Growth regulation during early fruit development in apple (Malus × domestica Borkh.): a temporal event map of transcriptome and phytohormone changes

Early fruit development (EFD) in apple (Malus × domestica Borkh.) involves fruit set and rapid growth supported by intensive metabolism. Growth during this period is separable into three phases: initiation of fruit growth, progression by primarily cell production-mediated growth, and a transition to cell-expansion mediated growth. Although EFD is a critical developmental stage, regulation of growth during this period remains poorly understood. To gain insights into the regulation of growth during EFD, the transcriptome, and the abundance of multiple phytohormones and related metabolites in the fruit cortex were analyzed. Initiation of fruit growth at the onset of EFD was associated with de-repression of growth facilitated by a decline in abscisic acid (ABA) concentration and signaling, decline in a general stress program, and an increase in cell division activity characterized by increase in transcript abundance of cell cycle and cytokinesis-related genes. Progression of cell production-mediated growth during EFD was associated with sustained GA1 (Gibberellin1), and tZ (trans-zeatin) concentrations, as well as consistent expression of their signaling-related genes. Concentrations of jasmonic acid (JA), JA-isoleucine (JA-Ile), and multiple other jasmonate-related compounds, and expression of JA signaling-related genes was high during this period suggesting a role for JAs in preventing premature cell differentiation. Exit from cell production-mediated growth and transition to cell expansion-mediated growth during late stages of EFD was a gradual process marked by an early decline in transcript abundance of HISTONES and RIBOSOMAL PROTEIN GENES (RPGs), followed by that of multiple cell cycle and cytokinesis-related genes. Sharp decreases in concentrations of GA1, tZ and multiple JA-related compounds, and complementary changes in the transcript abundance of multiple genes associated with their signaling was associated with exit from the cell production-mediated growth phase of EFD. Cell expansion-related gene expression increased gradually during EFD, particularly during later stages. This study provides a temporal map of transcriptomic events during different stages of EFD. Further, data from this study suggest that ABA, GA1, tZ and JAs are key phytohormones regulating the initiation, progression and transition phases of growth during EFD in apple.