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Regulation of Pyridine Nucleotide Metabolism During Tomato Fruit Development Through Transcript and Protein Profiling

Central metabolism is the engine of plant biomass, supplying fruit growth with building blocks, energy, and biochemical cofactors. Among metabolic cornerstones, nicotinamide adenine dinucleotide (NAD) is particularly pivotal for electron transfer through reduction–oxidation (redox) reactions, thus p...

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Autores principales: Decros, Guillaume, Beauvoit, Bertrand, Colombié, Sophie, Cabasson, Cécile, Bernillon, Stéphane, Arrivault, Stéphanie, Guenther, Manuela, Belouah, Isma, Prigent, Sylvain, Baldet, Pierre, Gibon, Yves, Pétriacq, Pierre
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6798084/
https://www.ncbi.nlm.nih.gov/pubmed/31681351
http://dx.doi.org/10.3389/fpls.2019.01201
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author Decros, Guillaume
Beauvoit, Bertrand
Colombié, Sophie
Cabasson, Cécile
Bernillon, Stéphane
Arrivault, Stéphanie
Guenther, Manuela
Belouah, Isma
Prigent, Sylvain
Baldet, Pierre
Gibon, Yves
Pétriacq, Pierre
author_facet Decros, Guillaume
Beauvoit, Bertrand
Colombié, Sophie
Cabasson, Cécile
Bernillon, Stéphane
Arrivault, Stéphanie
Guenther, Manuela
Belouah, Isma
Prigent, Sylvain
Baldet, Pierre
Gibon, Yves
Pétriacq, Pierre
author_sort Decros, Guillaume
collection PubMed
description Central metabolism is the engine of plant biomass, supplying fruit growth with building blocks, energy, and biochemical cofactors. Among metabolic cornerstones, nicotinamide adenine dinucleotide (NAD) is particularly pivotal for electron transfer through reduction–oxidation (redox) reactions, thus participating in a myriad of biochemical processes. Besides redox functions, NAD is now assumed to act as an integral regulator of signaling cascades involved in growth and environmental responses. However, the regulation of NAD metabolism and signaling during fruit development remains poorly studied and understood. Here, we benefit from RNAseq and proteomic data obtained from nine growth stages of tomato fruit (var. Moneymaker) to dissect mRNA and protein profiles that link to NAD metabolism, including de novo biosynthesis, recycling, utilization, and putative transport. As expected for a cofactor synthesis pathway, protein profiles failed to detect enzymes involved in NAD synthesis or utilization, except for nicotinic acid phosphoribosyltransferase (NaPT) and nicotinamidase (NIC), which suggested that most NAD metabolic enzymes were poorly represented quantitatively. Further investigations on transcript data unveiled differential expression patterns during fruit development. Interestingly, among specific NAD metabolism-related genes, early de novo biosynthetic genes were transcriptionally induced in very young fruits, in association with NAD kinase, while later stages of fruit growth rather showed an accumulation of transcripts involved in later stages of de novo synthesis and in NAD recycling, which agreed with augmented NAD(P) levels. In addition, a more global overview of 119 mRNA and 78 protein significant markers for NAD(P)-dependent enzymes revealed differential patterns during tomato growth that evidenced clear regulations of primary metabolism, notably with respect to mitochondrial functions. Overall, we propose that NAD metabolism and signaling are very dynamic in the developing tomato fruit and that its differential regulation is certainly critical to fuel central metabolism linking to growth mechanisms.
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spelling pubmed-67980842019-11-01 Regulation of Pyridine Nucleotide Metabolism During Tomato Fruit Development Through Transcript and Protein Profiling Decros, Guillaume Beauvoit, Bertrand Colombié, Sophie Cabasson, Cécile Bernillon, Stéphane Arrivault, Stéphanie Guenther, Manuela Belouah, Isma Prigent, Sylvain Baldet, Pierre Gibon, Yves Pétriacq, Pierre Front Plant Sci Plant Science Central metabolism is the engine of plant biomass, supplying fruit growth with building blocks, energy, and biochemical cofactors. Among metabolic cornerstones, nicotinamide adenine dinucleotide (NAD) is particularly pivotal for electron transfer through reduction–oxidation (redox) reactions, thus participating in a myriad of biochemical processes. Besides redox functions, NAD is now assumed to act as an integral regulator of signaling cascades involved in growth and environmental responses. However, the regulation of NAD metabolism and signaling during fruit development remains poorly studied and understood. Here, we benefit from RNAseq and proteomic data obtained from nine growth stages of tomato fruit (var. Moneymaker) to dissect mRNA and protein profiles that link to NAD metabolism, including de novo biosynthesis, recycling, utilization, and putative transport. As expected for a cofactor synthesis pathway, protein profiles failed to detect enzymes involved in NAD synthesis or utilization, except for nicotinic acid phosphoribosyltransferase (NaPT) and nicotinamidase (NIC), which suggested that most NAD metabolic enzymes were poorly represented quantitatively. Further investigations on transcript data unveiled differential expression patterns during fruit development. Interestingly, among specific NAD metabolism-related genes, early de novo biosynthetic genes were transcriptionally induced in very young fruits, in association with NAD kinase, while later stages of fruit growth rather showed an accumulation of transcripts involved in later stages of de novo synthesis and in NAD recycling, which agreed with augmented NAD(P) levels. In addition, a more global overview of 119 mRNA and 78 protein significant markers for NAD(P)-dependent enzymes revealed differential patterns during tomato growth that evidenced clear regulations of primary metabolism, notably with respect to mitochondrial functions. Overall, we propose that NAD metabolism and signaling are very dynamic in the developing tomato fruit and that its differential regulation is certainly critical to fuel central metabolism linking to growth mechanisms. Frontiers Media S.A. 2019-10-11 /pmc/articles/PMC6798084/ /pubmed/31681351 http://dx.doi.org/10.3389/fpls.2019.01201 Text en Copyright © 2019 Decros, Beauvoit, Colombié, Cabasson, Bernillon, Arrivault, Guenther, Belouah, Prigent, Baldet, Gibon and Pétriacq 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
Decros, Guillaume
Beauvoit, Bertrand
Colombié, Sophie
Cabasson, Cécile
Bernillon, Stéphane
Arrivault, Stéphanie
Guenther, Manuela
Belouah, Isma
Prigent, Sylvain
Baldet, Pierre
Gibon, Yves
Pétriacq, Pierre
Regulation of Pyridine Nucleotide Metabolism During Tomato Fruit Development Through Transcript and Protein Profiling
title Regulation of Pyridine Nucleotide Metabolism During Tomato Fruit Development Through Transcript and Protein Profiling
title_full Regulation of Pyridine Nucleotide Metabolism During Tomato Fruit Development Through Transcript and Protein Profiling
title_fullStr Regulation of Pyridine Nucleotide Metabolism During Tomato Fruit Development Through Transcript and Protein Profiling
title_full_unstemmed Regulation of Pyridine Nucleotide Metabolism During Tomato Fruit Development Through Transcript and Protein Profiling
title_short Regulation of Pyridine Nucleotide Metabolism During Tomato Fruit Development Through Transcript and Protein Profiling
title_sort regulation of pyridine nucleotide metabolism during tomato fruit development through transcript and protein profiling
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6798084/
https://www.ncbi.nlm.nih.gov/pubmed/31681351
http://dx.doi.org/10.3389/fpls.2019.01201
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