Biocontrol of Bacterial Wilt Disease Through Complex Interaction Between Tomato Plant, Antagonists, the Indigenous Rhizosphere Microbiota, and Ralstonia solanacearum

Ralstonia solanacearum (biovar2, race3) is the causal agent of bacterial wilt and this quarantine phytopathogen is responsible for massive losses in several commercially important crops. Biological control of this pathogen might become a suitable plant protection measure in areas where R. solanacear...

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Main Authors: Tarek R. Elsayed, Samuel Jacquiod, Eman H. Nour, Søren J. Sørensen, Kornelia Smalla
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.02835/full
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author Tarek R. Elsayed
Tarek R. Elsayed
Samuel Jacquiod
Samuel Jacquiod
Eman H. Nour
Søren J. Sørensen
Kornelia Smalla
author_facet Tarek R. Elsayed
Tarek R. Elsayed
Samuel Jacquiod
Samuel Jacquiod
Eman H. Nour
Søren J. Sørensen
Kornelia Smalla
author_sort Tarek R. Elsayed
collection DOAJ
description Ralstonia solanacearum (biovar2, race3) is the causal agent of bacterial wilt and this quarantine phytopathogen is responsible for massive losses in several commercially important crops. Biological control of this pathogen might become a suitable plant protection measure in areas where R. solanacearum is endemic. Two bacterial strains, Bacillus velezensis (B63) and Pseudomonas fluorescens (P142) with in vitro antagonistic activity toward R. solanacearum (B3B) were tested for rhizosphere competence, efficient biological control of wilt symptoms on greenhouse-grown tomato, and effects on the indigenous rhizosphere prokaryotic communities. The population densities of B3B and the antagonists were estimated in rhizosphere community DNA by selective plating, real-time quantitative PCR, and R. solanacearum-specific fliC PCR-Southern blot hybridization. Moreover, we investigated how the pathogen and/or the antagonists altered the composition of the tomato rhizosphere prokaryotic community by 16S rRNA gene amplicon sequencing. B. velezensis (B63) and P. fluorescens (P142)-inoculated plants showed drastically reduced wilt disease symptoms, accompanied by significantly lower abundance of the B3B population compared to the non-inoculated pathogen control. Pronounced shifts in prokaryotic community compositions were observed in response to the inoculation of B63 or P142 in the presence or absence of the pathogen B3B and numerous dynamic taxa were identified. Confocal laser scanning microscopy (CLSM) visualization of the gfp-tagged antagonist P142 revealed heterogeneous colonization patterns and P142 was detected in lateral roots, root hairs, epidermal cells, and within xylem vessels. Although competitive niche exclusion cannot be excluded, it is more likely that the inoculation of P142 or B63 and the corresponding microbiome shifts primed the plant defense against the pathogen B3B. Both inoculants are promising biological agents for efficient control of R. solanacearum under field conditions.
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spelling doaj.art-63c8b3712b164d6dafa731b4439550fe2022-12-21T18:49:26ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-01-011010.3389/fmicb.2019.02835484496Biocontrol of Bacterial Wilt Disease Through Complex Interaction Between Tomato Plant, Antagonists, the Indigenous Rhizosphere Microbiota, and Ralstonia solanacearumTarek R. Elsayed0Tarek R. Elsayed1Samuel Jacquiod2Samuel Jacquiod3Eman H. Nour4Søren J. Sørensen5Kornelia Smalla6Institute for Epidemiology and Pathogen Diagnostics, Julius Kühn-Institut, Federal Research Centre for Cultivated Plants, Braunschweig, GermanyDepartment of Microbiology, Faculty of Agriculture, Cairo University, Giza, EgyptMarine Microbiological Section, Department of Biology, Faculty of Natural and Life Sciences, University of Copenhagen, Copenhagen, DenmarkAgroécologie, AgroSup Dijon, INRAE, Université Bourgogne, Université Bourgogne Franche-Comté, Dijon, FranceInstitute for Epidemiology and Pathogen Diagnostics, Julius Kühn-Institut, Federal Research Centre for Cultivated Plants, Braunschweig, GermanyMarine Microbiological Section, Department of Biology, Faculty of Natural and Life Sciences, University of Copenhagen, Copenhagen, DenmarkInstitute for Epidemiology and Pathogen Diagnostics, Julius Kühn-Institut, Federal Research Centre for Cultivated Plants, Braunschweig, GermanyRalstonia solanacearum (biovar2, race3) is the causal agent of bacterial wilt and this quarantine phytopathogen is responsible for massive losses in several commercially important crops. Biological control of this pathogen might become a suitable plant protection measure in areas where R. solanacearum is endemic. Two bacterial strains, Bacillus velezensis (B63) and Pseudomonas fluorescens (P142) with in vitro antagonistic activity toward R. solanacearum (B3B) were tested for rhizosphere competence, efficient biological control of wilt symptoms on greenhouse-grown tomato, and effects on the indigenous rhizosphere prokaryotic communities. The population densities of B3B and the antagonists were estimated in rhizosphere community DNA by selective plating, real-time quantitative PCR, and R. solanacearum-specific fliC PCR-Southern blot hybridization. Moreover, we investigated how the pathogen and/or the antagonists altered the composition of the tomato rhizosphere prokaryotic community by 16S rRNA gene amplicon sequencing. B. velezensis (B63) and P. fluorescens (P142)-inoculated plants showed drastically reduced wilt disease symptoms, accompanied by significantly lower abundance of the B3B population compared to the non-inoculated pathogen control. Pronounced shifts in prokaryotic community compositions were observed in response to the inoculation of B63 or P142 in the presence or absence of the pathogen B3B and numerous dynamic taxa were identified. Confocal laser scanning microscopy (CLSM) visualization of the gfp-tagged antagonist P142 revealed heterogeneous colonization patterns and P142 was detected in lateral roots, root hairs, epidermal cells, and within xylem vessels. Although competitive niche exclusion cannot be excluded, it is more likely that the inoculation of P142 or B63 and the corresponding microbiome shifts primed the plant defense against the pathogen B3B. Both inoculants are promising biological agents for efficient control of R. solanacearum under field conditions.https://www.frontiersin.org/article/10.3389/fmicb.2019.02835/fullRalstonia solanacearumbiocontrollatent infectionfliCamplicon sequencing
spellingShingle Tarek R. Elsayed
Tarek R. Elsayed
Samuel Jacquiod
Samuel Jacquiod
Eman H. Nour
Søren J. Sørensen
Kornelia Smalla
Biocontrol of Bacterial Wilt Disease Through Complex Interaction Between Tomato Plant, Antagonists, the Indigenous Rhizosphere Microbiota, and Ralstonia solanacearum
Frontiers in Microbiology
Ralstonia solanacearum
biocontrol
latent infection
fliC
amplicon sequencing
title Biocontrol of Bacterial Wilt Disease Through Complex Interaction Between Tomato Plant, Antagonists, the Indigenous Rhizosphere Microbiota, and Ralstonia solanacearum
title_full Biocontrol of Bacterial Wilt Disease Through Complex Interaction Between Tomato Plant, Antagonists, the Indigenous Rhizosphere Microbiota, and Ralstonia solanacearum
title_fullStr Biocontrol of Bacterial Wilt Disease Through Complex Interaction Between Tomato Plant, Antagonists, the Indigenous Rhizosphere Microbiota, and Ralstonia solanacearum
title_full_unstemmed Biocontrol of Bacterial Wilt Disease Through Complex Interaction Between Tomato Plant, Antagonists, the Indigenous Rhizosphere Microbiota, and Ralstonia solanacearum
title_short Biocontrol of Bacterial Wilt Disease Through Complex Interaction Between Tomato Plant, Antagonists, the Indigenous Rhizosphere Microbiota, and Ralstonia solanacearum
title_sort biocontrol of bacterial wilt disease through complex interaction between tomato plant antagonists the indigenous rhizosphere microbiota and ralstonia solanacearum
topic Ralstonia solanacearum
biocontrol
latent infection
fliC
amplicon sequencing
url https://www.frontiersin.org/article/10.3389/fmicb.2019.02835/full
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