The polyphenol trade-off: leaf protection vs fruit attraction in apples driven by the phlorizin glycosyltransferase...

Polyphenols play key roles in plants' resistance to biotic and abiotic stresses. However, in fruits, these compounds are often antinutritive and unattractive to seed dispersers. How plants balance these competing requirements is critical to their survival. Here, we report that phlorizin (P2G), the predominant polyphenol in apples (Malus spp.), and phloretin-2'-O-xyloglucoside (P2XG), the xylosylated product of P2G, show different accumulation patterns in apple fruits. The addition of P2G to the diet of quails, zebra finches, and budgerigars reduced feeding, while the addition of P2XG did not. P2G treatment also lowered the blood sugar concentrations and significantly reduced egg weight in quail, consistent with its ability to inhibit glucose transport mediated by sodium-glucose transporters. Two glycoside-specific glycosyltransferase genes, PGGT1.1 and 1.2, which catalyze the conversion of P2G to P2XG, were identified and shown to be specifically expressed in apple fruits. Transgenic apple plants overexpressing PGGT1 in leaves produced more P2XG, but less P2G. Consequently, these plants became more susceptible to lepidopteran pests and to spider mites. Our results show that the differential expression of glycosyltransferases in apple provides a mechanism to regulate polyphenol metabolism in different tissues to balance the requirements for plant-seed dispersal and plant-pest interactions.