Influence of Seed Development of the Transcriptional Program of Grape Berries during the Ripening Phase

The ripening initiation is a transitional developmental phase characterized by a complete reprograming that leads to dramatic changes on the central and secondary metabolisms of the fruit, and that contributes to the final fruit composition in terms of flavor and aromas. In grape berry research, much scientific efforts have emphasized on understanding how environmental changes (macro, meso, and microclimate), and plant statuses are integrated to the fruit development. The influence of developmental cues such as seed and embryo development has yet to be characterized on the ripening program. One peculiar feature of a grape berry cluster, conserved across cultivated and wild species, is the uneven pattern of the developmental progression of individual fruits within a cluster. In our lab, we found a poor correlation between anthesis and the ripening status of individual berries at the ripening initiation; rather the seed content relative to the berry mass (Seed Index) showed a stronger correlation in seeded berries. Seeds are seen as a main reservoir for plant hormones dedicated to the embryo growth and differentiation embryo development. Whether the dynamics of hormone accumulation in the seed follow a similar trend during the ripening onset in the other tissues of the pericarp is unclear. We hypothesized that seeds contribute to the timing of ripening of individual berries through a gradual decline a seed-derived transport of auxin, a ripening delayer, near the ripening onset. We used a streamlined phenological procedure to segregate two populations of berries with distinct Seed Index at different developmental stages (pre- and post-ripening, and maturity stages). Combining hormone and metabolite profiles with genome-wide RNA sequencing analyses, we were able to identify clear transcript, hormone and metabolite signatures between the two classes initiated at a discrete pre-ripening stage, with the maximum differences observed around the ripening onset, before experiencing a developmental convergence at transcript and metabolite levels towards maturity stage. Such ability of individual fruit to first diverge and then converge can only be explained by a modification of their rate of ripening. The relationships between transcript, hormone and metabolite signatures overtime in both classes and difference in rate of ripening are discussed. Differences in transcript abundance associated Plant hormone signalings (ABA, Auxin, and brassinosteroids) and their transports seem to contribute to the developmental divergence and convergence. Research perspectives of these new findings to understand the timing of ripening initiation and the further developmental adjustment observed during the ripening are discussed.