Journal Article

Holocentromeres in Rhynchospora are associated with genome-wide centromere-specific repeat arrays interspersed among euchromatin

Tiago Ribeiro, Ronny Brandt, Marco Pellino, Tomáš Beseda, André Marques, André L. L. Vanzela, Wei Ma, Petr Novák, Hana Šimková, Jörg Fuchs, Pavel Neumann, Veit Schubert, Markus Kuhlmann, Jiří Macas, Andrea Pedrosa-Harand, Andreas Houben

2015

Overview

Holocentric chromosomes are characterized by kinetochore activity along each sister chromatid. Although the kinetochore structure seems to be well conserved, as in monocentric organisms, the organization of holocentromeres is still elusive, and no centromeric repeat has been found associated with centromeric histone H3 variant-positive centromeric nucleosomes for any holocentric organism studied hitherto. We demonstrate that holocentrics of the sedge (Cyperaceae) Rhynchospora pubera possess different classes of centromere-specific repeats. Holocentromeres are composed of multiple centromeric units interspersing the gene-containing chromatin, and, as a functional adaption, a cell-cycle–dependent shuffling of centromeric units results in the formation of functional (poly)centromeres during cell division. The genome-wide distribution of centromeric repeat arrays interspersing the euchromatin provides a previously unidentified type of centromere organization. Holocentric chromosomes lack a primary constriction, in contrast to monocentrics. They form kinetochores distributed along almost the entire poleward surface of the chromatids, to which spindle fibers attach. No centromere-specific DNA sequence has been found for any holocentric organism studied so far. It was proposed that centromeric repeats, typical for many monocentric species, could not occur in holocentrics, most likely because of differences in the centromere organization. Here we show that the holokinetic centromeres of the Cyperaceae Rhynchospora pubera are highly enriched by a centromeric histone H3 variant-interacting centromere-specific satellite family designated “Tyba” and by centromeric retrotransposons (i.e., CRRh) occurring as genome-wide interspersed arrays. Centromeric arrays vary in length from 3 to 16 kb and are intermingled with gene-coding sequences and transposable elements. We show that holocentromeres of metaphase chromosomes are composed of multiple centromeric units rather than possessing a diffuse organization, thus favoring the polycentric model. A cell-cycle–dependent shuffling of multiple centromeric units results in the formation of functional (poly)centromeres during mitosis. The genome-wide distribution of centromeric repeat arrays interspersing the euchromatin provides a previously unidentified type of centromeric chromatin organization among eukaryotes. Thus, different types of holocentromeres exist in different species, namely with and without centromeric repetitive sequences.

• Publisher: National Acad Sciences,National Academy of Sciences
• Subject: Biological Sciences / Cell cycle / Centromere / Chromatin / Chromosomes / Cyperaceae / Cyperaceae - genetics / DNA, Satellite - genetics / Euchromatin - genetics / Eukaryotes / Flowers & plants / Genome, Plant / Genomics / Molecular Sequence Data / Rhynchospora / Tandem Repeat Sequences