A Tonoplast Sugar Transporter Underlies a Sugar Accumulation QTL in Watermelon

Abstract

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.

Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.

“…In sugarcane and sweet sorghum, the stems are the principal sink tissues that store very high concentrations of sugars within the parenchyma cells [42][43][44] . Tonoplast sugar transporters (TSTs) have been characterized as sucrose transporters highly associated with vacuolar sucrose accumulation from sugar beet taproot 45 , sugarcane 46 and sweet sorghum stems 47 and watermelon fruit 48 . Whereas there are 3 TST genes in the sorghum genome 47 , the family has expanded in the S. spontaneum genome, which has 4 genes consisting of 13 homologs.…”

Resequencing of 414 cultivated and wild watermelon accessions identifies selection for fruit quality traits

“…A second GWAS signal associated with flesh color was found on chromosome 2 within the sweetness QTL QBRX2-1 (Fig. 2c); this QTL harbors the candidate gene ClTST2, which, when overexpressed, causes elevated sugar levels in fruit and also leads to flesh color development 35 . A previous study showed that an elevated sugar level activates the watermelon fruit chromoplast-localized phosphate transporter ClPHT4;2 (Cla97C10G205070), the function of which is necessary for carotenoid accumulation in fruit flesh 36 .…”

Natural genetic variation for expression of a SWEET transporter among wild species of Solanum lycopersicum (tomato) determines the hexose composition of ripening tomato fruit

“…Beyond such transporter identification and correlative studies, this report points to the potential contribution of natural allelic variation for sugar transporter genes to the improvement of fruit sugar accumulation, and the results of the present report extend the potential for the contribution of wild species to fruit sugar composition to include this mechanism of accumulation. Recently, a GWAS study of watermelon fruit pointed to a TST sugar transporter, indicating genetic variability (Ren et al, 2018). In light of the presence of orthologs of the SWEET protein present in fruit of other plant species, as well as the expression of other paralogs of SWEET in tomato and other fruit, it is likely that modulation of these orthologs and paralogs may affect the sugar content of tomato and other fruits, as well.…”