Natural occurring epialleles determine vitamin E accumulation in tomato fruits

Vitamin E (VTE) content is a low heritability nutritional trait for which the genetic determinants are poorly understood. Here, we focus on a previously detected major tomato VTE quantitative trait loci (QTL; mQTL9-2-6) and identify the causal gene as one encoding a 2-methyl-6-phytylquinol methyltransferase (namely VTE3(1)) that catalyses one of the final steps in the biosynthesis of γ- and α-tocopherols, which are the main forms of VTE. By reverse genetic approaches, expression analyses, siRNA profiling and DNA methylation assays, we demonstrate that mQTL9-2-6 is an expression QTL associated with differential methylation of a SINE retrotransposon located in the promoter region of VTE3(1). Promoter DNA methylation can be spontaneously reverted leading to different epialleles affecting VTE3(1) expression and VTE content in fruits. These findings indicate therefore that naturally occurring epialleles are responsible for regulation of a nutritionally important metabolic QTL and provide direct evidence of a role for epigenetics in the determination of agronomic traits.L.Q. was recipient of a fellowship of Agencia Nacional de Promoción Científica y Tecnológica and Consejo Nacional de Investigaciones Científicas y Técnicas in Argentina and supported by a postdoctral fellowship from Investissements d’Avenir ANR-10-LABX-54 MEMO LIFE in France. J.A. and L.B. were recipients of a fellowship of Fundação à Amparo da Pesquisa do Estado de São Paulo (Brazil). J.V.C.d.S. was recipient of a fellowship of Conselho Nacional de Desenvolvimento Científico e Tecnológico (Brazil). R.A., L.B. and F.C. are members of Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina). This work was carried out in compliance with current laws governing genetic experimentation in Brazil and in Argentina. This work was supported with grants from Instituto Nacional de Tecnologia Agropecuária, Consejo Nacional de Investigaciones Científicas y Técnicas and Agencia Nacional de Promoción Científica y Tecnológica (Argentina), Fundação à Amparo da Pesquisa do Estado de São Paulo, Conselho Nacional de Desenvolvimento Científico e Tecnológico and Universidade de São Paulo (Brazil); Max Planck Society (Germany); the Agence Nationale de la Recherche (Investissements d’Avenir ANR-10-LABX-54 MEMO LIFE and ANR-11-IDEX-0001-02 PSL* Research University to V.C.); and the European Union (EpiGeneSys FP7 Network of Excellence number 257082 to V.C. and the European Solanaceae Integrated Project FOOD-CT-2006-016214 to F.C., M.R. and A.R.F.)