Comparative genomics across Linum illuminates the evolutionary basis of flax domestication, genome diversification,...

Flax (Linum usitatissimum L.) is a globally significant dual-purpose crop cultivated for both bast fiber and seed oil, yet the genomic basis of its diversification and domestication from wild relatives remains incompletely understood. In this study, we performed a comprehensive comparative genomic analysis of 11 Linum accessions-including five cultivated flax accessions and their wild progenitor Linum bienne-alongside two outgroups (Populus trichocarpa and Erythroxylum novogranatense). To reduce annotation heterogeneity, we uniformly re-annotated all genomes using the deep-learning-based ANNEVO pipeline, which reduced apparent gene fragmentation and maintained broadly comparable annotation completeness under a unified framework. Phylogenomic analysis resolved a pre-domestication macro-evolutionary gene family expansion in the L. bienne-L. usitatissimum lineage, providing standing genetic variation that subsequently diverged into pathways enriched for cell wall biogenesis in fiber flax and lipid/photosynthetic metabolism in oil flax. Genome-wide NLR analysis revealed a globally contracted immune receptor repertoire in Linum and quantitative stability between cultivated flax and L. bienne, while chromosomal distribution and synteny analyses indicated that a major NLR-rich region differs in chromosome assignment between L. bienne and cultivated flax rather than providing definitive evidence for de novo cluster gain or complete cluster loss. Furthermore, genome size variation across Linum was predominantly driven by transposable elements, with remarkably recent bursts of long terminal repeat (LTR) retrotransposons (<0.5 Mya) shared by cultivated flax and L. bienne but clearly predating human domestication, indicating an inherited repeat landscape rather than a domestication-associated event. Finally, analysis of fatty acid desaturases revealed striking evolutionary asymmetry: the FAD3 family remained highly conserved, whereas FAD2 exhibited exceptional plasticity, characterized by lineage-specific tandem expansions and a putative large structural absence associated with the contracted FAD2 repertoire in the oil flax accession T397. Together, these findings provide a standardized genomic framework for Linum and illuminate the structural variations, repeat dynamics, and pre-adaptive gene duplications that may have contributed to flax domestication and agronomic specialization.