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Tandem Repeats in the Genome of Sus scrofa, Their Localization on Chromosomes and in the Spermatogenic Cell Nuclei

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Abstract

Bioinformatics methods make it possible to find and annotate large tandem repeats (TR) in the genome assemblies of different organisms. In this study, the genomic assembly of Sus scrofa (pig) (Sscrofa10.2, in the NCBI database) was examined and a set of species-specific TR was identified. In addition, using FISH and the designed short oligonucleotide probes (Sscrf_335A, Sscrf_243A, Sscrf_15A, and Sscrf_50A), some of these TR were mapped to metaphase chromosomes. All TR present in the Repbase database for pig are detected using bioinformatics methods, and in addition to these, another 18 new TR families were found in the genome assembly Sscrofa10.2. Compared to human and mouse, the set of TR identified in the Sscrofa10.2 assembly is characterized by longer monomer length. The Sscrf_15A and Sscrf_243A probes identify a set of acrocentric (Ac) chromosomes, the Sscrf_50A probe identifies a set of sub/metacentric (Mc) chromosomes, and the Sscrf_335A probe labels all chromosomes. Probes were used to follow the centromeric region organization during spermatogenesis. In meiotic prophase I, all probes labeled ring structures, which were not described in the literature. In this study it was demonstrated that (1) the designed probes detected the Ms and Ac chromosome sets; (2) in spermatozoa, there was a specific pattern for each probe; and (3) centromeric probes probably provided an opportunity to follow the centromeric region arrangement.

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REFERENCES

  1. Podgornaya, O.I., Ostromyshenskii, D.I., and Enukashvili, N.I., Who needs this junk, or genomic dark matter, Biochemistry (Moscow), 2018, vol. 83, no. 4, pp. 450—466. https://doi.org/10.1134/S0006297918040156

    Article  CAS  PubMed  Google Scholar 

  2. Komissarov, A.S., Gavrilova, E.V., Demin, S.J., et al., Tandemly repeated DNA families in the mouse genome, BMC Genomics, 2011, vol. 12, no. 531, pp. 1—21.

    Article  CAS  Google Scholar 

  3. Foster, H.A., Abeydeera, L.R., Griffin, D.K., and Bridger, J.M., Non-random chromosome positioning in mammalian sperm nuclei, with migration of the sex chromosomes during late spermatogenesis, J. Cell Sci., 2005, vol. 116, pp. 1811—1820. https://doi.org/10.1242/jcs.02301

    Article  CAS  Google Scholar 

  4. Zalensky, A. and Zalenskaya, I., Organization of chromosomes in spermatozoa: an additional layer of epigenetic information?, Biochem. Soc. Transact., 2007, vol. 35, no. 3, pp. 609—611.

    Article  CAS  Google Scholar 

  5. Ward, W.S., Organization of sperm DNA by the nuclear matrix, Am. J. Clin. Exp. Urol., 2018, vol. 6, no. 2, pp. 87—92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Govin, J., Escoffier, E., Rousseaux, S., et al., Pericentric heterochromatin reprogramming by new histone variants during mouse spermiogenesis, J. Cell Biol., 2007, vol. 176, pp. 283—294. https://doi.org/10.1083/jcb.200604141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ward, W.S., Function of sperm chromatin structural elements in fertilization, Mol. Hum. Reprod., 2010, vol. 16, no. 1, pp. 30—36. https://doi.org/10.1093/molehr/gap080

    Article  CAS  PubMed  Google Scholar 

  8. Chagin, V., Zalensky, A., Nazarov, I., and Mudrak, O., Preferable location of chromosomes 1, 29, and X in bovine spermatozoa, AIMS Genet., 2018, vol. 5, no. 2, pp. 113—123. https://doi.org/10.3934/genet.2018.2.113

    Article  PubMed  PubMed Central  Google Scholar 

  9. Acloque, H., Bonnet-Garnier, A., Mompart, F., et al., Sperm nuclear architecture is locally modified in presence of a Robertsonian translocation t(13;17), PLoS One, 2013, vol. 8, no. 10, pp. 1—12. https://doi.org/10.1371/journal.pone.0078005

    Article  CAS  Google Scholar 

  10. Benson, G., Tandem repeats finder: a program to analyze DNA sequences, Nucleic Acids Res., 1999, vol. 27, no. 2, p. 573.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Rizk, G., Lavenier, D., and Chikhi, R., DSK: k-mer counting with very low memory usage, Bioinformatics, 2013, vol. 29, no. 5, pp. 652—653.

    Article  CAS  PubMed  Google Scholar 

  12. Moorhead, P.S., Nowell, P.C., Mellman, W.J., et al., Chromosome preparations of leukocytes cultured from human peripheral blood, Exp. Cell Res., 1960, vol. 20, pp. 613—616.

    Article  CAS  PubMed  Google Scholar 

  13. Chowdhary, B.P., de la Sena, C., Harbitz, I., et al., FISH on metaphase and interphase chromosomes demonstrates the physical order of the genes for GPI, CRC, and LIPE in pigs, Cytogenet. Cell Genet., 1995, vol. 71, no. 2, pp. 175—178.

    Article  CAS  PubMed  Google Scholar 

  14. Zalenskaya, I. and Zalensky, A., Non-random positioning of chromosomes in human sperm nuclei, Chromosome Res., 2004, vol. 12, no. 2, pp. 163—173.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Earl, D., Bradnam, K., John, J.S., et al., A competitive assessment of de novo short read assembly methods, Genome Res., 2011, vol. 21, no. 12, pp. 2224—2241. https://doi.org/10.1101/gr.126599.111

  16. Gustavsson, I., Standard karyotype of the domestic pig, Hereditas, 1988, vol. 109, pp. 151—157.

    Article  CAS  PubMed  Google Scholar 

  17. Schnedl, W., Abraham, R., Forster, M., and Schweizer, D., Differential fluorescent staining of porcine heterochromatin by chromomycin A3/distamycin A/DAPI and D 287/170, Cytogenet. Cell Genet., 1981, vol. 31, no. 4, pp. 249—253.

    Article  CAS  PubMed  Google Scholar 

  18. Jantsch, M., Hamilton, B., Mayr, B., and Schweizer, D., Meiotic chromosome behaviour reflects levels of sequence divergence in Sus scrofa domestica satellite DNA, Chromosoma, 1990, vol. 99, pp. 330—335.

    Article  CAS  PubMed  Google Scholar 

  19. Riquet, J., Mulsant, P., Yerle, M., et al., Sequence analysis and genetic mapping of porcine chromosome 11 centromeric S0048 marker, Cytogenet. Cell Genet., 1996, vol. 74, pp. 127—132.

    Article  CAS  PubMed  Google Scholar 

  20. Miller, J.R., Hindkjaer, J., and Thomsen, P.D., A chromosomal basis for the differential organization of a porcine centromere-specific repeat, Cytogenet. Cell Genet., 1993, vol. 62, pp. 37—41.

    Article  CAS  PubMed  Google Scholar 

  21. Janzen, M.A., Buoen, L.B., Zhao, F., and Louis, C.F., Characterization of a swine chromosome-specific centromeric higher-order repeat, Mamm. Genome, 1999, vol. 10, pp. 579—584.

    Article  CAS  PubMed  Google Scholar 

  22. Rogel-Gaillard, C., Bourgeaux, N., Save, J.C., et al., Construction of a swine YAC library allowing an efficient recovery of unique and centromeric repeat sequences, Mamm. Genome, 1997, vol. 8, pp. 186—192.

    Article  CAS  PubMed  Google Scholar 

  23. Akamatsu, M., Chen, Z., Dziuk, P.J., and McGraw, R.A., A highly repeated sequence in the domestic pig: a gernder-neutral probell, Nucleic Acids Res., 1989, vol. 17, no. 23, p. 10120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ostromyshenskii, D.I., Chernyaeva, E.N., Kuznetsova, I.S., and Podgornaya, O.I., Mouse chromocenters DNA content: sequencing and in silico analysis, BMC Genomics, 2018, vol. 19, p. 159. https://doi.org/10.1186/s12864-018-4534-z

    Article  CAS  Google Scholar 

  25. O’Neill, M.J. and O’Neill, R.J., Sex chromosome repeats tip the balance towards speciation, Mol. Ecol., 2018, pp. 1—16. https://doi.org/10.1111/mec.14577

  26. Pertile, M.D., Graham, A.N., Choo, K.H., and Kalitsis, P., Rapid evolution of mouse Y centromere repeat DNA belies recent sequence stability, Genome Res., 2009, vol. 19, no. 12, pp. 2202—2213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Qiao, H., Chen, J.K., Reynolds, A., et al., Interplay between synaptonemal complex, homologous recombination, and centromeres during mammalian meiosis, PLoS Genet., 2012, vol. 8, no. 6, pp. 1—17. https://doi.org/10.1371/journal.pgen.1002790

    Article  CAS  Google Scholar 

  28. Muller, H., Scolari, V.F., Agier, N., et al., Characterizing meiotic chromosomes’ structure and pairing using a designer sequence optimized for Hi-C, Mol. Syst. Biol., 2018, vol. 14, pp. 1—19. https://doi.org/10.15252/msb.20188293

    Article  CAS  Google Scholar 

  29. Tortereau, F., Servin, B., Frantz, L., et al., A high density recombination map of the pig reveals a correlation between sex-specific recombination and GC content, BMC Genomics, 2012, vol. 13, no. 586, pp. 1—12.

    Article  CAS  Google Scholar 

  30. Manvelyan, M., Hunstig, F., Bhatt, S., et al., Chromosome distribution in human sperm—a 3D multicolor banding-study, Mol. Cytogenet., 2008, no. 1, p. 25. https://doi.org/10.1186/1755-8166-1-25

  31. Sembon, S., Fuchimoto, D., Iwamoto, M., et al., A simple method for producing tetraploid porcine parthenogenetic embryos, Theriogenology, 2011, vol. 76, pp. 598—606. https://doi.org/10.1016/j.theriogenology.2011.03.010

    Article  CAS  PubMed  Google Scholar 

  32. Orsztynowicz, M., Pawlak, P., Ole, D., et al., Low incidence of chromosome aberrations in spermatozoa of fertile boars, Orig. Res., 2011, vol. 11, no. 3, pp. 224—235.

    Google Scholar 

  33. Massip, K., Berland, H., Bonnet, N., et al., Study of inter- and intra-individual variation of meiotic segregation patterns in t(3;15)(q27;q13) boars, Theriogenology, 2008, vol. 70, pp. 655—661. https://doi.org/10.1016/j.theriogenology.2008.04.026

    Article  CAS  PubMed  Google Scholar 

  34. Massip, K., Bonnet, N., Calgaro, A., et al., Male meiotic segregation analyses of peri- and paracentric inversions in the pig species, Cytogenet. Genome Res., 2009, vol. 125, pp. 117—124. https://doi.org/10.1159/000227836

    Article  CAS  PubMed  Google Scholar 

  35. Bonnet-Garnier, A., Guardia, S., Pinton, A., Ducos, A., and Yerle, M., Analysis using sperm-FISH of a putative interchromosomal effect in boars carrying reciprocal translocations, Cytogenet. Genome Res., 2009, vol. 126, pp. 194—201. https://doi.org/10.1159/000245920

    Article  CAS  PubMed  Google Scholar 

  36. Barasc, H., Ferchaud, S., Mary, N., et al., Cytogenetic analysis of somatic and germinal cells from 38,XX/38,XY phenotypically normal boars, Theriogenology, 2013, vol. 30, pp. 1—5. https://doi.org/10.1016/j.theriogenology.2013.10.006

    Article  Google Scholar 

  37. Telenius, H., Carter, N.P., Bebb, C.E., et al., Degenerate oligonucleotide-primed PCR: general amplification of target DNA by a single degenerate primer, Genomics, 1992, vol. 13, pp. 718—725.

    Article  CAS  PubMed  Google Scholar 

  38. Kuznetsova, I.S., Ostromyshenskii, D.I., Komissarov, A.S., et al., LINE related component of mouse heterochromatin and complex chromocenters’ composition, Chromosome Res., 2016, vol. 24, no. 3, pp. 309—323.

    Article  CAS  PubMed  Google Scholar 

  39. Ioannou, D., Millan, N.M., Jordan, E., and Tempest, H.G., A new model of sperm nuclear architecture following assessment of the organization of centromeres and telomeres in three-dimensions, Nat. Sci. Rep., 2017, vol. 7, no. 41585, pp. 1—14. https://doi.org/10.1038/srep41585

    Article  CAS  Google Scholar 

  40. Zalensky, A.O., Allen, M.J., Kobayashi, A., et al., Well-defined genome architecture in the human sperm nucleus, Chromosoma, 1995, vol. 103, pp. 577—590.

    Article  CAS  PubMed  Google Scholar 

  41. Hansen-Melander, E. and Melander, Y., The karyotype of the pig, Hereditas, 1974, vol. 77, pp. 149—158.

    Article  CAS  PubMed  Google Scholar 

  42. Enukashvily, N.I., Malashicheva, A.B., and Waisertreiger, I.S.-R., Satellite DNA spatial localization and transcriptional activity in mouse embryonic E-14 and IOUD2 stem cells, Cytogenet. Genome Res., 2009, vol. 124, pp. 277—287.https://doi.org/10.1159/000218132

    Article  CAS  PubMed  Google Scholar 

  43. Probst, A.V., Okamoto, I., Casanova, M., et al., A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development, Dev. Cell, 2010, vol. 19, pp. 625—638. https://doi.org/10.1016/j.devcel.2010.09.002

    Article  CAS  PubMed  Google Scholar 

  44. Kuznetsova, I., Podgornaya, O., and Ferguson-Smith, M.A., High-resolution organization of mouse centromeric and pericentromeric DNA, Cytogenet. Genome Res., 2006, vol. 112, pp. 248—255. https://doi.org/10.1159/000089878

    Article  CAS  PubMed  Google Scholar 

  45. Kalitsis, P., Zhang, T., Marshall, K.M., et al., Condensin, master organizer of the genome, Chromosome Res., 2017, pp. 1—16. https://doi.org/10.1007/s10577-017-9553-0

  46. Berríos, S., Manterola, M., Prieto, Z., et al., Model of chromosome associations in Mus domesticus spermatocytes, Biol. Res., 2010, vol. 43, pp. 275—295.

    Article  PubMed  Google Scholar 

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ACKNOWLEDGMENTS

We thank A.F. Saifitdinova and I.L. Trofimova for helpful discussion, I.A. Gamaley for the assistance in editing the text of the article, and also the staff of the Khromas Center for Collective Use (St. Petersburg University) for methodological assistance.

Funding

This study was supported by the Russian Foundation for Basic Research (18-04-00238-mol_a), Molecular and Cell Biology Program of the Presidium of the Russian Academy of Sciences (grant no. 01.2.01457147), and the Russian Science Foundation (grant no. 19-74-20102).

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Authors and Affiliations

  1. Institute of Cytology, Russian Academy of Sciences, 194064, St. Petersburg, Russia

    N. G. Ivanova, V. N. Stefanova, D. I. Ostromyshenskii & O. I. Podgornaya

  2. Department Cytology and Histology, St. Petersburg State University, 199034, St. Petersburg, Russia

    O. I. Podgornaya

  3. School of Biomedicine, Far East Federal University, 690922, Vladivostok, Russia

    O. I. Podgornaya

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  1. N. G. Ivanova
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Correspondence to N. G. Ivanova.

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

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

The experiments were carried out in accordance with the Animal Welfare Assurance (Assurance Identification number F18-00380) of the Institute of Cytology, Russian Academy of Sciences (valid from October 12, 2017, to October 31, 2022) for the protection of animals that are reared at experimental farms and used for scientific purposes.

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Translated by N. Maleeva

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Ivanova, N.G., Stefanova, V.N., Ostromyshenskii, D.I. et al. Tandem Repeats in the Genome of Sus scrofa, Their Localization on Chromosomes and in the Spermatogenic Cell Nuclei. Russ J Genet 55, 835–846 (2019). https://doi.org/10.1134/S102279541907007X

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