Repetitive sequences form a substantial and still enigmatic part of the mammalian genome. We isolated repetitive DNA blocks of the X chromosomes of three species of the family Bovidae: Kobus defassa (KDEXr sequence), Bos taurus (BTAXr sequence) and Antilope cervicapra (ACEXr sequence). The copy numbers of the isolated sequences were assessed using qPCR, and their chromosomal localisations were analysed using FISH in ten bovid tribes and in outgroup species. Besides their localisation on the X chromosome, their presence was also revealed on the Y chromosome and autosomes in several species. The KDEXr sequence abundant in most Bovidae species also occurs in distant taxa (Perissodactyla and Carnivora) and seems to be evolutionarily older than BTAXr and ACEXr. The ACEXr sequence, visible only in several Antilopini species using FISH, is probably the youngest, and arised in an ancestor common to Bovidae and Cervidae. All three repetitive sequences analysed in this study are interspersed among gene-rich regions on the X chromosomes, apparently preventing the crossing-over in their close vicinity. This study demonstrates that repetitive sequences on the X chromosomes have undergone a fast evolution, and their variation among related species can be beneficial for evolutionary studies.

Department of Genetics and Reproductive Biotechnologies Central European Institute of Technology Veterinary Research Institute Hudcova 70 621 00 Brno Czech Republic

Zobrazit více v PubMed

Cioffi M.B., Bertollo L.A.C. Chromosomal Distribution and Evolution of Repetitive DNAs in Fish. Genome Dyn. 2012;7:197–221. doi: 10.1159/000337950. PubMed DOI

Bierhoff H., Postepska-Igielska A., Grummt I. Noisy Silence: Non-Coding RNA and Heterochromatin Formation at Repetitive Elements. Epigenetics. 2014;9:53–61. doi: 10.4161/epi.26485. PubMed DOI PMC

Protasova M.S., Andreeva T.V., Rogaev E.I. Factors Regulating the Activity of LINE1 Retrotransposons. Genes. 2021;12:1562. doi: 10.3390/genes12101562. PubMed DOI PMC

Ugarković Đ., Sermek A., Ljubić S., Feliciello I. Satellite DNAs in Health and Disease. Genes. 2022;13:1154. doi: 10.3390/genes13071154. PubMed DOI PMC

Chung T.H., Zhuravskaya A., Makeyev E.V. Regulation Potential of Transcribed Simple Repeated Sequences in Developing Neurons. Hum. Genet. 2023 doi: 10.1007/s00439-023-02626-1. PubMed DOI PMC

Vourc’h C., Biamonti G. Transcription of Satellite DNAs in Mammals. Prog. Mol. Subcell. Biol. 2011;51:95–118. doi: 10.1007/978-3-642-16502-3_5. PubMed DOI

Hall L.E., Mitchell S.E., O’Neill R.J. Pericentric and Centromeric Transcription: A Perfect Balance Required. Chromosome Res. 2012;20:535–546. doi: 10.1007/s10577-012-9297-9. PubMed DOI

Biémont C., Vieira C. Genetics: Junk DNA as an Evolutionary Force. Nature. 2006;443:521–524. doi: 10.1038/443521a. PubMed DOI

Escudeiro A., Adega F., Robinson T.J., Heslop-Harrison J.S., Chaves R. Conservation, Divergence, and Functions of Centromeric Satellite DNA Families in the Bovidae. Genome Biol. Evol. 2019;11:1152–1165. doi: 10.1093/gbe/evz061. PubMed DOI PMC

Raskina O., Barber J.C., Nevo E., Belyayev A. Repetitive DNA and Chromosomal Rearrangements: Speciation-Related Events in Plant Genomes. Cytogenet. Genome Res. 2008;120:351–357. doi: 10.1159/000121084. PubMed DOI

Żylicz J.J., Heard E. Molecular Mechanisms of Facultative Heterochromatin Formation: An X-Chromosome Perspective. Annu. Rev. Biochem. 2020;89:255–282. doi: 10.1146/annurev-biochem-062917-012655. PubMed DOI

Mezzasalma M., Andreone F., Glaw F., Guarino F.M., Odierna G., Petraccioli A., Picariello O. Changes in Heterochromatin Content and Ancient Chromosome Fusion in the Endemic Malagasy Boid Snakes Sanzinia and Acrantophis (Squamata: Serpentes) Salamandra. 2019;55:140–144.

Thelma B.K., Juyal R.C., Tewari R., Rao S.R. Does Heterochromatin Variation Potentiate Speciation? A Study in Nesokia. Cytogenet. Cell Genet. 1988;47:204–208. doi: 10.1159/000132550. PubMed DOI

Charlesworth D., Charlesworth B., Marais G. Steps in the Evolution of Heteromorphic Sex Chromosomes. Heredity. 2005;95:118–128. doi: 10.1038/sj.hdy.6800697. PubMed DOI

Piumi F., Schibler L., Vaiman D., Oustry A., Cribiu E.P. Comparative Cytogenetic Mapping Reveals Chromosome Rearrangements between the X Chromosomes of Two Closely Related Mammalian Species (Cattle and Goats) Cytogenet. Cell Genet. 1998;81:36–41. doi: 10.1159/000015004. PubMed DOI

Robinson T.J., Harrison W.R., Ponce de León F.A., Davis S.K., Elder F.F. A Molecular Cytogenetic Analysis of X Chromosome Repatterning in the Bovidae: Transpositions, Inversions, and Phylogenetic Inference. Cytogenet. Cell Genet. 1998;80:179–184. doi: 10.1159/000014976. PubMed DOI

Robinson T.J., Cernohorska H., Kubickova S., Vozdova M., Musilova P., Ruiz-Herrera A. Chromosomal Evolution in Raphicerus Antelope Suggests Divergent X Chromosomes May Drive Speciation through Females, Rather than Males, Contrary to Haldane’s Rule. Sci. Rep. 2021;11:3152. doi: 10.1038/s41598-021-82859-0. PubMed DOI PMC

Gallagher D.S., Davis S.K., De Donato M., Burzlaff J.D., Womack J.E., Taylor J.F., Kumamoto A.T. A Molecular Cytogenetic Analysis of the Tribe Bovini (Artiodactyla: Bovidae: Bovinae) with an Emphasis on Sex Chromosome Morphology and NOR Distribution. Chromosome Res. 1999;7:481–492. doi: 10.1023/A:1009254014526. PubMed DOI

Iannuzzi L., Di Meo G.P., Perucatti A., Incarnato D., Schibler L., Cribiu E.P. Comparative FISH Mapping of Bovid X Chromosomes Reveals Homologies and Divergences between the Subfamilies Bovinae and Caprinae. Cytogenet. Cell Genet. 2000;89:171–176. doi: 10.1159/000015607. PubMed DOI

Iannuzzi L., King W.A., Di Berardino D. Chromosome Evolution in Domestic Bovids as Revealed by Chromosome Banding and FISH-Mapping Techniques. Cytogenet. Genome Res. 2009;126:49–62. doi: 10.1159/000245906. PubMed DOI

Rubes J., Musilova P., Kopecna O., Kubickova S., Cernohorska H., Kulemsina A.I. Comparative Molecular Cytogenetics in Cetartiodactyla. Cytogenet. Genome Res. 2012;137:194–207. doi: 10.1159/000338932. PubMed DOI

Proskuryakova A.A., Kulemzina A.I., Perelman P.L., Makunin A.I., Larkin D.M., Farré M., Kukekova A.V., Lynn Johnson J., Lemskaya N.A., Beklemisheva V.R., et al. X Chromosome Evolution in Cetartiodactyla. Genes. 2017;8:216. doi: 10.3390/genes8090216. PubMed DOI PMC

Rubes J., Kubickova S., Pagacova E., Cernohorska H., Di Berardino D., Antoninova M., Vahala J., Robinson T.J. Phylogenomic Study of Spiral-Horned Antelope by Cross-Species Chromosome Painting. Chromosome Res. 2008;16:935–947. doi: 10.1007/s10577-008-1250-6. PubMed DOI

Cernohorska H., Kubickova S., Vahala J., Rubes J. Molecular Insights into X;BTA5 Chromosome Rearrangements in the Tribe Antilopini (Bovidae) Cytogenet. Genome Res. 2012;136:188–198. doi: 10.1159/000336248. PubMed DOI

Cernohorska H., Kubickova S., Kopecna O., Vozdova M., Matthee C.A., Robinson T.J., Rubes J. Nanger, Eudorcas, Gazella, and Antilope Form a Well-Supported Chromosomal Clade within Antilopini (Bovidae, Cetartiodactyla) Chromosoma. 2015;124:235–247. doi: 10.1007/s00412-014-0494-5. PubMed DOI

Chaves R., Guedes-Pinto H., Heslop-Harrison J.S. Phylogenetic Relationships and the Primitive X Chromosome Inferred from Chromosomal and Satellite DNA Analysis in Bovidae. Proc. Biol. Sci. 2005;272:2009–2016. doi: 10.1098/rspb.2005.3206. PubMed DOI PMC

Kopecna O., Kubickova S., Cernohorska H., Cabelova K., Vahala J., Rubes J. Isolation and Comparison of Tribe-Specific Centromeric Repeats within Bovidae. J. Appl. Genet. 2012;53:193–202. doi: 10.1007/s13353-011-0080-y. PubMed DOI

Kopecna O., Kubickova S., Cernohorska H., Cabelova K., Vahala J., Martinkova N., Rubes J. Tribe-specific satellite DNA in non-domestic Bovidae. Chromosome Res. 2014;22:277–291. doi: 10.1007/s10577-014-9401-4. PubMed DOI

Pauciullo A., Kubickova S., Cernohorska H., Petrova K., Di Berardino D., Ramunno L., Rubes J. Isolation and Physical Localization of New Chromosome-Specific Centromeric Repeats in Farm Animals. Veterinární Medicína. 2006;51:224–231. doi: 10.17221/5541-VETMED. DOI

Cabelova K., Kubickova S., Cernohorska H., Rubes J. Male-Specific Repeats in Wild Bovidae. J. Appl. Genet. 2012;53:423–433. doi: 10.1007/s13353-012-0108-y. PubMed DOI

Traut W., Vogel H., Glöckner G., Hartmann E., Heckel D.G. High-Throughput Sequencing of a Single Chromosome: A Moth W Chromosome. Chromosome Res. 2013;21:491–505. doi: 10.1007/s10577-013-9376-6. PubMed DOI

Rossetti C., Genualdo V., Incarnato D., Mottola F., Perucatti A., Pauciullo A. State of the Art on the Physical Mapping of the Y-Chromosome in the Bovidae and Comparison with Other Species—A Review. Anim. Biosci. 2022;35:1289–1302. doi: 10.5713/ab.21.0480. PubMed DOI PMC

Cernohorska H., Kubickova S., Vahala J., Robinson T.J., Rubes J. Cytotypes of Kirk’s Dik-Dik (Madoqua Kirkii, Bovidae) Show Multiple Tandem Fusions. Cytogenet. Genome Res. 2011;132:255–263. doi: 10.1159/000322483. PubMed DOI

Robinson T.J., Cernohorska H., Diedericks G., Cabelova K., Duran A., Matthee C.A. Phylogeny and Vicariant Speciation of the Grey Rhebok, Pelea Capreolus. Heredity. 2014;112:325–332. doi: 10.1038/hdy.2013.108. PubMed DOI PMC

Gallagher D.S., Jr., Womack J.E. Chromosome Conservation in the Bovidae. J. Hered. 1992;83:287–298. doi: 10.1093/oxfordjournals.jhered.a111215. PubMed DOI

Groves C., Grubb P. Ungulate Taxonomy. 1st ed. Johns Hopkins University Press; Baltimore, MD, USA: 2011.

Kubickova S., Cernohorska H., Musilova P., Rubes J. The Use of Laser Microdissection for the Preparation of Chromosome-Specific Painting Probes in Farm Animals. Chromosome Res. 2002;10:571–577. doi: 10.1023/A:1020914702767. PubMed DOI

Zimin A.V., Delcher A.L., Florea L., Kelley D.R., Schatz M.C., Puiu D., Hanrahan F., Pertea G., Van Tassell C.P., Sonstegard T.S., et al. A Whole-Genome Assembly of the Domestic Cow, Bos Taurus. Genome Biol. 2009;10:R42. doi: 10.1186/gb-2009-10-4-r42. PubMed DOI PMC

Spadafora C. A Reverse Transcriptase-Dependent Mechanism Plays Central Roles in Fundamental Biological Processes. Syst. Biol. Reprod. Med. 2008;54:11–21. doi: 10.1080/19396360701876815. PubMed DOI

Chow J.C., Ciaudo C., Fazzari M.J., Mise N., Servant N., Glass J.L., Attreed M., Avner P., Wutz A., Barillot E., et al. LINE-1 Activity in Facultative Heterochromatin Formation during X Chromosome Inactivation. Cell. 2010;141:956–969. doi: 10.1016/j.cell.2010.04.042. PubMed DOI

Macia A., Muñoz-Lopez M., Cortes J.L., Hastings R.K., Morell S., Lucena-Aguilar G., Marchal J.A., Badge R.M., Garcia-Perez J.L. Epigenetic Control of Retrotransposon Expression in Human Embryonic Stem Cells. Mol. Cell Biol. 2011;31:300–316. doi: 10.1128/MCB.00561-10. PubMed DOI PMC

Goldammer T., Brunner R.M., Rebl A., Wu C.H., Nomura K., Hadfield T., Maddox J.F., Cockett N.E. Cytogenetic Anchoring of Radiation Hybrid and Virtual Maps of Sheep Chromosome X and Comparison of X Chromosomes in Sheep, Cattle, and Human. Chromosome Res. 2009;17:497–506. doi: 10.1007/s10577-009-9047-9. PubMed DOI

Perucatti A., Genualdo V., Iannuzzi A., Rebl A., Di Berardino D., Goldammer T., Iannuzzi L. Advanced Comparative Cytogenetic Analysis of X Chromosomes in River Buffalo, Cattle, Sheep, and Human. Chromosome Res. 2012;20:413–425. doi: 10.1007/s10577-012-9285-0. PubMed DOI

Lee C., Griffin D.K., O’Brien P.C., Yang F., Lin C.C., Ferguson-Smith M.A. Defining the Anatomy of the Rangifer Tarandus Sex Chromosomes. Chromosoma. 1998;107:61–69. doi: 10.1007/s004120050281. PubMed DOI

Frohlich J., Kubickova S., Musilova P., Cernohorska H., Muskova H., Vodicka R., Rubes J. Karyotype Relationships among Selected Deer Species and Cattle Revealed by Bovine FISH Probes. PLoS ONE. 2017;12:e0187559. doi: 10.1371/journal.pone.0187559. PubMed DOI PMC

Li Y.-C., Cheng Y.-M., Hsieh L.-J., Ryder O.A., Yang F., Liao S.-J., Hsiao K.-M., Tsai F.-J., Tsai C.-H., Lin C.C. Karyotypic Evolution of a Novel Cervid Satellite DNA Family Isolated by Microdissection from the Indian Muntjac Y-Chromosome. Chromosoma. 2005;114:28–38. doi: 10.1007/s00412-005-0335-7. PubMed DOI

Steflova P., Tokan V., Vogel I., Lexa M., Macas J., Novak P., Hobza R., Vyskot B., Kejnovsky E. Contrasting Patterns of Transposable Element and Satellite Distribution on Sex Chromosomes (XY1Y2) in the Dioecious Plant Rumex Acetosa. Genome Biol. Evol. 2013;5:769–782. doi: 10.1093/gbe/evt049. PubMed DOI PMC

Fuková I., Traut W., Vítková M., Nguyen P., Kubícková S., Marec F. Probing the W Chromosome of the Codling Moth, Cydia Pomonella, with Sequences from Microdissected Sex Chromatin. Chromosoma. 2007;116:135–145. doi: 10.1007/s00412-006-0086-0. PubMed DOI

Dalíková M., Zrzavá M., Kubíčková S., Marec F. W-Enriched Satellite Sequence in the Indian Meal Moth, Plodia Interpunctella (Lepidoptera, Pyralidae) Chromosome Res. 2017;25:241–252. doi: 10.1007/s10577-017-9558-8. PubMed DOI

Cioffi M.B., Molina W.F., Moreira-Filho O., Bertollo L.A.C. Chromosomal Distribution of Repetitive DNA Sequences Highlights the Independent Differentiation of Multiple Sex Chromosomes in Two Closely Related Fish Species. Cytogenet. Genome Res. 2011;134:295–302. doi: 10.1159/000329481. PubMed DOI

Itoh Y., Kampf K., Arnold A.P. Molecular Cloning of Zebra Finch W Chromosome Repetitive Sequences: Evolution of the Avian W Chromosome. Chromosoma. 2008;117:111–121. doi: 10.1007/s00412-007-0130-8. PubMed DOI

Vozdova M., Ruiz-Herrera A., Fernandez J., Cernohorska H., Frohlich J., Sebestova H., Kubickova S., Rubes J. Meiotic Behaviour of Evolutionary Sex-Autosome Translocations in Bovidae. Chromosome Res. 2016;24:325–338. doi: 10.1007/s10577-016-9524-x. PubMed DOI

Milioto V., Perelman P.L., Paglia L.L., Biltueva L., Roelke M., Dumas F. Mapping Retrotransposon LINE-1 Sequences into Two Cebidae Species and Homo Sapiens Genomes and a Short Review on Primates. Genes. 2022;13:1742. doi: 10.3390/genes13101742. PubMed DOI PMC

Bailey J.A., Carrel L., Chakravarti A., Eichler E.E. Molecular Evidence for a Relationship between LINE-1 Elements and X Chromosome Inactivation: The Lyon Repeat Hypothesis. Proc. Natl. Acad. Sci. USA. 2000;97:6634–6639. doi: 10.1073/pnas.97.12.6634. PubMed DOI PMC

Decker J.E., Pires J.C., Conant G.C., McKay S.D., Heaton M.P., Chen K., Cooper A., Vilkki J., Seabury C.M., Caetano A.R., et al. Resolving the Evolution of Extant and Extinct Ruminants with High-Throughput Phylogenomics. Proc. Natl. Acad. Sci. USA. 2009;106:18644–18649. doi: 10.1073/pnas.0904691106. PubMed DOI PMC

Hassanin A., Delsuc F., Ropiquet A., Hammer C., Jansen van Vuuren B., Matthee C., Ruiz-Garcia M., Catzeflis F., Areskoug V., Nguyen T.T., et al. Pattern and Timing of Diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as Revealed by a Comprehensive Analysis of Mitochondrial Genomes. Comptes Rendus Biol. 2012;335:32–50. doi: 10.1016/j.crvi.2011.11.002. PubMed DOI

Bogenberger J.M., Neitzel H., Fittler F. A Highly Repetitive DNA Component Common to All Cervidae: Its Organization and Chromosomal Distribution during Evolution. Chromosoma. 1987;95:154–161. doi: 10.1007/BF00332189. PubMed DOI

O’Meally D., Patel H.R., Stiglec R., Sarre S.D., Georges A., Marshall Graves J.A., Ezaz T. Non-Homologous Sex Chromosomes of Birds and Snakes Share Repetitive Sequences. Chromosome Res. 2010;18:787–800. doi: 10.1007/s10577-010-9152-9. PubMed DOI

Spencer T.E., Palmarini M. Endogenous Retroviruses of Sheep: A Model System for Understanding Physiological Adaptation to an Evolving Ruminant Genome. J. Reprod. Dev. 2012;58:33–37. doi: 10.1262/jrd.2011-026. PubMed DOI

Garcia-Etxebarria K., Jugo B.M. Evolutionary History of Bovine Endogenous Retroviruses in the Bovidae Family. BMC Evol. Biol. 2013;13:256. doi: 10.1186/1471-2148-13-256. PubMed DOI PMC

Lowe C.B., Bejerano G., Haussler D. Thousands of Human Mobile Element Fragments Undergo Strong Purifying Selection near Developmental Genes. Proc. Natl. Acad. Sci. USA. 2007;104:8005–8010. doi: 10.1073/pnas.0611223104. PubMed DOI PMC

Plohl M., Luchetti A., Mestrović N., Mantovani B. Satellite DNAs between Selfishness and Functionality: Structure, Genomics and Evolution of Tandem Repeats in Centromeric (Hetero) Chromatin. Gene. 2008;409:72–82. doi: 10.1016/j.gene.2007.11.013. PubMed DOI

Hassanin A., Douzery E.J.P. Molecular and Morphological Phylogenies of Ruminantia and the Alternative Position of the Moschidae. Syst. Biol. 2003;52:206–228. doi: 10.1080/10635150390192726. PubMed DOI