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Impact of root-associated strains of three Paraburkholderia species on primary and secondary metabolism of Brassica oleracea

Several root-colonizing bacterial species can simultaneously promote plant growth and induce systemic resistance. How these rhizobacteria modulate plant metabolism to accommodate the carbon and energy demand from these two competing processes is largely unknown. Here, we show that strains of three P...

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Autores principales: Jeon, Je-Seung, Carreno-Quintero, Natalia, van Eekelen, Henriëtte D. L. M., De Vos, Ric C. H., Raaijmakers, Jos M., Etalo, Desalegn W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7854645/
https://www.ncbi.nlm.nih.gov/pubmed/33531553
http://dx.doi.org/10.1038/s41598-021-82238-9
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author Jeon, Je-Seung
Carreno-Quintero, Natalia
van Eekelen, Henriëtte D. L. M.
De Vos, Ric C. H.
Raaijmakers, Jos M.
Etalo, Desalegn W.
author_facet Jeon, Je-Seung
Carreno-Quintero, Natalia
van Eekelen, Henriëtte D. L. M.
De Vos, Ric C. H.
Raaijmakers, Jos M.
Etalo, Desalegn W.
author_sort Jeon, Je-Seung
collection PubMed
description Several root-colonizing bacterial species can simultaneously promote plant growth and induce systemic resistance. How these rhizobacteria modulate plant metabolism to accommodate the carbon and energy demand from these two competing processes is largely unknown. Here, we show that strains of three Paraburkholderia species, P. graminis PHS1 (Pbg), P. hospita mHSR1 (Pbh), and P. terricola mHS1 (Pbt), upon colonization of the roots of two Broccoli cultivars led to cultivar-dependent increases in biomass, changes in primary and secondary metabolism and induced resistance against the bacterial leaf pathogen Xanthomonas campestris. Strains that promoted growth led to greater accumulation of soluble sugars in the shoot and particularly fructose levels showed an increase of up to 280-fold relative to the non-treated control plants. Similarly, a number of secondary metabolites constituting chemical and structural defense, including flavonoids, hydroxycinnamates, stilbenoids, coumarins and lignins, showed greater accumulation while other resource-competing metabolite pathways were depleted. High soluble sugar generation, efficient sugar utilization, and suppression or remobilization of resource-competing metabolites potentially contributed to curb the tradeoff between the carbon and energy demanding processes induced by Paraburkholderia-Broccoli interaction. Collectively, our results provide a comprehensive and integrated view of the temporal changes in plant metabolome associated with rhizobacteria-mediated plant growth promotion and induced resistance.
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spelling pubmed-78546452021-02-03 Impact of root-associated strains of three Paraburkholderia species on primary and secondary metabolism of Brassica oleracea Jeon, Je-Seung Carreno-Quintero, Natalia van Eekelen, Henriëtte D. L. M. De Vos, Ric C. H. Raaijmakers, Jos M. Etalo, Desalegn W. Sci Rep Article Several root-colonizing bacterial species can simultaneously promote plant growth and induce systemic resistance. How these rhizobacteria modulate plant metabolism to accommodate the carbon and energy demand from these two competing processes is largely unknown. Here, we show that strains of three Paraburkholderia species, P. graminis PHS1 (Pbg), P. hospita mHSR1 (Pbh), and P. terricola mHS1 (Pbt), upon colonization of the roots of two Broccoli cultivars led to cultivar-dependent increases in biomass, changes in primary and secondary metabolism and induced resistance against the bacterial leaf pathogen Xanthomonas campestris. Strains that promoted growth led to greater accumulation of soluble sugars in the shoot and particularly fructose levels showed an increase of up to 280-fold relative to the non-treated control plants. Similarly, a number of secondary metabolites constituting chemical and structural defense, including flavonoids, hydroxycinnamates, stilbenoids, coumarins and lignins, showed greater accumulation while other resource-competing metabolite pathways were depleted. High soluble sugar generation, efficient sugar utilization, and suppression or remobilization of resource-competing metabolites potentially contributed to curb the tradeoff between the carbon and energy demanding processes induced by Paraburkholderia-Broccoli interaction. Collectively, our results provide a comprehensive and integrated view of the temporal changes in plant metabolome associated with rhizobacteria-mediated plant growth promotion and induced resistance. Nature Publishing Group UK 2021-02-02 /pmc/articles/PMC7854645/ /pubmed/33531553 http://dx.doi.org/10.1038/s41598-021-82238-9 Text en © The Author(s) 2021 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Jeon, Je-Seung
Carreno-Quintero, Natalia
van Eekelen, Henriëtte D. L. M.
De Vos, Ric C. H.
Raaijmakers, Jos M.
Etalo, Desalegn W.
Impact of root-associated strains of three Paraburkholderia species on primary and secondary metabolism of Brassica oleracea
title Impact of root-associated strains of three Paraburkholderia species on primary and secondary metabolism of Brassica oleracea
title_full Impact of root-associated strains of three Paraburkholderia species on primary and secondary metabolism of Brassica oleracea
title_fullStr Impact of root-associated strains of three Paraburkholderia species on primary and secondary metabolism of Brassica oleracea
title_full_unstemmed Impact of root-associated strains of three Paraburkholderia species on primary and secondary metabolism of Brassica oleracea
title_short Impact of root-associated strains of three Paraburkholderia species on primary and secondary metabolism of Brassica oleracea
title_sort impact of root-associated strains of three paraburkholderia species on primary and secondary metabolism of brassica oleracea
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7854645/
https://www.ncbi.nlm.nih.gov/pubmed/33531553
http://dx.doi.org/10.1038/s41598-021-82238-9
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