Autophagy Controls Sulphur Metabolism in the Rosette Leaves of Arabidopsis and Facilitates S Remobilization to the Seeds

Sulphur deficiency in crops became an agricultural concern several decades ago, due to the decrease of S deposition and the atmospheric sulphur dioxide emissions released by industrial plants. Autophagy, which is a conserved mechanism for nutrient recycling in eukaryotes, is involved in nitrogen, ir...

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Main Authors: Aurélia Lornac, Marien Havé, Fabien Chardon, Fabienne Soulay, Gilles Clément, Jean-Christophe Avice, Céline Masclaux-Daubresse
Format: Article
Language:English
Published: MDPI AG 2020-01-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/9/2/332
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author Aurélia Lornac
Marien Havé
Fabien Chardon
Fabienne Soulay
Gilles Clément
Jean-Christophe Avice
Céline Masclaux-Daubresse
author_facet Aurélia Lornac
Marien Havé
Fabien Chardon
Fabienne Soulay
Gilles Clément
Jean-Christophe Avice
Céline Masclaux-Daubresse
author_sort Aurélia Lornac
collection DOAJ
description Sulphur deficiency in crops became an agricultural concern several decades ago, due to the decrease of S deposition and the atmospheric sulphur dioxide emissions released by industrial plants. Autophagy, which is a conserved mechanism for nutrient recycling in eukaryotes, is involved in nitrogen, iron, zinc and manganese remobilizations from the rosette to the seeds in <i>Arabidopsis thaliana</i>. Here, we have compared the role of autophagy in sulphur and nitrogen management at the whole plant level, performing concurrent labelling with <sup>34</sup>S and <sup>15</sup>N isotopes on <i>atg5</i> mutants and control lines. We show that both <sup>34</sup>S and <sup>15</sup>N remobilizations from the rosette to the seeds are impaired in the <i>atg5</i> mutants irrespective of salicylic acid accumulation and of sulphur nutrition. The comparison in each genotype of the partitions of <sup>15</sup>N and <sup>34</sup>S in the seeds (as % of the whole plant) indicates that the remobilization of <sup>34</sup>S to the seeds was twice more efficient than that of <sup>15</sup>N in both autophagy mutants and control lines under high S conditions, and also in control lines under low S conditions. This was different in the autophagy mutants grown under low S conditions. Under low S, the partition of <sup>34</sup>S to their seeds was indeed not twice as high but similar to that of <sup>15</sup>N. Such discrepancy shows that when sulphate availability is scarce, autophagy mutants display stronger defects for <sup>34</sup>S remobilization relative to <sup>15</sup>N remobilization than under high S conditions. It suggests, moreover, that autophagy mainly affects the transport of N-poor S-containing molecules and possibly sulphate.
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spelling doaj.art-287cfb1483094279adfa825013f55b2a2023-08-02T01:13:06ZengMDPI AGCells2073-44092020-01-019233210.3390/cells9020332cells9020332Autophagy Controls Sulphur Metabolism in the Rosette Leaves of Arabidopsis and Facilitates S Remobilization to the SeedsAurélia Lornac0Marien Havé1Fabien Chardon2Fabienne Soulay3Gilles Clément4Jean-Christophe Avice5Céline Masclaux-Daubresse6UCBN, UMR INRA–UCBN 950 Ecophysiologie Végétale &amp;, Agronomie &amp; Nutritions N.C.S., SFR Normandie Végétal (FED 4277), Normandie Université, F-14032 Caen, 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, FranceInstitut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, FranceUCBN, UMR INRA–UCBN 950 Ecophysiologie Végétale &amp;, Agronomie &amp; Nutritions N.C.S., SFR Normandie Végétal (FED 4277), Normandie Université, F-14032 Caen, FranceInstitut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, 78000 Versailles, FranceSulphur deficiency in crops became an agricultural concern several decades ago, due to the decrease of S deposition and the atmospheric sulphur dioxide emissions released by industrial plants. Autophagy, which is a conserved mechanism for nutrient recycling in eukaryotes, is involved in nitrogen, iron, zinc and manganese remobilizations from the rosette to the seeds in <i>Arabidopsis thaliana</i>. Here, we have compared the role of autophagy in sulphur and nitrogen management at the whole plant level, performing concurrent labelling with <sup>34</sup>S and <sup>15</sup>N isotopes on <i>atg5</i> mutants and control lines. We show that both <sup>34</sup>S and <sup>15</sup>N remobilizations from the rosette to the seeds are impaired in the <i>atg5</i> mutants irrespective of salicylic acid accumulation and of sulphur nutrition. The comparison in each genotype of the partitions of <sup>15</sup>N and <sup>34</sup>S in the seeds (as % of the whole plant) indicates that the remobilization of <sup>34</sup>S to the seeds was twice more efficient than that of <sup>15</sup>N in both autophagy mutants and control lines under high S conditions, and also in control lines under low S conditions. This was different in the autophagy mutants grown under low S conditions. Under low S, the partition of <sup>34</sup>S to their seeds was indeed not twice as high but similar to that of <sup>15</sup>N. Such discrepancy shows that when sulphate availability is scarce, autophagy mutants display stronger defects for <sup>34</sup>S remobilization relative to <sup>15</sup>N remobilization than under high S conditions. It suggests, moreover, that autophagy mainly affects the transport of N-poor S-containing molecules and possibly sulphate.https://www.mdpi.com/2073-4409/9/2/332sulphateleaf senescenceseed fillingnitrogen use efficiencysulphur use efficiencyresource allocation
spellingShingle Aurélia Lornac
Marien Havé
Fabien Chardon
Fabienne Soulay
Gilles Clément
Jean-Christophe Avice
Céline Masclaux-Daubresse
Autophagy Controls Sulphur Metabolism in the Rosette Leaves of Arabidopsis and Facilitates S Remobilization to the Seeds
Cells
sulphate
leaf senescence
seed filling
nitrogen use efficiency
sulphur use efficiency
resource allocation
title Autophagy Controls Sulphur Metabolism in the Rosette Leaves of Arabidopsis and Facilitates S Remobilization to the Seeds
title_full Autophagy Controls Sulphur Metabolism in the Rosette Leaves of Arabidopsis and Facilitates S Remobilization to the Seeds
title_fullStr Autophagy Controls Sulphur Metabolism in the Rosette Leaves of Arabidopsis and Facilitates S Remobilization to the Seeds
title_full_unstemmed Autophagy Controls Sulphur Metabolism in the Rosette Leaves of Arabidopsis and Facilitates S Remobilization to the Seeds
title_short Autophagy Controls Sulphur Metabolism in the Rosette Leaves of Arabidopsis and Facilitates S Remobilization to the Seeds
title_sort autophagy controls sulphur metabolism in the rosette leaves of arabidopsis and facilitates s remobilization to the seeds
topic sulphate
leaf senescence
seed filling
nitrogen use efficiency
sulphur use efficiency
resource allocation
url https://www.mdpi.com/2073-4409/9/2/332
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