Three near-complete genome assemblies reveal substantial centromere dynamics from diploid to tetraploid in Brachypodium genus. Brachypodium

Centromeres are critical for maintaining genomic stability in eukaryotes, and their turnover can shape genome architectures and drive karyotype evolution. However, the co-evolution of centromeres from different species in allopolyploids over millions of years remains largely unknown. Here, we generated three near-complete genome assemblies, including a tetraploid Brachypodium hybridum and its two diploid ancestors, B. distachyon and B. stacei. We found high degrees of sequence, structural and epigenetic variations of centromeres at base-pair resolution between closely related Brachypodium genomes, indicating the appearance and accumulation of species-specific centromeres from a common origin during evolution. We also observed that centromere homogenization was accompanied by local satellite repeats bursting and retrotransposon purging, and the frequency of retrotransposon invasions drove the degree of inter-species centromere diversifications. We further surveyed the dynamics of centromeres during alloploidization process, and found that dramatic genetics and epigenetics architecture variations were associated with the turnover of centromeres between homologous chromosomal pairs from diploid to tetraploid. Additionally, our pangenomes analysis revealed that ongoing variations of satellite repeats and stable evolutionary homeostasis within centromeres among individuals of each Brachypodium genome with different polyploidy levels. Our results provide unprecedented information on the (epi)genomic and functional diversity of highly repetitive DNAs between closely related species and their allopolyploid genomes at both coarse and fine scale.