A Tonoplast Sugar Transporter Underlies a Sugar Accumulation QTL in Watermelon

How sugar transporters regulate sugar accumulation in fruits is poorly understood and particularly so for species storing high-concentration Suc. Accumulation of soluble sugars in watermelon () fruit, a major quality trait, had been selected during domestication. Still, the molecular mechanisms controlling this quantitative trait are unknown. We resequenced 96 recombinant inbred lines, derived from crossing sweet and unsweet accessions, to narrow down the size of a previously described sugar content quantitative trait locus, which contains a putative gene (). Molecular and biochemical analyses indicated that encodes a vacuolar membrane protein, whose expression is associated with tonoplast uptake and accumulation of sugars in watermelon fruit flesh cells. We measured fruit sugar content and resequenced the genomic region surrounding in 400 watermelon accessions and associated the most sugar-related significant single-nucleotide polymorphisms (SNPs) to the promoter. Large-scale population analyses strongly suggest increased expression of as a major molecular event in watermelon domestication associated with a selection sweep around the promoter. Further molecular analyses explored the binding of a sugar-induced transcription factor () to a sugar-responsive cis-element within the promoter, which contains the quantitative trait locus (QTL) causal SNP. The functional characterization of and its expression regulation by provide novel tools to increase sugar sink potency in watermelon and possibly in other vegetable and fruit crops.