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International journal of molecular sciences2023; 24(4); doi: 10.3390/ijms24044134

A Satellite-Free Centromere in Equus przewalskii Chromosome 10.

Abstract: In mammals, centromeres are epigenetically specified by the histone H3 variant CENP-A and are typically associated with satellite DNA. We previously described the first example of a natural satellite-free centromere on Equus caballus chromosome 11 (ECA11) and, subsequently, on several chromosomes in other species of the genus Equus. We discovered that these satellite-free neocentromeres arose recently during evolution through centromere repositioning and/or chromosomal fusion, after inactivation of the ancestral centromere, where, in many cases, blocks of satellite sequences were maintained. Here, we investigated by FISH the chromosomal distribution of satellite DNA families in Equus przewalskii (EPR), demonstrating a good degree of conservation of the localization of the major horse satellite families 37cen and 2PI with the domestic horse. Moreover, we demonstrated, by ChIP-seq, that 37cen is the satellite bound by CENP-A and that the centromere of EPR10, the ortholog of ECA11, is devoid of satellite sequences. Our results confirm that these two species are closely related and that the event of centromere repositioning which gave rise to EPR10/ECA11 centromeres occurred in the common ancestor, before the separation of the two horse lineages.
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Publication Date: 2023-02-18 PubMed ID: 36835543PubMed Central: PMC9961726DOI: 10.3390/ijms24044134Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article explores the unique aspect of certain chromosomes in the Equus przewalskii species, specifically chromosome 10, which unusually carries a satellite-free centromere.

Overview of the Study

  • The researchers’ objective was to understand the distribution of satellite DNA families in the Equus przewalskii species. As part of their investigation, they performed Fluorescence In Situ Hybridization (FISH).
  • The study recognized that the histone H3 variant CENP-A epigenetically describes centromeres in mammals, which are generally connected with satellite DNA. They sought to scrutinize Equus przewalskii chromosome 10 (EPR10), which defied this norm by having a centromere free of satellite DNA.
  • In previous studies, such satellite-free neocentromeres were found on chromosome 11 (ECA11) and on numerous chromosomes in different Equus species. The researchers utilized their understanding from these previous investigations.

Findings and Implications

  • The study confirmed that Equus przewalskii maintains a significant level of conservation concerning the locality of major horse satellite families 37cen and 2PI, as compared to the domestic horse.
  • CENP-A, the identified satellite bound to 37cen, was found through Chromatin Immunoprecipitation sequencing (ChIP-seq) method. It was observed that the centromere of EPR10 is lacking satellite sequences, making it different from the norm.
  • These outcomes support the close relation between these two Equus species. The repositioning event that resulted in the EPR10 and ECA11 centromeres likely happened in the common ancestor before the two horse lineages split.
  • The study adds to the field’s understanding of chromosome and centromere evolution and diversity. By highlighting the existence and creation of satellite-free centromeres, the research plays a vital role in advancing scientific knowledge in genetics, evolution, and potential biomedical applications.

Cite This Article

APA
Piras FM, Cappelletti E, Abdelgadir WA, Salamon G, Vignati S, Santagostino M, Sola L, Nergadze SG, Giulotto E. (2023). A Satellite-Free Centromere in Equus przewalskii Chromosome 10. Int J Mol Sci, 24(4). https://doi.org/10.3390/ijms24044134

Publication

International journal of molecular sciences
ISSN: 1422-0067
NlmUniqueID: 101092791
Country: Switzerland
Language: English
Volume: 24
Issue: 4

Researcher Affiliations

Piras, Francesca M
  • Department of Biology and Biotechnology "Lazzaro Spallanzani", University of Pavia, 27100 Pavia, Italy.
Cappelletti, Eleonora
  • Department of Biology and Biotechnology "Lazzaro Spallanzani", University of Pavia, 27100 Pavia, Italy.
Abdelgadir, Wasma A
  • Department of Biology and Biotechnology "Lazzaro Spallanzani", University of Pavia, 27100 Pavia, Italy.
Salamon, Giulio
  • Oasi di Sant'Alessio, Sant'Alessio con Vialone, 27016 Pavia, Italy.
Vignati, Simone
  • Independent Researcher, 27100 Pavia, Italy.
Santagostino, Marco
  • Department of Biology and Biotechnology "Lazzaro Spallanzani", University of Pavia, 27100 Pavia, Italy.
Sola, Lorenzo
  • Department of Biology and Biotechnology "Lazzaro Spallanzani", University of Pavia, 27100 Pavia, Italy.
Nergadze, Solomon G
  • Department of Biology and Biotechnology "Lazzaro Spallanzani", University of Pavia, 27100 Pavia, Italy.
Giulotto, Elena
  • Department of Biology and Biotechnology "Lazzaro Spallanzani", University of Pavia, 27100 Pavia, Italy.

MeSH Terms

  • Animals
  • Centromere / metabolism
  • Centromere Protein A / metabolism
  • DNA, Satellite
  • Horses / genetics

Grant Funding

  • Dipartimenti di Eccellenza Program (2018-2022)-Department of Biology and Biotechnology "L. Spallanzani", University of Pavia / the Italian Ministry of Education, University and Research (MIUR)
  • Grant 2019-67015-29340/Project Accession 1018854 / USDA National Institute of Food and Agriculture.

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 77 references
  1. Allshire R.C., Karpen G.H.. Epigenetic regulation of centromeric chromatin: Old dogs, new tricks?. Nat. Rev. Genet. 2008;9:923–937.
    doi: 10.1038/nrg2466pmc: PMC2586333pubmed: 19002142google scholar: lookup
  2. Choo K.H.. Centromerization. Trends Cell Biol. 2000;10:182–188.
    doi: 10.1016/S0962-8924(00)01739-6pubmed: 10754560google scholar: lookup
  3. Marshall O.J., Chueh A.C., Wong L.H., Choo K.H.. Neocentromeres: New insights into centromere structure, disease development, and karyotype evolution. Am. J. Hum. Genet. 2008;82:261–282.
    doi: 10.1016/j.ajhg.2007.11.009pmc: PMC2427194pubmed: 18252209google scholar: lookup
  4. Earnshaw W.C., Migeon B.R.. Three related centromere proteins are absent from the inactive centromere of a stable isodicentric chromosome. Chromosoma 1985;92:290–296.
    doi: 10.1007/BF00329812pubmed: 2994966google scholar: lookup
  5. Voullaire L.E., Slater H.R., Petrovic V., Choo K.H.. A functional marker centromere with no detectable alpha-satellite, satellite III, or CENP-B protein: Activation of a latent centromere?. Am. J. Hum. Genet. 1993;52:1153–1163.
    pmc: PMC1682274pubmed: 7684888
  6. 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.2007.11.013pubmed: 18182173google scholar: lookup
  7. Nergadze S.G., Piras F.M., Gamba R., Corbo M., Cerutti F., McCarter J.G.W., Cappelletti E., Gozzo F., Harman R.M., Antczak D.F.. Birth, evolution, and transmission of satellite-free mammalian centromeric domains. Genome Res. 2018;28:789–799.
    doi: 10.1101/gr.231159.117pmc: PMC5991519pubmed: 29712753google scholar: lookup
  8. Cappelletti E., Piras F.M., Badiale C., Bambi M., Santagostino M., Vara C., Masterson T.A., Sullivan K.F., Nergadze S.G., Ruiz-Herrera A.. CENP-A binding domains and recombination patterns in horse spermatocytes. Sci. Rep. 2019;9:15800.
    doi: 10.1038/s41598-019-52153-1pmc: PMC6825197pubmed: 31676881google scholar: lookup
  9. Purgato S., Belloni E., Piras F.M., Zoli M., Badiale C., Cerutti F., Mazzagatti A., Perini G., Della Valle G., Nergadze S.G.. Centromere sliding on a mammalian chromosome. Chromosoma 2015;124:277–287.
    doi: 10.1007/s00412-014-0493-6pmc: PMC4446527pubmed: 25413176google scholar: lookup
  10. Peng S., Petersen J.L., Bellone R.R., Kalbfleisch T., Kingsley N.B., Barber A.M., Cappelletti E., Giulotto E., Finno C.J.. Decoding the Equine Genome: Lessons from ENCODE. Genes 2021;12:1707.
    doi: 10.3390/genes12111707pmc: PMC8625040pubmed: 34828313google scholar: lookup
  11. Carbone L., Nergadze S.G., Magnani E., Misceo D., Francesca Cardone M., Roberto R., Bertoni L., Attolini C., Francesca Piras M., de Jong P.. Evolutionary movement of centromeres in horse, donkey, and zebra. Genomics 2006;87:777–782.
    doi: 10.1016/j.ygeno.2005.11.012pubmed: 16413164google scholar: lookup
  12. Wade C.M., Giulotto E., Sigurdsson S., Zoli M., Gnerre S., Imsland F., Lear T.L., Adelson D.L., Bailey E., Bellone R.R.. Genome sequence, comparative analysis, and population genetics of the domestic horse. Science 2009;326:865–867.
    doi: 10.1126/science.1178158pmc: PMC3785132pubmed: 19892987google scholar: lookup
  13. Piras F.M., Cappelletti E., Santagostino M., Nergadze S.G., Giulotto E., Raimondi E.. Molecular Dynamics and Evolution of Centromeres in the Genus Equus. Int. J. Mol. Sci. 2022;23:4183.
    doi: 10.3390/ijms23084183pmc: PMC9024551pubmed: 35457002google scholar: lookup
  14. Cappelletti E., Piras F.M., Sola L., Santagostino M., Abdelgadir W.A., Raimondi E., Lescai F., Nergadze S.G., Giulotto E.. Robertsonian Fusion and Centromere Repositioning Contributed to the Formation of Satellite-free Centromeres During the Evolution of Zebras. Mol. Biol. Evol. 2022;39:msac162.
    doi: 10.1093/molbev/msac162pmc: PMC9356731pubmed: 35881460google scholar: lookup
  15. Roberti A., Bensi M., Mazzagatti A., Piras F.M., Nergadze S.G., Giulotto E., Raimondi E.. Satellite DNA at the Centromere is Dispensable for Segregation Fidelity. Genes 2019;10:469.
    doi: 10.3390/genes10060469pmc: PMC6627300pubmed: 31226862google scholar: lookup
  16. Piras F.M., Nergadze S.G., Magnani E., Bertoni L., Attolini C., Khoriauli L., Raimondi E., Giulotto E.. Uncoupling of satellite DNA and centromeric function in the genus Equus. PLoS Genet. 2010;6:e1000845.
    doi: 10.1371/journal.pgen.1000845pmc: PMC2820525pubmed: 20169180google scholar: lookup
  17. Giulotto E., Raimondi E., Sullivan K.F.. The Unique DNA Sequences Underlying Equine Centromeres. Prog. Mol. Subcell Biol. 2017;56:337–354.
    doi: 10.1007/978-3-319-58592-5_14pubmed: 28840244google scholar: lookup
  18. Trifonov V.A., Musilova P., Kulemsina A.I.. Chromosome evolution in Perissodactyla. Cytogenet. Genome Res. 2012;137:208–217.
    doi: 10.1159/000339900pubmed: 22813844google scholar: lookup
  19. Trifonov V.A., Stanyon R., Nesterenko A.I., Fu B., Perelman P.L., O’Brien P.C., Stone G., Rubtsova N.V., Houck M.L., Robinson T.J.. Multidirectional cross-species painting illuminates the history of karyotypic evolution in Perissodactyla. Chromosome Res. 2008;16:89–107.
    doi: 10.1007/s10577-007-1201-7pubmed: 18293107google scholar: lookup
  20. Musilova P., Kubickova S., Vahala J., Rubes J.. Subchromosomal karyotype evolution in Equidae. Chromosome Res. 2013;21:175–187.
    doi: 10.1007/s10577-013-9346-zpubmed: 23532666google scholar: lookup
  21. Montefalcone G., Tempesta S., Rocchi M., Archidiacono N.. Centromere repositioning. Genome Res. 1999;9:1184–1188.
    doi: 10.1101/gr.9.12.1184pmc: PMC311001pubmed: 10613840google scholar: lookup
  22. Rocchi M., Archidiacono N., Schempp W., Capozzi O., Stanyon R.. Centromere repositioning in mammals. Heredity 2012;108:59–67.
    doi: 10.1038/hdy.2011.101pmc: PMC3238114pubmed: 22045381google scholar: lookup
  23. Piras F.M., Nergadze S.G., Poletto V., Cerutti F., Ryder O.A., Leeb T., Raimondi E., Giulotto E.. Phylogeny of horse chromosome 5q in the genus Equus and centromere repositioning. Cytogenet. Genome Res. 2009;126:165–172.
    doi: 10.1159/000245916pubmed: 20016166google scholar: lookup
  24. Wijers E.R., Zijlstra C., Lenstra J.A.. Rapid evolution of horse satellite DNA. Genomics 1993;18:113–117.
    doi: 10.1006/geno.1993.1433pubmed: 8276394google scholar: lookup
  25. Sakagami M., Hirota K., Awata T., Yasue H.. Molecular cloning of an equine satellite-type DNA sequence and its chromosomal localization. Cytogenet. Cell Genet. 1994;66:27–30.
    doi: 10.1159/000133657pubmed: 8275703google scholar: lookup
  26. Broad T.E., Forrest J.W., Lewis P.E., Pearce P.D., Phua S.H., Pugh P.A., Stewart-Scott I.A.. Cloning of a DNA repeat element from horse: DNA sequence and chromosomal localization. Genome 1995;38:1132–1138.
    doi: 10.1139/g95-150pubmed: 8654911google scholar: lookup
  27. Broad T.E., Ede A.J., Forrest J.W., Lewis P.E., Phua S.H., Pugh P.A.. Families of tandemly repeated DNA elements from horse: Cloning, nucleotide sequence, and organization. Genome 1995;38:1285–1289.
    doi: 10.1139/g95-169pubmed: 8654920google scholar: lookup
  28. Cerutti F., Gamba R., Mazzagatti A., Piras F.M., Cappelletti E., Belloni E., Nergadze S.G., Raimondi E., Giulotto E.. The major horse satellite DNA family is associated with centromere competence. Mol. Cytogenet. 2016;9:35.
    doi: 10.1186/s13039-016-0242-zpmc: PMC4847189pubmed: 27123044google scholar: lookup
  29. Nergadze S.G., Belloni E., Piras F.M., Khoriauli L., Mazzagatti A., Vella F., Bensi M., Vitelli V., Giulotto E., Raimondi E.. Discovery and comparative analysis of a novel satellite, EC137, in horses and other equids. Cytogenet. Genome Res. 2014;144:114–123.
    doi: 10.1159/000368138pubmed: 25342230google scholar: lookup
  30. Ryder O.. Genetic studies of Przewalski’s horses and their impact on conservation. 1994. pp. 75–92.
  31. Ransom J., Kaczensky P.. Wild Equids: Ecology, Management, and Conservation. 2016. pp. 1–229.
  32. Goto H., Ryder O.A., Fisher A.R., Schultz B., Kosakovsky Pond S.L., Nekrutenko A., Makova K.D.. A massively parallel sequencing approach uncovers ancient origins and high genetic variability of endangered Przewalski’s horses. Genome Biol. Evol. 2011;3:1096–1106.
    doi: 10.1093/gbe/evr067pmc: PMC3194890pubmed: 21803766google scholar: lookup
  33. Wallner B., Brem G., Müller M., Achmann R.. Fixed nucleotide differences on the Y chromosome indicate clear divergence between Equus przewalskii and Equus caballus. Anim. Genet. 2003;34:453–456.
    doi: 10.1046/j.0268-9146.2003.01044.xpubmed: 14687077google scholar: lookup
  34. Orlando L., Ginolhac A., Zhang G., Froese D., Albrechtsen A., Stiller M., Schubert M., Cappellini E., Petersen B., Moltke I.. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 2013;499:74–78.
    doi: 10.1038/nature12323pubmed: 23803765google scholar: lookup
  35. Der Sarkissian C., Ermini L., Schubert M., Yang M.A., Librado P., Fumagalli M., Jónsson H., Bar-Gal G.K., Albrechtsen A., Vieira F.G.. Evolutionary Genomics and Conservation of the Endangered Przewalski’s Horse. Curr. Biol. 2015;25:2577–2583.
    doi: 10.1016/j.cub.2015.08.032pmc: PMC5104162pubmed: 26412128google scholar: lookup
  36. Gaunitz C., Fages A., Hanghøj K., Albrechtsen A., Khan N., Schubert M., Seguin-Orlando A., Owens I.J., Felkel S., Bignon-Lau O.. Ancient genomes revisit the ancestry of domestic and Przewalski’s horses. Science 2018;360:111–114.
    doi: 10.1126/science.aao3297pubmed: 29472442google scholar: lookup
  37. Orlando L.. Ancient Genomes Reveal Unexpected Horse Domestication and Management Dynamics. Bioessays 2020;42:e1900164.
    doi: 10.1002/bies.201900164pubmed: 31808562google scholar: lookup
  38. Bouman D.T., Bouman J.G.. The history of Przewalski’s Horse. 1994. pp. 5–38.
  39. Jiang Z., Zong H.. Reintroduction of the Przewalski’s Horse in China: Status Quo and Outlook. Nat. Conserv. Res. 2019;4:15–22.
    doi: 10.24189/ncr.2019.045google scholar: lookup
  40. Turghan M.A., Jiang Z., Niu Z.. An Update on Status and Conservation of the Przewalski’s Horse (Equus ferus przewalskii): Captive Breeding and Reintroduction Projects. Animals 2022;12:3158.
    doi: 10.3390/ani12223158pmc: PMC9686875pubmed: 36428386google scholar: lookup
  41. Oakenfull E.A., Ryder O.A.. Mitochondrial control region and 12S rRNA variation in Przewalski’s horse (Equus przewalskii). Anim. Genet. 1998;29:456–459.
    doi: 10.1046/j.1365-2052.1998.296380.xpubmed: 9883508google scholar: lookup
  42. Kerekes V., Sándor I., Nagy D., Ozogány K., Göczi L., Ibler B., Széles L., Barta Z.. Trends in demography, genetics, and social structure of Przewalski’s horses in the Hortobagy National Park, Hungary over the last 22 years. Glob. Ecol. Conserv. 2021;25:e01407.
    doi: 10.1016/j.gecco.2020.e01407google scholar: lookup
  43. Bakirova R.T., Zharkikh T.L.. Programme on Establishing a Semi-Free Population of Przewalski’s Horse in Orenburg State Nature Reserve: The First Successful Project on the Reintroduction of the Species in Russia. Nat. Conserv. Res. 2019;4:57–64.
    doi: 10.24189/ncr.2019.025google scholar: lookup
  44. Bernatkova A., Oyunsaikhan G., Šimek J., Komárková M., Bobek M., Ceacero F.. Influence of weather on the behaviour of reintroduced Przewalski’s horses in the Great Gobi B Strictly Protected Area (Mongolia): Implications for conservation. BMC Zool. 2022;7.
    doi: 10.1186/s40850-022-00130-zpmc: PMC10127430pubmed: 37170378google scholar: lookup
  45. Oakenfull E.A., Lim H.N., Ryder O.A.. A survey of equid mitochondrial DNA: Implications for the evolution, genetic diversity and conservation of Equus. Conserv. Genet. 2000;1:341–355.
    doi: 10.1023/A:1011559200897google scholar: lookup
  46. Jansen T., Forster P., Levine M.A., Oelke H., Hurles M., Renfrew C., Weber J., Olek K.. Mitochondrial DNA and the origins of the domestic horse. Proc. Natl. Acad. Sci. USA 2002;99:10905–10910.
    doi: 10.1073/pnas.152330099pmc: PMC125071pubmed: 12130666google scholar: lookup
  47. Achilli A., Olivieri A., Soares P., Lancioni H., Hooshiar Kashani B., Perego U.A., Nergadze S.G., Carossa V., Santagostino M., Capomaccio S.. Mitochondrial genomes from modern horses reveal the major haplogroups that underwent domestication. Proc. Natl. Acad. Sci. USA 2012;109:2449–2454.
    doi: 10.1073/pnas.1111637109pmc: PMC3289334pubmed: 22308342google scholar: lookup
  48. Ryder O.A., Hansen S.K.. Molecular cytogenetics of the Equidae. I. Purification and cytological localization of a (G + C)-rich satellite DNA from Equus przewalskii. Chromosoma 1979;72:115–129.
    doi: 10.1007/BF00293229pubmed: 456203google scholar: lookup
  49. Myka J.L., Lear T.L., Houck M.L., Ryder O.A., Bailey E.. FISH analysis comparing genome organization in the domestic horse (Equus caballus) to that of the Mongolian wild horse (E. przewalskii). Cytogenet. Genome Res. 2003;102:222–225.
    doi: 10.1159/000075753pubmed: 14970707google scholar: lookup
  50. Yang F., Fu B., O’Brien P.C., Robinson T.J., Ryder O.A., Ferguson-Smith M.A.. Karyotypic relationships of horses and zebras: Results of cross-species chromosome painting. Cytogenet. Genome Res. 2003;102:235–243.
    doi: 10.1159/000075755pubmed: 14970709google scholar: lookup
  51. Ahrens E., Stranzinger G.. Comparative chromosomal studies of E. caballus (ECA) and E. przewalskii (EPR) in a female F1 hybrid. J. Anim. Breed Genet. 2005;122((Suppl. S1)):97–102.
    doi: 10.1111/j.1439-0388.2005.00494.xpubmed: 16130463google scholar: lookup
  52. Kvist L., Niskanen M.. Modern Northern Domestic Horses Carry Mitochondrial DNA Similar to Przewalski’s Horse. J. Mamm. Evol. 2021;28:371–376.
    doi: 10.1007/s10914-020-09517-6google scholar: lookup
  53. Anglana M., Bertoni L., Giulotto E.. Cloning of a polymorphic sequence from the nontranscribed spacer of horse rDNA. Mamm. Genome 1996;7:539–541.
    doi: 10.1007/s003359900159pubmed: 8672135google scholar: lookup
  54. Benirschke K., Malouf N., Low R.J., Heck H.. Chromosome complement: Differences between Equus caballus and Equus przewalskii, Poliakoff. Science 1965;148:382–383.
    doi: 10.1126/science.148.3668.382pubmed: 14261533google scholar: lookup
  55. Fry K., Salser W.. Nucleotide sequences of HS-alpha satellite DNA from kangaroo rat Dipodomys ordii and characterization of similar sequences in other rodents. Cell 1977;12:1069–1084.
    doi: 10.1016/0092-8674(77)90170-2pubmed: 597857google scholar: lookup
  56. Salser W., Bowen S., Browne D., el-Adli F., Fedoroff N., Fry K., Heindell H., Paddock G., Poon R., Wallace B.. Investigation of the organization of mammalian chromosomes at the DNA sequence level. Fed. Proc. 1976;35:23–35.
    pubmed: 1107072
  57. Ryder O.A., Epel N.C., Benirschke K.. Chromosome banding studies of the Equidae. Cytogenet Cell Genet. 1978;20:332–350.
    doi: 10.1159/000130862pubmed: 648186google scholar: lookup
  58. Liu G., Xu C.Q., Cao Q., Zimmermann W., Songer M., Zhao S.S., Li K., Hu D.F.. Mitochondrial and pedigree analysis in Przewalski’s horse populations: Implications for genetic management and reintroductions. Mitochondrial DNA 2014;25:313–318.
    doi: 10.3109/19401736.2013.800487pubmed: 23808923google scholar: lookup
  59. Breen M., Downs P., Irvin Z., Bell K.. Intrageneric amplification of horse microsatellite markers with emphasis on the Przewalski’s horse (E. przewalskii). Anim. Genet. 1994;25:401–405.
    doi: 10.1111/j.1365-2052.1994.tb00530.xpubmed: 7695120google scholar: lookup
  60. Liu G., Shafer A.B.A., Zimmermann W., Hu D., Wang W., Chu H., Cao J., Zhao C.. Evaluating the reintroduction project of Przewalski’s horse in China using genetic and pedigree data. Biol. Conserv. 2014;171:288–298.
    doi: 10.1016/j.biocon.2013.11.022google scholar: lookup
  61. Tang Y., Liu G., Zhao S., Li K., Zhang D., Liu S., Hu D.. Major Histocompatibility Complex (MHC) Diversity of the Reintroduction Populations of Endangered Przewalski’s Horse. Genes 2022;13:928.
    doi: 10.3390/genes13050928pmc: PMC9140943pubmed: 35627313google scholar: lookup
  62. Jónsson H., Schubert M., Seguin-Orlando A., Ginolhac A., Petersen L., Fumagalli M., Albrechtsen A., Petersen B., Korneliussen T.S., Vilstrup J.T.. Speciation with gene flow in equids despite extensive chromosomal plasticity. Proc. Natl. Acad. Sci. USA 2014;111:18655–18660.
    doi: 10.1073/pnas.1412627111pmc: PMC4284605pubmed: 25453089google scholar: lookup
  63. Vidale P., Magnani E., Nergadze S.G., Santagostino M., Cristofari G., Smirnova A., Mondello C., Giulotto E.. The catalytic and the RNA subunits of human telomerase are required to immortalize equid primary fibroblasts. Chromosoma 2012;121:475–488.
    doi: 10.1007/s00412-012-0379-4pmc: PMC3443485pubmed: 22797876google scholar: lookup
  64. Vidale P., Piras F.M., Nergadze S.G., Bertoni L., Verini-Supplizi A., Adelson D., Guérin G., Giulotto E.. Chromosomal assignment of six genes (EIF4G3, HSP90, RBBP6, IL8, TERT, and TERC) in four species of the genus Equus. Anim. Biotechnol. 2011;22:119–123.
    doi: 10.1080/10495398.2011.575300pubmed: 21774619google scholar: lookup
  65. Santagostino M., Khoriauli L., Gamba R., Bonuglia M., Klipstein O., Piras F.M., Vella F., Russo A., Badiale C., Mazzagatti A.. Genome-wide evolutionary and functional analysis of the Equine Repetitive Element 1: An insertion in the myostatin promoter affects gene expression. BMC Genet. 2015;16:126.
    doi: 10.1186/s12863-015-0281-1pmc: PMC4623272pubmed: 26503543google scholar: lookup
  66. Santagostino M., Piras F.M., Cappelletti E., Del Giudice S., Semino O., Nergadze S.G., Giulotto E.. Insertion of Telomeric Repeats in the Human and Horse Genomes: An Evolutionary Perspective. Int. J. Mol. Sci. 2020;21:2838.
    doi: 10.3390/ijms21082838pmc: PMC7215372pubmed: 32325780google scholar: lookup
  67. Nergadze S.G., Lupotto M., Pellanda P., Santagostino M., Vitelli V., Giulotto E.. Mitochondrial DNA insertions in the nuclear horse genome. Anim. Genet. 2010;41((Suppl. S2)):176–185.
    doi: 10.1111/j.1365-2052.2010.02130.xpubmed: 21070293google scholar: lookup
  68. Raimondi E., Piras F.M., Nergadze S.G., Di Meo G.P., Ruiz-Herrera A., Ponsà M., Ianuzzi L., Giulotto E.. Polymorphic organization of constitutive heterochromatin in Equus asinus (2n = 62) chromosome 1. Hereditas 2011;148:110–113.
    doi: 10.1111/j.1601-5223.2011.02218.xpubmed: 21756256google scholar: lookup
  69. Vangipuram M., Ting D., Kim S., Diaz R., Schüle B.. Skin punch biopsy explant culture for derivation of primary human fibroblasts. J. Vis. Exp. 2013;77:e3779.
    doi: 10.3791/3779pmc: PMC3731437pubmed: 23852182google scholar: lookup
  70. Langmead B., Salzberg S.L.. Fast gapped-read alignment with Bowtie 2. Nat. Methods 2012;9:357–359.
    doi: 10.1038/nmeth.1923pmc: PMC3322381pubmed: 22388286google scholar: lookup
  71. Langmead B., Trapnell C., Pop M., Salzberg S.L.. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25.
    doi: 10.1186/gb-2009-10-3-r25pmc: PMC2690996pubmed: 19261174google scholar: lookup
  72. Ramírez F., Ryan D.P., Grüning B., Bhardwaj V., Kilpert F., Richter A.S., Heyne S., Dündar F., Manke T.. deepTools2: A next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 2016;44:W160–W165.
    doi: 10.1093/nar/gkw257pmc: PMC4987876pubmed: 27079975google scholar: lookup
  73. Lopez-Delisle L., Rabbani L., Wolff J., Bhardwaj V., Backofen R., Grüning B., Ramírez F., Manke T.. pyGenomeTracks: Reproducible plots for multivariate genomic datasets. Bioinformatics 2021;37:422–423.
    doi: 10.1093/bioinformatics/btaa692pmc: PMC8058774pubmed: 32745185google scholar: lookup
  74. Jurka J., Kapitonov V.V., Pavlicek A., Klonowski P., Kohany O., Walichiewicz J.. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 2005;110:462–467.
    doi: 10.1159/000084979pubmed: 16093699google scholar: lookup
  75. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R., Subgroup G.P.D.P.. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009;25:2078–2079.
    doi: 10.1093/bioinformatics/btp352pmc: PMC2723002pubmed: 19505943google scholar: lookup
  76. Danecek P., Bonfield J.K., Liddle J., Marshall J., Ohan V., Pollard M.O., Whitwham A., Keane T., McCarthy S.A., Davies R.M.. Twelve years of SAMtools and BCFtools. Gigascience 2021;10:giab008.
    doi: 10.1093/gigascience/giab008pmc: PMC7931819pubmed: 33590861google scholar: lookup
  77. Kumar S., Stecher G., Li M., Knyaz C., Tamura K.. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018;35:1547–1549.
    doi: 10.1093/molbev/msy096pmc: PMC5967553pubmed: 29722887google scholar: lookup

Citations

This article has been cited 5 times.
  1. Cappelletti E, Piras FM, Biundo M, Bellone RR, Finno CJ, Kalbfleisch TS, Petersen JL, Nergadze SG, Giulotto E. CENP-A and centromere evolution in equids. Chromosome Res 2025 Jun 30;33(1):13.
    doi: 10.1007/s10577-025-09773-3pubmed: 40586953google scholar: lookup
  2. Cappelletti E, Piras FM, Biundo M, Raimondi E, Nergadze SG, Giulotto E. CENP-A/CENP-B uncoupling in the evolutionary reshuffling of centromeres in equids. Genome Biol 2025 Feb 6;26(1):23.
    doi: 10.1186/s13059-025-03490-0pubmed: 39915813google scholar: lookup
  3. Chabot BJ, Sun R, Amjad A, Hoyt SJ, Ouyang L, Courret C, Drennan R, Leo L, Larracuente AM, Core LJ, O'Neill RJ, Mellone BG. Transcription of a centromere-enriched retroelement and local retention of its RNA are significant features of the CENP-A chromatin landscape. Genome Biol 2024 Nov 18;25(1):295.
    doi: 10.1186/s13059-024-03433-1pubmed: 39558354google scholar: lookup
  4. Brannan EO, Hartley GA, O'Neill RJ. Mechanisms of Rapid Karyotype Evolution in Mammals. Genes (Basel) 2023 Dec 31;15(1).
    doi: 10.3390/genes15010062pubmed: 38254952google scholar: lookup
  5. Cappelletti E, Piras FM, Sola L, Santagostino M, Petersen JL, Bellone RR, Finno CJ, Peng S, Kalbfleisch TS, Bailey E, Nergadze SG, Giulotto E. The localization of centromere protein A is conserved among tissues. Commun Biol 2023 Sep 21;6(1):963.
    doi: 10.1038/s42003-023-05335-7pubmed: 37735603google scholar: lookup
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