Divergent Effects of Distinct SlCRTISO Alleles on Phenolic Content, Fruit Size, and Transcriptomic Profiles in Tangerine Tomatoes

Carotenoids are essential nutritional compounds in tomato (Solanum lycopersicum), and mutations in carotenoid biosynthesis genes can alter both fruit color and other quality traits. Carotenoid isomerase (CRTISO) converts prolycopene to all-trans-lycopene; its mutation results in the orange-fruited tangerine mutant characterized by prolycopene accumulation. However, the broader impacts of distinct SlCRTISO mutations on fruit quality traits and agronomic performance remain largely unexplored. Here, we evaluated agronomic traits and nutritional quality in two tangerine mutants carrying distinct SlCRTISO alleles. The yellow/orange-fruited tomato 5 (yft5) mutant, which harbors a single point mutation in SlCRTISO, exhibited lower flavonoids, chlorogenic acid, and prolycopene than the CRISPR/Cas9-mediated knockout mutants, but maintained fruit size and weight comparable to wild type, whereas knockout lines showed severely reduced fruit size, highlighting the potential agronomic advantage of yft5. Pearson correlation analysis revealed negative associations between abscisic acid (ABA) levels and rutin, chlorogenic acid, as well as the prolycopene-to-lycopene ratio during fruit ripening. Transcriptome analysis demonstrated that knockout mutations more profoundly affected primary metabolism than the yft5 point mutation. Notably, 9-cis-epoxycarotenoid dioxygenase 2 (NCED2), a gene involved in ABA biosynthesis, was specifically upregulated in yft5 fruits at the mature green stage (38 days post-anthesis (dpa)), consistent with ABA levels. Quality-related genes including chalcone synthase (CHS), citrate synthase (CS), and invertase (INV) were significantly upregulated in knockout lines during ripening. These findings reveal a trade-off between phenolic content and fruit size in tangerine tomatoes carrying distinct SlCRTISO alleles, positioning yft5 as a valuable genetic resource for breeding high-quality varieties.