Skip to main content
SpringerLink
Log in

Chromosomes of the Indian Muntjac (Muntiacus muntjak): Comeback

  • Published:
Cell and Tissue Biology Aims and scope Submit manuscript

Abstract

The chromosomes of the Indian muntjac (Muntiacus muntjak, 2n = 6 in females and 2n = 7 in males) are described using the methods of G-, C-, CDAG-, and AgNOR-staining, and in situ localization of 18S, 5.8S, 28S rRNA genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.

Similar content being viewed by others

REFERENCES

  1. An Atlas of Mammalian Chromosomes, Graphodatsky, A., Perelman, P., and O’Brien, S.J., Eds., New York, NY: Wiley, 2020, 2nd ed.

  2. Babu, A. and Verma, R.S., Expression of heterochromatin by restriction endonuclease treatment and distamycin A/DAPI staining of Indian muntjac (Muntiacus muntjak) chromosomes, Cytogenet. Genome Res., 1986, vol. 41, p. 96.

    Article  CAS  Google Scholar 

  3. Bogenberger, J., Schnell, H., and Fittler, F., Characterization of X-chromosome specific satellite DNA of Muntiacus muntjak vaginalis, Chromosoma, 1982, vol. 87, p. 9.

    Article  CAS  PubMed  Google Scholar 

  4. Bogenberger, J.M., Neumaier, P.S., and Fittler, F., The muntjac satellite IA sequence is composed of 31-base-pair internal repeats that are highly homologous to the 31-base-pair subrepeats of the bovine satellite 1.715, Eur. J. Biochem., 1985, vol. 148, p. 55.

    Article  CAS  PubMed  Google Scholar 

  5. Bogenberger, J.M., Neitzel, H., and Fittler, F., A highly repetitive DNA component common to all Cervidae: its organization and chromosomal distribution during evolution, Chromosoma, 1987, vol. 95, p. 154.

    Article  CAS  PubMed  Google Scholar 

  6. Brat, S.V., Verma, R.S., and Dosik, H., Structural organization of chromosomes of the Indian muntjac (Muntiacus muntjak), Cytogenet. Cell Genet., 1979, vol. 24, p. 201.

    Article  Google Scholar 

  7. Carrano, A.V., Gray, J.W., Moore, I.I., Minkler, J.L., Mayall, B.H., van Dilla, M.A., and Mendelsohn, M.L., Purification of the chromosomes of the Indian muntjac by flow sorting, J. Histochem. Cytochem., 1976, vol. 24, p. 348.

    Article  CAS  PubMed  Google Scholar 

  8. Chi, J.X., Huang, L., Nie, W., Wang, J., Su, B., and Yang, F., Defining the orientation of the tandem fusions that occurred during the evolution of Indian muntjac chromosomes by BAC mapping, Chromosoma, 2005, vol. 114, p. 167.

    Article  CAS  PubMed  Google Scholar 

  9. Comings, D.E., Heterochromatin of the Indian muntjac. Replication, condensation, DNA ultracentrifugation, fluorescent and heterochromatin staining, Exp. Cell Res., 1971, vol. 67, p. 441.

    Article  CAS  PubMed  Google Scholar 

  10. Ferguson-Smith, M.A. and Trifonov, V., Mammalian karyotype evolution, Nat. Rev. Genet., 2007, vol. 8, p. 950.

    Article  CAS  PubMed  Google Scholar 

  11. Elder, F.F.B. and Hsu, T.C., Tandem fusions in the evolution of mammalian chromosomes, in The Cytogenetics of Mammalian Autochromosomal Rearrangements, Sandberg, A.A., Ed., New York: Alan R Liss, 1988, p. 481.

    Google Scholar 

  12. Farré, M., Kim, J., Proskuryakova, A.A., Zhang, Y., Kulemzina, A.I., Li, Q., Zhou, Y., Xiong, Y., Johnson, J.L., Perelman, P., Johnson, W.E., Warren, W.C., Kukekova, A.V., Zhang, G., O’Brien, S.J., et al., Evolution of gene regulation in ruminants differs between evolutionary breakpoint regions and homologous synteny blocks, Genome Res, 2019a, vol. 29, p. 576.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Farré, M., Li, Q., Darolti, I., Zhou, Y., Damas, J., Proskuryakova, A.A., Kulemzina, A.I., Chemnick, L.G., Kim, J., Ryder, O.A., Ma, J., Graphodatsky, A.S., Zhang, G., Larkin, D.M., and Lewin, H.A., An integrated chromosome-scale genome assembly of the Masai giraffe (Giraffa camelopardalis tippelskirchi), GigaScience, 2019b, vol. 8, giz090.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Fontana, F. and Rubini, M., Chromosomal evolution in Cervidae, Biosystems, 1990, vol. 24, p. 157.

    Article  CAS  PubMed  Google Scholar 

  15. Fronicke, L. and Scherthan, H., Zoo-fluorescence in situ hybridization analysis of human and Indian muntjac karyotypes (Muntiacus muntjak vaginalis) reveals satellite DNA clusters at the margins of conserved synthetic segments, Chromosome Res., 1997, vol. 5, p. 254.

    Article  CAS  PubMed  Google Scholar 

  16. Fronicke, L., Chowdhary, B.P., and Scherthan, H., Segmental homology among cattle (Bos taurus), Indian muntjac (Muntiacus muntjak vaginalis), and Chinese muntjac (M. reevesi) karyotypes, Cytogenet. Cell Genet., 1997, vol. 77, p. 223.

    Article  CAS  PubMed  Google Scholar 

  17. Goodpasture, C. and Bloom, S.E., Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining, Chromosoma, 1975, vol. 53, p. 37.

    Article  CAS  PubMed  Google Scholar 

  18. Graphodatsky, A.S. and Radzhabli, S.I., Khromosomy sel’skokhozyaistvennykh i laboratornykh mlekopitayushchikh (Chromosomes of Farming and Laboratory Mammals), Novosibirsk: Nauka, 1988.

  19. Graphodatsky, A.S., Trifonov, V.A., and Stanyon, R., The genome diversity and karyotype evolution of mammals, Mol. Cytogenet., 2011, vol. 4, pp. 22.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Green, R. and Bahr, G., Comparison of G-, Q-, and EM-banding patterns exhibited by the chromosome complement of the Indian muntjac, Muntiacus muntjak, with reference to nuclear DNA content and chromatin ultrastructure, Chromosoma, 1975, vol. 50, p. 53.

    Article  CAS  PubMed  Google Scholar 

  21. Hartmann, N. and Scherthan, H., Characterization of ancestral chromosome fusion points in the Indian muntjac deer, Chromosoma, 2004, vol. 112, p. 213.

    Article  CAS  PubMed  Google Scholar 

  22. Howell, W.M. and Black, D.A., Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method, Experientia, 1980, vol. 36, p. 1014.

    Article  CAS  PubMed  Google Scholar 

  23. Johnston, F.P., Church, R.B., and Lin, C.C., Chromosome rearrangement between the Indian muntjac and Chinese muntjac is accompanied by a deletion of middle repetitive DNA, Can. J. Biochem., 1982, vol. 60, p. 497.

    Article  CAS  PubMed  Google Scholar 

  24. Kato, H., Tsuchiya, K., and Yosida, T.H., Constitutive heterochromatin of Indian muntjac chromosomes revealed by DNAse treatment and a C-banding technique, Can. J. Genet. Cytol., 1974, vol. 16, p. 273.

    Article  CAS  PubMed  Google Scholar 

  25. Lee, C., Sasi, R., and Lin, C.C., Interstitial localization of telomeric DNA sequences in the Indian muntjac chromosomes: further evidence for tandem chromosome fusions in the karyotypic evolution of the Asian muntjacs, Cytogenet. Cell Genet., 1993, vol. 63, p. 156.

    Article  CAS  PubMed  Google Scholar 

  26. Lee, C., Court, D.R., Cho, C., Haslett, J.L., and Lin, C.C., Higher-order organization of subrepeats and the evolution of cervid satellite I DNA, J. Mol. Evol., 1997, vol. 44, p. 327.

    Article  CAS  PubMed  Google Scholar 

  27. Lemskaya, N.A., Kulemzina, A.I., Beklemisheva, V.R., Biltueva, L.S., Proskuryakova, A.A., Perelman, P.L., and Graphodatsky, A.S., The combined method of heterogeneous heterochromatin detection (CDAG) in different mammalian species, Chromosoma, 2018, vol. 26, p. 307.

    Article  CAS  Google Scholar 

  28. Levy, H.P., Schultz, R.A., Ordonez, J.V., and Cohen, M.M., DNA content measurements and an improved idiogram for the Indian muntjac, Cytometry, 1993, vol. 14, p. 362.

    Article  CAS  PubMed  Google Scholar 

  29. Lewin, H.A., Robinson, G.E., Kress, W.J., Baker, W.J., Coddington, J., Crandall, K.A., Durbin, R., Edwards, S.V., Forest, F., Gilbert, M.T.P., Goldstein, M.M., Gri-goriev, I.V., Hackett, K.J., Haussler, D., Jarvis, E.D., et al., Earth BioGenome project: sequencing life for the future of life, Proc. Natl. Acad. Sci. U.S.A., 2018, vol. 115, p. 4325.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Lewin, H.A., Graves, J.A.M., Ryder, O.A., Graphodat-sky, A.S., and O’Brien, S.J., Precision nomenclature for the new genomics, GigaScience, 2019, vol. 8, p. giz086.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Li, Y-C., Lee, C., Sanoudou, D., Hseu, T-H., Li, S-Y., and Lin, C.C., Interstitial colocalization of two cervid satellite DNAs involved in the genesis of the Indian muntjac karyotype, Chromosome Res., 2000, vol. 8, p. 363.

    Article  CAS  PubMed  Google Scholar 

  32. Li, Y.C., Lee, C., Chang, W.S., Li, S.Y., and Lin, C.C., Isolation and identification of a novel satellite DNA family highly conserved in several Cervidae species, Chromosoma, 2002, vol. 111, p. 176.

    Article  CAS  PubMed  Google Scholar 

  33. Lin, C.C., Sasi, R., Fan, Y.S., and Chen, Z.Q., New evidence for tandem chromosome fusions in the karyotypic evolution of Asian muntjacs, Chromosoma, 1991, vol. 101, p. 19.

    Article  CAS  PubMed  Google Scholar 

  34. Lin, C.-C., Hsu, P.-C., Li, T.-S., Liao, S.-J., Cheng, Y.-M., Hsieh, L.-J., and Li, Y.-S., Construction of an Indian muntjac BAC library and production of the most highly dense FISH map of the species, Zool. Stud., 2008, vol. 47, p. 283.

    Google Scholar 

  35. Matthey, R., Chromosome formulae of eutherian mammals, in Cytotaxonomy and Vertebrate Evolution, Chiarelli, A.B. and Capanna, E., Eds., London: Academic, 1973, p. 531.

    Google Scholar 

  36. Mudd, A.B., Bredeson, J.V., Baum, R., Hockemeyer, D., and Rokhsar, D.S., Muntjac chromosome evolution and architecture, BioRxiv, 2019. https://doi.org/10.1101/772343

  37. Murmann, A.E., Mincheva, A., Scheuermann, M.O., Gautier, M., Yang, F., Buitkamp, J., Strissel, P.L., Strick, R., Rowley, J.D., and Lichter, P., Comparative gene mapping in cattle, Indian muntjac, and Chinese muntjac by fluorescence in situ hybridization, Genetica, 2008, vol. 134, p. 345.

    Article  CAS  PubMed  Google Scholar 

  38. Pardue, M.L. and Hsu, T.C., Locations of 18S and 28S ribosomal genes on the chromosomes of the Indian muntjac, J. Cell Biol., 1975, vol. 64, p. 251.

    Article  CAS  PubMed  Google Scholar 

  39. Patterson, R.M. and Petricciani, J.C., A comparison of prophase and metaphase G-bands in the muntjac, J. Hered., 1973, vol. 64, p. 80.

    Article  CAS  PubMed  Google Scholar 

  40. Proskuryakova, A.A., Kulemzina, A.I., Perelman, P.L., Makunin, A.I., Larkin, D.M., Farré, M., Kukekova, A.V., Johnson, J.L., Lemskaya, N.A., Beklemisheva, V.R., Roelke-Parker, M.E., Bellizzi, J., Ryder, O.A., O’Brien, S.J., and Graphodatsky, A.S., X chromosome evolution in Cetartiodactyla, Genes, 2017, vol. 8, p. 216.

    Article  PubMed Central  CAS  Google Scholar 

  41. Proskuryakova, A.A., Kulemzina, A.I., Perelman, P.L., Serdukova, N.A., Ryder, O.A., and Graphodatsky, A.S., The case of X and Y localization of nucleolus organizer regions (NORs) in Tragulus javanicus (Cetartiodactyla, Mammalia), Genes, 2018, vol. 9, p. 312.

    Article  PubMed Central  CAS  Google Scholar 

  42. Proskuryakova, A.A, Kulemzina, A.I., Perelman, P.L., Yudkin, D.V., Lemskaya, N.A., Okhlopkov, I.M., Kirillin, E.V., Farré, M., Larkin, D.M., Roelke-Par-ker, M.E., O’Brien, S.J., Bush, M., and Graphodat-sky, A.S., Comparative chromosome mapping of musk ox and the X chromosome among some Bovidae species, Genes, 2019, vol. 10, p. 857.

    Article  PubMed Central  CAS  Google Scholar 

  43. Saitoh, Y. and Laemmli, U.K., Metaphase chromosome structure: Bands arise from a differential folding path of the highly AT-rich scaffold, Cell, 1994, vol. 76, p. 609.

    Article  CAS  PubMed  Google Scholar 

  44. Sharma, T. and Dhaliwal, M.K., Relationship between patterns of late S DNA synthesis and C- and G-banding in muntjac chromosomes, Exp. Cell Res., 1974, vol. 87, p. 394.

    Article  CAS  PubMed  Google Scholar 

  45. Seabright, M., A rapid banding technique for human chromosomes, Lancet, 1971, vol. 298, p. 971.

    Article  Google Scholar 

  46. Scherthan, H., The localization of the repetitive telomeric sequence (TTAGGG)n in two muntjac species and implications for their karyotypic evolution, Cytogenet. Cell Ge-net., 1990, vol. 53, p. 115.

    Article  CAS  Google Scholar 

  47. Schmid, M., Steinlein, C., Lomb, C., Sperling, K., and Neitzel, H., 5-methylcytosine-rich heterochromatin in the Indian muntjac, Cytogenet. Genome Res., 2016, vol. 147, p. 240.

    Article  CAS  Google Scholar 

  48. Shi, L. and Pathak, S., Gametogenesis in a male Indian muntjac × Chinese muntjac hybrid, Cytogenet. Cell Genet., 1981, vol. 30, p. 152.

    Article  Google Scholar 

  49. Shi, L., Ye, Y., and Duan, X.S., Comparative cytogenetic studies on the red muntjac, Chinese muntjac and their F1 hybrids, Cytogenet. Cell Genet., 1980, vol. 26, p. 22.

    Article  Google Scholar 

  50. Sumner, A.T., A simple technique for demonstrating centromeric heterochromatin, Exp. Cell Res., 1972, vol. 75, p. 304.

    Article  CAS  PubMed  Google Scholar 

  51. Tsipouri, V., Schueler, M.G., Hu, S., Dutra, A., Pak, E., Riethman, H., and Green, ED., Comparative sequence analyses reveal sites of ancestral chromosomal fusions in the Indian muntjac genome, Genome Biol., 2008, vol. 9, p. R155.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Verma, R.S., Ved Brat, S., and Dosik, H., Heterochromatin of chromosomes of Indian muntjac as revealed by fluorescent banding techniques, J. Hered., 1979, vol. 70, p. 438.

    Article  Google Scholar 

  53. Wurster, D.H. and Benirschke, K., Indian muntjac, Muntiacus muntjak: a deer with a low diploid chromosome number, Science, 1970, vol. 168, p. 1364.

    Article  CAS  PubMed  Google Scholar 

  54. Yamaguchi, N. and Huh, N., Establishment and characterization of Indian muntjac cell lines transformed with simian virus 40, J. Gen. Virol., 1979, vol. 42, p. 289.

    Article  CAS  PubMed  Google Scholar 

  55. Yang, F. and Graphodatsky, A.S., Animal probes and ZOO-FISH, in Fluorescence In Situ Hybridization (FISH). Application Guide, Liehr, T., Ed., 2nd ed., Berlin: Springer-Verlag, 2017, p. 395.

    Google Scholar 

  56. Yang, F., Carter, N.P., Shi, L., and Ferguson-Smith, M.A., A comparative study of karyotypes of muntjacs by chromosome painting, Chromosoma, 1995, vol. 103, p. 642.

    Article  CAS  PubMed  Google Scholar 

  57. Yang, F., O’Brien, P.C., Wienberg, J., and Ferguson-Smith, M.A., A reappraisal of the tandem fusion theory of karyotype evolution in Indian muntjac using chromosome painting, Chromosome Res., 1997a, vol. 5, p. 109.

    Article  CAS  PubMed  Google Scholar 

  58. Yang, F., Muller, S., Just, R., Ferguson-Smith, M.A., and Wienberg, J., Comparative chromosome painting in mammals: human and the Indian muntjac (Muntiacus muntjak vaginalis), Genomics, 1997b, vol. 39, p. 396.

    Article  CAS  PubMed  Google Scholar 

  59. Zhou, Q., Huang, L., Zhang, J., Zhao, X., Zhang, Q., Song, F., Chi, J., Yang, F., and Wang, W., Comparative genomic analysis links karyotypic evolution with genomic evolution in the Indian muntjac (Muntiacus muntjak vaginalis), Chromosoma, 2006, vol. 115, p. 427.

    Article  CAS  PubMed  Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors are grateful to Prof. F. Yang, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge, United Kingdom), who responded positively to the great scientific, as well as gastronomic, interest of one of the paper coauthors (A. Grafodatsky) in muntjacs, which resulted in the production of tissue samples, DNA, and cell culture of the animal, which has become the object of our study and many others. The authors are grateful to Prof. Malcolm Ferguson-Smith (Cambridge Resource Centre for Comparative Genomics, University of Cambridge, Cambridge, United Kingdom), who transferred a unique collection of vertebrate cell cultures, including cells of several muntjac species, to the Institute of Molecular and Cellular Biology, Siberian Branch, Russian Academy of Sciences.

Funding

This work was financially supported by the Russian Science Foundation, project no. 19-14-00034.

Author information

Authors and Affiliations

  1. Institute of Molecular and Cellular Biology, Siberian Branch, Russian Academy of Sciences, 630090, Novosibirsk, Russia

    L. S. Biltueva, P. L. Perelman, A. A. Proskuryakova, N. A. Lemskaya, N. A. Serdyukova & A. S. Grafodatsky

Authors
  1. L. S. Biltueva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. L. Perelman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. A. Proskuryakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. A. Lemskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N. A. Serdyukova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. S. Grafodatsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to L. S. Biltueva or A. S. Grafodatsky.

Ethics declarations

Conflict of interests. The authors declare that they have no conflicts of interest.

Statement on the welfare of humans or animals. This article does not contain any studies involving animals performed by any of the authors.

Additional information

Abbreviations: NOR—nucleolus organizer region.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Biltueva, L.S., Perelman, P.L., Proskuryakova, A.A. et al. Chromosomes of the Indian Muntjac (Muntiacus muntjak): Comeback. Cell Tiss. Biol. 14, 407–412 (2020). https://doi.org/10.1134/S1990519X20060048

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990519X20060048

Keywords:

Search

Navigation