WRINKLED 1 and ACYL‐COA:DIACYLGLYCEROL ACYLTRANSFERASE 1 regulate tocochromanol metabolism in Arabidopsis

Summary Photosynthetic organisms such as plants, algae and some cyanobacteria synthesize tocochromanols, a group of compounds that encompasses tocopherols and tocotrienols and that exhibits vitamin E activity in animals. While most vitamin E biosynthetic genes have been identified in plant genomes, regulatory genes controlling tocopherol accumulation are currently unknown. We isolated by forward genetics Arabidopsis enhanced vitamin E ( eve ) mutants that overaccumulate the classic tocopherols and plastochromanol‐8, and a tocochromanol unknown in this species. We mapped eve1 and eve4 , and identified the unknown Arabidopsis tocochromanol by using a combination of analytical tools. In addition, we determined its biosynthetic pathway with a series of tocochromanol biosynthetic mutants and transgenic lines. eve1 and eve4 are two seed lipid mutants affecting the WRINKLED 1 ( WRI1 ) and ACYL‐COA:DIACYLGLYCEROLACYLTRANSFERASE 1 ( DGAT1 ) genes, respectively. The unknown tocochromanol is 11′‐12′ γ‐tocomonoenol, whose biosynthesis is VITAMIN E 1 ( VTE 1) ‐ and VTE 2‐dependent and is initiated by the condensation of homogentisate ( HGA ) and tetrahydrogeranylgeranyl pyrophosphate. This study identifies the first two regulatory genes, WRI 1 and DGAT 1 , that control the synthesis of all tocochromanol forms in seeds, and shows the existence of a metabolic trade‐off between lipid and tocochromanol metabolisms. Moreover, it shows that Arabidopsis possesses a tocomonoenol biosynthetic pathway that competes with tocopherol synthesis.