Overexpression of the sugar transporter gene VvSWEET15 enhances sucrose synthase VvSUSY3-driven sucrose degradation to promote hexose accumulation in grape berries

Abstract In fruit crops, sugar accumulation is a highly orchestrated process that requires coordination among numerous sugar transporters and metabolic enzymes. However, much remains unknown about how the underlying mechanisms coordinating these genes contribute to controlling sugar movement across the apoplasmic gap and sugar accumulation in fruits. In this study, we identified a cytoplasmic membrane-localized sucrose transporter, VvSWEET15, from grapevine (Vitis vinifera L.), whose expression was associated with significant hexose accumulation during berry ripening and exhibited expression patterns similar to those of the sucrose synthase VvSUSY3. Although overexpressing VvSWEET15 increased fructose and glucose concentrations in transgenic grape calli, it unexpectedly decreased that of sucrose. RNA sequencing (RNA-seq) and expression analyses revealed that VvSUSY3 was up-regulated in the transgenic calli lines overexpressing VvSWEET15. Further analyses suggested that the increased hexose concentration in the transgenic lines correlated with the up-regulation of VvSUSY3 expression. Suppressing VvSUSY3 in the VvSWEET15-overexpressing grape calli reduced the positive effect of VvSWEET15 on sugar accumulation. These findings demonstrate that the increased sucrose transport into the cytosol, mediated by VvSWEET15, up-regulates sucrose synthase VvSUSY3 expression to promote hexose accumulation in the berries. Thus, our study establishes a framework for understanding how sugar transporters and metabolic genes are integrated to facilitate sugar partitioning and accumulation in plants.