillus velezensis E9 produced bacillaene to inhibit R. solanacearum. Consortia containing keystone microorganisms and beneficial endophytic bacteria significantly regulated the endophytic microbiome and attenuated bacterial wilt by inducing systemic resistance and producing antibiotic. Overall, the endophytic root microbiome and network structure in diseased plants were different from those in healthy plants. The endophytic root microbiome of diseased plants had low abundances of beneficial bacteria and an unstable network and lacked beneficial keystone microorganisms, which favored infection. Synthetic microbial consortia were effective measures for preventing R. solanacearum infection. IMPORTANCE Bacterial wilt disease causes heavy yield losses in many crops. Endophytic microbiomes play important roles in control of plant diseases. However, the role of the endophytic root microbiome in controlling bacterial wilt disease is poorly understood. Here, differences in endophytic root microbiomes and network structures between healthy and diseased tobacco plants are reported. A synthetic microbial consortium containing beneficial endophytic bacteria was used to regulate the endophytic microbiome and attenuate bacterial wilt disease. The results could be generally used to guide control of bacterial wilt disease. |
| first_indexed | 2024-04-10T15:20:15Z |
| format | Article |
| id | doaj.art-3c0242ec14f949daba2fc02fcb04cf8f |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-10T15:20:15Z |
| publishDate | 2023-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-3c0242ec14f949daba2fc02fcb04cf8f2023-02-14T14:15:50ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-02-0111110.1128/spectrum.02031-22The Endophytic Root Microbiome Is Different in Healthy and Ralstonia solanacearum-Infected Plants and Is Regulated by a Consortium Containing Beneficial Endophytic BacteriaYiting Li0Gaofu Qi1Ziqiong Xie2Baolong Li3Rui Wang4Jun Tan5Heli Shi6Bikun Xiang7Xiuyun Zhao8College of Life Science and Technology, Huazhong Agricultural University, Wuhan, ChinaCollege of Life Science and Technology, Huazhong Agricultural University, Wuhan, ChinaCollege of Life Science and Technology, Huazhong Agricultural University, Wuhan, ChinaCollege of Life Science and Technology, Huazhong Agricultural University, Wuhan, ChinaEnshi Tobacco Company of Hubei Province, Enshi, ChinaEnshi Tobacco Company of Hubei Province, Enshi, ChinaEnshi Tobacco Company of Hubei Province, Enshi, ChinaEnshi Tobacco Company of Hubei Province, Enshi, ChinaCollege of Life Science and Technology, Huazhong Agricultural University, Wuhan, ChinaABSTRACT Plant bacterial wilt disease caused by Ralstonia solanacearum leads to huge economic losses worldwide. Endophytes play vital roles in promoting plant growth and health. It is hypothesized that the endophytic root microbiome and network structure are different in healthy and diseased plants. Here, the endophytic root microbiomes and network structures of healthy and diseased tobacco plants were investigated. Composition and network structures of endophytic root microbiomes were distinct between healthy and diseased plants. Healthy plants were enriched with more beneficial bacteria and bacteria with antagonistic activity against R. solanacearum. R. solanacearum was most abundant in diseased plants. Microbial networks in diseased plants had fewer modules and edges, lower connectivity, and fewer keystone microorganisms than those in healthy plants. Almost half of the nodes were unique in the two networks. Ralstonia was identified as a key microorganism of the diseased-plant network. In healthy plants, abundant bacteria and biomarkers (Pseudomonas and Streptomyces) and keystone microorganisms (Bacillus, Lysobacter, and Paenibacillus) were plant-beneficial bacteria and showed antibacterial and plant growth-promoting activities. The endophytic strain Bacillus velezensis E9 produced bacillaene to inhibit R. solanacearum. Consortia containing keystone microorganisms and beneficial endophytic bacteria significantly regulated the endophytic microbiome and attenuated bacterial wilt by inducing systemic resistance and producing antibiotic. Overall, the endophytic root microbiome and network structure in diseased plants were different from those in healthy plants. The endophytic root microbiome of diseased plants had low abundances of beneficial bacteria and an unstable network and lacked beneficial keystone microorganisms, which favored infection. Synthetic microbial consortia were effective measures for preventing R. solanacearum infection. IMPORTANCE Bacterial wilt disease causes heavy yield losses in many crops. Endophytic microbiomes play important roles in control of plant diseases. However, the role of the endophytic root microbiome in controlling bacterial wilt disease is poorly understood. Here, differences in endophytic root microbiomes and network structures between healthy and diseased tobacco plants are reported. A synthetic microbial consortium containing beneficial endophytic bacteria was used to regulate the endophytic microbiome and attenuate bacterial wilt disease. The results could be generally used to guide control of bacterial wilt disease.https://journals.asm.org/doi/10.1128/spectrum.02031-22Ralstonia solanacearumendophytic root microbiomemicrobial networksynthetic microbial consortiabacillaeneinduced systemic resistance |
| spellingShingle | Yiting Li Gaofu Qi Ziqiong Xie Baolong Li Rui Wang Jun Tan Heli Shi Bikun Xiang Xiuyun Zhao The Endophytic Root Microbiome Is Different in Healthy and Ralstonia solanacearum-Infected Plants and Is Regulated by a Consortium Containing Beneficial Endophytic Bacteria Microbiology Spectrum Ralstonia solanacearum endophytic root microbiome microbial network synthetic microbial consortia bacillaene induced systemic resistance |
| title | The Endophytic Root Microbiome Is Different in Healthy and Ralstonia solanacearum-Infected Plants and Is Regulated by a Consortium Containing Beneficial Endophytic Bacteria |
| title_full | The Endophytic Root Microbiome Is Different in Healthy and Ralstonia solanacearum-Infected Plants and Is Regulated by a Consortium Containing Beneficial Endophytic Bacteria |
| title_fullStr | The Endophytic Root Microbiome Is Different in Healthy and Ralstonia solanacearum-Infected Plants and Is Regulated by a Consortium Containing Beneficial Endophytic Bacteria |
| title_full_unstemmed | The Endophytic Root Microbiome Is Different in Healthy and Ralstonia solanacearum-Infected Plants and Is Regulated by a Consortium Containing Beneficial Endophytic Bacteria |
| title_short | The Endophytic Root Microbiome Is Different in Healthy and Ralstonia solanacearum-Infected Plants and Is Regulated by a Consortium Containing Beneficial Endophytic Bacteria |
| title_sort | endophytic root microbiome is different in healthy and ralstonia solanacearum infected plants and is regulated by a consortium containing beneficial endophytic bacteria |
| topic | Ralstonia solanacearum endophytic root microbiome microbial network synthetic microbial consortia bacillaene induced systemic resistance |
| url | https://journals.asm.org/doi/10.1128/spectrum.02031-22 |
| work_keys_str_mv | AT yitingli theendophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT gaofuqi theendophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT ziqiongxie theendophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT baolongli theendophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT ruiwang theendophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT juntan theendophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT helishi theendophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT bikunxiang theendophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT xiuyunzhao theendophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT yitingli endophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT gaofuqi endophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT ziqiongxie endophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT baolongli endophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT ruiwang endophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT juntan endophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT helishi endophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT bikunxiang endophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria AT xiuyunzhao endophyticrootmicrobiomeisdifferentinhealthyandralstoniasolanacearuminfectedplantsandisregulatedbyaconsortiumcontainingbeneficialendophyticbacteria |