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Transcriptional dynamics of Chitinophaga sp. strain R-73072-mediated alkannin/shikonin biosynthesis in Lithospermum officinale

Plants are colonized by a wide range of bacteria, several of which are known to confer benefits to their hosts such as enhancing plant growth and the biosynthesis of secondary metabolites (SMs). Recently, it has been shown that Chitinophaga sp. strain R-73072 enhances the production of alkannin/shik...

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Autores principales: Ahmad, Muhammad, Varela Alonso, Alicia, Koletti, Antigoni E., Assimopoulou, Andreana N., Declerck, Stéphane, Schneider, Carolin, Molin, Eva M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9441710/
https://www.ncbi.nlm.nih.gov/pubmed/36071973
http://dx.doi.org/10.3389/fmicb.2022.978021
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author Ahmad, Muhammad
Varela Alonso, Alicia
Koletti, Antigoni E.
Assimopoulou, Andreana N.
Declerck, Stéphane
Schneider, Carolin
Molin, Eva M.
author_facet Ahmad, Muhammad
Varela Alonso, Alicia
Koletti, Antigoni E.
Assimopoulou, Andreana N.
Declerck, Stéphane
Schneider, Carolin
Molin, Eva M.
author_sort Ahmad, Muhammad
collection PubMed
description Plants are colonized by a wide range of bacteria, several of which are known to confer benefits to their hosts such as enhancing plant growth and the biosynthesis of secondary metabolites (SMs). Recently, it has been shown that Chitinophaga sp. strain R-73072 enhances the production of alkannin/shikonin, SMs of pharmaceutical and ecological importance. However, the mechanisms by which this bacterial strain increases these SMs in plants are not yet understood. To gain insight into these mechanisms, we analyzed the molecular responses of Lithospermum officinale, an alkannin/shikonin producing member of Boraginaceae, to inoculation with R-73072 in a gnotobiotic system using comparative transcriptomics and targeted metabolite profiling of root samples. We found that R-73072 modulated the expression of 1,328 genes, of which the majority appeared to be involved in plant defense and SMs biosynthesis including alkannin/shikonin derivatives. Importantly, bacterial inoculation induced the expression of genes that predominately participate in jasmonate and ethylene biosynthesis and signaling, suggesting an important role of these phytohormones in R-73072-mediated alkannin/shikonin biosynthesis. A detached leaf bioassay further showed that R-73072 confers systemic protection against Botrytis cinerea. Finally, R-73072-mediated coregulation of genes involved in plant defense and the enhanced production of alkannin/shikonin esters further suggest that these SMs could be important components of the plant defense machinery in alkannin/shikonin producing species.
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spelling pubmed-94417102022-09-06 Transcriptional dynamics of Chitinophaga sp. strain R-73072-mediated alkannin/shikonin biosynthesis in Lithospermum officinale Ahmad, Muhammad Varela Alonso, Alicia Koletti, Antigoni E. Assimopoulou, Andreana N. Declerck, Stéphane Schneider, Carolin Molin, Eva M. Front Microbiol Microbiology Plants are colonized by a wide range of bacteria, several of which are known to confer benefits to their hosts such as enhancing plant growth and the biosynthesis of secondary metabolites (SMs). Recently, it has been shown that Chitinophaga sp. strain R-73072 enhances the production of alkannin/shikonin, SMs of pharmaceutical and ecological importance. However, the mechanisms by which this bacterial strain increases these SMs in plants are not yet understood. To gain insight into these mechanisms, we analyzed the molecular responses of Lithospermum officinale, an alkannin/shikonin producing member of Boraginaceae, to inoculation with R-73072 in a gnotobiotic system using comparative transcriptomics and targeted metabolite profiling of root samples. We found that R-73072 modulated the expression of 1,328 genes, of which the majority appeared to be involved in plant defense and SMs biosynthesis including alkannin/shikonin derivatives. Importantly, bacterial inoculation induced the expression of genes that predominately participate in jasmonate and ethylene biosynthesis and signaling, suggesting an important role of these phytohormones in R-73072-mediated alkannin/shikonin biosynthesis. A detached leaf bioassay further showed that R-73072 confers systemic protection against Botrytis cinerea. Finally, R-73072-mediated coregulation of genes involved in plant defense and the enhanced production of alkannin/shikonin esters further suggest that these SMs could be important components of the plant defense machinery in alkannin/shikonin producing species. Frontiers Media S.A. 2022-08-22 /pmc/articles/PMC9441710/ /pubmed/36071973 http://dx.doi.org/10.3389/fmicb.2022.978021 Text en Copyright © 2022 Ahmad, Varela Alonso, Koletti, Assimopoulou, Declerck, Schneider and Molin. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Ahmad, Muhammad
Varela Alonso, Alicia
Koletti, Antigoni E.
Assimopoulou, Andreana N.
Declerck, Stéphane
Schneider, Carolin
Molin, Eva M.
Transcriptional dynamics of Chitinophaga sp. strain R-73072-mediated alkannin/shikonin biosynthesis in Lithospermum officinale
title Transcriptional dynamics of Chitinophaga sp. strain R-73072-mediated alkannin/shikonin biosynthesis in Lithospermum officinale
title_full Transcriptional dynamics of Chitinophaga sp. strain R-73072-mediated alkannin/shikonin biosynthesis in Lithospermum officinale
title_fullStr Transcriptional dynamics of Chitinophaga sp. strain R-73072-mediated alkannin/shikonin biosynthesis in Lithospermum officinale
title_full_unstemmed Transcriptional dynamics of Chitinophaga sp. strain R-73072-mediated alkannin/shikonin biosynthesis in Lithospermum officinale
title_short Transcriptional dynamics of Chitinophaga sp. strain R-73072-mediated alkannin/shikonin biosynthesis in Lithospermum officinale
title_sort transcriptional dynamics of chitinophaga sp. strain r-73072-mediated alkannin/shikonin biosynthesis in lithospermum officinale
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9441710/
https://www.ncbi.nlm.nih.gov/pubmed/36071973
http://dx.doi.org/10.3389/fmicb.2022.978021
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