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Localized osmotic stress activates systemic responses to N limitation in Medicago truncatula–Sinorhizobium symbiotic plants

In mature symbiotic root nodules, differentiated rhizobia fix atmospheric dinitrogen and provide ammonium to fulfill the plant nitrogen (N) demand. The plant enables this process by providing photosynthates to the nodules. The symbiosis is adjusted to the whole plant N demand thanks to systemic N si...

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Autores principales: Martin, Marie-Laure, Pervent, Marjorie, Lambert, Ilana, Colella, Stefano, Tancelin, Mathilde, Severac, Dany, Clément, Gilles, Tillard, Pascal, Frugier, Florian, Lepetit, Marc
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10694431/
http://dx.doi.org/10.3389/fpls.2023.1288070
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author Martin, Marie-Laure
Pervent, Marjorie
Lambert, Ilana
Colella, Stefano
Tancelin, Mathilde
Severac, Dany
Clément, Gilles
Tillard, Pascal
Frugier, Florian
Lepetit, Marc
author_facet Martin, Marie-Laure
Pervent, Marjorie
Lambert, Ilana
Colella, Stefano
Tancelin, Mathilde
Severac, Dany
Clément, Gilles
Tillard, Pascal
Frugier, Florian
Lepetit, Marc
author_sort Martin, Marie-Laure
collection PubMed
description In mature symbiotic root nodules, differentiated rhizobia fix atmospheric dinitrogen and provide ammonium to fulfill the plant nitrogen (N) demand. The plant enables this process by providing photosynthates to the nodules. The symbiosis is adjusted to the whole plant N demand thanks to systemic N signaling controlling nodule development. Symbiotic plants under N deficit stimulate nodule expansion and activate nodule senescence under N satiety. Besides, nodules are highly sensitive to drought. Here, we used split-root systems to characterize the systemic responses of symbiotic plants to a localized osmotic stress. We showed that polyéthylène glycol (PEG) application rapidly inhibited the symbiotic dinitrogen fixation activity of nodules locally exposed to the treatment, resulting to the N limitation of the plant supplied exclusively by symbiotic dinitrogen fixation. The localized PEG treatment triggered systemic signaling stimulating nodule development in the distant untreated roots. This response was associated with an enhancement of the sucrose allocation. Our analyses showed that transcriptomic reprogramming associated with PEG and N deficit systemic signaling(s) shared many targets transcripts. Altogether, our study suggests that systemic N signaling is a component of the adaptation of the symbiotic plant to the local variations of its edaphic environment.
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spelling pubmed-106944312023-12-05 Localized osmotic stress activates systemic responses to N limitation in Medicago truncatula–Sinorhizobium symbiotic plants Martin, Marie-Laure Pervent, Marjorie Lambert, Ilana Colella, Stefano Tancelin, Mathilde Severac, Dany Clément, Gilles Tillard, Pascal Frugier, Florian Lepetit, Marc Front Plant Sci Plant Science In mature symbiotic root nodules, differentiated rhizobia fix atmospheric dinitrogen and provide ammonium to fulfill the plant nitrogen (N) demand. The plant enables this process by providing photosynthates to the nodules. The symbiosis is adjusted to the whole plant N demand thanks to systemic N signaling controlling nodule development. Symbiotic plants under N deficit stimulate nodule expansion and activate nodule senescence under N satiety. Besides, nodules are highly sensitive to drought. Here, we used split-root systems to characterize the systemic responses of symbiotic plants to a localized osmotic stress. We showed that polyéthylène glycol (PEG) application rapidly inhibited the symbiotic dinitrogen fixation activity of nodules locally exposed to the treatment, resulting to the N limitation of the plant supplied exclusively by symbiotic dinitrogen fixation. The localized PEG treatment triggered systemic signaling stimulating nodule development in the distant untreated roots. This response was associated with an enhancement of the sucrose allocation. Our analyses showed that transcriptomic reprogramming associated with PEG and N deficit systemic signaling(s) shared many targets transcripts. Altogether, our study suggests that systemic N signaling is a component of the adaptation of the symbiotic plant to the local variations of its edaphic environment. Frontiers Media S.A. 2023-11-20 /pmc/articles/PMC10694431/ http://dx.doi.org/10.3389/fpls.2023.1288070 Text en Copyright © 2023 Martin, Pervent, Lambert, Colella, Tancelin, Severac, Clément, Tillard, Frugier and Lepetit 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 Plant Science
Martin, Marie-Laure
Pervent, Marjorie
Lambert, Ilana
Colella, Stefano
Tancelin, Mathilde
Severac, Dany
Clément, Gilles
Tillard, Pascal
Frugier, Florian
Lepetit, Marc
Localized osmotic stress activates systemic responses to N limitation in Medicago truncatula–Sinorhizobium symbiotic plants
title Localized osmotic stress activates systemic responses to N limitation in Medicago truncatula–Sinorhizobium symbiotic plants
title_full Localized osmotic stress activates systemic responses to N limitation in Medicago truncatula–Sinorhizobium symbiotic plants
title_fullStr Localized osmotic stress activates systemic responses to N limitation in Medicago truncatula–Sinorhizobium symbiotic plants
title_full_unstemmed Localized osmotic stress activates systemic responses to N limitation in Medicago truncatula–Sinorhizobium symbiotic plants
title_short Localized osmotic stress activates systemic responses to N limitation in Medicago truncatula–Sinorhizobium symbiotic plants
title_sort localized osmotic stress activates systemic responses to n limitation in medicago truncatula–sinorhizobium symbiotic plants
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10694431/
http://dx.doi.org/10.3389/fpls.2023.1288070
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