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The  Dormancy-associated MADS-box  ( DAM ) gene cluster in peach serves as a key regulatory hub on which the seasonal temperatures act and orchestrate dormancy onset and exit, chilling response and floral bud developmental pace. Yet, how different temperature regimes interact with and regulate the six linked  DAM  genes remains unclear. Here, we demonstrate that chilling downregulates  DAM1 and DAM3–6  in dormant floral buds with distinct patterns and identify  DAM4  as the most abundantly expressed one. We reveal multiple epigenetic events, with tri-methyl histone H3 lysine 27 (H3K27me3) induced by chilling specifically in  DAM1  and  DAM5 , a 21-nt sRNA in  DAM3  and a ncRNA induced in  DAM 4. Such induction is inversely correlated with downregulation of their cognate  DAM s. We also show that the six  DAM s were hypermethylated, associating with the production of 24-nt sRNAs. Hence, the chilling-responsive dynamic of the different epigenetic elements and their interactions likely define distinct expression abundance and downregulation pattern of each  DAM . We further show that the expression of the five  DAM s remains steadily unchanged or continuously downregulated at the ensuing warm temperature after chilling, and this state of regulation correlates with robust increase of sRNA expression, H3K27me3 and CHH methylation, which is particularly pronounced in  DAM4 . Such robust increase of repressive epigenetic marks may irreversibly reinforce the chilling-imposed repression of  DAM s to ensure flower-developmental programming free from any residual  DAM  inhibition. Taken together, we reveal novel information about genetic and epigenetic regulation of the  DAM  cluster in peach, which will be of fundamental significance in understanding of the regulatory mechanisms underlying chilling requirement and dormancy release, and of practical application for improvement of plasticity of flower time and bud break in fruit trees to adapt changing climates.

Thermal-responsive genetic and epigenetic regulation of DAM cluster controlling dormancy and chilling requirement in peach floral buds