A 21-bp InDel in the promoter of selected during tomato improvement accounts for soluble solid content in fruits.

Domestication and improvement are important processes that generate the variation in genome and phonotypes underlying crop improvement. Unfortunately, during selection for certain attributes, other valuable traits may be inadvertently discarded. One example is the decline in fruit soluble solids content (SSC) during tomato breeding. Several genetic loci for SSC have been identified, but few reports on the underlying mechanisms are available. In this study we 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, , encoding a sugar transporter protein. The causal variation of , a 21-bp InDel located in the promoter region 1124 bp upstream of the start codon, alters its expression. accessions with an 21-bp insertion have higher SSC than accessions with the 21-bp deletion. Knockout of in TS-23 with high SSC using CRISPR/Cas9 greatly decreased SSC in fruits. and assays demonstrated that ZAT10-LIKE, a zinc finger protein transcription factor (ZFP TF), can specifically bind to the promoter of to enhance expression, but not to the promoter of , leading to lower fruit SSC in modern tomatoes. Diversity analysis revealed that was selected during tomato improvement. Taking these results together, we identified a naturally occurring causal variation underlying SSC in tomato, and a new role for ZFP TFs in regulating sugar transporters. The findings enrich our understanding of tomato evolution and domestication, and provide a genetic basis for genome design for improving fruit taste.