Skip to main content
Log in

DNA replication in nurse cell polytene chromosomes of Drosophila melanogaster otu mutants

Chromosoma Aims and scope Submit manuscript

Abstract

Drosophila cell lines are used extensively to study replication timing, yet data about DNA replication in larval and adult tissues are extremely limited. To address this gap, we traced DNA replication in polytene chromosomes from nurse cells of Drosophila melanogaster otu mutants using bromodeoxyuridine incorporation. Importantly, nurse cells are of female germline origin, unlike the classical larval salivary glands, that are somatic. In contrast to salivary gland polytene chromosomes, where replication begins simultaneously across all puffs and interbands, replication in nurse cells is first observed at several specific chromosomal regions. For instance, in the chromosome 2L, these include the regions 31B-E and 37E and proximal parts of 34B and 35B, with the rest of the decondensed chromosomal regions joining replication process a little later. We observed that replication timing of pericentric heterochromatin in nurse cells was shifted from late S phase to early and mid stages. Curiously, chromosome 4 may represent a special domain of the genome, as it replicates on its own schedule which is uncoupled from the rest of the chromosomes. Finally, we report that SUUR protein, an established marker of late replication in salivary gland polytene chromosomes, does not always colocalize with late-replicating regions in nurse cells.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Belyakin SN, Christophides GK, Alekseyenko AA, Kriventseva EV, Belyaeva ES, Nanayev RA, Makunin IV, Heidelberg Fly Array Consortium, Kafatos FC, Zhimulev IF (2005) Genomic analysis of Drosophila chromosome underreplication reveals a link between replication control and transcriptional territories. Proc Natl Acad Sci U S A 102:8269–8274

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Belyakin SN, Babenko VN, Maksimov DA, Shloma VV, Kvon EZ, Belyaeva ES, Zhimulev IF (2010) Gene density profile reveals the marking of late replicated domains in the Drosophila melanogaster genome. Chromosoma 119:589–600

    Article  PubMed  Google Scholar 

  • Berendes HD (1966) Differential replication of male and female X-chromosomes in Drosophila. Chromosoma 20:32–43

    Article  Google Scholar 

  • Chadwick BP, Willard HF (2003) Barring gene expression after XIST: maintaining facultative heterochromatin on the inactive X. Semin Cell Dev Biol 14:359–367

    Article  CAS  PubMed  Google Scholar 

  • Chatterjee SN, Mondal SN, Mukherjee AS (1976) Interchromosomal asynchrony of DNA replication in polytene chromosomes of Drosophila pseudoobscura. Chromosoma 54:117–125

    Article  CAS  PubMed  Google Scholar 

  • Dej KJ, Spradling AC (1999) The endocycle controls nurse cell polytene chromosome structure during Drosophila oogenesis. Development 126:293–303

    CAS  PubMed  Google Scholar 

  • Eaton ML, Prinz JA, MacAlpine HK, Tretyakov G, Kharchenko PV, MacAlpine DM (2011) Chromatin signatures of the Drosophila replication program. Genome Res 21:164–174

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Edgar BA, Orr-Weaver TL (2001) Endoreplication cell cycles: more for less. Cell 105:297–306

    Article  CAS  PubMed  Google Scholar 

  • Gilbert DM (2002) Replication timing and transcriptional control: beyond cause and effect. Curr Opin Cell Biol 14:377–383

    Article  CAS  PubMed  Google Scholar 

  • Gilbert CW, Muldal S, Lajtha LG, Rowley J (1962) Time-sequence of human chromosome duplication. Nature 195:869–873

    Article  CAS  PubMed  Google Scholar 

  • Graveley BR, May G, Brooks AN, Carlson JW, Cherbas L, Davis CA, Duff M, Eads B, Landolin J, Sandler J, Wan KH, Andrews J, Brenner SE, Cherbas P, Gingeras TR, Hoskins R, Kaufman T, Celniker SE (2011). The D. melanogaster transcriptome: modENCODE RNA-Seq data for dissected tissues. http://www.modencode.org/Celniker.shtml

  • Hammond MP, Laird CD (1985) Chromosome structure and DNA replication in nurse and follicle cells of Drosophila melanogaster. Chromosoma 91:267–278

    Article  CAS  PubMed  Google Scholar 

  • Heino TI (1989) Polytene chromosomes from ovarian pseudonurse cells of the Drosophila melanogaster otu mutant. I. Photographic map of chromosome 3. Chromosoma 97:363–373

    Article  CAS  PubMed  Google Scholar 

  • Hiratani I, Takebayashi S, Lu J, Gilbert DM (2009) Replication timing and transcriptional control: beyond cause and effect-part II. Curr Opin Genet Dev 19:142–149

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • King RC, Riley SF, Cassidy JD, White PE, Paik YK (1981) Giant polytene chromosomes from the ovaries of a Drosophila mutant. Science 212:441–443

    Article  CAS  PubMed  Google Scholar 

  • King RC, Mohler D, Riley SF, Storto PD, Nicolazzo PS (1986) Complementation between alleles at the ovarian tumor locus of Drosophila melanogaster. Dev Genet 7:1–20

    Article  CAS  PubMed  Google Scholar 

  • Kolesnikova TD, Posukh OV, Andreyeva EN, Bebyakina DS, Ivankin AV, Zhimulev IF (2013) Drosophila SUUR protein associates with PCNA and binds chromatin in a cell cycle-dependent manner. Chromosoma 122:55–66

    Article  CAS  PubMed  Google Scholar 

  • Koren A, McCarroll SA (2014) Random replication of the inactive X chromosome. Genome Res 24:64–69

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Koryakov DE, Belyaeva ES, Alekseyenko AA, Zhimulev IF (1996) Alpha and beta heterochromatin in polytene chromosome 2 of Drosophila melanogaster. Chromosoma 105:310–319

    Article  CAS  PubMed  Google Scholar 

  • Koryakov DE, Alekseyenko AA, Zhimulev IF (1999) Dynamic organization of the b-heterochromatin in the Drosophila melanogaster polytene X chromosome. Mol Gen Genet 260:503–509

    Article  CAS  PubMed  Google Scholar 

  • Koryakov DE, Domanitskaya EV, Belyakin SN, Zhimulev IF (2003) Abnormal tissue-dependent polytenization of a block of chromosome 3 pericentric heterochromatin in Drosophila melanogaster. J Cell Sci 116:1035–1044

    Article  CAS  PubMed  Google Scholar 

  • Koryakov DE, Reuter G, Dimitri P, Zhimulev IF (2006) The SuUR gene influences the distribution of heterochromatic proteins HP1 and SU(VAR)3-9 on nurse cell polytene chromosomes of Drosophila melanogaster. Chromosoma 115:296–310

    Article  CAS  PubMed  Google Scholar 

  • Koryakov DE, Pokholkova GV, Maksimov DA, Belyakin SN, Belyaeva ES, Zhimulev IF (2012) Induced transcription results in local changes in chromatin structure, replication timing, and DNA polytenization in a site of intercalary heterochromatin. Chromosoma 121:573–583

    Article  CAS  PubMed  Google Scholar 

  • Larsson J, Chen JD, Rasheva V, Rasmuson-Lestander A, Pirrotta V (2001) Painting of fourth, a chromosome-specific protein in Drosophila. Proc Natl Acad Sci U S A 98:6273–6278

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lilly MA, Spradling AC (1996) The Drosophila endocycle is controlled by Cyclin E and lacks a checkpoint ensuring S-phase completion. Genes Dev 10:2514–2526

    Article  CAS  PubMed  Google Scholar 

  • MacAlpine DM, Bell SP (2005) A genomic view of eukaryotic DNA replication. Chromosome Res 13:309–326

    Article  CAS  PubMed  Google Scholar 

  • Mahowald AP, Kambysellis MP (1980) Oogenesis. In: Ashburner M, Wright TRF (eds) The genetics and biology of Drosophila. Acad Press Inc. V. 2d. pp 141–225

  • Maksimov DA, Koryakov DE, Belyakin SN (2014) Developmental variation of the SUUR protein binding correlates with gene regulation and specific chromatin types in D. melanogaster. Chromosoma 123:253–264

    Article  CAS  PubMed  Google Scholar 

  • Makunin IV, Volkova EI, Belyaeva ES, Nabirochkina EN, Pirrotta V, Zhimulev IF (2002) The Drosophila suppressor of underreplication protein binds to late-replicating regions of polytene chromosomes. Genetics 160:1023–1034

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mal’ceva NI, Zhimulev IF (1993) Extent of polytene in the pericentric heterochromatin of polytene chromosomes of pseudonurse cells of otu (ovarian tumor) mutants of Drosophila melanogaster. Mol Gen Genet 240:273–276

    Article  PubMed  Google Scholar 

  • Mal’ceva NI, Gyurkovics H, Zhimulev IF (1995) General characteristics of the polytene chromosome from ovarian pseudonurse cells of the Drosophila melanogaster otu 11 and fs(2)B mutants. Chromosome Res 3:191–200

    Article  PubMed  Google Scholar 

  • Mal’ceva NI, Belyaeva ES, King RC, Zhimulev IF (1997) Nurse cell polytene chromosomes of Drosophila melanogaster otu mutants: morphological changes accompanying interallelic complementation and position effect variegation. Dev Genet 20:163–174

    Article  PubMed  Google Scholar 

  • Painter RB (1961) Asynchronous replication of HeLa S3 chromosomal deoxyribonucleic acid. J Biophys Biochem Cytol 11:485–488

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pindyurin AV, Moorman C, de Wit E, Belyakin SN, Belyaeva ES, Christophides GK, Kafatos FC, van Steensel B, Zhimulev IF (2007) SUUR joins separate subsets of PcG, HP1 and B-type lamin targets in Drosophila. J Cell Sci 120:2344–2351

    Article  CAS  PubMed  Google Scholar 

  • Pindyurin AV, Boldyreva LV, Shloma VV, Kolesnikova TD, Pokholkova GV, Andreyeva EN, Kozhevnikova EN, Ivanoschuk IG, Zarutskaya EA, Demakov SA, Gorchakov AA, Belyaeva ES, Zhimulev IF (2008) Interaction between the Drosophila heterochromatin proteins SUUR and HP1. J Cell Sci 121:1693–1703

    Article  CAS  PubMed  Google Scholar 

  • Rasch EM, King RC, Rasch RW (1984) Cytophotometric studies on cells from the ovaries of otu mutants of Drosophila melanogaster. Histochemistry 81:105–110

    Article  CAS  PubMed  Google Scholar 

  • Riddle NC, Leung W, Haynes KA, Granok H, Wuller J, Elgin SCR (2008) An investigation of heterochromatin domains on the fourth chromosome of Drosophila melanogaster. Genetics 178:1177–1191

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Riddle NC, Jung YL, Gu T, Alekseyenko AA, Asker D, Gui H, Kharchenko PV, Minoda A, Plachetka A, Schwartz YB, Tolstorukov MY, Kuroda MI, Pirrotta V, Karpen GH, Park PJ, Elgin SCR (2012) Enrichment of HP1a on Drosophila chromosome 4 genes creates an alternate chromatin structure critical for regulation in this heterochromatic domain. PLoS Genet 8(9):e1002954

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rodesch C, Pettus J, Nagoshi RN (1997) The Drosophila ovarian tumor gene is required for the organization of actin filaments during multiple stages in oogenesis. Dev Biol 190:153–164

    Article  CAS  PubMed  Google Scholar 

  • Schübeler D, Scalzo D, Kooperberg C, van Steensel B, Delrow J, Groudine M (2002) Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing. Nat Genet 32:438–442

    Article  PubMed  Google Scholar 

  • Schwaiger M, Schübeler D (2006) A question of timing: emerging links between transcription and replication. Curr Opin Genet Dev 16:177–183

    Article  CAS  PubMed  Google Scholar 

  • Schwaiger M, Stadler MB, Bell O, Kohler H, Oakeley EJ, Schübeler D (2009) Chromatin state marks cell-type- and gender-specific replication of the Drosophila genome. Genes Dev 23:589–601

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sclafani RA, Holzen TM (2007) Cell cycle regulation of DNA replication. Annu Rev Genet 41:237–280

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sher N, Bell GW, Li S, Nordman J, Eng T, Eaton ML, MacAlpine DM, Orr-Weaver TL (2012) Developmental control of gene copy number by repression of replication initiation and fork progression. Genome Res 22:64–75

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sinha P, Mishra A, Lakhotia SC (1987) Chromosomal organization of Drosophila tumours. I. Polytene chromosome organization and DNA synthesis in ovarian pseudonurse cells in otu mutants of D. melanogaster. Chromosoma 95:108–116

    Article  Google Scholar 

  • Stoffregen EP, Donley N, Stauffer D, Smith L, Thayer MJ (2011) An autosomal locus that controls chromosome-wide replication timing and mono-allelic expression. Hum Mol Genet 20:2366–2378

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thayer MJ (2012) Mammalian chromosomes contain cis-acting elements that control replication timing, mitotic condensation, and stability of entire chromosomes. Bioessays 34:760–770

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tzeng TY, Lee CH, Chan LW, Shen CK (2007) Epigenetic regulation of the Drosophila chromosome 4 by the histone H3K9 methyltransferase dSETDB1. Proc Natl Acad Sci U S A 104:12691–12696

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vicoso B, Bachtrog D (2013) Reversal of an ancient sex chromosome to an autosome in Drosophila. Nature 499:332–335

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang N, Trend B, Kaung HL, Wang T (1982) Chromosomal replication asynchrony of a human breast carcinoma cell line. I. Studied by continuous BrdU incorporation and G-banding analysis. Cancer Genet Cytogenet 7:173–180

    Article  CAS  PubMed  Google Scholar 

  • Zhimulev IF (1999) Genetic organization of polytene chromosomes. Adv Genet 39:1–599

    Article  CAS  PubMed  Google Scholar 

  • Zhimulev IF, Semeshin VF, Kulichkov VA, Belyaeva ES (1982) Intercalary рeterochromatin in Drosophila. I. Localization and general characteristics. Chromosoma 87:197–228

    Article  Google Scholar 

  • Zhimulev IF, Belyaeva ES, Makunin IV, Pirrotta V, Volkova EI, Alekseyenko AA, Andreyeva EN, Makarevich GF, Boldyreva LV, Nanayev RA, Demakova OV (2003) Influence of the SuUR gene on intercalary heterochromatin in Drosophila melanogaster polytene chromosomes. Chromosoma 111:377–398

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to A.A. Gorchakov, O.V. Demakova, D.A. Maksimov, and E.S. Belyaeva for their comments and help in data interpretation. The work was supported by the grant of the Russian Science Foundation (14-14-00934).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dmitry E. Koryakov.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Koryakov, D.E., Zhimulev, I.F. DNA replication in nurse cell polytene chromosomes of Drosophila melanogaster otu mutants. Chromosoma 124, 95–106 (2015). https://doi.org/10.1007/s00412-014-0487-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-014-0487-4

Keywords

Navigation