Aging‐dependent temporal regulation of MIR156 epigenetic silencing by CiLDL1 and CiNF‐YB8 in chrysanthemum

Summary Temporal decline in microRNA miR156 expression is crucial for the transition to, and maintenance of, the adult phase and flowering competence in flowering plants. However, the molecular mechanisms underlying the temporal regulation of miR156 reduction remain largely unknown. Here, we investigated the epigenetic mechanism regulating the temporal silencing of cin‐MIR156 in wild chrysanthemum ( Chrysanthemum indicum ), focusing on the role of the lysine‐specific demethylase CiLDL1 and the nuclear factor Y complex. CiLDL1 and CiNF‐YB8 interact with the classical histone‐like fold domain (HFD) of CiNF‐YC1 and CiNF‐YA3, which form distinct heterotrimers binding to the ‘CCAAT’ box in the promoter region of cin‐MIR156ab . CiLDL1 and CiNF‐YB8 have opposing effects on cin‐MIR156ab expression, with influencing histone 3 lysine 4 demethylation (H3K4me2) levels at the cin‐MIR156ab locus. During aging, decreased CiNF‐YB8 expression leads to a quantitative switch from the CiNF‐YA3–CiNF‐YC1–CiNF‐YB8 heterotrimer to the CiNF‐YA3–CiNF‐YC1–CiLDL1 heterotrimer, which reduces H3K4me2 levels at the cin‐MIR156ab locus, thus temporal silencing its expression. Our results thus reveal that the dynamic regulatory shift between CiLDL1 and CiNF‐YB8 ensures proper aging‐dependent flowering in chrysanthemum.