Biochemistry (Moscow)

, Volume 83, Issue 4, pp 338–349 | Cite as

Banding Pattern of Polytene Chromosomes as a Representation of Universal Principles of Chromatin Organization into Topological Domains

  • T. D. KolesnikovaEmail author


Drosophila polytene chromosomes are widely used as a model of eukaryotic interphase chromosomes. The most noticeable feature of polytene chromosome is transverse banding associated with alternation of dense stripes (dark or black bands) and light diffuse areas that encompass alternating less compact gray bands and interbands visible with an electron microscope. In recent years, several approaches have been developed to predict location of morphological structures of polytene chromosomes based on the distribution of proteins on the molecular map of Drosophila genome. Comparison of these structures with the results of analysis of the three-dimensional chromatin organization by the Hi-C method indicates that the morphology of polytene chromosomes represents direct visualization of the interphase nucleus spatial organization into topological domains. Compact black bands correspond to the extended topological domains of inactive chromatin, while interbands are the barriers between the adjacent domains. Here, we discuss the prospects of using polytene chromosomes to study mechanisms of spatial organization of interphase chromosomes, as well as their dynamics and evolution.


polytene chromosomes topologically associating domain TADs spatial organization of interphase chromosome 3D chromatin organization interband Hi-C 



intercalary heterochromatin


polytene chromosomes


topologically associating domain


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  1. 1.
    Zhimulev, I. F. (1999) Genetic organization of polytene chromosomes, Adv. Genet., 39, 1–589.PubMedGoogle Scholar
  2. 2.
    Spierer, A., and Spierer, P. (1984) Similar level of polyteny in bands and interbands of Drosophila giant chromosomes, Nature, 307, 176–178.CrossRefPubMedGoogle Scholar
  3. 3.
    Kozlova, T., Semeshin, V. F., Tretyakova, I. V., Kokoza, E. B., Pirrotta, V., Grafodatskaya, V. E., Belyaeva, E. S., and Zhimulev, I. F. (1994) Molecular and cytogenetical characterization of the 10A1-2 band and adjoining region in the Drosophila melanogaster polytene X chromosome, Genetics, 136, 1063–1073.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Vatolina, T. Y., Boldyreva, L. V., Demakova, O. V., Demakov, S. A., Kokoza, E. B., Semeshin, V. F., Babenko, V. N., Goncharov, F. P., Belyaeva, E. S., and Zhimulev, I. F. (2011) Identical functional organization of nonpolytene and polytene chromosomes in Drosophila melanogaster, PLoS One, 6, e25960.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Zhimulev, I. F., Zykova, T. Y., Goncharov, F. P., Khoroshko, V. A., Demakova, O. V., Semeshin, V. F., Pokholkova, G. V., Boldyreva, L. V., Demidova, D. S., Babenko, V. N., Demakov, S. A., and Belyaeva, E. S. (2014) Genetic organization of interphase chromosome bands and interbands in Drosophila melanogaster, PLoS One, 9, e101631.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Bridges, C. B. (1935) Salivary chromosome maps with a key to the banding of the chromosomes of Drosophila melanogaster, J. Hered., 26, 60–64.CrossRefGoogle Scholar
  7. 7.
    Lefevre, E. G. (1976) A Photographic Representation and Interpretation of the Polytene Chromosomes of Drosophila melanogaster Salivary Glands (Ashburner, M., ed.) Academic Press, London-New York.Google Scholar
  8. 8.
    Zhimulev, I. F., Semeshin, V. F., Kulichkov, V. A., and Belyaeva, E. S. (1982) Intercalary heterochromatin in Drosophila. I. Localization and general characteristics, Chromosoma, 87, 197–228.CrossRefGoogle Scholar
  9. 9.
    Beermann, W. (1952) Chromomerenkonstanz und specifische modifikationen der chromosomenstruktur in der entwicklung und organdifferenzierung von Chironomus tentans, Chromosoma, 5, 139–198.CrossRefGoogle Scholar
  10. 10.
    Beermann, W. (1965) Structure and Function of Interphase Chromosomes (Gerts, S. J., ed.) Pergamon Press, Oxford-London-Edinburgh-NewYork-Paris-Frankfurt, pp. 375–384.Google Scholar
  11. 11.
    Sinha, P., Mishra, A., and Lakhotia, S. C. (1987) Chromosomal organization of Drosophila tumors. I. Polytene chromosome organization and DNA synthesis in ovarian pseudonurse cells in otu mutants of D. melanogaster, Chromosoma, 95, 108–116.CrossRefGoogle Scholar
  12. 12.
    Mal’ceva, N. I., Gyurkovics, H., and Zhimulev, I. F. (1995) General characteristics of the polytene chromosome from ovarian pseudonurse cells of the Drosophila melanogaster otu11 and fs(2)B mutants, Chromosome Res., 3, 191–200.CrossRefPubMedGoogle Scholar
  13. 13.
    Heino, T. I. (1994) Polytene chromosomes from ovarian pseudonurse cells of the Drosophila melanogaster out mutant. II. Photographic map of the X chromosome, Chromosoma, 103, 4–15.CrossRefPubMedGoogle Scholar
  14. 14.
    Demakov, S. A., Vatolina, T. Y., Babenko, V. N., Semeshin, V. F., Belyaeva, E. S., and Zhimulev, I. F. (2011) Protein composition of interband regions in polytene and cell line chromosomes of Drosophila melanogaster, BMC Genomics, 12, 566.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Vatolina, T., Demakov, S. A., Semeshin, V. F., Makunin, I. V., Babenko, V. N., Beliaeva, E. S., and Zhimulev, I. F. (2011) Identification and molecular genetic characterization of the polytene chromosome interbands in Drosophila melanogaster, Russ. J. Genet., 47, 521–532.CrossRefGoogle Scholar
  16. 16.
    Zhimulev, I. F., Belyaeva, E. S., Vatolina, T. Y., and Demakov, S. A. (2012) Banding patterns in Drosophila melanogaster polytene chromosomes correlate with DNA-binding protein occupancy, Bioessays, 34, 498–508.CrossRefPubMedGoogle Scholar
  17. 17.
    Boldyreva, L. V., Goncharov, F. P., Demakova, O. V., Zykova, T. Y., Levitsky, V. G., Kolesnikov, N. N., Pindyurin, A. V., Semeshin, V. F., and Zhimulev, I. F. (2017) Protein and genetic composition of four chromatin types in Drosophila melanogaster cell lines, Curr. Genomics, 18, 214–226.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Gortchakov, A. A., Eggert, H., Gan, M., Mattow, J., Zhimulev, I. F., and Saumweber, H. (2005) CHRIZ, a chromodomain protein specific for the interbands of Drosophila melanogaster polytene chromosomes, Chromosoma, 114, 54–66.CrossRefPubMedGoogle Scholar
  19. 19.
    Filion, G. J., van Bemmel, J. G., Braunschweig, U., Talhout, W., Kind, J., Ward, L. D., Brugman, W., de Castro, I. J., Kerkhoven, R. M., Bussemaker, H. J., and van Steensel, B. (2010) Systematic protein location mapping reveals five principal chromatin types in Drosophila cells, Cell, 143, 212–224.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Kharchenko, P. V., Alekseyenko, A. A., Schwartz, Y. B., Minoda, A., Riddle, N. C., Ernst, J., Sabo, P. J., Larschan, E., Gorchakov, A. A., Gu, T., Linder-Basso, D., Plachetka, A., Shanower, G., Tolstorukov, M. Y., Luquette, L. J., Xi, R., Jung, Y. L., Park, R. W., Bishop, E. P., Canfield, T. K., Sandstrom, R., Thurman, R. E., MacAlpine, D. M., Stamatoyannopoulos, J. A., Kellis, M., Elgin, S. C., Kuroda, M. I., Pirrotta, V., Karpen, G. H., and Park, P. J. (2011) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster, Nature, 471, 480–485.CrossRefPubMedGoogle Scholar
  21. 21.
    Khoroshko, V. A., Levitsky, V. G., Zykova, T. Y., Antonenko, O. V., Belyaeva, E. S., and Zhimulev, I. F. (2016) Chromatin heterogeneity and distribution of regulatory elements in the late-replicating intercalary heterochromatin domains of Drosophila melanogaster chromosomes, PLoS One, 11, e0157147.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Demakova, O. V., Boldyreva, L. V., Demakov, S. A., Goncharov, F. P., Antonenko, O. V., and Zhimulev, I. F. (2016) Characteristic of the chromatin type corresponding to thin “grey” bands in polythene chromosomes of Drosophila melanogaster, Tsitologiya, 58, 248–252.Google Scholar
  23. 23.
    Kolesnikova, T. D., and Zhimulev, I. F. (2016) Comprehensive approach to mapping late-replicating bands in polytene chromosomes of Drosophila melanogaster, Tsitologiya, 58, 262–266.Google Scholar
  24. 24.
    Beermann, W. (1972) Chromomeres and Genes in Results and Problems in Cell Differentiation (Beermann, W., ed.) Springer, Berlin-Heidelberg-New York, pp. 1–33.Google Scholar
  25. 25.
    Sorsa, V. (1984) Electron microscopic mapping and ultrastructure of Drosophila polytene chromosomes, in Insect Ultrastructure (King, R. C., and Akai, H., eds.) Plenum Press, New York, pp. 75–107.Google Scholar
  26. 26.
    Saura, A. (1986) Electron Microscopic Mapping of the Second Polytene Chromosome of Drosophila melanogaster, Ph. D. Thesis, University of Helsinki, Dept. of Genetics., p. 58.Google Scholar
  27. 27.
    Celniker, S. E., Dillon, L. A., Gerstein, M. B., Gunsalus, K. C., Henikoff, S., Karpen, G. H., Kellis, M., Lai, E. C., Lieb, J. D., MacAlpine, D. M., Micklem, G., Piano, F., Snyder, M., Stein, L., White, K. P., Waterston, R. H., and modENCODE Consortium (2009) Unlocking the secrets of the genome, Nature, 459, 927–930.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Eagen, K. P., Hartl, T. A., and Kornberg, R. D. (2015) Stable chromosome condensation revealed by chromosome conformation capture, Cell, 163, 934–946.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Ulianov, S. V., Khrameeva, E. E., Gavrilov, A. A., Flyamer, I. M., Kos, P., Mikhaleva, E. A., Penin, A. A., Logacheva, M. D., Imakaev, M. V., Chertovich, A., Gelfand, M. S., Shevelyov, Y. Y., and Razin, S. V. (2016) Active chromatin and transcription play a key role in chromosome partitioning into topologically associating domains, Genome Res., 26, 70–84.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Sexton, T., Yaffe, E., Kenigsberg, E., Bantignies, F., Leblanc, B., Hoichman, M., Parrinello, H., Tanay, A., and Cavalli, G. (2012) Three-dimensional folding and functional organization principles of the Drosophila genome, Cell, 148, 458–472.CrossRefPubMedGoogle Scholar
  31. 31.
    White, R. (2012) Packaging the fly genome: domains and dynamics, Brief. Funct. Genomics, 11, 347–355.CrossRefPubMedGoogle Scholar
  32. 32.
    Stadler, M. R., Haines, J. E., and Eisen, M. B. (2017) Convergence of topological domain boundaries, insulators, and polytene interbands revealed by high-resolution mapping of chromatin contacts in the early Drosophila melanogaster embryo, Elife, 6, e29550.PubMedGoogle Scholar
  33. 33.
    Ea, V., Baudement, M. O., Lesne, A., and Forne, T. (2015) Contribution of topological domains and loop formation to 3D chromatin organization, Genes (Basel), 6, 734–750.CrossRefGoogle Scholar
  34. 34.
    Razin, S. V., and Ulianov, S. V. (2017) Gene functioning and storage within a folded genome, Cell. Mol. Biol. Lett., 22, 18.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Weinreb, C., and Raphael, B. J. (2016) Identification of hierarchical chromatin domains, Bioinformatics, 32, 1601–1609.CrossRefPubMedGoogle Scholar
  36. 36.
    Hou, C., Li, L., Qin, Z. S., and Corces, V. G. (2012) Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains, Mol. Cell, 48, 471–484.PubMedGoogle Scholar
  37. 37.
    El-Sharnouby, S., Fischer, B., Magbanua, J. P., Umans, B., Flower, R., Choo, S. W., Russell, S., and White, R. (2017) Regions of very low H3K27me3 partition the Drosophila genome into topological domains, PLoS One, 12, e0172725.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Van Bortle, K., Nichols, M. H., Li, L., Ong, C. T., Takenaka, N., Qin, Z. S., and Corces, V. G. (2014) Insulator function and topological domain border strength scale with architectural protein occupancy, Genome Biol., 15, R82.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Belyaeva, E. S., Goncharov, F. P., Demakova, O. V., Kolesnikova, T. D., Boldyreva, L. V., Semeshin, V. F., and Zhimulev, I. F. (2012) Late replication domains in polytene and non-polytene cells of Drosophila melanogaster, PLoS One, 7, e30035.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Dixon, J. R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J. S., and Ren, B. (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions, Nature, 485, 376–380.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Andreyenkova, N. G., Kolesnikova, T. D., Makunin, I. V., Pokholkova, G. V., Boldyreva, L. V., Zykova, T. Y., Zhimulev, I. F., and Belyaeva, E. S. (2013) Late replication domains are evolutionary conserved in the Drosophila genome, PLoS One, 8, e83319.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Kolesnikova, T. D., Goncharov, F. P., and Zhimulev, I. F. (2018) Similarity in replication timing between polytene and diploid cells is associated with the organization of the Drosophila genome, PLoS One, in press.Google Scholar
  43. 43.
    Saura, A. O., Heino, T. I., and Sorsa, V. (1994) Electron micrograph map of the Drosophila melanogaster polytene chromosome 3R divisions 81 through 90, Hereditas, 121, 1–20.CrossRefPubMedGoogle Scholar
  44. 44.
    Semeshin, V. F., Demakov, S. A., Shloma, V. V., Vatolina, T. Y., Gorchakov, A. A., and Zhimulev, I. F. (2008) Interbands behave as decompacted autonomous units in Drosophila melanogaster polytene chromosomes, Genetica, 132, 267–279.CrossRefPubMedGoogle Scholar
  45. 45.
    Zhimulev, I. F., Belyaeva, E. S., Semeshin, V. F., Koryakov, D. E., Demakov, S. A., Demakova, O. V., Pokholkova, G. V., and Andreyeva, E. N. (2004) Polytene chromosomes: 70 years of genetic research, Int. Rev. Cytol., 241, 203–275.CrossRefPubMedGoogle Scholar
  46. 46.
    Andreenkov, O. V., Andreenkova, N. G., Volkova, E. I., Georgiev, P. G., Goncharova, A. A., Pokholkova, G. V., and Demakov, S. A. (2016) Ectopic attraction of the Chromator protein in the UAS>DBD(GAL4) system as a method for investigation of insulator proteins in polytene chromosomes from Drosophila melanogaster, Tsitologiya, 58, 493–496.Google Scholar
  47. 47.
    Zhimulev, I. F., and Belyaeva, E. S. (1999) Detailed description of puffing patterns in the salivary gland chromosomes of normally developing larvae and prepupae of Drosophila melanogaster, Dros. Inf. Serv., 82, 9–20.Google Scholar
  48. 48.
    Semeshin, V. F., Baricheva, E. M., Belyaeva, E. S., and Zhimulev, I. F. (1985) Electron microscopical analysis of Drosophila polytene chromosomes. II. Development of complex puffs, Chromosoma, 91, 210–233.CrossRefPubMedGoogle Scholar
  49. 49.
    Semeshin, V. F., Zhimulev, I. F., and Belyaeva, E. S. (1979) Electron microscope autoradiographic study on transcriptional activity of Drosophila melanogaster polytene chromosomes, Chromosoma, 73, 163–177.CrossRefGoogle Scholar
  50. 50.
    Vlassova, I. E., Umbetova, G. H., Zimmermann, V. H., Alonso, C., Belyaeva, E. S., and Zhimulev, I. F. (1985) Immunofluorescence localization of DNA:RNA hybrids in Drosophila melanogaster polytene chromosomes, Chromosoma, 91, 251–258.CrossRefPubMedGoogle Scholar
  51. 51.
    Semeshin, V. F., Shloma, V. V., and Zhimulev, I. F. (2001) Formation and morphology of dark puffs in Drosophila melanogaster polytene chromosomes, Hereditas, 134, 15–22.CrossRefPubMedGoogle Scholar
  52. 52.
    Khoroshko, V. A., Zykova, T. Yu., Popova, O. O., and Zhimulev, I. F. (2018) Boundary structure of intercalary heterochromatin bands in Drosophila melanogaster polytene chromosomes, Dokl. Akad. Nauk, 5, 1–4.Google Scholar
  53. 53.
    Zielke. T., Glotov, A., and Saumweber, H. (2015) High-resolution in situ hybridization analysis on the chromosomal interval 61C7-61C8 of Drosophila melanogaster reveals interbands as open chromatin domains, Chromosoma, 125, 423–435.CrossRefPubMedGoogle Scholar
  54. 54.
    Belyaeva, E. S., Demakov, S. A., Pokholkova, G. V., Alekseyenko, A. A., Kolesnikova, T. D., and Zhimulev, I. F. (2006) DNA underreplication in intercalary heterochromatin regions in polytene chromosomes of Drosophila melanogaster correlates with the formation of partial chromosomal aberrations and ectopic pairing, Chromosoma, 115, 355–366.CrossRefPubMedGoogle Scholar
  55. 55.
    Yarosh, W., and Spradling, A. C. (2014) Incomplete replication generates somatic DNA alterations within Drosophila polytene salivary gland cells, Genes Dev., 28, 1840–1855.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Maqbool, S. B., Mehrotra, S., Kolpakas, A., Durden, C., Zhang, B., Zhong, H., and Calvi, B. R. (2010) Dampened activity of E2F1-DP and Myb-MuvB transcription factors in Drosophila endocycling cells, J. Cell Sci., 123, 4095–4106.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Ulianov, S. V., Tachibana-Konwalski, K., and Razin, S. V. (2017) Single-cell Hi-C bridges microscopy and genome-wide sequencing approaches to study 3D chromatin organization, Bioessays, 39, doi: 10.1002/bies.201700104.Google Scholar
  58. 58.
    Semeshin, V. F., Artero, R., Perez-Alonso, M., and Shloma, V. V. (1998) Electron microscopic in situ hybridization of digoxigenin-dUTP-labelled DNA probes with Drosophila melanogaster polytene chromosomes, Chromosome Res., 6, 405–410.CrossRefPubMedGoogle Scholar
  59. 59.
    Kolesnikova, T. D., Semeshin, V. F., Andreyeva, E. N., Zykov, I. A., Kokoza, E. B., Kalashnikova, D. A., Belyaeva, E. S., and Zhimulev, I. F. (2011) Induced decondensation of heterochromatin in Drosophila melanogaster polytene chromosomes under condition of ectopic expression of the Suppressor of underreplication gene, Fly (Austin), 5, 181–190.CrossRefGoogle Scholar
  60. 60.
    Zhimulev, I. F., Belyaeva, E. S., Semeshin, V. F., Shloma, V. V., Makunin, I. V., and Volkova, E. I. (2003) Overexpression of the SuUR gene induces reversible modifications at pericentric, telomeric and intercalary heterochromatin of Drosophila melanogaster polytene chromosomes, J. Cell Sci., 116, 169–176.PubMedGoogle Scholar
  61. 61.
    Boettiger, A. N., Bintu, B., Moffitt, J. R., Wang, S., Beliveau, B. J., Fudenberg, G., Imakaev, M., Mirny, L. A., Wu, C. T., and Zhuang, X. (2016) Super-resolution imaging reveals distinct chromatin folding for different epigenetic states, Nature, 529, 418–422.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Ghavi-Helm, Y., Klein, F. A., Pakozdi, T., Ciglar, L., Noordermeer, D., Huber, W., and Furlong, E. E. (2014) Enhancer loops appear stable during development and are associated with paused polymerase, Nature, 512, 96–100.CrossRefPubMedGoogle Scholar
  63. 63.
    Engstrom, P. G., Ho Sui, S. J., Drivenes, O., Becker, T. S., and Lenhard, B. (2007) Genomic regulatory blocks underlie extensive microsynteny conservation in insects, Genome Res., 17, 1898–1908.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Harmston, N., Ing-Simmons, E., Tan, G., Perry, M., Merkenschlager, M., and Lenhard, B. (2017) Topologically associating domains are ancient features that coincide with Metazoan clusters of extreme noncoding conservation, Nat. Commun., 8, 441.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Makunin, I. V., Kolesnikova, T. D., and Andreyenkova, N. G. (2014) Underreplicated regions in Drosophila melanogaster are enriched with fast-evolving genes and highly conserved noncoding sequences, Genome Biol. Evol., 6, 2050–2060.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Von Grotthuss, M., Ashburner, M., and Ranz, J. M. (2010) Fragile regions and not functional constraints predominate in shaping gene organization in the genus Drosophila, Genome Res., 20, 1084–1096.CrossRefGoogle Scholar

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© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  1. 1.Institute of Molecular and Cellular BiologySiberian Branch of the Russian Academy of SciencesNovosibirskRussia
  2. 2.Novosibirsk State UniversityNovosibirskRussia

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