Identification of potential regulators of cell production and early fruit growth in apple (Malus × domestica Borkh.)

Abstract

Fruit size is a commercially valuable trait that is determined by the extent of fruit growth. In apple, (Malus × domestica Borkh.), early fruit growth is facilitated by intensive cell production, but mechanisms regulating these processes are not well understood. In this study, members of five gene families involved in growth regulation were identified and evaluated in apple: AUXIN-REGULATED GENE INVOLVED IN ORGAN SIZE (ARGOS); CELL NUMBER REGULATOR (CNR); GROWTH REGULATING FACTOR (GRF); GRF INTERACTING FACTOR (GIF); and KLUH. MdARGOS1 and MdARGOS2 transcript abundance was higher during early fruit growth but was also enhanced by up to 18-fold under conditions of reduced cell production during flower and fruit development, indicating that their gene products play complex roles in regulating growth mechanisms during early development. MdCNR20a and MdCNR20b transcript abundance decreased during early fruit growth and increased during the transition from cell production to cell expansion. MdCNR20a transcript abundance was negatively correlated with the relative cell production rate (RCPR; ρ = - 0.82; P = 0.002), was enhanced in response to shading, and reduced in response to lower fruit load, indicating that it's gene product negatively regulates cell production and early fruit growth. Transcript abundance of MdGRF11 and MdGRF16 was greater during cell production-mediated fruit growth, and higher in the cortex than in the pith. MdGIF3 transcript abundance was greater during early fruit development, higher in the cortex, enhanced under reduced fruit load conditions, and strongly correlated with RCPR (ρ = 0.93; P < 0.0001). Further, it was correlated with that of MdGRF11 and MdGRF16 (ρ = 0.87 and 0.89, respectively; P < 0.0001), indicating that the GRF11/16-GIF3 module is co-regulated and involved in spatio-temporal regulation of cell production and fruit growth. Transcript abundance of MdKLUH1 was low and not consistent with a role in regulating cell production and fruit growth. Together, this study demonstrates coordinated control of cell production during early fruit growth by multiple regulatory components, identifies candidates for functional characterization, and provides potential tools for enhancing growth of the apple fruit.