Core content: In this study, the authors performed a genome-wide association study (GWAS) for SSC of the red-ripe fruits in a population consisting of 481 tomato accessions with large natural variations and found a new quantitative trait locus, STP1, encoding a Sugar Transporter Protein. The causal variation of STP1, a 21-bp InDel, located in promoter region 1,124 bp upstream of the start codon, alters its expression. STP1Insertion accessions with 21-bp insertion have higher SSC than STP1Deletion accessions with 21-bp deletion. Knockout of STP1 in TS-23 with high SSC using CRISPR/Cas9 greatly decreased SSC in fruits. In vivo and in vitro assays demonstrated ZAT10-LIKE, a zinc finger protein transcription factor (ZFP TF), can specifically bind to the promoter of STP1Insertion to enhance STP1 expression, but not to the promoter of STP1Deletion, leading to lower fruit SSC in modern tomatoes. Diversity analysis revealed that STP1 was selected during tomato improvement.
Innovation: The authors identified a naturally occurring causal variation underlying SSC in tomato, and a new role for ZFP TFs in regulating sugar transporters. The findings enrich the understanding of tomato evolution and domestication, and provide a genetic basis for breeding tasty tomato.