The Consequences of a Disruption in Cyto-Nuclear Coadaptation on the Molecular Response to a Nitrate Starvation in Arabidopsis

Mitochondria and chloroplasts are important actors in the plant nutritional efficiency. So, it could be expected that a disruption of the coadaptation between nuclear and organellar genomes impact plant response to nutrient stresses. We addressed this issue using two <i>Arabidopsis</i> a...

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Main Authors: Fabien Chardon, Gwendal Cueff, Etienne Delannoy, Fabien Aubé, Aurélia Lornac, Magali Bedu, Françoise Gilard, Stéphanie Pateyron, Hélène Rogniaux, Audrey Gargaros, Hakim Mireau, Loïc Rajjou, Marie-Laure Martin-Magniette, Françoise Budar
Format: Article
Language:English
Published: MDPI AG 2020-05-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/9/5/573
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author Fabien Chardon
Gwendal Cueff
Etienne Delannoy
Fabien Aubé
Aurélia Lornac
Magali Bedu
Françoise Gilard
Stéphanie Pateyron
Hélène Rogniaux
Audrey Gargaros
Hakim Mireau
Loïc Rajjou
Marie-Laure Martin-Magniette
Françoise Budar
author_facet Fabien Chardon
Gwendal Cueff
Etienne Delannoy
Fabien Aubé
Aurélia Lornac
Magali Bedu
Françoise Gilard
Stéphanie Pateyron
Hélène Rogniaux
Audrey Gargaros
Hakim Mireau
Loïc Rajjou
Marie-Laure Martin-Magniette
Françoise Budar
author_sort Fabien Chardon
collection DOAJ
description Mitochondria and chloroplasts are important actors in the plant nutritional efficiency. So, it could be expected that a disruption of the coadaptation between nuclear and organellar genomes impact plant response to nutrient stresses. We addressed this issue using two <i>Arabidopsis</i> accessions, namely <i>Ct-1</i> and <i>Jea</i>, and their reciprocal cytolines possessing the nuclear genome from one parent and the organellar genomes of the other one. We measured gene expression, and quantified proteins and metabolites under N starvation and non-limiting conditions. We observed a typical response to N starvation at the phenotype and molecular levels. The phenotypical response to N starvation was similar in the cytolines compared to the parents. However, we observed an effect of the disruption of genomic coadaptation at the molecular levels, distinct from the previously described responses to organellar stresses. Strikingly, genes differentially expressed in cytolines compared to parents were mainly repressed in the cytolines. These genes encoded more mitochondrial and nuclear proteins than randomly expected, while N starvation responsive ones were enriched in genes for chloroplast and nuclear proteins. In cytolines, the non-coadapted cytonuclear genomic combination tends to modulate the response to N starvation observed in the parental lines on various biological processes.
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spelling doaj.art-2aa9d94c85414131b0c800f509a770ad2023-11-19T23:13:19ZengMDPI AGPlants2223-77472020-05-019557310.3390/plants9050573The Consequences of a Disruption in Cyto-Nuclear Coadaptation on the Molecular Response to a Nitrate Starvation in ArabidopsisFabien Chardon0Gwendal Cueff1Etienne Delannoy2Fabien Aubé3Aurélia Lornac4Magali Bedu5Françoise Gilard6Stéphanie Pateyron7Hélène Rogniaux8Audrey Gargaros9Hakim Mireau10Loïc Rajjou11Marie-Laure Martin-Magniette12Françoise Budar13Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, FranceInstitut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, FranceInstitute of Plant Sciences Paris-Saclay (IPS2), Université Paris-Saclay, CNRS, INRAE, Univ Evry, 91405 Orsay, FranceInstitut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, FranceInstitut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, FranceInstitut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, FranceInstitute of Plant Sciences Paris-Saclay (IPS2), Université Paris-Saclay, CNRS, INRAE, Univ Evry, 91405 Orsay, FranceInstitute of Plant Sciences Paris-Saclay (IPS2), Université Paris-Saclay, CNRS, INRAE, Univ Evry, 91405 Orsay, FranceINRAE, UR BIA, F-44316 Nantes, FranceINRAE, UR BIA, F-44316 Nantes, FranceInstitut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, FranceInstitut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, FranceInstitute of Plant Sciences Paris-Saclay (IPS2), Université Paris-Saclay, CNRS, INRAE, Univ Evry, 91405 Orsay, FranceInstitut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, FranceMitochondria and chloroplasts are important actors in the plant nutritional efficiency. So, it could be expected that a disruption of the coadaptation between nuclear and organellar genomes impact plant response to nutrient stresses. We addressed this issue using two <i>Arabidopsis</i> accessions, namely <i>Ct-1</i> and <i>Jea</i>, and their reciprocal cytolines possessing the nuclear genome from one parent and the organellar genomes of the other one. We measured gene expression, and quantified proteins and metabolites under N starvation and non-limiting conditions. We observed a typical response to N starvation at the phenotype and molecular levels. The phenotypical response to N starvation was similar in the cytolines compared to the parents. However, we observed an effect of the disruption of genomic coadaptation at the molecular levels, distinct from the previously described responses to organellar stresses. Strikingly, genes differentially expressed in cytolines compared to parents were mainly repressed in the cytolines. These genes encoded more mitochondrial and nuclear proteins than randomly expected, while N starvation responsive ones were enriched in genes for chloroplast and nuclear proteins. In cytolines, the non-coadapted cytonuclear genomic combination tends to modulate the response to N starvation observed in the parental lines on various biological processes.https://www.mdpi.com/2223-7747/9/5/573nutrient stressnatural variationcytonuclear co adaptationtranscriptomeproteomemetabolome
spellingShingle Fabien Chardon
Gwendal Cueff
Etienne Delannoy
Fabien Aubé
Aurélia Lornac
Magali Bedu
Françoise Gilard
Stéphanie Pateyron
Hélène Rogniaux
Audrey Gargaros
Hakim Mireau
Loïc Rajjou
Marie-Laure Martin-Magniette
Françoise Budar
The Consequences of a Disruption in Cyto-Nuclear Coadaptation on the Molecular Response to a Nitrate Starvation in Arabidopsis
Plants
nutrient stress
natural variation
cytonuclear co adaptation
transcriptome
proteome
metabolome
title The Consequences of a Disruption in Cyto-Nuclear Coadaptation on the Molecular Response to a Nitrate Starvation in Arabidopsis
title_full The Consequences of a Disruption in Cyto-Nuclear Coadaptation on the Molecular Response to a Nitrate Starvation in Arabidopsis
title_fullStr The Consequences of a Disruption in Cyto-Nuclear Coadaptation on the Molecular Response to a Nitrate Starvation in Arabidopsis
title_full_unstemmed The Consequences of a Disruption in Cyto-Nuclear Coadaptation on the Molecular Response to a Nitrate Starvation in Arabidopsis
title_short The Consequences of a Disruption in Cyto-Nuclear Coadaptation on the Molecular Response to a Nitrate Starvation in Arabidopsis
title_sort consequences of a disruption in cyto nuclear coadaptation on the molecular response to a nitrate starvation in arabidopsis
topic nutrient stress
natural variation
cytonuclear co adaptation
transcriptome
proteome
metabolome
url https://www.mdpi.com/2223-7747/9/5/573
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