G2-LIKE CAROTENOID REGULATOR (SlGCR) is a positive regulator of lutein biosynthesis in tomato

Lutein is an oxygen-containing carotenoid synthesized in plant chloroplasts and chromoplasts. It plays an indispensable role in promoting plant growth and maintaining eye health in humans. The rate-limiting step of lutein biosynthesis is catalyzed by the lycopene ε-cyclase enzyme (LCYE). Although great progress has been made in the identification of transcription factors involved in the lutein biosynthetic pathway, many systematic molecular mechanisms remain to be elucidated. Here, using co-expression analysis, we identified a gene, G2-LIKE CAROTENOID REGULATOR (SlGCR), encoding a GARP G2-like transcription factor, as the potential regulator of SlLCYE in tomato. Silencing of SlGCR reduced the expression of carotenoid biosynthetic genes and the accumulation of carotenoids in tomato leaves. By contrast, overexpression of SlGCR in tomato fruit significantly increased the expression of relevant genes and enhanced the accumulation of carotenoids. SlGCR can directly bind to the SlLCYE promoter and activate its expression. In addition, we also discovered that expression of SlGCR was negatively regulated by the master regulator SlRIN, thereby inhibiting lutein synthesis during tomato fruit ripening. Taken together, we identified SlGCR as a novel regulator involved in tomato lutein biosynthesis, elucidated the regulatory mechanism, and provided a potential tool for tomato lutein metabolic engineering. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s42994-022-00088-z.