Pan-genomic and pan-transcriptomic integration unveils evolutionary dynamics and regulatory diversification of the WRKY gene family in Camellia sinensis.

BACKGROUND

The WRKY transcription factor family, characterized by its conserved WRKYGQK motif and zinc finger structure, serves as a central regulatory module in plants, mediating developmental, stress-responsive, and metabolic processes through W-box binding. In Camellia sinensis, WRKY genes act as molecular integrators that link environmental cues to the biosynthesis of quality-related compounds, underscoring the importance of understanding their evolutionary patterns for genetic improvement. However, previous research has been limited by single-reference genome approaches, which fail to capture the full spectrum of WRKY gene presence-absence variation across diverse tea plant cultivars.

RESULTS

This study presents the first pan-genome-wide analysis of the WRKY family in any plant species, integrating data from 22 tea plant genomes. We identified a comprehensive set of WRKY genes and classified them into core and dispensable categories, revealing extensive presence-absence variants (PAVs) that were overlooked in single-reference studies. Phylogenetic reconstruction resolved 11 subfamilies, with notable lineage-specific expansions. Mechanistically, core gene evolution was predominantly driven by whole-genome or segmental duplication under strong purifying selection, whereas dispensable genes, particularly in certain subfamilies, showed signals of adaptive evolution and were enriched through dispersed duplication. Transcriptomic analysis uncovered co-expression networks among highly expressed WRKY clusters, indicating functional redundancy and sub-functionalization in stress adaptation.

CONCLUSIONS

The findings from the present study provide insights into the evolutionary dynamics of presence-absence and copy-number variation within the WRKY family in tea plants, establishing a valuable genetic resource for enhancing stress resilience and metabolic traits in tea breeding programs.