Epigenetic regulation and transcriptional divergence underpin lignification in rapidly growing Moso bamboo

Moso bamboo (Phyllostachys edulis) is characterized by its unparalleled rapid growth (up to 114.5 cm d-1) and concurrent lignification; however, the genetic and epigenetic mechanisms orchestrating this process remain largely unexplored. Here, we integrated RNA-seq, ATAC-seq, and DAP-seq analyses across three defined developmental stages (start of cell division, rapid cell division, and rapid elongation) to decipher the molecular regulatory networks underlying this phenomenon. Our transcriptomic profiling revealed that interindividual variation primarily reflects developmental progression, with active lignification occurring predominantly in the rapid elongation stage. Time-ordered gene coexpression network (TO-GCN) analysis demonstrated strong convergence of lignin biosynthesis-related gene expression during the rapid elongation stage, despite persistent individual-specific transcriptional divergence, particularly during the rapid cell division stage. Integration of RNA-seq and ATAC-seq data demonstrated that chromatin accessibility dynamics underlie this divergence, highlighting epigenetically regulated transcription factor (TF) expression as a critical determinant of lignification trajectories. Notably, we identified three novel TFs as potential regulators of the lignin biosynthesis pathway, including ERF (clrGene014320) and MYB family members (clrGene027449 and clrGene040715). Evolutionary analysis suggested that neofunctionalization following recent whole-genome duplication events contributed to the specialized regulatory functions of these genes during bamboo shoot lignification. Functional validation confirmed the direct regulatory roles of these TFs in controlling lignin biosynthetic genes. This study provides integrated insights into the genetic and epigenetic control of extreme plant growth and cell wall plasticity, offering valuable genetic resources for sustainable biomass improvement.