Cell Quiescence Is the Fountain of Youth in Plants

What determines the rate at which a multicellular organism matures is a fundamental question in biology. In plants, the decline of miR156 with age serves as an intrinsic, evolutionarily conserved timer for the juvenile-to-adult phase transition. However, the way in which age regulates miR156 abundance is poorly understood. Here, we show that the rate of decline in miR156 is correlated with developmental age rather than chronological age. Mechanistically, we found that cell division in the apical meristem is a trigger for miR156 decline. The transcriptional activity of MIR156 genes is gradually attenuated by the deposition of the repressive histone mark H3K27me3 along with cell division. In perennial plants, the quiescent axillary shoot meristematic cells preserve their original epigenetic status at the MIR156 gene loci, thereby contributing to the formation of juvenile zones at the root crown. Our findings thus provide a plausible explanation of why the maturation program of a multicellular organism is unidirectional and irreversible, and uncover a molecular mechanism underlying the unique life-cycle strategy of long-lived perennial plants.