Islands of retroelements are major components of Drosophila centromeres

Abstract

Centromeres are essential chromosomal regions that mediate kinetochore assembly and spindle attachments during cell division. Despite their functional conservation, centromeres are among the most rapidly evolving genomic regions and can shape karyotype evolution and speciation across taxa. Although significant progress has been made in identifying centromere-associated proteins, the highly repetitive centromeres of metazoans have been refractory to DNA sequencing and assembly, leaving large gaps in our understanding of their functional organization and evolution. Here, we identify the sequence composition and organization of the centromeres of Drosophila melanogaster by combining long-read sequencing, chromatin immunoprecipitation for the centromeric histone CENP-A, and high-resolution chromatin fiber imaging. Contrary to previous models that heralded satellite repeats as the major functional components, we demonstrate that functional centromeres form on islands of complex DNA sequences enriched in retroelements that are flanked by large arrays of satellite repeats. Each centromere displays distinct size and arrangement of its DNA elements but is similar in composition overall. We discover that a specific retroelement, G2/Jockey-3 , is the most highly enriched sequence in CENP-A chromatin and is the only element shared among all centromeres. G2/Jockey-3 is also associated with CENP-A in the sister species D . simulans , revealing an unexpected conservation despite the reported turnover of centromeric satellite DNA. Our work reveals the DNA sequence identity of the active centromeres of a premier model organism and implicates retroelements as conserved features of centromeric DNA.

Long transposon-rich centromeres in an oomycete reveal divergence of centromere features in Stramenopila-Alveolata-Rhizaria lineages

“…The distribution of H3K9me3 and H3K27me3 is generally coincident throughout the genome, and both were colocalized with the CENP-A binding regions (S7 Fig). Intriguingly, the heterochromatic region extended 8 kb to 64 kb beyond each CENP-A binding region (Table 1 and Fig 4A), similar to pericentromeric heterochromatin regions described in other species [14,22,42]. In contrast, the euchromatic mark H3K4me2 was excluded from the CENP-A region and its flanking heterochromatic https://doi.org/10.1371/journal.pgen.1008646.g003 https://doi.org/10.1371/journal.pgen.1008646.g005…”

“…Emerging long-read sequencing technologies, such as Pacific Bioscience (PacBio) and Oxford Nanopore Technology (ONT), have led to substantial advances in resolution of chromosomal structures including highly repetitive sequences such as centromeres. Using these technologies, centromeres that were difficult to resolve using short-read sequencing, were defined in various organisms, from fungi [13,20,21] to insects [22], plants [23] and humans [24].…”

Host–transposon interactions: conflict, cooperation, and cooption

“…As such, telomeric retroelements have long been regarded as the prototypical example of host-TE mutualism (Kidwell and Lisch 2001), although recent data have challenged this view (see below). Intriguingly, evidence is mounting that a distantly related family of non-LTR retrotransposons (G2/jockey3) contributes directly to the organization and function of centromeres of D. melanogaster and its sister species, D. simulans (Chang et al 2019). Thus, several Drosophila retroelements appear directly involved in the faithful replication and segregation of chromosomes.…”

“What You Need, Baby, I Got It”: Transposable Elements as Suppliers of Cis-Operating Sequences in Drosophila

“…A profound cooperation between three LINE-like elements (HeT-A, TAHRE, and TART) allows both their transposition and stability of host chromosomes [105]. In addition, a suggestive hypothesis has been proposed that directly links the organization and function of centromeres of D. melanogaster and D. simulans to the ability of the G2/Jockey-3 transposon to recruit the centromeric protein CENP-A [106].…”