Conserved DNA methylation architectures are associated with transcriptional robustness and regulatory plasticity in the woody perennial tea plant.

Abstract

DNA methylation is an important mechanism in plant development and environmental adaptation, yet how distinct methylation features contribute to transcriptional stability and regulatory flexibility in long-lived woody plants remains poorly understood. Here, we integrated DNA methylomes, transcriptomes, and chromatin accessibility profiles from two Camellia sinensis varieties to examine the regulatory characteristics and conservation of two specific methylation architectures: gene body methylation (gbM) and DNA methylation valleys (DMVs). We found that gbM genes showed distinctive gene structures, broad and relatively stable expression, and highly conserved methylation states between orthologs. gbM-gbM orthologs also showed evidence of stronger selective constraint in a sequence-length-dependent manner, consistent with a close relationship between gbM and stable transcription of housekeeping genes. In contrast, DMVs were highly hypomethylated regions associated with TE depletion and pronounced TF footprint signals, both of which were closely linked with methylation level, while DMV-associated genes were enriched for developmental and stress-responsive functions. Genome synteny analyses further revealed substantial conservation of DMV patterns and TF footprint profiles between tea varieties, indicating broad conservation of DMV-associated regulatory features across divergent genetic backgrounds. Together, these findings reveal two complementary epigenetic architectures in a woody perennial plant, with gbM preferentially associated with transcriptional robustness and DMVs with regulatory features linked to development and environmental responses.