Functional monocentricity with holocentric characteristics and chromosome-specific centromeres in a stick insect.

Abstract

Centromeres are essential for chromosome segregation in eukaryotes, yet their specification is unexpectedly diverse among species and can involve major transitions such as those from localized to chromosome-wide centromeres between monocentric and holocentric species. How this diversity evolves remains elusive. We discovered within-cell variation in the recruitment of the major centromere protein CenH3, reminiscent of variation typically observed among species. While CenH3-containing nucleosomes are distributed in a monocentric fashion on autosomes and bind tandem repeat sequences specific to individual or groups of chromosomes, they show a longitudinal distribution and broad intergenic binding on the X chromosome, which partially recapitulates phenotypes known from holocentric species. Despite this variable CenH3 distribution among chromosomes, all chromosomes are functionally monocentric, marking the first instance of a monocentric species with chromosome-wide CenH3 deposition. Together, our findings illustrate a potential transitional state between mono- and holocentricity or toward CenH3-independent centromere determination and help to understand the rapid centromere sequence divergence between species.