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Sucrose triggers a novel signaling cascade promoting Bacillus subtilis rhizosphere colonization

Beneficial rhizobacteria promote plant growth and protect plants against phytopathogens. Effective colonization on plant roots is critical for the rhizobacteria to exert beneficial activities. How bacteria migrate swiftly in the soil of semisolid or solid nature remains unclear. Here we report that...

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Autores principales: Tian, Tao, Sun, Bingbing, Shi, Haowen, Gao, Tantan, He, Yinghao, Li, Yan, Liu, Yixue, Li, Xuexian, Zhang, Liqun, Li, Shidong, Wang, Qi, Chai, Yunrong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8397739/
https://www.ncbi.nlm.nih.gov/pubmed/33772107
http://dx.doi.org/10.1038/s41396-021-00966-2
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author Tian, Tao
Sun, Bingbing
Shi, Haowen
Gao, Tantan
He, Yinghao
Li, Yan
Liu, Yixue
Li, Xuexian
Zhang, Liqun
Li, Shidong
Wang, Qi
Chai, Yunrong
author_facet Tian, Tao
Sun, Bingbing
Shi, Haowen
Gao, Tantan
He, Yinghao
Li, Yan
Liu, Yixue
Li, Xuexian
Zhang, Liqun
Li, Shidong
Wang, Qi
Chai, Yunrong
author_sort Tian, Tao
collection PubMed
description Beneficial rhizobacteria promote plant growth and protect plants against phytopathogens. Effective colonization on plant roots is critical for the rhizobacteria to exert beneficial activities. How bacteria migrate swiftly in the soil of semisolid or solid nature remains unclear. Here we report that sucrose, a disaccharide ubiquitously deployed by photosynthetic plants for fixed carbon transport and storage, and abundantly secreted from plant roots, promotes solid surface motility (SSM) and root colonization by Bacillus subtilis through a previously uncharacterized mechanism. Sucrose induces robust SSM by triggering a signaling cascade, first through extracellular synthesis of polymeric levan, which in turn stimulates strong production of surfactin and hyper-flagellation of the cells. B. subtilis poorly colonizes the roots of Arabidopsis thaliana mutants deficient in root-exudation of sucrose, while exogenously added sucrose selectively shapes the rhizomicrobiome associated with the tomato plant roots, promoting specifically bacilli and pseudomonad. We propose that sucrose activates a signaling cascade to trigger SSM and promote rhizosphere colonization by B. subtilis. Our findings also suggest a practicable approach to boost prevalence of beneficial Bacillus species in plant protection.
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spelling pubmed-83977392021-09-15 Sucrose triggers a novel signaling cascade promoting Bacillus subtilis rhizosphere colonization Tian, Tao Sun, Bingbing Shi, Haowen Gao, Tantan He, Yinghao Li, Yan Liu, Yixue Li, Xuexian Zhang, Liqun Li, Shidong Wang, Qi Chai, Yunrong ISME J Article Beneficial rhizobacteria promote plant growth and protect plants against phytopathogens. Effective colonization on plant roots is critical for the rhizobacteria to exert beneficial activities. How bacteria migrate swiftly in the soil of semisolid or solid nature remains unclear. Here we report that sucrose, a disaccharide ubiquitously deployed by photosynthetic plants for fixed carbon transport and storage, and abundantly secreted from plant roots, promotes solid surface motility (SSM) and root colonization by Bacillus subtilis through a previously uncharacterized mechanism. Sucrose induces robust SSM by triggering a signaling cascade, first through extracellular synthesis of polymeric levan, which in turn stimulates strong production of surfactin and hyper-flagellation of the cells. B. subtilis poorly colonizes the roots of Arabidopsis thaliana mutants deficient in root-exudation of sucrose, while exogenously added sucrose selectively shapes the rhizomicrobiome associated with the tomato plant roots, promoting specifically bacilli and pseudomonad. We propose that sucrose activates a signaling cascade to trigger SSM and promote rhizosphere colonization by B. subtilis. Our findings also suggest a practicable approach to boost prevalence of beneficial Bacillus species in plant protection. Nature Publishing Group UK 2021-03-26 2021-09 /pmc/articles/PMC8397739/ /pubmed/33772107 http://dx.doi.org/10.1038/s41396-021-00966-2 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Tian, Tao
Sun, Bingbing
Shi, Haowen
Gao, Tantan
He, Yinghao
Li, Yan
Liu, Yixue
Li, Xuexian
Zhang, Liqun
Li, Shidong
Wang, Qi
Chai, Yunrong
Sucrose triggers a novel signaling cascade promoting Bacillus subtilis rhizosphere colonization
title Sucrose triggers a novel signaling cascade promoting Bacillus subtilis rhizosphere colonization
title_full Sucrose triggers a novel signaling cascade promoting Bacillus subtilis rhizosphere colonization
title_fullStr Sucrose triggers a novel signaling cascade promoting Bacillus subtilis rhizosphere colonization
title_full_unstemmed Sucrose triggers a novel signaling cascade promoting Bacillus subtilis rhizosphere colonization
title_short Sucrose triggers a novel signaling cascade promoting Bacillus subtilis rhizosphere colonization
title_sort sucrose triggers a novel signaling cascade promoting bacillus subtilis rhizosphere colonization
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8397739/
https://www.ncbi.nlm.nih.gov/pubmed/33772107
http://dx.doi.org/10.1038/s41396-021-00966-2
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