Holocentromeres inRhynchosporaare associated with genome-wide centromere-specific repeat arrays interspersed among euchromatin

Abstract

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.

Absence of positive selection on CenH3 inLuzulasuggests that holokinetic chromosomes may suppress centromere drive

“…The observed absence of positive selection on CenH3 in Luzula is in accordance with a recent finding in Luzula elegans which lacks centromeric repeats that would co-localize with kinetochore formation along an entire chromosome (Heckmann et al, 2013). In contrast, Marques et al (2015) have found a centromeric satellite repeat Tyba co-localized with kinetochore formation in holokinetic Rhynchospora pubera (Cyperaceae). The authors offer two explanations, either the preferential insertion of Tyba sequences into centromeric chromatin might have been facilitated by CenH3 itself or, alternatively, Tyba might define the preferential sites for CenH3 accumulation (Marques et al, 2015).…”

“…In contrast, Marques et al (2015) have found a centromeric satellite repeat Tyba co-localized with kinetochore formation in holokinetic Rhynchospora pubera (Cyperaceae). The authors offer two explanations, either the preferential insertion of Tyba sequences into centromeric chromatin might have been facilitated by CenH3 itself or, alternatively, Tyba might define the preferential sites for CenH3 accumulation (Marques et al, 2015). Analysis of selection on CenH3 in Rhynchospora could help to resolve this dilemma; positively selected CenH3 could support Tybadirected CenH3 accumulation in a centromere drive fashion, while absence of positive selection on CenH3 could suggest that CenH3 facilitated Tyba insertion.…”

“…In holokinetics, however, the dispersion of centromeric nucleosomes in holokinetic chromosomes may make it difficult for any particular sequence to gain an advantage and be amplified the way centromeric satellites can be in monocentrics because the holokinetic kinetochore is already everywhere. In accordance with that, kinetochore formation in monocentrics is mostly colocalized with arrays of centromeric sequences, while such colocalization is mostly absent in holokinetics (Heckman et al, 2013; but see Marques et al, 2015). In fact, all the studies that have addressed selection regimes acting on CenH3 have been carried out on monocentric organisms (e.g.…”

Restructuring of Holocentric Centromeres During Meiosis in the Plant Rhynchospora pubera

“…In interphase, the holocentromeres dissociate and form multiple individual centromere units. During chromosome condensation toward mitotic metaphase, the centromeric units rejoin and form a linear distinct longitudinal centromere within a groove to ensure faithful chromosome segregation (Marques et al 2015).In contrast to mitotic chromosomes, where the (peri)centromeric histone marker H2AThr120ph is also organized in a linear manner, a dispersed distribution was found in meiotic chromosomes of R. pubera. In addition, multiple CENH3 patches enhanced at the poleward chromosome surface of highly condensed metaphase I bivalents were reported (Cabral et al 2014).…”

Chromatin and epigenetics in all their states: Meeting report of the first conference on Epigenetic and Chromatin Regulation of Plant Traits - January 14 – 15, 2016 - Strasbourg, France

“…During mitosis CENH3-containing nucleosomes join, forming a polycentromeric band along the chromosomes. 1 A fraction of histones are non-allelic variants whose incorporation in place of canonical histones can lead to dynamic changes in chromatin structure and functions. Frederic Berger (GMI, Vienna, Austria) presented the work of his group on the histone variant H2A.W in Arabidopsis.…”