Non-CG DNA methylation represses SDC expression to modulate hypocotyl elongation during thermormorphogenesis in Arabidopsis

Plants adapt to warm environments through physiological and morphological changes termed thermomorphogenesis, which involve transcriptional reprogramming exerted mainly by PHYTOCHROME INTERACTING FACTOR 4 (PIF4). Fluctuating temperatures can also influence the patterns of cytosine DNA methylation (DNAme), thereby influencing gene expression; however, whether these epigenetic changes provide an adaptative advantage remains unclear. Here, we provide evidence that DNAme is required to regulate thermomorphogenesis in Arabidopsis. Hypomethylated drm1 drm2 cmt3 mutants and seedlings treated with 5-azacytidine to block DNAme exhibited reduced hypocotyl growth at warm temperatures, primarily due to impaired cell elongation. Moreover, DNA hypomethylation compromised auxin biosynthesis and transport in response to warmth, partially by reducing PIF4 protein levels. Notably, the loss of DNAme led to increased expression of SUPPRESSOR OF drm1 drm2 cmt3 (SDC), which in turn restricted hypocotyl elongation during thermomorphogenesis. Finally, DNAme was found to regulate the inhibition of SDC expression to promote gibberellin biosynthesis. Our findings underscore the critical role of DNAme in modulating gene expression in response to temperature fluctuations and provide new insights into the epigenetic regulation of thermomorphogenesis.