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Molecular and genetic organization of Drosophila melanogasterpolytene chromosomes: evidence for two types of interband regions

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Abstract

The 3A and 60E regions of Drosophila melanogaster polytene chromosomes containing inserted copies of the P{lArB} transposon have been subjected to an electron microscopic (EM) analysis. We show that both inserts led to formation of new bands within the interband regions 3A4/A6 and 60E8-9/E10. This allowed us to clone DNA of these interbands. Their sequences, as well as those of DNA from other four interbands described earlier, have been analyzed. We have found that, with the exception of 60E8-9/E10 interband, all other five regions under study corresponded to 5' or 3' ends of genes. We have further obtained the evidence for 60E8-9/E10 interband to harbor the 'housekeeping' RpL19 gene, which is transcribed in many tissues, including salivary glands. Based upon the genetic heterogeneity of the interbands observed a revised model of polytene chromosome organization is discussed.

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References

  • Adams, M. D., S. E. Celniker, R. A. Holt, C. A. Evans et al., 2000. The genome sequence of Drosophila melanogaster. Science 287: 2185–2195.

    PubMed  Google Scholar 

  • Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Zh. Zhang, W. Miller & D. J. Lipman, 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25: 3389–3402.

    PubMed  Google Scholar 

  • Beermann, W., 1972. Chromomeres and genes, pp.1–33 in Results and Problems in Cell Differentiation, Vol. 4, edited by W. Beermann. Springer, Berlin, Heidelberg, New York.

    Google Scholar 

  • Bonner, J. J., C. Parks, J. Parker-Thornburg, M. A. Mortin & H. R. B. Pelham, 1984. The use of promoter fusions in Drosophila genetics: isolation of mutations a. ecting the heat shock response. Cell 37: 979–991.

    PubMed  Google Scholar 

  • Bridges, C. B., 1938. A revised map of the salivary gland X-chromosome of Drosophila melanogaster. J. Hered. 29: 11–13.

    Google Scholar 

  • Carrera, P., S. Abrell, B. Kerber, U. Walldorf, A. Preiss, M. Hoch & H. Jackle, 1998. A modifier screen in the eye reveals control genes for Kruppel activity in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 9: 10779–10784.

    Google Scholar 

  • Crick, F., 1971. General model for the chromosomes of higher organisms. Nature 234: 25–27.

    PubMed  Google Scholar 

  • Cuvier, O., C. M. Hart & U. K. Laemmli, 1998. Identification of a class of chromatin boundary elements. Mol. Cell Biol. 18: 7478–7486.

    PubMed  Google Scholar 

  • Dahmus, M. E., 1996. Reversible phosphorylation of the C-terminal domain of RNA polymerase II. J. Biol. Chem. 271: 19009–19012.

    PubMed  Google Scholar 

  • Demakov, S. A., V. F. Semeshin & I. F. Zhimulev, 1993. Cloning and molecular genetic analysis of Drosophila melanogaster interband DNA. Mol. Gen. Genet. 238: 437–443.

    PubMed  Google Scholar 

  • Frisch, M., K. Frech, A. Klingenho., K. Quandt, I. Liebich & T. Werner, 2000. A new tool for the in silico prediction of matrix attachment regions in large genomic sequences, pp. 27–34 in Proceedings of the German Conference on Bioinformatics, edited by E. Bornberg-Bauer, U. Rost, J. Stoye & M. Vingron. Logos Verlag, Berlin.

    Google Scholar 

  • Gersh, E. S., 1975. Sites of gene activity and of inactive genes in polytene chromosomes of Diptera. J. Theor. Biol. 50: 413–428.

    PubMed  Google Scholar 

  • Gilmour, D. S. & J. T. Lis, 1986. RNA polymerase II interacts with the promoter region of the noninduced hsp-70 gene in Drosophila melanogaster cells. Mol. Cell Biol. 6: 3984–3989.

    PubMed  Google Scholar 

  • Goode, S., M. Melnick, T. B. Chou & N. Perrimon, 1996. The neurogenic genes egghead and brainiac define a novel signaling pathway essential for epithelial morphogenesis during Drosophila oogenesis. Development 122: 3863–3879.

    PubMed  Google Scholar 

  • Hancock, R., 2000. A new look at the nuclear matrix. Chromosoma 109: 219–225.

    PubMed  Google Scholar 

  • Hart, K., T. Klein & M. Wilcox, 1993. A Minute encoding a ribosomal protein enhances wing morphogenesis mutants. Mech. Dev. 43: 101–110.

    PubMed  Google Scholar 

  • Hollmann, M., 2000. Drosophila melanogaster WDS (wds)and egghead (egh)genes, complete cds. GenBank/EMBL/DDBJ 2000.2.9. AF233288.

  • Jamrich, M., A. L. Greenleaf & E. K. F. Bautz, 1977. Locali-zation of RNA-polymerase in Drosophila melanogaster polytene chromosomes. Proc. Nat. Acad. Sci. USA 74: 2079–2083.

    PubMed  Google Scholar 

  • Jenuwein, T. & C. D. Allis, 2001. Translating the histone code. Science 293: 1074–1080.

    PubMed  Google Scholar 

  • Jin, Y., Y. Wang, D. L. Walker, H. Dong, C. Conley, J. Johansen & K. M. Johansen, 1999. JIL-1: a novel chromosomal tandem kinase implicated in transcriptional regulation in Drosophila. Mol. Cell 4: 129—135.

    Google Scholar 

  • Kaplan, C. D., J. R. Morris, C.-T. Wu & F. Winston, 2000. Spt5 and Spt6 are associated with active transcription and have characteristics of general elongation factors in D. melano-gaster. Genes Dev. 14: 2623–2634.

    PubMed  Google Scholar 

  • Kellum, R. & P. Schedl, 1992. A group of scs elements function as domain boundaries in enhancer-blocking assay. Mol. Cell Biol. 12: 2424–2431.

    Google Scholar 

  • Kelley, M. R., S. Kidd, R. L. Berg & M. W. Young, 1987. Restriction of P element insertions at the Notch locus of Drosophila melanogaster. Mol. Cell Biol. 7: 1545–1548.

    PubMed  Google Scholar 

  • Keppy, D. O. & W. J. Welshons, 1977. The cytogenetics of a recessive visible mutant associated with a de ciency adja-cent to the Notch locus in Drosophila melanogaster. Genet-ics 85: 497–506.

    Google Scholar 

  • Korge, G., I. Heide, M. Sehnert & A. Hofmann, 1980. Promoter is a important determinant of developmentally regulated pu. ng at the Sgs-4 locus of Drosophila melano-gaster. Develop. Biol. 138: 324–337.

    Google Scholar 

  • Kozlova, T., I. F. Zhimulev & F. C. Kafatos, 1997. Molecular organization of an individual Drosophila polytene chromo-some chromomere: transcribed sequences in the 10A1-2 band. Mol. Gen. Genet. 257: 55–61.

    PubMed  Google Scholar 

  • Laemmli, U. K., E. Kas, L. Poljak & Y. Adachi, 1992. Sca. old-associated regions: cis-acting determinants of chromatin structural loops and functional domains. Curr. Opin. Genet. Dev. 2: 275–285.

    PubMed  Google Scholar 

  • Law, A., K. Hirayoshi, T. O' Brien & J. T. Lis, 1998. Direct cloning of DNA that interacts in vivo with a speci c protein: application to RNA polymerase II and sites of pausing in Drosophila. Nucl. Acids Res. 26: 919–924.

    PubMed  Google Scholar 

  • Levy, A. & M. Nöll, 1981. Chromatin fine structure of active and repressed genes. Nature 289: 198–203.

    PubMed  Google Scholar 

  • Liao, G., E. J. Rehm & G. M. Rubin, 2000. Insertion site preferences of the P transposable element in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 97: 3347–3351.

    PubMed  Google Scholar 

  • Mott, M. R. & R. J. Hill, 1986. The ultrastructural morphology of native salivary gland chromosomes of Drosophila mela-nogaster: the band-interband question. Chromosoma 94: 403–411.

    PubMed  Google Scholar 

  • O' Kane, C. J. & W. C. Gehring, 1987. Detection in situ of genomic regulatory elements in Drosophila. Proc. Natl. Acad. Sci. USA 84: 9123–9127.

    PubMed  Google Scholar 

  • Paul, J., 1972. General theory of chromosomes structure and gene activation in eukaryotes. Nature 238: 444–446.

    PubMed  Google Scholar 

  • Pirrotta, V., 1999. Transvection and chromosomal trans-interaction effects. Biochim. Biophys. Acta 1424: M1–M8.

    PubMed  Google Scholar 

  • Pirrotta, V. & Ch. Bröckl, 1984. Transcription of the Drosoph-ila white locus and some of its mutants. EMBO J. 3: 563–568.

    PubMed  Google Scholar 

  • Prokopenko, S. N. & H. J. Bellen, 2000. From phenotype to gene function: a molecular screen for novel genes required for the development of the peripheral nervous system. Dros. Res. Conf. 41: 727C.

  • Ramos, R. G. P., B. G. Grimwade, K. A. Wharton, T. N. Scott-gale & S. Artavanis-Tsakonas, 1989. Physical and func-tional de nition of the Drosophila Notch locus by P element transformation. Genetics 123: 337–348.

    PubMed  Google Scholar 

  • Razin, S. V., I. I. Gromova & O. V. Iarovaia, 1995. Specificity and functional signi cance of DNA interactions with the nuclear matrix: new approaches to clarify the old questions. Int. Rev. Cytol. 162B: 405–448.

    PubMed  Google Scholar 

  • Rykowski, M. C., S. J. Parmelee, D. A. Agard & J. W. Sedat, 1988. Precise determination of the molecular limits of a polytene chromosome band: regulatory sequences for the Notch gene are in the interband. Cell 54: 461–472.

    PubMed  Google Scholar 

  • Sambrook, J., E. F. Fritsch & T. Maniatis, 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.

    Google Scholar 

  • Sass, H. & E. K. F. Bautz, 1982. Interbands of polytene chromosomes: binding sites and start points for RNA polymerase. Chromosoma 86: 77–93.

    PubMed  Google Scholar 

  • Schwartz, Yu. B., S. A. Demakov & I. F. Zhimulev, 1998. Cloning and analysis of DNA from 85D9/D10 and 86B4/ B6 interband region. Genetika 34: 905-913 (in Russian).

    Google Scholar 

  • Schwartz, Yu. B., E. S. Ioudinkova, S. A. Demakov, S. V. Razin & I. F. Zhimulev, 1999. Interbands of Drosophila melano-gaster polytene chromosomes contain matrix association regions. J. Cell Biochem. 72: 368–372.

    PubMed  Google Scholar 

  • Schwartz, Yu. B., S. A. Demakov & I. F. Zhimulev, 2001. Polytene chromosome interband DNA is organized into nucleosomes. Mol. Genet. Genom. 265: 311–315.

    Google Scholar 

  • Semeshin, V. F., I. F. Zhimulev & E. S. Belyaeva, 1979. Electron microscope autoradiographic study of transcriptional activ-ity of Drosophila melanogaster polytene chromosomes. Chromosoma 73: 163–177.

    Google Scholar 

  • Semeshin, V. F., E. M. Baricheva, E. S. Belyaeva & I. F. Zhimu-lev, 1982. Electron microscopical analysis of Drosophila polytene chromosomes. I. Mapping of the 87A and 87C heat shock pu. s in development. Chromosoma 87: 229–237.

    Google Scholar 

  • Semeshin, V. F., E. S. Belyaeva, I. F. Zhimulev, J. T. Lis, G. Richards & M. Bourouis, 1986. Electron microscopical analysis of Drosophila polytene chromosomes. IV. Mapping of morphological structures appearing as a result of transformation of DNA sequences into chromosomes. Chromosoma 93: 461–468.

    Google Scholar 

  • Semeshin, V. F., S. A. Demakov, M. Perez Alonso, E. S. Belya-eva, J. J. Bonner & I. F. Zhimulev, 1989. Electron micro-scopical analysis of Drosophila polytene chromosomes. V. Characteristics of structures formed by transposed DNA segments of mobile elements. Chromosoma 97: 396–412.

    PubMed  Google Scholar 

  • Semeshin, V. F., V. A. Chernukhin, I. V. Shabel' nikov, L. V. Omel' yanchuk, E. S. Belyaeva & I. F. Zhimulev, 1994. Cytogenetic analysis of insertions belong to interbands of Drosophila polytene chromosomes. Genetika 30: 927-933 (in Russian).

    PubMed  Google Scholar 

  • Semeshin, V. F., R. Artero, M. Perez Alonso & V. V. Shloma, 1998. Electron microscopic in situ hybridization of digox-igenin-dUTP-labelled DNA probes with Drosophila poly-tene chromosomes. Chromosome Res. 6: 405–410.

    PubMed  Google Scholar 

  • Siden-Kiamos, I., R. D. Saunders, L. Spanos, T. Majerus, J. Treanear, C. Savakis, C. Louis, D. M. Glover, M. Ash-burner & F. C. Kafatos, 1990. Towards a physical map of the Drosophila melanogaster genome: mapping of cosmid clones within defined genomic divisions. Nucl. Acids Res. 18: 6261–6270.

    PubMed  Google Scholar 

  • Singh, G. A., J. A. Kramer & S. A. Krawetz, 1997. Mathematical model to predict regions of chromatin attachment to the nuclear matrix. Nucl. Acids Res. 25: 1419–1425 (http: // www. futuresoft. org/MAR-Wiz).

    PubMed  Google Scholar 

  • Skaer, R. J., 1977. Interband transcription in Drosophila. J. Cell Sci. 26: 251–266.

    PubMed  Google Scholar 

  • Sorsa, V., 1984. Electron microscopic mapping and ultrastruc-ture of Drosophila polytene chromosomes, 2, pp.75–107 in Insect Ultratructure, edited by King, R. C. & H. Akai. Plenum Press, New York.

    Google Scholar 

  • Spradling, A. C., D. M. Stern, I. Kiss, J. Roote, T. Laverty & G. M. Rubin, 1995. Gene disruptions using P transposable elements: an integral component of Drosophila genome project. Proc. Natl. Acad. Sci. USA 92: 10824–10830.

    PubMed  Google Scholar 

  • Spradling, A. C., D. Stern, A. Beaton, E. J. Rehm, T. Laverty, N. Mozden, S. Misra & G. M. Rubin, 1999. The Berkeley Drosophila genome project gene disruptions project: single P element insertions mutating 25 %of vital Drosophila genes. Genetics 153: 135–177.

    PubMed  Google Scholar 

  • Udvardy, A., E. Maine & P. Schedl, 1985. The 87A chromo-mere. Identi cation of novel chromatin structures. anking the heat shock locus that may de ne the boundaries of higher order domains. J. Mol. Biol. 185: 341–358.

    PubMed  Google Scholar 

  • Vazquez, J. & P. Schedl, 1994. Sequences required for enhancer blocking activity of scs are located within two nuclease-hypersensitive regions. EMBO J. 13: 5984–5993.

    PubMed  Google Scholar 

  • Vazquez, J. & P. Schedl, 2000. Deletion of an insulator element by the mutation facet-strawberry in Drosophila melanogas-ter. Genetics 155: 1297–1311.

    PubMed  Google Scholar 

  • Vlassova, I. E., G. H. Umbetova, V. H. Zimmermann, C. Alonso, E. S. Belyaeva & I. F. Zhimulev, 1985. Immuno-fluorescence localization of DNA: RNA hybrids in Drosophila melanogaster polytene chromosomes. Chromosoma 91: 251–258.

    PubMed  Google Scholar 

  • Wang, Y., W. Zheng, Y. Jin, J. Johansen & K. M. Johansen, 2001. The JIL-1 tandem kinase mediates histone H3 phosphorylation and is required for maintenance of chro-matin structure in Drosophila. Cell 105: 433–443.

    PubMed  Google Scholar 

  • Weeks, J. R., S. E. Hardin, J. Shen, J. M. Lee & A. L. Greenleaf, 1993. Locus-specific variation in phosphorylation state of RNA polymerase II in vivo: correlations with gene activ-ity and transcript processing. Genes Dev. 7: 2329–2344.

    Google Scholar 

  • Zhao, K., C. M. Hart & U. K. Laemmli, 1995. Visualization of chromosomal domains with Boundary Element Associated Factor BEAF-32. Cell 81: 879–889.

    PubMed  Google Scholar 

  • Zhimulev, I. F., 1996. Morphology and structure of polytene chromosomes. Adv. Genet. 34: 1–497.

    PubMed  Google Scholar 

  • Zhimulev, I. F., 1999. Genetic organization of polytene chro-mosomes. Adv. Genet. 39: 1–589.

    PubMed  Google Scholar 

  • Zhimulev, I. F. & E. S. Belyaeva, 1975. 3H-uridine labelling patterns in the Drosophila melanogaster salivary gland chromosomes X,2R and 3L. Chromosoma 49: 219–231.

    Google Scholar 

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Authors and Affiliations

  1. Institute of Cytology and Genetics, Russia

    Sergei Demakov, Andrei Gortchakov, Valery Semeshin & Igor Zhimulev

  2. Department of Zoology, University of Geneva, Switzerland

    Yuri Schwartz

  3. Centro de Biología Molecular Severo Ochoa, Universidad Autonoma de Madrid, Spain

    Sonsoles Campuzano & Juan Modolell

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  1. Sergei Demakov
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  2. Andrei Gortchakov
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  3. Yuri Schwartz
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  4. Valery Semeshin
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  6. Juan Modolell
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  7. Igor Zhimulev
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Demakov, S., Gortchakov, A., Schwartz, Y. et al. Molecular and genetic organization of Drosophila melanogasterpolytene chromosomes: evidence for two types of interband regions. Genetica 122, 311–324 (2004). https://doi.org/10.1007/s10709-004-2839-0

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