Rapid chromosomal evolution and oligocentromeric drive in sedges and rushes

The chromosomes of most eukaryotes have a single centromere, a specialised region involved in chromosome partitioning to daughter cells. Inter-chromosomal rearrangement risks generating chromosomes with two centromeres or none, disrupting segregation. Holocentric chromosomes, with centromere function distributed along the chromosome, are hypothesised to better tolerate inter-chromosomal rearrangement. However, evidence linking centromere organisation to rearrangement rate has been lacking. Sedges and rushes (Cyperaceae and Juncaceae) are specifically oligocentric: they have several satellite-based centromeres per chromosome. Using 36 chromosome-level genomes, we reconstruct ancestral linkage groups, quantify extraordinary rearrangement rates, and annotate candidate oligocentromeres. Under our model of oligocentromeric drive, we expected satellite sequence, oligocentromere organisation, and karyotype to evolve to exploit biased segregation into the gamete during asymmetric meiosis. We find satellite turnover but also deep sequence conservation. Further, oligocentromeric organisation seems constrained by chromosome size, and rearrangements are more stable when chromosomes have fewer oligocentromeres, despite breakpoint regions being enriched for oligocentromeres. Notably, we find putative monocentromeres in Carex myosuroides, which would be the first evidence for reversion to monocentricity in any eukaryote, and no identifiable oligocentromeres in Cyperus rotundus, possibly a transition to asatellitic holocentricity. Overall, we demonstrate that this clade is powerful for linking centromere organisation to genome evolution.