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Central Metabolism Is Tuned to the Availability of Oxygen in Developing Melon Fruit

Respiration of bulky plant organs such as fleshy fruits depends on oxygen (O(2)) availability and often decreases with O(2) concentration to avoid anoxia, but the relationship between O(2) diffusional resistance and metabolic adjustments remains unclear. Melon fruit (Cucumis melo L.) was used to stu...

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Autores principales: Mori, Kentaro, Beauvoit, Bertrand P., Biais, Benoît, Chabane, Maxime, Allwood, J. William, Deborde, Catherine, Maucourt, Mickaël, Goodacre, Royston, Cabasson, Cécile, Moing, Annick, Rolin, Dominique, Gibon, Yves
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6529934/
https://www.ncbi.nlm.nih.gov/pubmed/31156666
http://dx.doi.org/10.3389/fpls.2019.00594
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author Mori, Kentaro
Beauvoit, Bertrand P.
Biais, Benoît
Chabane, Maxime
Allwood, J. William
Deborde, Catherine
Maucourt, Mickaël
Goodacre, Royston
Cabasson, Cécile
Moing, Annick
Rolin, Dominique
Gibon, Yves
author_facet Mori, Kentaro
Beauvoit, Bertrand P.
Biais, Benoît
Chabane, Maxime
Allwood, J. William
Deborde, Catherine
Maucourt, Mickaël
Goodacre, Royston
Cabasson, Cécile
Moing, Annick
Rolin, Dominique
Gibon, Yves
author_sort Mori, Kentaro
collection PubMed
description Respiration of bulky plant organs such as fleshy fruits depends on oxygen (O(2)) availability and often decreases with O(2) concentration to avoid anoxia, but the relationship between O(2) diffusional resistance and metabolic adjustments remains unclear. Melon fruit (Cucumis melo L.) was used to study relationships between O(2) availability and metabolism in fleshy fruits. Enzyme activities, primary metabolites and O(2) partial pressure were quantified from the periphery to the inner fruit mesocarp, at three stages of development. Hypoxia was gradually established during fruit development, but there was no strong oxygen gradient between the outer- and the inner mesocarp. These trends were confirmed by a mathematical modeling approach combining O(2) diffusion equations and O(2) demand estimates of the mesocarp tissue. A multivariate analysis of metabolites, enzyme activities, O(2) demand and concentration reveals that metabolite gradients and enzyme capacities observed in melon fruits reflect continuous metabolic adjustments thus ensuring a timely maturation of the mesocarp. The present results suggest that the metabolic adjustments, especially the tuning of the capacity of cytochrome c oxidase (COX) to O(2)-availability that occurs during growth development, contribute to optimizing the O(2)-demand and avoiding the establishment of an O(2) gradient within the flesh.
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spelling pubmed-65299342019-05-31 Central Metabolism Is Tuned to the Availability of Oxygen in Developing Melon Fruit Mori, Kentaro Beauvoit, Bertrand P. Biais, Benoît Chabane, Maxime Allwood, J. William Deborde, Catherine Maucourt, Mickaël Goodacre, Royston Cabasson, Cécile Moing, Annick Rolin, Dominique Gibon, Yves Front Plant Sci Plant Science Respiration of bulky plant organs such as fleshy fruits depends on oxygen (O(2)) availability and often decreases with O(2) concentration to avoid anoxia, but the relationship between O(2) diffusional resistance and metabolic adjustments remains unclear. Melon fruit (Cucumis melo L.) was used to study relationships between O(2) availability and metabolism in fleshy fruits. Enzyme activities, primary metabolites and O(2) partial pressure were quantified from the periphery to the inner fruit mesocarp, at three stages of development. Hypoxia was gradually established during fruit development, but there was no strong oxygen gradient between the outer- and the inner mesocarp. These trends were confirmed by a mathematical modeling approach combining O(2) diffusion equations and O(2) demand estimates of the mesocarp tissue. A multivariate analysis of metabolites, enzyme activities, O(2) demand and concentration reveals that metabolite gradients and enzyme capacities observed in melon fruits reflect continuous metabolic adjustments thus ensuring a timely maturation of the mesocarp. The present results suggest that the metabolic adjustments, especially the tuning of the capacity of cytochrome c oxidase (COX) to O(2)-availability that occurs during growth development, contribute to optimizing the O(2)-demand and avoiding the establishment of an O(2) gradient within the flesh. Frontiers Media S.A. 2019-05-15 /pmc/articles/PMC6529934/ /pubmed/31156666 http://dx.doi.org/10.3389/fpls.2019.00594 Text en Copyright © 2019 Mori, Beauvoit, Biais, Chabane, Allwood, Deborde, Maucourt, Goodacre, Cabasson, Moing, Rolin and Gibon. 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
Mori, Kentaro
Beauvoit, Bertrand P.
Biais, Benoît
Chabane, Maxime
Allwood, J. William
Deborde, Catherine
Maucourt, Mickaël
Goodacre, Royston
Cabasson, Cécile
Moing, Annick
Rolin, Dominique
Gibon, Yves
Central Metabolism Is Tuned to the Availability of Oxygen in Developing Melon Fruit
title Central Metabolism Is Tuned to the Availability of Oxygen in Developing Melon Fruit
title_full Central Metabolism Is Tuned to the Availability of Oxygen in Developing Melon Fruit
title_fullStr Central Metabolism Is Tuned to the Availability of Oxygen in Developing Melon Fruit
title_full_unstemmed Central Metabolism Is Tuned to the Availability of Oxygen in Developing Melon Fruit
title_short Central Metabolism Is Tuned to the Availability of Oxygen in Developing Melon Fruit
title_sort central metabolism is tuned to the availability of oxygen in developing melon fruit
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6529934/
https://www.ncbi.nlm.nih.gov/pubmed/31156666
http://dx.doi.org/10.3389/fpls.2019.00594
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