GREEN STRIPE, encoding methylated TOMATO AGAMOUS-LIKE 1, regulates chloroplast development and chlorophyll synthesis in fruit.

Fruit development involves chloroplast development, carotenoid accumulation and fruit coloration. Although genetic regulation of fruit development has been extensively investigated, epigenetic regulation on fruit coloration remains largely unexplored. Here, we report a naturally occurring epigenetic regulation of TAGL1, and its impact on chloroplast development and fruit coloration. We used a genome-wide association study in combination with map-based cloning to identify GREEN STRIPE (GS) locus, a methylated isoform of TAGL1 regulating diversified chloroplast development and carotenoid accumulation. Nonuniform pigmentation of fruit produced by GS was highly associated with methylation of TAGL1 promoter, which is linked to a SNP at SL2.50ch07_63842838. High levels of methylation of TAGL1 promoter down-regulated its expression leading to green stripes. In contrast, low levels of methylation led to light green stripes in gs. RNA-seq and ChIP collectively showed expression of genes involved with chlorophyll synthesis, chloroplast development were significantly up-regulated in green stripes relative to light green stripes. Quantitative PCR and dual luciferase assay confirmed TAGL1 down-regulates expression of SlMPEC, SlPsbQ, SlCAB and up-regulates expression of PSY1, which are associated with chloroplast development and carotenoid accumulation. Altogether, GS locus demonstrates naturally occurring methylation of TAGL1 has diverse effects on plastid development in fruit.