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Leaf nodule endosymbiotic Burkholderia confer targeted allelopathy to their Psychotria hosts

After a century of investigations, the function of the obligate betaproteobacterial endosymbionts accommodated in leaf nodules of tropical Rubiaceae remained enigmatic. We report that the α-d-glucose analogue (+)-streptol, systemically supplied by mature Ca. Burkholderia kirkii nodules to their Psyc...

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Autores principales: Georgiou, Antri, Sieber, Simon, Hsiao, Chien-Chi, Grayfer, Tatyana, Gorenflos López, Jacob L., Gademann, Karl, Eberl, Leo, Bailly, Aurélien
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8599487/
https://www.ncbi.nlm.nih.gov/pubmed/34789815
http://dx.doi.org/10.1038/s41598-021-01867-2
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author Georgiou, Antri
Sieber, Simon
Hsiao, Chien-Chi
Grayfer, Tatyana
Gorenflos López, Jacob L.
Gademann, Karl
Eberl, Leo
Bailly, Aurélien
author_facet Georgiou, Antri
Sieber, Simon
Hsiao, Chien-Chi
Grayfer, Tatyana
Gorenflos López, Jacob L.
Gademann, Karl
Eberl, Leo
Bailly, Aurélien
author_sort Georgiou, Antri
collection PubMed
description After a century of investigations, the function of the obligate betaproteobacterial endosymbionts accommodated in leaf nodules of tropical Rubiaceae remained enigmatic. We report that the α-d-glucose analogue (+)-streptol, systemically supplied by mature Ca. Burkholderia kirkii nodules to their Psychotria hosts, exhibits potent and selective root growth inhibiting activity. We provide compelling evidence that (+)-streptol specifically affects meristematic root cells transitioning to anisotropic elongation by disrupting cell wall organization in a mechanism of action that is distinct from canonical cellulose biosynthesis inhibitors. We observed no inhibitory or cytotoxic effects on organisms other than seed plants, further suggesting (+)-streptol as a bona fide allelochemical. We propose that the suppression of growth of plant competitors is a major driver of the formation and maintenance of the Psychotria–Burkholderia association. In addition to potential agricultural applications as a herbicidal agent, (+)-streptol might also prove useful to dissect plant cell and organ growth processes.
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spelling pubmed-85994872021-11-19 Leaf nodule endosymbiotic Burkholderia confer targeted allelopathy to their Psychotria hosts Georgiou, Antri Sieber, Simon Hsiao, Chien-Chi Grayfer, Tatyana Gorenflos López, Jacob L. Gademann, Karl Eberl, Leo Bailly, Aurélien Sci Rep Article After a century of investigations, the function of the obligate betaproteobacterial endosymbionts accommodated in leaf nodules of tropical Rubiaceae remained enigmatic. We report that the α-d-glucose analogue (+)-streptol, systemically supplied by mature Ca. Burkholderia kirkii nodules to their Psychotria hosts, exhibits potent and selective root growth inhibiting activity. We provide compelling evidence that (+)-streptol specifically affects meristematic root cells transitioning to anisotropic elongation by disrupting cell wall organization in a mechanism of action that is distinct from canonical cellulose biosynthesis inhibitors. We observed no inhibitory or cytotoxic effects on organisms other than seed plants, further suggesting (+)-streptol as a bona fide allelochemical. We propose that the suppression of growth of plant competitors is a major driver of the formation and maintenance of the Psychotria–Burkholderia association. In addition to potential agricultural applications as a herbicidal agent, (+)-streptol might also prove useful to dissect plant cell and organ growth processes. Nature Publishing Group UK 2021-11-17 /pmc/articles/PMC8599487/ /pubmed/34789815 http://dx.doi.org/10.1038/s41598-021-01867-2 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 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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Georgiou, Antri
Sieber, Simon
Hsiao, Chien-Chi
Grayfer, Tatyana
Gorenflos López, Jacob L.
Gademann, Karl
Eberl, Leo
Bailly, Aurélien
Leaf nodule endosymbiotic Burkholderia confer targeted allelopathy to their Psychotria hosts
title Leaf nodule endosymbiotic Burkholderia confer targeted allelopathy to their Psychotria hosts
title_full Leaf nodule endosymbiotic Burkholderia confer targeted allelopathy to their Psychotria hosts
title_fullStr Leaf nodule endosymbiotic Burkholderia confer targeted allelopathy to their Psychotria hosts
title_full_unstemmed Leaf nodule endosymbiotic Burkholderia confer targeted allelopathy to their Psychotria hosts
title_short Leaf nodule endosymbiotic Burkholderia confer targeted allelopathy to their Psychotria hosts
title_sort leaf nodule endosymbiotic burkholderia confer targeted allelopathy to their psychotria hosts
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8599487/
https://www.ncbi.nlm.nih.gov/pubmed/34789815
http://dx.doi.org/10.1038/s41598-021-01867-2
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