PHYTOCHROME‐INTERACTING FACTOR 3 mediates light‐dependent induction of tocopherol biosynthesis during tomato fruit ripening

• Published in: Plant, cell and environment Vol. 42; no. 4; pp. 1328 - 1339
• Main Authors: Gramegna, Giovanna, Rosado, Daniele, Sánchez Carranza, Ana Paula, Cruz, Aline Bertinatto, Simon‐Moya, Miguel, Llorente, Briardo, Rodríguez‐Concepcíon, Manuel, Freschi, Luciano, Rossi, Magdalena
• Format: Journal Article
• Language: English
• Published: United States Wiley Subscription Services, Inc 01.04.2019
• Subjects: Antioxidants; Biosynthesis; Chromatin Immunoprecipitation; Derepression; Fruit - growth & development; Fruit - metabolism; Fruits; Gene expression; Gene Expression Regulation, Plant - radiation effects; Gene regulation; geranylgeranyl diphosphate reductase; Light; Lycopersicon esculentum - growth & development; Lycopersicon esculentum - metabolism; Lycopersicon esculentum - radiation effects; Metabolic Networks and Pathways; Metabolism; methylerythritol 4‐phosphate pathway; Nutrients; Nutritive value; Oxidative stress; Photosynthesis; Photosynthetic apparatus; Phytochromes; phytochrome‐interacting factor; Plant Proteins - metabolism; Plant Proteins - physiology; Plastids; Precursors; Reductase; Regulatory mechanisms (biology); Ripening; Solanum lycopersicum; Tocopherol; Tocopherols; Tocopherols - metabolism; Tomatoes; Transcription; Transcription Factors - metabolism; Transcription Factors - physiology; Transcriptome; Vitamin E; tocopherol; geranylgeranyl diphosphate reductase; methylerythritol 4-phosphate pathway; light; phytochrome-interacting factor; Solanum lycopersicum
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.13467

Tocopherols are important antioxidants exclusively produced in plastids that protect the photosynthetic apparatus from oxidative stress. These compounds with vitamin E activity are also essential dietary nutrients for humans. Although the tocopherol biosynthetic pathway has been elucidated, the mechanisms that regulate tocopherol production and accumulation remain elusive. Here, we investigated the regulatory mechanism underlying tocopherol biosynthesis during ripening in tomato fruits, which are an important source of vitamin E. Our results show that ripening under light conditions increases tocopherol fruit content in a phytochrome‐dependent manner by the transcriptional regulation of biosynthetic genes. Moreover, we show that light‐controlled expression of the GERANYLGERANYL DIPHOSPHATE REDUCTASE (SlGGDR) gene, responsible for the synthesis of the central tocopherol precursor phytyl diphosphate, is mediated by PHYTOCHROME‐INTERACTING FACTOR 3 (SlPIF3). In the absence of light, SlPIF3 physically interacts with the promoter of SlGGDR, down‐regulating its expression. By contrast, light activation of phytochromes prevents the interaction between SlPIF3 and the SlGGDR promoter, leading to transcriptional derepression and higher availability of the PDP precursor for tocopherol biosynthesis. The unraveled mechanism provides a new strategy to manipulate fruit metabolism towards improving tomato nutritional quality. In this study, we demonstrated that SlPIF3 represses phytyl diphosphate de novo production in a PHY‐dependent manner, regulating the accumulation of vitamin E during fruit ripening in Solanum lycopersicum.