Transcriptome dynamics during dormancy and budbreak in early and late grapevine cultivars

In grapevine phenological development, including the transition from dormancy to budbreak, is strongly affected by changes and fluctuations in environmental stimuli such as temperature. The rising winter temperatures recorded in several areas of the world as a consequence of climate change cause an anticipation of dormancy release and budbreak, leading to an increased exposure of vulnerable tissues to the damage caused by spring frost events, which in turn negatively impacts bud survival and production. However, a great degree of variability is observed in the budbreak timing of grapevine cultivars. Understanding the molecular regulation of dormancy release and budbreak, as well as the determinants shaping cultivar variability is therefore essential to assist the selection of varieties better suited to the changing climate. In order to investigate the molecular changes associated with grapevine budbreak, we implemented an experimental setup based on the monitoring of bud cold hardiness and dormancy-to-budbreak transitions in single-bud cuttings placed under controlled conditions. This system was successfully applied to the cultivars Chardonnay and Cabernet Sauvignon, which in the field exhibit an early- and a late-budbreak phenotype respectively, as it allowed us to replicate in the lab the phenotypic difference in the timing of budbreak between the two cultivars. Phenological observations and whole transcriptome analyses were carried out on buds collected at five different points during dormancy and budbreak in order to compare the dynamics of gene expression between the two cultivars. During dormancy, both cultivars showed downregulation of cell cycle, metabolism, and growth pathways, whereas budbreak induction was characterised by the reactivation of genes involved in cell cycle, metabolism, and organ development, as well as the repression of dormancy-related hormonal and stress responses. Nevertheless, the specific time course used was suitable to capture key points where the transcriptomic differences expected between the cultivars during dormancy and budbreak induction were clear, showing the presence of cultivar-specific drivers for dormancy release at the gene expression level. The upregulation of metabolic processes and cell wall remodelling pathways was observed during dormancy only in Chardonnay, suggesting an early reactivation prior to deacclimation. This contrasts with the delayed response of Cabernet Sauvignon to forcing temperature conditions, which is reflected by a delayed activation or repression of several genes including known regulators of budbreak such as EARLY BUDBREAK and FLOWERING LOCUS C. The gene expression dynamics observed in the two cultivars and their biological implications will be discussed.