Repeat-based holocentromeres of the woodrushLuzula sylvaticareveal new insights into the evolutionary transition from mono- to holocentricity

Abstract

AbstractAlthough the centromere is restricted to a single region of the chromosome in most studied eukaryotes, members of the rush family (Juncaceae) harbor either monocentric (Juncus)or holocentric (Luzula) chromosomes. This provides an opportunity to study the evolutionary mechanisms involved in the transition to holocentricity. Here by combining chromosome-scale genome assembly, epigenetic analyses, immuno-FISH, and super-resolution microscopy, we report the occurrence of repeat-based holocentromeres inL. sylvatica. We found an irregular distribution of genes, centromeric units, and most repeats along the chromosomes. We determined the centromere function predominantly associated with two satellite DNA repeats,Lusy1andLusy2of 124– and 174-bp monomer length, respectively, while CENH3 also binds satellite-free gene-poor regions. Comparative repeat analysis revealed thatLusy1is present in mostLuzulaspecies, suggesting a conserved centromere role of this repeat. Synteny betweenL. sylvatica(n= 6) andJ. effusus(n= 21) genomes further evidenced a chromosome number reduction inLuzuladerived from multiple chromosome fusions of ancestralJ. effusus-like chromosomes. We propose that the transition to holocentricity inLuzulainvolves: (i) fusion of small chromosomes resemblingJuncus-like centromeres; (ii) expansion of atypical centromeric units; and (iii) colonization of satellite DNA for centromere stabilization.