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Combined Allosteric Responses Explain the Bifurcation in Non-Linear Dynamics of (15)N Root Fluxes Under Nutritional Steady-State Conditions for Nitrate

With regard to thermodynamics out of equilibrium, seedlings are open systems that dissipate energy towards their environment. Accordingly, under nutritional steady-state conditions, changes in external concentrations of one single ion provokes instability and reorganization in the metabolic and stru...

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Autores principales: Le Deunff, Erwan, Beauclair, Patrick, Lecourt, Julien, Deleu, Carole, Malagoli, Philippe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7770280/
https://www.ncbi.nlm.nih.gov/pubmed/33384698
http://dx.doi.org/10.3389/fpls.2020.01253
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author Le Deunff, Erwan
Beauclair, Patrick
Lecourt, Julien
Deleu, Carole
Malagoli, Philippe
author_facet Le Deunff, Erwan
Beauclair, Patrick
Lecourt, Julien
Deleu, Carole
Malagoli, Philippe
author_sort Le Deunff, Erwan
collection PubMed
description With regard to thermodynamics out of equilibrium, seedlings are open systems that dissipate energy towards their environment. Accordingly, under nutritional steady-state conditions, changes in external concentrations of one single ion provokes instability and reorganization in the metabolic and structure/architecture of the seedling that is more favorable to the fluxes of energy and matter. This reorganization is called a bifurcation and is described in mathematics as a non-linear dynamic system. In this study, we investigate the non-linear dynamics of (15)N fluxes among cellular compartments of B. napus seedlings in response to a wide range of external [Formula: see text] concentrations (from 0.05 to 20 mM): this allows to determine whether any stationary states and bifurcations could be found. The biphasic behavior of the root [Formula: see text] uptake rate (v(in)) was explained by the combined cooperative properties between the v(app) (N uptake, storage and assimilation rate) and v(out) (N translocation rate) (15)N fluxes that revealed a unique and stable stationary state around 0.28 mM nitrate. The disappearance of this stationary state around 0.5 mM external nitrate concentrations provokes a dramatic bifurcation in (15)N flux pattern. This bifurcation in the v(in) and v(out) (15)N fluxes fits better with the increase of BnNPF6.3/NRT1.1 expression than BnNRT2.1 nitrate transporter genes, confirming the allosteric property of the BnNPF6/NRT1.1 transporter, as reported in the literature between low and high nitrate concentrations. Moreover, several statistically significant power-law equations were found between variations in the shoots tryptophan concentrations (i.e., IAA precursor) with changes in the v(app) and v(out) (15)N fluxes as well as a synthetic parameter of plant N status estimated from the root/shoot ratio of total free amino acids concentrations. These relationships designate IAA as one of the major biological parameters related to metabolic and structural-morphological reorganization coupled with the N and water fluxes induced by nitrate. The results seriously challenge the scientific grounds of the concept of high- and low-affinity of nitrate transporters and are therefore discussed in terms of the ecological significance and physiological implications on the basis of recent agronomic, physiological and molecular data of the literature.
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spelling pubmed-77702802020-12-30 Combined Allosteric Responses Explain the Bifurcation in Non-Linear Dynamics of (15)N Root Fluxes Under Nutritional Steady-State Conditions for Nitrate Le Deunff, Erwan Beauclair, Patrick Lecourt, Julien Deleu, Carole Malagoli, Philippe Front Plant Sci Plant Science With regard to thermodynamics out of equilibrium, seedlings are open systems that dissipate energy towards their environment. Accordingly, under nutritional steady-state conditions, changes in external concentrations of one single ion provokes instability and reorganization in the metabolic and structure/architecture of the seedling that is more favorable to the fluxes of energy and matter. This reorganization is called a bifurcation and is described in mathematics as a non-linear dynamic system. In this study, we investigate the non-linear dynamics of (15)N fluxes among cellular compartments of B. napus seedlings in response to a wide range of external [Formula: see text] concentrations (from 0.05 to 20 mM): this allows to determine whether any stationary states and bifurcations could be found. The biphasic behavior of the root [Formula: see text] uptake rate (v(in)) was explained by the combined cooperative properties between the v(app) (N uptake, storage and assimilation rate) and v(out) (N translocation rate) (15)N fluxes that revealed a unique and stable stationary state around 0.28 mM nitrate. The disappearance of this stationary state around 0.5 mM external nitrate concentrations provokes a dramatic bifurcation in (15)N flux pattern. This bifurcation in the v(in) and v(out) (15)N fluxes fits better with the increase of BnNPF6.3/NRT1.1 expression than BnNRT2.1 nitrate transporter genes, confirming the allosteric property of the BnNPF6/NRT1.1 transporter, as reported in the literature between low and high nitrate concentrations. Moreover, several statistically significant power-law equations were found between variations in the shoots tryptophan concentrations (i.e., IAA precursor) with changes in the v(app) and v(out) (15)N fluxes as well as a synthetic parameter of plant N status estimated from the root/shoot ratio of total free amino acids concentrations. These relationships designate IAA as one of the major biological parameters related to metabolic and structural-morphological reorganization coupled with the N and water fluxes induced by nitrate. The results seriously challenge the scientific grounds of the concept of high- and low-affinity of nitrate transporters and are therefore discussed in terms of the ecological significance and physiological implications on the basis of recent agronomic, physiological and molecular data of the literature. Frontiers Media S.A. 2020-08-28 /pmc/articles/PMC7770280/ /pubmed/33384698 http://dx.doi.org/10.3389/fpls.2020.01253 Text en Copyright © 2020 Le Deunff, Beauclair, Lecourt, Deleu and Malagoli http://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
Le Deunff, Erwan
Beauclair, Patrick
Lecourt, Julien
Deleu, Carole
Malagoli, Philippe
Combined Allosteric Responses Explain the Bifurcation in Non-Linear Dynamics of (15)N Root Fluxes Under Nutritional Steady-State Conditions for Nitrate
title Combined Allosteric Responses Explain the Bifurcation in Non-Linear Dynamics of (15)N Root Fluxes Under Nutritional Steady-State Conditions for Nitrate
title_full Combined Allosteric Responses Explain the Bifurcation in Non-Linear Dynamics of (15)N Root Fluxes Under Nutritional Steady-State Conditions for Nitrate
title_fullStr Combined Allosteric Responses Explain the Bifurcation in Non-Linear Dynamics of (15)N Root Fluxes Under Nutritional Steady-State Conditions for Nitrate
title_full_unstemmed Combined Allosteric Responses Explain the Bifurcation in Non-Linear Dynamics of (15)N Root Fluxes Under Nutritional Steady-State Conditions for Nitrate
title_short Combined Allosteric Responses Explain the Bifurcation in Non-Linear Dynamics of (15)N Root Fluxes Under Nutritional Steady-State Conditions for Nitrate
title_sort combined allosteric responses explain the bifurcation in non-linear dynamics of (15)n root fluxes under nutritional steady-state conditions for nitrate
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7770280/
https://www.ncbi.nlm.nih.gov/pubmed/33384698
http://dx.doi.org/10.3389/fpls.2020.01253
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