Validated MAGIC and GWAS population mapping reveals the link between vitamin E content and natural variation in chorismate metabolism in tomato. (22nd December 2020)

• Record Type: Journal Article
• Authors: Burgos, Estanislao; Belen De Luca, Maria; Diouf, Isidore; de Haro, Luis A.; Albert, Elise; Sauvage, Christopher; Tao, Zhao J.; Bermudez, Luisa; Asís, Ramon; Nesi, Adriano N.; Matringe, Michel; Bréhélin, Claire; Guiraud, Thomas; Ferrand, Carine; Atienza, Isabelle; Jorly, Joana; Mauxion, Jean P.; Baldet, Pierre; Fernie, Alisdair R.; Quadrana, Leandro; Rothan, Christophe; Causse, Mathilde; Carrari, Fernando
• Is Part Of: Plant journal. Volume 105:Number 4(2021)
• Page Start: 907
• Page End: 923
• Publication Date: 2020-12-22
• Subjects: tocopherol -- tocotrienol -- vitamin E -- tomato fruit -- Solanum lycopersicum; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.15077
• Languages: English
• ISSNs: 0960-7412

Abstract

Summary: Tocochromanols constitute the different forms of vitamin E (VTE), essential components of the human diet, and display a high membrane protectant activity. By combining interval mapping and genome‐wide association studies (GWAS), we unveiled the genetic determinants of tocochromanol accumulation in tomato ( Solanum lycopersicum ) fruits. To enhance the nutritional value of this highly consumed vegetable, we dissected the natural intraspecific variability of tocochromanols in tomato fruits and genetically engineered their biosynthetic pathway. These analyses allowed the identification of a total of 25 quantitative trait loci interspersed across the genome pinpointing the chorismate–tyrosine pathway as a regulatory hub controlling the supply of the aromatic head group for tocochromanol biosynthesis. To validate the link between the chorismate–tyrosine pathway and VTE, we engineered tomato plants to bypass the pathway at the arogenate branch point. Transgenic tomatoes showed moderate increments in tocopherols (up to approximately 20%) and a massive accumulation of tocotrienols (up to approximately 3400%). Gene expression analyses of these plants reveal a trade‐off between VTE and natural variation in chorismate metabolism explained by transcriptional reprogramming of specific structural genes of the pathway. By restoring the accumulation of alpha‐tocotrienols (α‐t3) in fruits, the plants produced here are of high pharmacological and nutritional interest. Significance Statement: In this ms, we contribute with a large scale genetic analysis applying multi‐parental advanced generation intercross and genome‐wide association study population mapping, which allowed us to detect a trade‐off between vitamin E accumulation and chorismate metabolism. Moreover, validation experiments with engineered transgenic plants revealed massive accumulation of α‐tocotrienol, a minor form of tocochromanol with higher VTE activity than that recognized to date. By restoring the accumulation of this compound in fruits, the plants produced here are of pharmacological and nutritional interest.