Recent gene duplication and structural remodeling drive rapid lineage-specific gene family evolution in plants

Gene duplication promotes the generation of novel gene functions and trait diversity across species. Here, we present DupHIST, a computational pipeline that reconstructs the hierarchical timing of gene duplications by integrating maximum likelihood (ML)-based phylogeny with substitution-derived timing via statistical smoothing. Applied to over 4.5 million genes from 114 plant genomes, we successfully inferred duplication histories across nearly 130,000 orthogroups. This large-scale analysis showed that 53.0% of genes arose from recent, lineage-specific duplications, with high concentrations in particular multi-copy families. Among these, NLR, C48, and P450 families exemplified how recently duplicated genes undergo rapid stepwise structural remodeling. This process was primarily driven by small-scale mutations, including insertions, deletions, and frameshifts, that rapidly accumulated shortly after duplication. By resolving the precise duplication order, we reconstructed these architectural changes, thereby enabling both the inference of putative ancestral structures and the exploration of functional diversification arising from structural remodeling. Structure-based clustering further uncovered that recently duplicated, uncharacterized genes retain core domain structures resembling known functional proteins even across phylogenetically distant species lacking sequence homology. Our findings reveal that recent gene duplications and subsequent structural remodeling represent a widespread and lineage-specific force driving rapid diversification of gene families in plants.