From chill to bloom: seasonal coordination of reproductive development in peach and temperate fruit trees

Seasonal temperature is the primary environmental cue controlling reproductive development in temperate fruit trees, yet its role has largely been interpreted through dormancy-based models that view winter cold as a passive prerequisite for growth resumption. This review reassesses this framework by examining cold and warmth as sequential developmental signals acting during late flower development, after inflorescence meristem identity has been established. Integrating anatomical, cytological, and transcriptomic evidence, we show that reproductive development follows a biphasic thermal organization. Microsporogenesis can progress during winter under chilling temperatures in a species-dependent manner, with peach representing a clear case of cold-driven meiotic progression. In contrast, pollen maturation and female gametophyte development remain dependent on rising spring temperatures and occur within a narrow pre-bloom window across major Rosaceae fruit crops. We further discuss how this sequential thermal control is coordinated by multiple regulatory layers involving transcriptional regulation, hormonal balance, carbohydrate metabolism, and chromatin dynamics. Disruption of the sequence of cold and warm periods under recent climate variability uncouples male and female gametophyte development, leading to recurrent failure modes that compromise fertility. We conclude that winter represents an active developmental phase and that reproductive vulnerability arises primarily from altered thermal sequencing rather than cumulative temperature deficits.