Localization shift of a sugar transporter contributes to phloem unloading in sweet watermelons

Unloading sugar from sink phloem by transporters is complex and much remains to be understood about this phenomenon in the watermelon fruit. Here, we report a novel vacuolar sugar transporter (ClVST1) identified through map-based cloning and association study, whose expression in fruit phloem is associated with accumulation of sucrose (Suc) in watermelon fruit. ClVST1⁹⁷ knockout lines show decreased sugar content and total biomass, whereas overexpression of ClVST1⁹⁷ increases Suc content. Population genomic and subcellular localization analyses strongly suggest a single-base change at the coding region of ClVST1⁹⁷ as a major molecular event during watermelon domestication, which results in the truncation of 45 amino acids and shifts the localization of ClVST1⁹⁷ to plasma membranes in sweet watermelons. Molecular, biochemical and phenotypic analyses indicate that ClVST1⁹⁷ is a novel sugar transporter for Suc and glucose efflux and unloading. Functional characterization of ClVST1 provides a novel strategy to increase sugar sink potency during watermelon domestication.