Timing and Order of the Molecular Events Marking the Onset of Berry Ripening in Grapevine

Grapevine (Vitis vinifera) is a model for the investigation of physiological and biochemical changes during the formation and ripening of nonclimacteric fleshy fruits. However, the order and complexity of the molecular events during fruit development remain poorly understood. To identify the key molecular events controlling berry formation and ripening, we created a highly detailed transcriptomic and metabolomic map of berry development, based on samples collected every week from fruit set to maturity in two grapevine genotypes for three consecutive years, resulting in 219 samples. Major transcriptomic changes were represented by coordinated waves of gene expression associated with early development, veraison (onset of ripening)/midripening, and late-ripening and were consistent across vintages. The two genotypes were clearly distinguished by metabolite profiles and transcriptional changes occurring primarily at the veraison/midripening phase. Coexpression analysis identified a core network of transcripts as well as variations in the within-module connections representing varietal differences. By focusing on transcriptome rearrangements close to veraison, we identified two rapid and successive shared transitions involving genes whose expression profiles precisely locate the timing of the molecular reprogramming of berry development. Functional analyses of two transcription factors, markers of the first transition, suggested that they participate in a hierarchical cascade of gene activation at the onset of ripening. This study defined the initial transcriptional events that mark and trigger the onset of ripening and the molecular network that characterizes the whole process of berry development, providing a framework to model fruit development and maturation in grapevine.