Grafting onto pumpkin alters the evolution of fruit sugar profile and increases fruit weight through invertase and sugar transporters in watermelon

Abstract

Sweetness is an essential quality trait of watermelon (Citrullus lanatus (Thunb.) Matsum. & Nakai), and it depends on both the concentration and composition of sugars. Grafting is a routine technique for watermelon production globally. However, it remains unknown whether rootstock alter the profiles of sugars in watermelon. To address this issue, we grafted watermelon seedlings onto a Cucurbita maxima × Cucurbita moschata rootstock, photosynthesis in leaves, contents of main carbohydrates, activities of invertase and sucrose synthase and expressions of invertase genes and sugar transporters in watermelon fruits were examined. Results showed that grafting could have delayed fruit ripening as fruits from grafted plants had a higher hexose/sucrose ratio (increased concentration of glucose and fructose and decreased concentration of sucrose) compared to fruits from self-grafted plants. These changes were associated with increased vacuolar invertase (VIN) activity. Meanwhile, a watermelon VIN gene (ClVIN2) and two CWIN genes (ClCWIN1 and ClCWIN4) were identified in updated watermelon genome, and ClVIN2 was upregulated accompanied by the elevated activity of VIN. In addition, rootstock grafted plants displayed improved net photosynthesis rate, increased expression of ClAGA2 (coding alkaline alpha-galactosidase), ClVST1 (coding vacuolar sugar transporter) and ClCWIN4 (coding cell wall invertase), and higher activity of cell wall invertase when compared with self-grafted plants, contributing to increased fruit weight. In summary, our results imply that invertase and related sugar transporters might play a role in sugar profiles and fruit weight differentiation observed during fruit maturity evolution.