Reduction of Fruit Load Affects Early Fruit Growth in Apple by Enhancing Carbohydrate Availability, Altering the Expression of Cell Production-related Genes, and Increasing Cell Production

Carbohydrate availability is a key factor determining fruit growth in apple (Malus xdomestica) and other fruits. However, the molecular mechanisms regulating fleshy fruit growth in response to changes in carbohydrate availability are not well understood. In this study, carbohydrate availability was manipulated by reducing fruit load, and its effects on apple fruit growth, cell production and expansion, and the expression of genes associated with these processes was investigated. Reduction of fruit load during early fruit development led to a rapid increase in early fruit growth. The increase in fruit growth was associated with a transient increase in sorbitol and fructose concentrations and altered expression of sorbitol dehydrogenase and sucrose synthase genes. Increase in early fruit growth was mediated primarily by an increase in cell production. The aintegumenta gene, MdANT1, an AP2-domain transcription factor associated with the regulation of cell production and fruit growth, displayed an increase in expression by up to 5-fold during early fruit development in response to the reduction in fruit load. Additionally, multiple cell cycle genes positively associated with cell production such as the cyclins, MdCYCA2;1, MdCYCA2;3, MdCYCB1;1, and MdCYCB2;2, and the B-type cyclin-dependent kinases, MdCDKB1;1, MdCDKB1;2, and MdCDKB2;2, displayed higher expression by up to 5-fold under reduced fruit load conditions during early fruit growth. These data indicate that carbohydrate availability affects the expression of key transcription factors and cell proliferation genes, thereby regulating cell production during early fruit growth. Several genes associated with cell expansion such as the expansins, and cobra and cobra-like genes, also displayed altered expression in response to the reduction in fruit load. The expression of three expansin genes was higher under reduced fruit load conditions at maturity, a stage at which a minor increase in cell size was apparent. Together, data from this study indicate that fruit load reduction induces changes in carbohydrate availability and metabolism, which in turn affect cell production-related mechanisms, thereby enhancing early fruit growth.