Population Scale Analysis of Centromeric Satellite DNA Reveals Highly Dynamic Evolutionary Patterns and Genomic Organization in Long-Tailed and Rhesus Macaques

Singchat, Worapong; Ahmad, Syed Farhan; Jaisamut, Kitipong; Panthum, Thitipong; Ariyaraphong, Nattakan; Kraichak, Ekaphan; Muangmai, Narongrit; Duengkae, Prateep; Payungporn, Sunchai; Malaivijitnond, Suchinda; Srikulnath, Kornsorn

doi:10.3390/cells11121953

Cited by 3 publications

(3 citation statements)

References 153 publications

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“…In the last decade, several studies have shed light on the rapid evolution of centromere sequences in a wide range of species 9 . However in most studies, centromeres generally remain associated with the same type of repeat element, shifting to different variants of related repeats (either retroelements or satellites) [43][44][45][46][47][48][49][50] thus maintaining a certain homogeneity in the type of centromeric sequence among closely related species. For example, human and its closely related species -chimpanzee, orangutan, and macaque -diverged about 7 million years ago but all centromeres are populated by different subfamilies of the 𝛼-satellite repeat 44,45 .…”

Section: Discussionmentioning

confidence: 99%

“…For example, human and its closely related species -chimpanzee, orangutan, and macaque -diverged about 7 million years ago but all centromeres are populated by different subfamilies of the 𝛼-satellite repeat 44,45 . Arabidopsis species, A. thaliana and A. lyrate, also experienced a turnover of centromere sequences in the 5-6 My since their divergence 51 , but between related satellites 46 . In our study of Drosophila, we highlight a complete turnover of centromere sequences to categorically different repeats -satellites and retroelements -between closely related species.…”

Section: Discussionmentioning

confidence: 99%

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

Courret,

Hemmer,

Wei

et al. 2023

Preprint

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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

Courret,

Hemmer,

Wei

et al. 2023

Preprint

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“…This may be explained by the fact that centromeric repeat variation occurred via deletion, insertion, and inversion or by mixing of different parental sequences during allopolyploid formation. These processes actively contribute to variability in retrotransposon nucleotide sequences, size, and number in oat centromeres ( 60 , 61 ), and also result in the variation of non–B-DNA structures, affecting centromere function. Despite the differences in sequence composition, the enrichment of predicted non–B-DNA structures was remarkably conserved in oat centromeres with different ploidy levels ( Fig.…”

Section: Discussionmentioning

confidence: 99%

Non–B-form DNA tends to form in centromeric regions and has undergone changes in polyploid oat subgenomes

Liu

Zhang

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Centromeres are the specialized regions of the chromosomes that direct faithful chromosome segregation during cell division. Despite their functional conservation, centromeres display features of rapidly evolving DNA and wide evolutionary diversity in size and organization. Previous work found that the noncanonical B-form DNA structures are abundant in the centromeres of several eukaryotic species with a possible implication for centromere specification. Thus far, systematic studies into the organization and function of non–B-form DNA in plants remain scarce. Here, we applied the oat system to investigate the role of non–B-form DNA in centromeres. We conducted chromatin immunoprecipitation sequencing using an antibody to the centromere-specific histone H3 variant (CENH3); this accurately positioned oat centromeres with different ploidy levels and identified a series of centromere-specific sequences including minisatellites and retrotransposons. To define genetic characteristics of oat centromeres, we surveyed the repeat sequences and found that dyad symmetries were abundant in oat centromeres and were predicted to form non–B-DNA structures in vivo. These structures including bent DNA, slipped DNA, Z-DNA, G-quadruplexes, and R-loops were prone to form within CENH3-binding regions. Dynamic conformational changes of predicted non–B-DNA occurred during the evolution from diploid to tetraploid to hexaploid oat. Furthermore, we applied the single-molecule technique of AFM and DNA:RNA immunoprecipitation with deep sequencing to validate R-loop enrichment in oat centromeres. Centromeric retrotransposons exhibited strong associations with R-loop formation. Taken together, our study elucidates the fundamental character of non–B-form DNA in the oat genome and reveals its potential role in centromeres.

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

Courret,

Hemmer,

Wei

et al. 2024

PLoS Biol

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Centromeres reside in rapidly evolving, repeat-rich genomic regions, despite their essential function in chromosome segregation. Across organisms, centromeres are rich in selfish genetic elements such as transposable elements and satellite DNAs that can bias their transmission through meiosis. However, these elements still need to cooperate at some level and contribute to, or avoid interfering with, 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. Using chromatin profiling combined with high-resolution fluorescence in situ hybridization on stretched chromatin fibers, we characterize all centromeres across these species. 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 telocentric chromosomes in D. sechellia, where the X and fourth centromeres now sit on telomere-specific retroelements. Finally, the Y chromosome centromeres, which are the only chromosomes that do not experience female meiosis, do not show dynamic cycling between satDNA and TEs. The patterns of rapid centromere turnover in these species are consistent with genetic conflicts in the female germline and have implications for centromeric DNA function and karyotype evolution. Regardless of the evolutionary forces driving this turnover, the rapid reorganization of centromeric sequences over short evolutionary timescales highlights their potential as hotspots for evolutionary innovation.

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Population Scale Analysis of Centromeric Satellite DNA Reveals Highly Dynamic Evolutionary Patterns and Genomic Organization in Long-Tailed and Rhesus Macaques

Cited by 3 publications

References 153 publications

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

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

Non–B-form DNA tends to form in centromeric regions and has undergone changes in polyploid oat subgenomes

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

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