Structural variations in the phytoene synthase 1 gene affect carotenoid accumulation in tomato fruits and result in bicolor and yellow phenotypes

Tomato fruits normally accumulate large amounts of the red pigment lycopene in their chromoplasts. Some tomato cultivars (Solanum lycopersicum) show however distinct phenotypes, from a pure yellow hue to bicolor fruits with red and yellow sections. In this study, we show that alleles of the phytoene synthase 1 gene (PSY1), the first gene of carotenoid synthesis pathway, are responsible for the yellow, but also the bicolor phenotype. Introgression lines with the PSY1 allele from the green-fruited species S. habrochaites express less the enzyme, resulting in a bicolor phenotype. On the other hand, in tomato bicolor cultivars, the same coloration pattern is caused by a 3789 bp-deletion in the promoter region of PSY1. Since the deletion contains part of the 5UTR region of PSY1, translation efficiency is likely decreased resulting in a reduction of lycopene accumulation. Furthermore, we identified that the yellow ry phenotype is caused by a duplication and an inversion implicating PSY1 and the downstream neighbor gene. The genomic rearrangement change the end of PSY1 amino acid sequence. The fruits of yellow ry cultivars are still able in certain conditions to accumulate lycopene near the blossom-end of the fruit, though to a lesser extent than in bicolor cultivars. In contrast, fruits of the yellow r cultivars never present fleshy red sections. These cultivars have an insertion of a single long terminal repeat from the Rider transposon in the first exon of PSY1 resulting in a non-functional protein. These results demonstrate how multiple phenotypes can arise from structural variations in a key gene.