The fusion transcript of Phytoene synthase 1 controls yellow fruit in tomato

Tomato (Solanum lycopersicum) fruit color is an important aspect of quality in terms of appearance and nutrient content. Carotenoids, chlorophyll, and flavonoids are the main components responsible for tomato fruit color. Phytoene synthase (PSY) is the key regulatory enzyme involved in the first committed step of carotenoid biosynthesis. Here, we found that the yellow fruit of S. lycopersicum ‘YF2359’, which lacks carotenoids, was regulated by a single recessive gene and cosegregated with PSY1 in the F₂ population. Two different PSY1 transcripts, including the wild-type and mutant (fusion-type), were discovered in YF2359. The mutant was generated by the fusion of exons from two different DNA strands, namely, PSY1 and the antisense strand of CoA ligase, by trans-splicing. This yellow flesh phenotype, which was caused by a mutation of PSY1 and was undetected in S. lycopersicum ‘LA4044’, was predicted to nullify PSY because of amino acid substitutions in the conserved trans-isoprenyl diphosphate synthase domain. Additionally, the trans-splicing of PSY1 reduced wild-type PSY1 expression, suggesting that the metabolic flux in the carotenoid pathway was suppressed in the presence of this mutation. Carotenoid biosynthetic genes were expressed significantly less in ‘YF2359’ than in the red-fruited wild-type tomato ‘M82’. Information on this unusual mutation in PSY1 will improve the understanding of genetic variations in plants and enable novel strategies for improving fruit quality.