Evolution of the TCP gene family and pan-genome analysis in tea (Camellia sinensis)

TCP transcription factors are key regulators of plant architecture and development, yet their evolution is often inferred from a single reference genome. Using a dataset of 1,015 plant genomes, we observed a pronounced clade-level gradient in TCP copy number, including complete absence in algae and expanded repertoires in angiosperms, with retention after WGD/segmental duplication emerging as a major contributor. We then leveraged a tea pangenome of nine Camellia genomes (three wild species and six cultivated Camellia sinensis varieties) to resolve pangenome-scale TCP dynamics. A total of 292 TCP genes were identified and grouped into three lineages (PCF, CIN and CYC/TB1). Cultivated accessions in this sampled panel harbored fewer annotated TCP genes than the sampled wild relatives, with an average reduction of approximately 27%. Orthogroup analysis revealed a compact core (4 orthogroups; 57 genes, 19.5%) and a large dispensable component (25 orthogroups; 235 genes, 80.5%) that showed extensive copy-number variation and lineage-specific loss/expansion; core enrichment was strongest in CYC/TB1, whereas PCF was biased toward dispensable genes. Tea TCP expansion was mainly attributed to WGD/segmental duplication (60.3%) and dispersed duplication (26.7%). Most homologous pairs evolved under purifying selection, but dispensable pairs exhibited higher Ka/Ks than core pairs, consistent with relaxed constraint. Pan-transcriptome comparisons across eight tissues showed generally higher TCP expression in cultivated materials, particularly in apical bud and stem/fruit-related tissues. Together, these results establish a pangenome-informed TCP resource and suggest that dosage remodeling and structural variation may have contributed to lineage diversification in tea and provide candidates for future studies of domestication-related evolution.