Leaf nodule endosymbiotic Burkholderia confer targeted allelopathy to their Psychotria hosts

Abstract 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 t...

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Main Authors: Antri Georgiou, Simon Sieber, Chien-Chi Hsiao, Tatyana Grayfer, Jacob L. Gorenflos López, Karl Gademann, Leo Eberl, Aurélien Bailly
Format: Article
Language:English
Published: Nature Portfolio 2021-11-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-01867-2
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author Antri Georgiou
Simon Sieber
Chien-Chi Hsiao
Tatyana Grayfer
Jacob L. Gorenflos López
Karl Gademann
Leo Eberl
Aurélien Bailly
author_facet Antri Georgiou
Simon Sieber
Chien-Chi Hsiao
Tatyana Grayfer
Jacob L. Gorenflos López
Karl Gademann
Leo Eberl
Aurélien Bailly
author_sort Antri Georgiou
collection DOAJ
description Abstract 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 doaj.art-fa73c84b271f49648365643bfb0333952022-12-21T23:08:13ZengNature PortfolioScientific Reports2045-23222021-11-0111111510.1038/s41598-021-01867-2Leaf nodule endosymbiotic Burkholderia confer targeted allelopathy to their Psychotria hostsAntri Georgiou0Simon Sieber1Chien-Chi Hsiao2Tatyana Grayfer3Jacob L. Gorenflos López4Karl Gademann5Leo Eberl6Aurélien Bailly7Institute of Plant and Microbial Biology, University of ZürichDepartment of Chemistry, University of ZürichDepartment of Chemistry, University of ZürichDepartment of Chemistry, University of ZürichDepartment of Chemistry, University of ZürichDepartment of Chemistry, University of ZürichInstitute of Plant and Microbial Biology, University of ZürichInstitute of Plant and Microbial Biology, University of ZürichAbstract 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.https://doi.org/10.1038/s41598-021-01867-2
spellingShingle Antri Georgiou
Simon Sieber
Chien-Chi Hsiao
Tatyana Grayfer
Jacob L. Gorenflos López
Karl Gademann
Leo Eberl
Aurélien Bailly
Leaf nodule endosymbiotic Burkholderia confer targeted allelopathy to their Psychotria hosts
Scientific Reports
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
url https://doi.org/10.1038/s41598-021-01867-2
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