The holocentric species Luzula elegans shows interplay between centromere and large‐scale genome organization

Abstract

SUMMARYIn higher plants, the large-scale structure of monocentric chromosomes consists of distinguishable eu-and heterochromatic regions, the proportions and organization of which depend on a species' genome size. To determine whether the same interplay is maintained for holocentric chromosomes, we investigated the distribution of repetitive sequences and epigenetic marks in the woodrush Luzula elegans (3.81 Gbp/1C). Sixtyone per cent of the L. elegans genome is characterized by highly repetitive DNA, with over 30 distinct sequence families encoding an exceptionally high diversity of satellite repeats. Over 33% of the genome is composed of the Angela clade of Ty1/copia LTR retrotransposons, which are uniformly dispersed along the chromosomes, while the satellite repeats occur as bands whose distribution appears to be biased towards the chromosome termini. No satellite showed an almost chromosome-wide distribution pattern as expected for a holocentric chromosome and no typical centromere-associated LTR retrotransposons were found either. No distinguishable large-scale patterns of eu-and heterochromatin-typical epigenetic marks or early/late DNA replicating domains were found along mitotic chromosomes, although super-high-resolution light microscopy revealed distinguishable interspersed units of various chromatin types. Our data suggest a correlation between the centromere and overall genome organization in species with holocentric chromosomes.

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

“…Therefore, we applied antibodies against typical euchromatin-and heterochromatin-associated histone methylation marks (H3K4me3 and H3K9me2, respectively). In agreement with other holocentric species (15,27) the euchromatin and heterochromatic domains in R. pubera were found dispersed along the entire chromosomes (SI Appendix, Fig. S1 C and D).…”

“…far for any species possessing holocentric chromosomes (14)(15)(16)(17). For instance, Heckmann, et al (15) have characterized the high-copy fraction of the Luzula elegans genome in detail, and none of the identified repeats showed colocalization with the holokinetic centromere.…”

“…For instance, Heckmann, et al (15) have characterized the high-copy fraction of the Luzula elegans genome in detail, and none of the identified repeats showed colocalization with the holokinetic centromere. Even in C. elegans, where robust studies [Chip-on chip (ChIP-chip) and ChIP sequencing (ChIP-seq)] were performed, no centromere-specific repeats were identified (14,16).…”

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).…”

“…Henikoff et al, 2001;Talbert et al, 2004;Hirsch et al, 2009;Schueler et al, 2010) or on Caenorhabditis (Zedek and Bures, 2012) which is holokinetic in mitosis but forms a cup-like kinetochore in meiosis with ambiguous utilization of CenH3 (Chan et al, 2004;Monen et al, 2005). If the recurrent adaptive evolution of CenH3 is really a consequence of centromere drive, it should be missing (or at least less frequent) not only in lineages with symmetric meiosis but also in lineages with asymmetric meiosis that possess holokinetic chromosomes, such as the plant genus Luzula (Heckmann et al, 2013).…”