Influence of seed development on the timing of ripening initiation in grape berry and its ripening progress toward maturity

The ripening initiation is a transitional developmental phase characterized by a complete reprogramming to primarily facilitate the dispersal of the seeds with significant implications on the final fruit composition. Several signaling pathways will integrate changes in the environmental and development cues to ensure the fruits’ transition to the ripening phase until maturity. While environmental cues have been extensively studied to examine the ripening onset, the influence of any developmental signal associated with the timing of ripening initiation has yet to be characterized. The uneven ripening of a cluster reflects the implication of a developmental program that controls the entry of each berry into the ripening onset. Recent evidence suggests that uneven ripening poorly correlates with differential anthesis time. Instead, a high seed index (seed mass relative to the berry mass) was observed in most lagging fruits at véraison in conjunction with a more significant accumulation of auxin in the pericarp tissues of these fruits at a pre-véraison time. Seeds are a reservoir of many plant hormones that are particularly active until pre-véraison. Therefore, we hypothesized that a differential decline of seed-derived auxin associated with the seed index would explain the differential entry of individual berries in the ripening phase resulting in significant molecular changes in the pericarp tissues. Using an integrated approach combining genome-wide transcript profiles and metabolite signatures, we found that the developmental divergence observed between two véraison berry populations with contrasted seed indices (high and low seed index) is a discrete and dynamic process during pre-véraison times responsible for significant transcriptional and metabolite changes. This developmental divergence will reach its maximum at mid-véraison. Still, a developmental convergence between the two berry classes will follow for the remaining berry ripening, which will result in mitigating the previous differences. This developmental convergence appears to be a coordinated program involving a transcriptional readjustment of the differentially expressed genes (DEGs) in order to reach a transcriptional state similar in both berry classes to maturity regardless of the tissues.