Turnover of retroelements and satellite DNA drives centromere reorganization over short evolutionary timescales in Drosophila

Abstract

Despite their essential function in chromosome segregation, centromeres reside in rapidly evolving, repeat-rich genomic regions. Across organisms, centromeres are rich in selfish genetic elements like transposable elements and satellite DNAs that can bias their transmission through meiosis, but still need to contribute to centromere function. To gain insight into the balance between conflict and cooperation at centromeric DNA, we take advantage of the close evolutionary relationships within the Drosophila simulans clade - D. simulans, D. sechellia, and D. mauritiana - and their relative, D. melanogaster. We discovered dramatic centromere reorganization involving recurrent shifts between retroelements and satellite DNAs over short evolutionary timescales. We also reveal the recent origin (<240 Kya) of truly telocentric chromosomes in D. sechellia, where X and dot centromeres now sit on telomere-specific retroelements. This rapid centromere turnover is consistent with genetic conflicts in the female germline and has implications for centromeric DNA function and karyotype evolution.

Transcription of a centromere-enriched retroelement and local retention of its RNA are significant features of the CENP-A chromatin landscape

“…Jockey-3 is enriched at the centromere compared to the rest of the genome (Chang et al, 2019) and is a recently active retroelement with weak insertional bias for the centromere in population studies (Hemmer et al, 2023). The centromeres of three species within the Drosophila simulans clade, D. simulans , D. mauritiana , and D. sechellia , and D. melanogaster display a remarkable turnover in sequence composition suggesting the existence of a genetic conflict between satellites and retroelements (Courret et al, 2023). To ensure their own propagation through generations, these selfish genetic elements appear to compete for dominance at the centromere, a region with low recombination that can tolerate variation in sequence composition without loss of functionality.…”

“…To ensure their own propagation through generations, these selfish genetic elements appear to compete for dominance at the centromere, a region with low recombination that can tolerate variation in sequence composition without loss of functionality. Since Jockey-3 is targeted by piRNA-mediated silencing in the germline (Courret et al, 2023), its preferential insertion at centromeres could provide an advantage for its continuous propagation since centromeres are typically not associated with heterochromatin (Courret et al, 2023; Hemmer et al, 2023; McKinley and Cheeseman, 2016; Sullivan and Karpen, 2004). In turn, Jockey-3 could benefit the host by promoting local transcription, which would facilitate chromatin remodeling during CENP-A deposition.…”

The structure, function, and evolution of plant centromeres

“…Outside of land plants, the green algae Chlamydomonas reinhardtii has centromeres composed of ZeppL LINE retroelements ( Craig et al 2021 , 2023 ). In animals, retrotransposons also show strong associations with centromeres, including LINE elements in humans ( Logsdon et al 2021 ; Hoyt et al 2022 ), KERV endogenous retroviruses in kangaroo ( Ferreri et al 2011 ), and Jockey LINE elements in Drosophila ( Chang et al 2019 ; Courret et al 2023 ). Hence, diverse families of centrophilic retroelements are observed across eukaryotic species, potentially representing multiple instances of convergent centrophilic adaptation.…”

“…3 C). It is easy to conceive how a successful centrophilic retrotransposon could colonize and take over a satellite-based centromere, such as observed in Einkorn wheat and Drosophila ( Ahmed et al 2023 ; Courret et al 2023 ). Yet, how centromere satellite arrays can emerge from a transposon-based architecture remains unclear, although evidence exists for formation of tandem repeats from centrophilic retrotransposons in plants ( Cheng and Murata 2003 ; Ito et al 2004 ; Sharma et al 2013 ), CR1-C retrotransposons in chicken ( Shang et al 2010 ), and centromeric KERVs in kangaroo ( Koga et al 2023 ).…”

High levels of intra-strain structural variation in Drosophila simulans X pericentric heterochromatin

“…We use a cytogenetic approach to document high levels of structural polymorphism in satellite DNAs in the X pericentromere: Rsp-like and 500-bp satellites. Rsp-like is a complex satellite specific to the X pericentromere in D. simulans ( Sproul et al 2020 ) and the 500-bp satellite is associated with the centromere and pericentromere of the X chromosome and the autosomes in D. simulans ( Talbert et al 2018 ; Courret et al 2023a ). The structural polymorphisms we detect involve large blocks of satellite repeats and occur between different strains, within a strain, and even within individual isolates of strains kept in a single lab.…”