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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Detalles Bibliográficos
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
Descripción
Sumario:[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.