The miPEP171b-miR171b-SCL15/HDA19 module regulates histone deacetylation to confer cold tolerance in grapevine.

Abstract

Cold stress is a major environmental factor limiting the cultivation and productivity of grapevine (Vitis vinifera L.). While microRNAs (miRNAs) are well-established post-transcriptional regulators, the functional roles of microRNA-encoded peptides (miPEPs) in cold adaptation remain poorly understood. Through quantitative proteomics, we identified miPEP171b, encoded within the pri-miR171b transcript, as a key regulator of the grapevine cold stress response. Cold stress induces pri-miR171b expression, significantly upregulating both miPEP171b and pre-miR171b. As a small peptide, miPEP171b further promotes the accumulation of vvi-miR171b. Subsequent investigations reveal that miPEP171b and vvi-miR171b enhance cold tolerance by suppressing their target gene, VvSCL15, which acts as a negative regulator of the cold stress response. Under normal conditions, VvSCL15 recruits the histone deacetylase VvHDA19 to form a regulatory complex, which maintains low histone H3 acetylation levels and suppresses the expression of key cold-responsive genes, such as VvCOR27, VvCAM-1, and VvCML46. Upon cold exposure, the accumulation of miPEP171b and vvi-miR171b suppresses the expression of VvSCL15, dismantling this repressor complex and initiating extensive transcriptional reprogramming. Metabolomic analysis further demonstrates that miPEP171b orchestrates adaptive shifts in amino acid and sugar metabolism. Collectively, our findings define a novel miPEP171b-miR171b-SCL15/HDA19 module that integrates peptide signaling with chromatin remodeling to confer cold tolerance in grapevine. This study uncovers a previously unrecognized epigenetic switch for cold adaptation and provides a strategic target for enhancing environmental resilience in horticultural crops.