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Engineering banana endosphere microbiome to improve Fusarium wilt resistance in banana

BACKGROUND: Plant microbiome highlights the importance of endosphere microbiome for growth and health of the host plant. Microbial community analysis represents an elegant way to identify keystone microbial species that have a more central position in the community. The aim of this study was to acce...

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Autores principales: Liu, Yupei, Zhu, Aiping, Tan, Hongming, Cao, Lixiang, Zhang, Renduo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6521393/
https://www.ncbi.nlm.nih.gov/pubmed/31092296
http://dx.doi.org/10.1186/s40168-019-0690-x
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author Liu, Yupei
Zhu, Aiping
Tan, Hongming
Cao, Lixiang
Zhang, Renduo
author_facet Liu, Yupei
Zhu, Aiping
Tan, Hongming
Cao, Lixiang
Zhang, Renduo
author_sort Liu, Yupei
collection PubMed
description BACKGROUND: Plant microbiome highlights the importance of endosphere microbiome for growth and health of the host plant. Microbial community analysis represents an elegant way to identify keystone microbial species that have a more central position in the community. The aim of this study was to access the interactions between the keystone bacterial species and plants during banana Fusarium wilt process, by comparing the endophytic bacterial and fungal community in banana roots and shoot tips during growth and wilting processes. The keystone bacterial species were isolated and further engineered to improve banana wilt resistance. RESULTS: Banana endosphere microbiome structure varied during plant growth and wilting processes. Bacterial and fungal diversity in the shoot tips and roots increased with the development of the banana plantlets. The bacterial groups belonging to the Enterobacteriaceae family with different relative abundances were detected in all the samples. The Klebsiella spp. might be the keystone bacteria during the growth of banana plantlets. The relative abundance of Fusarium associated with the wilt disease did not increase during the wilting process. The endophytic Enterobacteriaceae strains Enterobacter sp. E5, Kosakonia sp. S1, and Klebsiella sp. Kb were isolated on Enterobacteriaceae selective medium and further engineered by expressing 1-aminocyclopropane-1-carboxylate (ACC) deaminase on the bacterial cell walls (designated as E5P, S1P, and KbP, respectively). Pot experiments suggested that plants inoculated with strains E5, E5P, S1, and S1P increased resistance to the Fusarium wilt disease compared with the controls without inoculation, whereas the Klebsiella inoculation (Kb and KbP) did not increase the wilt resistance. Compared with the inoculation with the wild strains E5 and S1, the inoculation with engineered strains E5P and S1P significantly increased wilt resistance and promoted plant growth, respectively. The results illustrated that the keystone species in the banana microbiome may not be dominant in numbers and the functional role of keystone species should be involved in the wilt resistance. CONCLUSION: The ACC deaminase activity of engineered bacteria was essential to the Fusarium wilt resistance and growth promotion of banana plants. Engineering keystone bacteria in plant microbiome with ACC deaminase on the cell walls should be a promising method to improve plant growth and disease resistance. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0690-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-65213932019-05-23 Engineering banana endosphere microbiome to improve Fusarium wilt resistance in banana Liu, Yupei Zhu, Aiping Tan, Hongming Cao, Lixiang Zhang, Renduo Microbiome Research BACKGROUND: Plant microbiome highlights the importance of endosphere microbiome for growth and health of the host plant. Microbial community analysis represents an elegant way to identify keystone microbial species that have a more central position in the community. The aim of this study was to access the interactions between the keystone bacterial species and plants during banana Fusarium wilt process, by comparing the endophytic bacterial and fungal community in banana roots and shoot tips during growth and wilting processes. The keystone bacterial species were isolated and further engineered to improve banana wilt resistance. RESULTS: Banana endosphere microbiome structure varied during plant growth and wilting processes. Bacterial and fungal diversity in the shoot tips and roots increased with the development of the banana plantlets. The bacterial groups belonging to the Enterobacteriaceae family with different relative abundances were detected in all the samples. The Klebsiella spp. might be the keystone bacteria during the growth of banana plantlets. The relative abundance of Fusarium associated with the wilt disease did not increase during the wilting process. The endophytic Enterobacteriaceae strains Enterobacter sp. E5, Kosakonia sp. S1, and Klebsiella sp. Kb were isolated on Enterobacteriaceae selective medium and further engineered by expressing 1-aminocyclopropane-1-carboxylate (ACC) deaminase on the bacterial cell walls (designated as E5P, S1P, and KbP, respectively). Pot experiments suggested that plants inoculated with strains E5, E5P, S1, and S1P increased resistance to the Fusarium wilt disease compared with the controls without inoculation, whereas the Klebsiella inoculation (Kb and KbP) did not increase the wilt resistance. Compared with the inoculation with the wild strains E5 and S1, the inoculation with engineered strains E5P and S1P significantly increased wilt resistance and promoted plant growth, respectively. The results illustrated that the keystone species in the banana microbiome may not be dominant in numbers and the functional role of keystone species should be involved in the wilt resistance. CONCLUSION: The ACC deaminase activity of engineered bacteria was essential to the Fusarium wilt resistance and growth promotion of banana plants. Engineering keystone bacteria in plant microbiome with ACC deaminase on the cell walls should be a promising method to improve plant growth and disease resistance. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0690-x) contains supplementary material, which is available to authorized users. BioMed Central 2019-05-15 /pmc/articles/PMC6521393/ /pubmed/31092296 http://dx.doi.org/10.1186/s40168-019-0690-x Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Liu, Yupei
Zhu, Aiping
Tan, Hongming
Cao, Lixiang
Zhang, Renduo
Engineering banana endosphere microbiome to improve Fusarium wilt resistance in banana
title Engineering banana endosphere microbiome to improve Fusarium wilt resistance in banana
title_full Engineering banana endosphere microbiome to improve Fusarium wilt resistance in banana
title_fullStr Engineering banana endosphere microbiome to improve Fusarium wilt resistance in banana
title_full_unstemmed Engineering banana endosphere microbiome to improve Fusarium wilt resistance in banana
title_short Engineering banana endosphere microbiome to improve Fusarium wilt resistance in banana
title_sort engineering banana endosphere microbiome to improve fusarium wilt resistance in banana
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6521393/
https://www.ncbi.nlm.nih.gov/pubmed/31092296
http://dx.doi.org/10.1186/s40168-019-0690-x
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