Activation of alternative oxidase ensures carbon supply for ethylene and carotenoid biosynthesis during tomato fruit ripening

[EN] Tomato (Solanum lycopersicum) is a climacteric fruit displaying a respiration peak at the onset of ripening accompanied by increased synthesis of ethylene and carotenoid pigments. Chromoplast and mitochondrial respiration participate at different stages of fruit ripening, but their in vivo regu...

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Autores: Iglesias-Sanchez, Ariadna, Fernandez Del-Saz, Nestor, Ezquerro, Miguel, Feixes-Prats, Elisenda, Ribas-Carbo, Miquel, Fernie, Alisdair R., Florez-Sarasa, Igor, RODRIGUEZ-CONCEPCION, Manuel|||0000-0002-1280-2305
Tipo de recurso: artículo
Fecha de publicación:2025
País:España
Institución:Universitat Politècnica de València (UPV)
Repositorio:RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
Idioma:inglés
OAI Identifier:oai:dnet:riunet______::bd77dc1a2fce18c86ac7f059229aa733
Acceso en línea:https://riunet.upv.es/handle/10251/234941
Access Level:acceso abierto
Palabra clave:Tomato fruit ripening
Alternative oxidase
Chromorespiration
Carotenoid biosynthesis
Climacteric respiration
Ethylene production
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dc.title.none.fl_str_mv Activation of alternative oxidase ensures carbon supply for ethylene and carotenoid biosynthesis during tomato fruit ripening
title Activation of alternative oxidase ensures carbon supply for ethylene and carotenoid biosynthesis during tomato fruit ripening
spellingShingle Activation of alternative oxidase ensures carbon supply for ethylene and carotenoid biosynthesis during tomato fruit ripening
Iglesias-Sanchez, Ariadna
Tomato fruit ripening
Alternative oxidase
Chromorespiration
Carotenoid biosynthesis
Climacteric respiration
Ethylene production
title_short Activation of alternative oxidase ensures carbon supply for ethylene and carotenoid biosynthesis during tomato fruit ripening
title_full Activation of alternative oxidase ensures carbon supply for ethylene and carotenoid biosynthesis during tomato fruit ripening
title_fullStr Activation of alternative oxidase ensures carbon supply for ethylene and carotenoid biosynthesis during tomato fruit ripening
title_full_unstemmed Activation of alternative oxidase ensures carbon supply for ethylene and carotenoid biosynthesis during tomato fruit ripening
title_sort Activation of alternative oxidase ensures carbon supply for ethylene and carotenoid biosynthesis during tomato fruit ripening
dc.creator.none.fl_str_mv Iglesias-Sanchez, Ariadna
Fernandez Del-Saz, Nestor
Ezquerro, Miguel
Feixes-Prats, Elisenda
Ribas-Carbo, Miquel
Fernie, Alisdair R.
Florez-Sarasa, Igor
RODRIGUEZ-CONCEPCION, Manuel|||0000-0002-1280-2305
author Iglesias-Sanchez, Ariadna
author_facet Iglesias-Sanchez, Ariadna
Fernandez Del-Saz, Nestor
Ezquerro, Miguel
Feixes-Prats, Elisenda
Ribas-Carbo, Miquel
Fernie, Alisdair R.
Florez-Sarasa, Igor
RODRIGUEZ-CONCEPCION, Manuel|||0000-0002-1280-2305
author_role author
author2 Fernandez Del-Saz, Nestor
Ezquerro, Miguel
Feixes-Prats, Elisenda
Ribas-Carbo, Miquel
Fernie, Alisdair R.
Florez-Sarasa, Igor
RODRIGUEZ-CONCEPCION, Manuel|||0000-0002-1280-2305
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Instituto Universitario Mixto de Biología Molecular y Celular de Plantas
European Commission
European Social Fund
Generalitat Valenciana
Centres de Recerca de Catalunya
Agencia Estatal de Investigación
European Regional Development Fund
Ministerio de Ciencia e Innovación
Repositorio Institucional de la Universitat Politècnica de València Riunet
dc.subject.none.fl_str_mv Tomato fruit ripening
Alternative oxidase
Chromorespiration
Carotenoid biosynthesis
Climacteric respiration
Ethylene production
topic Tomato fruit ripening
Alternative oxidase
Chromorespiration
Carotenoid biosynthesis
Climacteric respiration
Ethylene production
description [EN] Tomato (Solanum lycopersicum) is a climacteric fruit displaying a respiration peak at the onset of ripening accompanied by increased synthesis of ethylene and carotenoid pigments. Chromoplast and mitochondrial respiration participate at different stages of fruit ripening, but their in vivo regulation and function remain unclear. We determined the in vivo activities of the mitochondrial alternative oxidase (AOX) and cytochrome oxidase pathways and quantified the levels of respiratory- and ripening-related gene transcripts, primary metabolites and carotenoids in ripening tomato fruits with or without functional chromorespiration. Furthermore, we carried out physiological, molecular, and metabolic analyses of CRISPR¿Cas9 mutants defective in AOX1a, the main AOX isoform upregulated during tomato fruit ripening. We confirmed that plastid terminal oxidase-dependent chromorespiration is only relevant at late stages of ripening and found that in vivo AOX activity significantly increased at the breaker stage, becoming the main contributor to climacteric respiration when ripening initiates. This activation did not correlate with gene expression but was likely due to increased levels of AOX activators such as pyruvate (a metabolic precursor of carotenoids), 2-oxoglutarate, and succinate. A strong alteration of ripening-related metabolites was observed in aox1a mutant fruits, highlighting a key role of the AOX pathway at the onset of ripening. Our data suggest that increased supply of tricarboxylic acid cycle intermediates at the climacteric stage allosterically enhances AOX activity, thus allowing the reoxidation of NAD(P)H to ensure carbon supply for triggering ethylene and carotenoid biosynthesis.
publishDate 2025
dc.date.none.fl_str_mv 2025
2025-11-01
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://riunet.upv.es/handle/10251/234941
url https://riunet.upv.es/handle/10251/234941
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.relation.none.fl_str_mv Agencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020 PCI2021-121941 USE OF TOMATO LINES TOLERANT TO PROXIMITY SHADE TO INCREASE YIELD AND QUALITY IN INTERCROPPING AGROSYSTEMS
Agencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020 PID2020-115810GB-I00 MECANISMOS MOLECULARES DE LA BIOGENESIS DE CROMOPLASTOS
Agencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020 PID2020-120229RA-I00 HACIA UNA INGENIERIA DEL METABOLISMO MITOCONDRIAL PARA LA MEJORA DE LA PRODUCTIVIDAD Y CALIDAD DE FRUTOS DE CULTIVOS HORTICOLAS BAJO CONDICIONES DE CAMBIO CLIMATICO
European Commission https://doi.org/10.13039/501100000780 CA22157
Generalitat Valenciana https://doi.org/10.13039/501100003359 AGROALNEXT%2F2022%2F067
Agencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 PID2024-163099NB-I00
Agencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 RED2022-134577-T
Agencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 RED2022-134072-T
Agencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 RYC2019-028030-I
Ministerio de Ciencia e Innovación http://dx.doi.org/10.13039/501100004837 CEX2019-000902-S
Ministerio de Ciencia e Innovación http://dx.doi.org/10.13039/501100004837 PRE2018-083610
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
Reconocimiento (by)
http://creativecommons.org/licenses/by/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
Reconocimiento (by)
http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv American Society of Plant Biologists
publisher.none.fl_str_mv American Society of Plant Biologists
dc.source.none.fl_str_mv reponame:RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
instname:Universitat Politècnica de València (UPV)
instname_str Universitat Politècnica de València (UPV)
reponame_str RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
collection RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling Activation of alternative oxidase ensures carbon supply for ethylene and carotenoid biosynthesis during tomato fruit ripeningIglesias-Sanchez, AriadnaFernandez Del-Saz, NestorEzquerro, MiguelFeixes-Prats, ElisendaRibas-Carbo, MiquelFernie, Alisdair R.Florez-Sarasa, IgorRODRIGUEZ-CONCEPCION, Manuel|||0000-0002-1280-2305Tomato fruit ripeningAlternative oxidaseChromorespirationCarotenoid biosynthesisClimacteric respirationEthylene production[EN] Tomato (Solanum lycopersicum) is a climacteric fruit displaying a respiration peak at the onset of ripening accompanied by increased synthesis of ethylene and carotenoid pigments. Chromoplast and mitochondrial respiration participate at different stages of fruit ripening, but their in vivo regulation and function remain unclear. We determined the in vivo activities of the mitochondrial alternative oxidase (AOX) and cytochrome oxidase pathways and quantified the levels of respiratory- and ripening-related gene transcripts, primary metabolites and carotenoids in ripening tomato fruits with or without functional chromorespiration. Furthermore, we carried out physiological, molecular, and metabolic analyses of CRISPR¿Cas9 mutants defective in AOX1a, the main AOX isoform upregulated during tomato fruit ripening. We confirmed that plastid terminal oxidase-dependent chromorespiration is only relevant at late stages of ripening and found that in vivo AOX activity significantly increased at the breaker stage, becoming the main contributor to climacteric respiration when ripening initiates. This activation did not correlate with gene expression but was likely due to increased levels of AOX activators such as pyruvate (a metabolic precursor of carotenoids), 2-oxoglutarate, and succinate. A strong alteration of ripening-related metabolites was observed in aox1a mutant fruits, highlighting a key role of the AOX pathway at the onset of ripening. Our data suggest that increased supply of tricarboxylic acid cycle intermediates at the climacteric stage allosterically enhances AOX activity, thus allowing the reoxidation of NAD(P)H to ensure carbon supply for triggering ethylene and carotenoid biosynthesis.This work was supported by grants PID2020-115810GB-I00 to M.R.-Co., PID2020-120229RA-I00 and PID2024-163099NB-I00 to I.F.-S., all funded by MICIU/AEI/10.13039/501100011033 and by "ERDF/EU," Ministerio de Ciencia, Innovacion y Universidades-Agencia Estatal de Investigacion (MCIU/AEI, Spain). We also thank the support of grants RECROP-CA22157 (European Cooperation in Science and Technology COST Actions), CaRed-RED2022-134577-T funded by MICIU/AEI/10.13039/501100011033 (MCIU/AEI, Spain), UToPIQ-PCI2021-121941 funded by MICIU/AEI/10.13039/501100011033 and by the "European Union NextGenerationEU/PRTR" (MCIU/AEI/PRIMA, Spain), and BioVal+-AGROALNEXT/2022/067 (Generalitat Valenciana) to M.R.-Co.; RedoxPlant-RED2022-134072-T funded by MICIU/AEI/10.13039/501100011033 (MCIU/AEI, Spain) to I.F.-S.; and CEX2019-000902-S funded by MCIU/AEI/10.13039/501100011033 and CERCA Programme (Generalitat de Catalunya) to CRAG. A.I.-S. received a predoctoral fellowship (PRE2018-083610) funded by MICIU/AEI/10.13039/501100011033 and by "ESF Investing in your future." I.F.-S. received funding from the "Ramon y Cajal" contract RYC2019-028030-I funded by MCIU/AEI/10.13039/501100011033 and by "ESF Investing in your future."American Society of Plant BiologistsInstituto Universitario Mixto de Biología Molecular y Celular de PlantasEuropean CommissionEuropean Social FundGeneralitat ValencianaCentres de Recerca de CatalunyaAgencia Estatal de InvestigaciónEuropean Regional Development FundMinisterio de Ciencia e InnovaciónRepositorio Institucional de la Universitat Politècnica de València Riunet20252025-11-01journal articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://riunet.upv.es/handle/10251/234941reponame:RiuNet. Repositorio Institucional de la Universitat Politécnica de Valénciainstname:Universitat Politècnica de València (UPV)InglésengAgencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020 PCI2021-121941 USE OF TOMATO LINES TOLERANT TO PROXIMITY SHADE TO INCREASE YIELD AND QUALITY IN INTERCROPPING AGROSYSTEMSAgencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020 PID2020-115810GB-I00 MECANISMOS MOLECULARES DE LA BIOGENESIS DE CROMOPLASTOSAgencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020 PID2020-120229RA-I00 HACIA UNA INGENIERIA DEL METABOLISMO MITOCONDRIAL PARA LA MEJORA DE LA PRODUCTIVIDAD Y CALIDAD DE FRUTOS DE CULTIVOS HORTICOLAS BAJO CONDICIONES DE CAMBIO CLIMATICOEuropean Commission https://doi.org/10.13039/501100000780 CA22157Generalitat Valenciana https://doi.org/10.13039/501100003359 AGROALNEXT%2F2022%2F067Agencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 PID2024-163099NB-I00Agencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 RED2022-134577-TAgencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 RED2022-134072-TAgencia Estatal de Investigación http://dx.doi.org/10.13039/501100011033 RYC2019-028030-IMinisterio de Ciencia e Innovación http://dx.doi.org/10.13039/501100004837 CEX2019-000902-SMinisterio de Ciencia e Innovación http://dx.doi.org/10.13039/501100004837 PRE2018-083610open accesshttp://purl.org/coar/access_right/c_abf2Reconocimiento (by)http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:dnet:riunet______::bd77dc1a2fce18c86ac7f059229aa7332026-06-13T07:49:27Z
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