Repeat-based holocentromeres influence genome architecture and karyotype evolution

The centromere represents a single region in most eukaryotic chromosomes. However, several plant and animal lineages assemble holocentromeres along the entire chromosome length. Here, we compare genome organization and evolution as a function of centromere type by assembling chromosome-scale holocentric genomes with repeat-based holocentromeres from three beak-sedge (Rhynchospora pubera, R. breviuscula, and R. tenuis) and their closest monocentric relative, Juncus effusus. We demonstrate that transition to holocentricity affected 3D genome architecture by redefining genomic compartments, while distributing centromere function to thousands of repeat-based centromere units genome-wide. We uncover a complex genome organization in R. pubera that hides its unexpected octoploidy and describe a marked reduction in chromosome number for R. tenuis, which has only two chromosomes. We show that chromosome fusions, facilitated by repeat-based holocentromeres, promoted karyotype evolution and diploidization. Our study thus sheds light on several important aspects of genome architecture and evolution influenced by centromere organization. [Display omitted] •Chromosome-scale genomes for holocentric plants with repeat-based holocentromeres•Transition to holocentricity influenced the 3D (epi)genome architecture•Regulation of repeat-based centromeres is conserved in mono- and holocentrics•Chromosome fusions drive karyotype evolution and structural diploidization While most eukaryotes contain single regional centromeres, several plant and animal lineages assemble holocentromeres along the entire chromosome length. The assembly of chromosome-scale holocentric genomes with repeat-based holocentromeres from beak-sedges and their closest monocentric relative sheds light on important aspects of genome architecture and evolution influenced by centromere organization.