Genetic diversity and evolution of rice centromeres

Understanding the mechanisms driving centromere evolution is crucial for deciphering eukaryotic evolution and speciation processes. Despite their widely recognized characteristics of conserved function in cell division, the centromeres have showed high diversity in composition and structure between species. The mechanism underlying this paradox remain poorly understood. Here, we assembled 67 high-quality rice genomes from Oryza AA group, encompassing both Asian and African rice species, and conducted an extensive analysis of over 800 nearly complete centromeres. Through de novo annotation of satellite sequences and employing a progressive compression strategy, we quantified the local homogenization and multi-layer nested structures of rice centromeres and found that genetic innovations in rice centromeres primarily arise from internal structural variations and retrotransposon insertions, along with a certain number of non-canonical satellite repeats (sati). Despite these rapid structural alterations, the single-base substitution rate in rice centromeres appears relatively lower compared to the chromosome arms. Contrary to the KARMA model for Arabidopsis centromere evolution, our model (RICE) suggests that centrophilic LTRs contribute to the decline of progenitor centromeres composed of satellite repeats, and facilitate the formation of evolutionary neo-centromeres, which are enriched with extended CENH3 binding regions beyond the native satellite arrays in plant genomes. In summary, this study provides novel insights into genomic divergence and reproductive barriers among rice species and subspecies, and advances our understanding of plant centromere evolution.