A Centromere Satellite Concomitant with Extensive Karyotypic Diversity Across the Peromyscus Genus Defies Predictions of Molecular Drive

Overview

Journal Chromosome Res

Date 2019 Feb 17

PMID 30771198

Citations 18

Authors

Brendan M Smalec

Thomas N Heider

Brianna L Flynn

Rachel J ONeill

Affiliations

Soon will be listed here.

Abstract

A common feature of eukaryotic centromeres is the presence of large tracts of tandemly arranged repeats, known as satellite DNA. However, these centromeric repeats appear to experience rapid evolution under forces such as molecular drive and centromere drive, seemingly without consequence to the integrity of the centromere. Moreover, blocks of heterochromatin within the karyotype, including the centromere, are hotspots for chromosome rearrangements that may drive speciation events by contributing to reproductive isolation. However, the relationship between the evolution of heterochromatic sequences and the karyotypic dynamics of these regions remains largely unknown. Here, we show that a single conserved satellite DNA sequence in the order Rodentia of the genus Peromyscus localizes to recurrent sites of chromosome rearrangements and heterochromatic amplifications. Peromyscine species display several unique features of chromosome evolution compared to other Rodentia, including stable maintenance of a strict chromosome number of 48 among all known species in the absence of any detectable interchromosomal rearrangements. Rather, the diverse karyotypes of Peromyscine species are due to intrachromosomal variation in blocks of repeated DNA content. Despite wide variation in the copy number and location of repeat blocks among different species, we find that a single satellite monomer maintains a conserved sequence and homogenized tandem repeat structure, defying predictions of molecular drive. The conservation of this satellite monomer results in common, abundant, and large blocks of chromatin that are homologous among chromosomes within one species and among diverged species. Thus, such a conserved repeat may have facilitated the retention of polymorphic chromosome variants within individuals and intrachromosomal rearrangements between species-both factors that have previously been hypothesized to contribute towards the extremely wide range of ecological adaptations that this genus exhibits.

Citing Articles

Meiosis-specific distal cohesion site decoupled from the kinetochore.

Pan B, Bruno M, Macfarlan T, Akera T Nat Commun. 2025; 16(1):2116.

PMID: 40032846 PMC: 11876576. DOI: 10.1038/s41467-025-57438-w.

Meiosis-specific decoupling of the pericentromere from the kinetochore.

Pan B, Bruno M, Macfarlan T, Akera T bioRxiv. 2024; .

PMID: 39091844 PMC: 11291024. DOI: 10.1101/2024.07.21.604490.

Comparative analysis of repetitive DNA in dysploid and non-dysploid Phaseolus beans.

Ferraz M, Ribeiro T, Sader M, Nascimento T, Pedrosa-Harand A Chromosome Res. 2023; 31(4):30.

PMID: 37812264 DOI: 10.1007/s10577-023-09739-3.

Satellite DNAs-From Localized to Highly Dispersed Genome Components.

Satovic-Vuksic E, Plohl M Genes (Basel). 2023; 14(3).

PMID: 36981013 PMC: 10048060. DOI: 10.3390/genes14030742.

Maps of Constitutive-Heterochromatin Distribution for Four Species (Mustelidae, Carnivora, Mammalia) Show the Formative Role of Macrosatellite Repeats in Interspecific Variation of Chromosome Structure.

Beklemisheva V, Lemskaya N, Prokopov D, Perelman P, Romanenko S, Proskuryakova A Genes (Basel). 2023; 14(2).

PMID: 36833416 PMC: 9957230. DOI: 10.3390/genes14020489.

References

Alkan C, Ventura M, Archidiacono N, Rocchi M, Sahinalp S, Eichler E . Organization and evolution of primate centromeric DNA from whole-genome shotgun sequence data. PLoS Comput Biol. 2007; 3(9):1807-18. PMC: 1994983. DOI: 10.1371/journal.pcbi.0030181. View

Salser W, Bowen S, Browne D, Fedoroff N, Fry K, Heindell H . Investigation of the organization of mammalian chromosomes at the DNA sequence level. Fed Proc. 1976; 35(1):23-35. View

ARAKAKI D, Sparkes R . The chromosomes of Peromyscus maniculatus hollesteri (deer mouse). Cytologia (Tokyo). 1967; 32(2):180-3. DOI: 10.1508/cytologia.32.180. View

Masumoto H, Nakano M, Ohzeki J . The role of CENP-B and alpha-satellite DNA: de novo assembly and epigenetic maintenance of human centromeres. Chromosome Res. 2004; 12(6):543-56. DOI: 10.1023/B:CHRO.0000036593.72788.99. View

Henikoff S, Malik H . Centromeres: selfish drivers. Nature. 2002; 417(6886):227. DOI: 10.1038/417227a. View

Greenbaum I, Baker R . Determination of the primitive karyotype for Peromyscus. J Mammal. 1978; 59(4):820-34. View

Cacheux L, Ponger L, Gerbault-Seureau M, Loll F, Gey D, Richard F . The Targeted Sequencing of Alpha Satellite DNA in Cercopithecus pogonias Provides New Insight Into the Diversity and Dynamics of Centromeric Repeats in Old World Monkeys. Genome Biol Evol. 2018; 10(7):1837-1851. PMC: 6061836. DOI: 10.1093/gbe/evy109. View

Masumoto H, Masukata H, Muro Y, Nozaki N, Okazaki T . A human centromere antigen (CENP-B) interacts with a short specific sequence in alphoid DNA, a human centromeric satellite. J Cell Biol. 1989; 109(5):1963-73. PMC: 2115871. DOI: 10.1083/jcb.109.5.1963. View

Te G, Dawson W . Chromosomal polymorphism in Peromyscus polionotus. Cytogenetics. 1971; 10(4):225-34. View

10.

Walsh J . Persistence of tandem arrays: implications for satellite and simple-sequence DNAs. Genetics. 1987; 115(3):553-67. PMC: 1216357. DOI: 10.1093/genetics/115.3.553. View

11.

da Silva E, Busso A, Parise-Maltempi P . Characterization and genome organization of a repetitive element associated with the nucleolus organizer region in Leporinus elongatus (Anostomidae: Characiformes). Cytogenet Genome Res. 2012; 139(1):22-8. DOI: 10.1159/000342957. View

12.

Faravelli M, Moralli D, Bertoni L, Attolini C, Chernova O, Raimondi E . Two extended arrays of a satellite DNA sequence at the centromere and at the short-arm telomere of Chinese hamster chromosome 5. Cytogenet Cell Genet. 1999; 83(3-4):281-6. DOI: 10.1159/000015171. View

13.

Fu L, Niu B, Zhu Z, Wu S, Li W . CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012; 28(23):3150-2. PMC: 3516142. DOI: 10.1093/bioinformatics/bts565. View

14.

Gong Z, Wu Y, Koblizkova A, Torres G, Wang K, Iovene M . Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell. 2012; 24(9):3559-74. PMC: 3480287. DOI: 10.1105/tpc.112.100511. View

15.

DAiuto L, Barsanti P, Mauro S, Cserpan I, Lanave C, Ciccarese S . Physical relationship between satellite I and II DNA in centromeric regions of sheep chromosomes. Chromosome Res. 1997; 5(6):375-81. DOI: 10.1023/a:1018444325085. View

16.

Brown J, Strbuncelj M, Giardina C, ONeill R . Interspecific hybridization induced amplification of Mdm2 on double minutes in a Mus hybrid. Cytogenet Genome Res. 2003; 98(2-3):184-8. DOI: 10.1159/000069806. View

17.

ONeill R, ONeill M, Graves J . Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature. 1998; 393(6680):68-72. DOI: 10.1038/29985. View

18.

Bertelsen A, Humayun M, Karfopoulos S, Rush M . Molecular characterization of small polydisperse circular deoxyribonucleic acid from an African green monkey cell line. Biochemistry. 1982; 21(9):2076-85. DOI: 10.1021/bi00538a015. View

19.

LARKIN M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H . Clustal W and Clustal X version 2.0. Bioinformatics. 2007; 23(21):2947-8. DOI: 10.1093/bioinformatics/btm404. View

20.

Pathak S, Hsu T, Arrighi F . Chromosomes of Peromyscus (Rodentia, Cricetidae). IV. The role of heterochromatin in karyotypic evolution. Cytogenet Cell Genet. 1973; 12(5):315-26. DOI: 10.1159/000130470. View