Genome stabilization in the neotetraploid wasabi (Eutrema japonicum): subgenome dominance and extensive chromosomal rearrangements

Wasabi (Eutrema japonicum), a commercially important crop in the Brassicaceae family, is prized for its unique pungent flavor, yet its genome evolution and polyploid origin remain poorly understood. This study presents a detailed evolutionary analysis of the wasabi genome. The diploid progenitors of E. japonicum diverged approximately 2 MYA, while the allotetraploid hybridization event that formed E. japonicum occurred more recently (~ 0.268 MYA). Following this whole-genome duplication, its genome stabilized through extensive chromosomal rearrangements and subgenome dominance. We also characterized transposable elements, including long terminal repeat retrotransposons (LTR-RTs), and analyzed gene expression patterns between subgenomes to further understand genome evolution and functional differentiation in E. japonicum. Notably, wasabi's distinct flavor is linked to a unique glucosinolate gene profile. This profile is characterized by a significant expansion of the epithiospecifier-modifying protein (ESM1) gene family, which promotes pungent isothiocyanate formation, and a contraction of the competing epithiospecifier protein (ESP) gene. The resulting high ESM1:ESP gene copy ratio is a key contributor to wasabi's characteristic properties. This study offers crucial insights into wasabi's genomic evolution, establishing a foundation for future research into the genetic basis of its unique flavor and other valuable traits.