Skip to main content
SpringerLink
Log in
Book cover

Proteins of the Nucleolus pp 39–78Cite as

rDNA and Nucleologenesis in Drosophila

Abstract

The study of Drosophila ribosomal DNA (rDNA) dates back to the first bobbed mutations discovered by T.H. Morgan’s group nearly 100 years ago. From these earliest discoveries to the current day, Drosophila has proven to be a valuable system to study the genetic, molecular, and cellular aspects of rDNA in ribosome biogenesis. Our goal in writing this review was to describe the various aspects Drosophila rDNA, but within a historical context. We describe Drosophila nucleolar organizers and their flanking heterochromatin, how intergenic regions function in X-Y chromosome pairing, the fundamentals of Drosophila rDNA magnification and compensation, the fascinating biology of R1 and R2 retrotransposons and their mechanism of transposition, and the latest work on how rDNA acts as an epigenetic regulator of genome-wide gene expression in Drosophila. Expression of the rDNA itself is the driving mechanism in nucleologenesis (the formation of nucleoli), and we describe how Drosophila has contributed to our understanding of nucleologenesis. With the nucleolus now considered an important stress sensor within the cell, Drosophila will likely provide new insights into cell homeostasis as regulated by the nucleolus.

Keywords

  • Drosophila
  • rDNA
  • Nucleologenesis

This is a preview of subscription content, access via your institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Abbreviations

bb :

Bobbed

CAT:

Chloramphenicol acetytransferase

CTCF:

CCCTC-binding factor

DFC:

Dense fibrillar component

ECC:

Extrachromosomal circular copies

ETS:

External transcribed spacer

FISH:

Fluorescence in situ hybridization

GFP:

Green fluorescent protein

HSF:

Heat shock factor

IGS:

Intergenic spacer regions

IRES:

Internal ribosome entry site

ITS1 and 2:

Internal transcribed spacers 1 and 2

Kb:

Kilobase

MNM:

Modifier of Mdg4 in Meiosis

Nopp140:

Nucleolar phosphoprotein of 140 kDa

NOR:

Nucleolar organizer region

NoRC:

Nucleolar remodeling complex

ORF:

Open reading frame

PEV:

Position effect variegation

P5CDh:

Pyrroline-5-carboxylate dehydrogenase

rDNA:

Ribosomal RNA genes

rRNA:

Ribosomal RNA

RNP:

Ribonucleoprotein

RT-PCR:

Reverse transcriptase polymerase chain reaction

SAT:

Sine acido thymonucleinico

SNM:

Stromalin in Meiosis

TIF-IA:

Transcription initiation factor IA

TOR:

Target of rapamycin

TPA:

12-O-tetradecanoylphorbol-13-acetate

TPRT:

Target-primed reverse transcription

TU:

Transcription unit

UBF:

Upstream binding factor

References

  • Averbeck KT, Eickbush TH (2005) Monitoring the mode and tempo of concerted evolution in the Drosophila melanogaster rDNA locus. Genetics 171:1837–1846

    PubMed  CAS  Google Scholar 

  • Berendes HD, Keyl HG (1967) Distribution of DNA in heterochromatin and euchromatin of polytene nuclei of Drosophila hydei. Genetics 57:1–13

    PubMed  CAS  Google Scholar 

  • Botchan M, Kram R, Schmid CW, Hearst JE (1971) Isolation and chromosomal localization of highly repeated DNA sequences in Drosophila melanogaster. Proc Natl Acad Sci USA 68:1125–1129

    PubMed  CAS  Google Scholar 

  • Brown DD, Gurdon JD (1964) Absence of ribosomal RNA synthesis in the anucleate mutant of Xenopus laevis. Proc Natl Acad Sci U S A 51:139–146

    PubMed  CAS  Google Scholar 

  • Browne MJ, Read CA, Roiha H, Glover DM (1984) Site specific insertion of a type I rDNA element into a unique sequence in the Drosophila melanogaster genome. Nucleic Acids Res 12:9111–9122

    PubMed  CAS  Google Scholar 

  • Burke WD, Calalang CC, Eickbush TH (1987) The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme. Mol Cell Biol 7:2221–2230

    PubMed  CAS  Google Scholar 

  • Burke WD, Malik HS, Lathe WC III, Eickbush TH (1998) Are retrotransposons longterm hitchhikers? Nature 392:141–142

    PubMed  CAS  Google Scholar 

  • Chao Y, Pelligrini M (1993) In vitro transcription of Drosophila rDNA genes shows stimulation by a phorbol ester and serum. Mol Cell Biol 13:934–941

    PubMed  CAS  Google Scholar 

  • Chooi WY (1976) RNA transcription and ribosomal protein assembly in Drosophila melanogaster. In: King RC (ed) Handbook of genetics, vol 5, Molecular genetics. Plenum, New York

    Google Scholar 

  • Chooi YW (1979) The occurrence of long transcription units among the X and Y ribosomal genes of Drosophila melanogaster: transcription of insertion sequences. Chromosoma 74:57–74

    PubMed  CAS  Google Scholar 

  • Christensen SM, Eickbush TM (2005) R2 target-primed reverse transcription: ordered cleavage and polymerization steps by protein subunits asymmetrically bound to the target DNA. Mol Cell Biol 25:6617–6628

    PubMed  CAS  Google Scholar 

  • Christensen SM, Ye J, Eickbush TH (2006) RNA from the 5’ end of the R2 retrotransposon controls R2 protein binding to and cleavage of its DNA target site. Proc Natl Acad Sci USA 103:17602–17607

    PubMed  CAS  Google Scholar 

  • Coen ES, Dover GA (1982) Multiple Pol I initiation sequences in rDNA spacers of Drosophila melanogaster. Nucleic Acids Res 10:7017–7026

    PubMed  CAS  Google Scholar 

  • Cooper KW (1950) Normal spermatogenesis in Drosophila. In: Demerec M (ed) Biology of Drosophila. Wiley, New York

    Google Scholar 

  • Cooper KW (1958) A probable heterochromatic deficiency in In(1)sc L8, the approximate location of bobbed, and the size of block A. Dros Inf Serv 32:118–119

    Google Scholar 

  • Cooper KW (1959) Cytogenetic analysis of major heterochromatic elements (especially Xh and Y) in Drosophila melanogaster, and the theory of ‘heterochromatin’. Chromosoma 10:535–588

    PubMed  CAS  Google Scholar 

  • Cooper KW (1964) Meiotic conjunctive elements not involving chiasmata. Proc Natl Acad Sci USA 52:1248–1255

    PubMed  CAS  Google Scholar 

  • Cost GJ, Feng Q, Jacquier A, Boeke JD (2002) Human L1 element target-primed reverse transcription in vitro. EMBO J 21:5899–5910

    PubMed  CAS  Google Scholar 

  • Dawid IB, Botchan P (1977) Sequences homologous to ribosomal insertions occur in the Drosophila genome outside the nucleolus organizer. Proc Natl Acad Sci U S A 74:4233–4237

    PubMed  CAS  Google Scholar 

  • Dawid IB, Rebbert ML (1981) Nucleotide sequences at the boundaries between gene and insertion regions in the rDNA of Drosophila melanogaster. Nucleic Acids Res 9:5011–5020

    PubMed  CAS  Google Scholar 

  • Dawid IB, Wellauer PK, Long EO (1978) Ribosomal DNA in Drosophila melanogaster. I. Isolation and characterization of cloned fragments. J Mol Biol 126:749–768

    PubMed  CAS  Google Scholar 

  • Dickson E, Boyd JB, Laird CD (1971) Sequence diversity of polytene chromosome DNA from Drosophila hydei. J Mol Biol 61:615–627

    PubMed  CAS  Google Scholar 

  • DiMario PJ (2004) Cell and molecular biology of nucleolar assembly and disassembly. Int Rev Cytol 239:99–178

    PubMed  CAS  Google Scholar 

  • Edgar BA, Schubiger G (1986) Parameters controlling transcriptional activation during early Drosophila development. Cell 44:871–877

    PubMed  CAS  Google Scholar 

  • Eickbush TH (2002) R2 and related site-specific non-long terminal repeat retrotransposons. In: Craig NL et al (eds) Mobile DNA II. ASM, Washington, DC

    Google Scholar 

  • Eickbush TH, Eickbush DG (2007) Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175:477–485

    PubMed  CAS  Google Scholar 

  • Eickbush DG, Eickbush TH (2010) R2 retrotransposons encode a self-cleaving ribozyme for processing from an rRNA cotranscript. Mol Cell Biol 30:3142–3150

    PubMed  CAS  Google Scholar 

  • Eickbush TH, Robins B (1985) B. mori 28S genes contain insertion elements similar to the type I and type II elements of D. melanogaster. EMBO J 4:2281–2285

    PubMed  CAS  Google Scholar 

  • Eickbush DG, Ye J, Zhang X, Burke WD, Eickbush TH (2008) Epigenetic regulation of retrotransposons within the nucleolus of Drosophila. Mol Cell Biol 28:6452–6461

    PubMed  CAS  Google Scholar 

  • Endow SA (1980) On ribosomal gene compensation in Drosophila. Cell 22:149–155

    PubMed  CAS  Google Scholar 

  • Endow SA, Atwood KC (1988) Magnification: gene amplification by an inducible system of sister chromatid exchange. Trends Genet 4:348–351

    PubMed  CAS  Google Scholar 

  • Endow SA, Glover DM (1979) Differential replication of ribosomal gene repeats in polytene nuclei of Drosophila. Cell 17:597–605

    PubMed  CAS  Google Scholar 

  • Endow SA, Komma DJ (1986) One-step and stepwise magnification of a bobbed lethal chromosome in Drosophila melanogaster. Genetics 114:511–523

    PubMed  CAS  Google Scholar 

  • Feng Q, Moran JV, Kazazian HH Jr, Boeke JD (1996) Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87:905–916

    PubMed  CAS  Google Scholar 

  • Feng Q, Schuman G, Boeke JD (1998) Retrotransposon R1Bm endonuclease cleaves the target sequence. Proc Natl Acad Sci U S A 95:2083–2088

    PubMed  CAS  Google Scholar 

  • Foe VE, Alberts BM (1983) Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Biol 61:31–70

    CAS  Google Scholar 

  • Foe VE, Alberts BM (1985) Reversible chromosome condensation induced in Drosophila embryos by anoxia: visualization of interphase nuclear organization. J Cell Biol 100:1623–1636

    PubMed  CAS  Google Scholar 

  • Foe VE, Odell GM, Edgar BA (1993) Mitosis and morphogenesis in the Drosophila embryo: point and counterpoint. In: Bate M, Martinez Arias A (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Fujiwara H, Orgura T, Takada N, Miyajima N, Ishikawa H, Maekawa H (1984) Introns and their flanking sequences of B. mori rDNA. Nucleic Acids Res 12:6861–6869

    PubMed  CAS  Google Scholar 

  • Fullilove SL, Jacobson AG (1971) Nuclear elongation and cytokinesis in Drosophila montana. Dev Biol 26:560–577

    PubMed  CAS  Google Scholar 

  • Gall JG, Pardue ML (1969) Formation and detection of RNA-DNA hybrids in cytological preparations. Proc Natl Acad Sci U S A 63:378–383

    PubMed  CAS  Google Scholar 

  • Gall JG, Cohen EH, Lake Polan M (1971) Repetitive DNA sequences in Drosophila. Chromosoma 33:319–344

    PubMed  CAS  Google Scholar 

  • George JA, Eickbush TH (1999) Conserved features at the 5′ end of Drosophila R2 retrotransosable elements: implications for transcription and translation. Insect Mol Biol 8:3–10

    PubMed  CAS  Google Scholar 

  • Gershenson S (1933) Studies on the genetically inert region of the X chromosome of Drosophila. I. Behavior of an X chromosome deficient for a part of the inert region. J Genet 28:297–312

    Google Scholar 

  • Glover DM (1977) Cloned segment of Drosophila melanogaster rDNA containing new types of sequence insertion. Proc Natl Acad Sci U S A 74:4932–4936

    PubMed  CAS  Google Scholar 

  • Glover DM (1981) The rDNA of Drosophila melanogaster. Cell 26:297–298

    PubMed  CAS  Google Scholar 

  • Glover DM, Hogness DS (1977) A novel arrangement of the 18S and 28S sequences in a repeating unit of Drosophila melanogaster rDNA. Cell 10:167–176

    PubMed  CAS  Google Scholar 

  • Glover DM, White RL, Finnegan DJ, Hogness DS (1975) Characterization of six cloned DNAs from Drosophila melanogaster, including one that contains the genes for rRNA. Cell 5:149–157

    PubMed  CAS  Google Scholar 

  • Graziani F, Gargano S (1976) Ribosomal DNA transcription products during the first steps of magnification in Drosophila melanogaster. J Mol Biol 100:59–71

    PubMed  CAS  Google Scholar 

  • Grewal SS, Li L, Orian A, Eisenman RN, Edgar BA (2005) Myc-dependent regulation of ribosomal RNA synthesis during Drosophila development. Nat Cell Biol 7:295–302

    PubMed  CAS  Google Scholar 

  • Grewal SS, Evans JR, Edgar BA (2007) Drosophila TIF-IA is required for ribosome synthesis and cell growth and is regulated by the TOR pathway. J Cell Biol 179:1105–1113

    PubMed  CAS  Google Scholar 

  • Grimaldi G, Di Nocera PP (1986) Transient expression of Drosophila melanogaster rDNA promoter into cultured Drosophila cells. Nucleic Acids Res 14:6417–6432

    PubMed  CAS  Google Scholar 

  • Grimaldi G, Di Nocera PP (1988) Multiple repeated units in Drosophila melanogaster ribosomal DNA spacer stimulate rRNA precursor transcription. Proc Natl Acad Sci U S A 85:5502–5506

    PubMed  CAS  Google Scholar 

  • Grimaldi G, Fiorentini P, Di Nocera PP (1990) Spacer promoters are orientation-dependent activators of pre-rRNA transcription in Drosophila melanogaster. Mol Cell Biol 10:4667–4677

    PubMed  CAS  Google Scholar 

  • Guerrero PA, Maggert KA (2011) The CCCTC-binding factor (CTCF) of Drosophila contributes to the regulation of the ribosomal DNA and nucleolar stability. PLoS One 6:e16401

    PubMed  CAS  Google Scholar 

  • Hadjiolov AA (1985) The nucleolus and ribosome biogenesis. Cell biology monographs. Springer, Wien

    Google Scholar 

  • Hamkalo BA, Miller OL Jr (1973) Electronmicroscopy of genetic activity. Annu Rev Biochem 42:379–396

    PubMed  CAS  Google Scholar 

  • Hammond MP, Laird CD (1985) Control of DNA replication and spatial distribution of defined DNA sequences in salivary gland cells of Drosophila melanogaster. Chromosoma 91:279–286

    PubMed  CAS  Google Scholar 

  • Han JS (2010) Non-long terminal repeat (non-LTR) retrotransposons: mechanisms, recent developments, and unanswered questions. Mobile DNA 1:15

    PubMed  Google Scholar 

  • Hawley RS, Marcus CH (1989) Recombinational controls of rDNA redundancy in Drosophila. Annu Rev Genet 23:87–120

    PubMed  CAS  Google Scholar 

  • Hawley RS, Tartof KD (1983) The effect of mei-41 on rDNA redundancy in Drosophila melanogaster. Genetics 104:63–80

    PubMed  CAS  Google Scholar 

  • Hawley RS, Tartof KD (1985) A two-stage model for the control of rDNA magnification. Genetics 109:691–700

    PubMed  CAS  Google Scholar 

  • Hawley RS, Marcus CH, Cameron ML, Schwartz RL, Zitron AE (1985) Repair-defect mutations inhibit rDNA magnification in Drosophila and discriminate between meiotic and premeiotic magnification. Proc Natl Acad Sci U S A 82:8095–8099

    PubMed  CAS  Google Scholar 

  • Hayward DC, Glover DM (1989) The promoters and spacers in the rDNAs of the melanogaster species subgroup of Drosophila. Gene 77:271–285

    PubMed  CAS  Google Scholar 

  • He F, DiMario PJ (2011a) Drosophila delta-1-pyrroline-5-carboxylate dehydrogenase (P5CDh) is required for proline breakdown and mitochondrial integrity - establishing a fly model for human type II hyperprolinemia. Mitochondrion 11:397–404

    PubMed  CAS  Google Scholar 

  • He F, DiMario PJ (2011b) Structure and function of Nopp140 and treacle. In: Olson MOJ (ed) The nucleolus: protein reviews, vol 15, Part 2. Springer, New York

    Google Scholar 

  • Heitz E (1931) Die ursache der gesetzmässigen zahl, lage, form und grösse pflanzlicher nukleolen. Planta 12:775–844

    Google Scholar 

  • Heitz E (1934) Über α- und β-heterochromatin sowie konstanz und bau der chromomeren bei Drosophila. Biol Zentralbl 54:588–609

    Google Scholar 

  • Hennig W, Meer B (1971) Reduced polyteny of ribosomal RNA cistrons in giant chromosomes of Drosophila hydei. Nature (New Biol) 233:70–72

    CAS  Google Scholar 

  • Hernandez-Verdun D (2011) Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2:189–194

    PubMed  Google Scholar 

  • Hilliker AJ, Appels R (1982) Pleiotropic effects associated with the deletion of heterochromatin surrounding rDNA on the X chromosome of Drosophila. Chromosoma 86:469–490

    PubMed  CAS  Google Scholar 

  • Hiraoka Y, Agard DA, Sedat JW (1990) Temporal and spatial coordination of chromosome movement, spindle formation, and nuclear envelope breakdown during prometaphase in Drosophila melanogaster embryos. J Cell Biol 111:2815–2828

    PubMed  CAS  Google Scholar 

  • Hohjoh H, Singer MF (1996) Cytoplasmic ribonucleoprotein complexes containing human LINE-1 protein and RNA. EMBO J 115:630–639

    Google Scholar 

  • Hollenberg CP (1976) Proportionate representation of rDNA and Balbiani ring DNA in polytene chromosomes of Chironomus tentans. Chromosoma 57:185–197

    PubMed  CAS  Google Scholar 

  • Ide S, Miyazaki T, Maki H, Kobayashi T (2010) Abundance of ribosomal RNA gene copies maintains genome integrity. Science 327:693–696

    PubMed  CAS  Google Scholar 

  • Jakubczak JL, Xiong Y, Eickbush TH (1990) Type I (R1) and type II (R2) ribosomal DNA insertions of Drosophila melanogaster are retrotransposable elements closely related to those of Bombyx mori. J Mol Biol 212:37–52

    PubMed  CAS  Google Scholar 

  • Jakubczak JL, Burke WD, Eickbush TH (1991) Retrotransposable elements R1 and R2 interrupt the rRNA genes of most insects. Proc Natl Acad Sci U S A 88:3295–3299

    PubMed  CAS  Google Scholar 

  • Jamrich M, Miller OL Jr (1984) The rare transcripts of interrupted genes in Drosophila melanogaster are processed or degraded during synthesis. EMBO J 3:1541–1545

    PubMed  CAS  Google Scholar 

  • John HA, Birnstiel ML, Jones KW (1969) RNA-DNA hybrids at the cytological level. Nature 223:582–587

    PubMed  CAS  Google Scholar 

  • Jolly DJ, Thomas CA (1980) Nuclear RNA transcripts from Drosophila melanogaster ribosomal RNA genes containing introns. Nucleic Acids Res 8:67–84

    PubMed  CAS  Google Scholar 

  • Jordan BR (1974) ‘2S’ RNA, a new ribosomal RNA component in cultured Drosophila cells. FEBS Lett 44:39–42

    PubMed  CAS  Google Scholar 

  • Jordan BR, Glover DM (1977) 5.8S and 2S rDNA is located in the ‘transcribed spacer’ region between the 18S and 26S genes in Drosophila melanogaster. FEBS Lett 78:271–274

    PubMed  CAS  Google Scholar 

  • Karpen GH, Schaefer JE, Laird CD (1988) A Drosophila rRNA gene located in euchromatin is active in transcription and nucleolus formation. Genes Dev 2:1745–1763

    PubMed  CAS  Google Scholar 

  • Kaufmann BP (1933) Interchange between X- and Y-chromosomes in attached X females of Drosophila melanogaster. Proc Natl Acad Sci U S A 19:830–838

    PubMed  CAS  Google Scholar 

  • Kaufmann BP (1934) Somatic mitoses in Drosophila melanogaster. J Morphol 56:125–155

    Google Scholar 

  • Kidd SJ, Glover DM (1980) A DNA segment from D. melanogaster which contains five tandemly repeating units homologous to the major rDNA insertion. Cell 19:103–119

    PubMed  CAS  Google Scholar 

  • Kidd SJ, Glover DM (1981) Drosophila melanogaster ribosomal DNA containing Type II insertions is variably transcribed in different strains and tissues. J Mol Biol 151:645–662

    PubMed  CAS  Google Scholar 

  • Kohorn BD, Rae PMM (1982) Nontranscribed spacer sequences promote in vitro transcription of Drosophila ribosomal DNA. Nucleic Acids Res 10:6879–6886

    PubMed  CAS  Google Scholar 

  • Kohorn BD, Rae PMM (1983) Localization of DNA sequences promoting RNA polymerase I activity in Drosophila. Proc Natl Acad Sci U S A 80:3265–3268

    PubMed  CAS  Google Scholar 

  • Kurzynska-Kokorniak A, Jamburuthugoda VK, Bibillo A, Eickbush TH (2007) DNA-directed DNA polymerase and strand displacement activity of the reverse transcriptase encoded by the R2 retrotransposon. J Mol Biol 374:322–333

    PubMed  CAS  Google Scholar 

  • Labella T, Vicari L, Manzi A, Graziani F (1983) Expression of rDNA insertions during rDNA magnification in D. melanogaster. Mol Gen Genet 190:487–493

    PubMed  CAS  Google Scholar 

  • Lakhotia SC (1974) EM autoradiographic studies on polytene nuclei of Drosophila melanogaster. III. Localization of non-replicating chromatin in the chromocenter heterochromatin. Chromosoma 46:145–159

    PubMed  CAS  Google Scholar 

  • Lo D, Lu H (2010) Nucleostemin: another nucleolar “Twister” of the p53-MDM2 loop. Cell Cycle 9:1–6

    Google Scholar 

  • Long EO, Dawid IB (1979) Expression of ribosomal DNA insertions in Drosophila melanogaster. Cell 18:1185–1196

    PubMed  CAS  Google Scholar 

  • Long EO, Dawid IB (1980a) Alternative pathways in the processing of ribosomal RNA precursor in Drosophila melanogaster. J Mol Biol 138:873–878

    PubMed  CAS  Google Scholar 

  • Long EO, Dawid IB (1980b) Repeated genes in eukaryotes. Annu Rev Biochem 49:727–764

    PubMed  CAS  Google Scholar 

  • Long EO, Rebbert ML, Dawid IB (1981) Structure and expression of ribosomal RNA genes of Drosophila melanogaster interrupted by type-2 insertions. Cold Spring Harb Symp Quant Biol 45:667–672

    PubMed  CAS  Google Scholar 

  • Luan DD, Eickbush TH (1995) RNA template requirements for target DNA-primed reverse transcription by the R2 retrotransposable element. Mol Cell Biol 15:3882–3891

    PubMed  CAS  Google Scholar 

  • Luan DD, Korman MH, Jakubczak JL, Eickbush TH (1993) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72:595–605

    PubMed  CAS  Google Scholar 

  • Mahowald AP (1963a) Ultrastructural differentiations during formation of the blastoderm in the Drosophila melanogaster embryo. Dev Biol 8:186–204

    PubMed  CAS  Google Scholar 

  • Mahowald AP (1963b) Electron microscopy of the formation of the cellular blastoderm in Drosophila melanogaster. Exp Cell Res 32:457–468

    PubMed  CAS  Google Scholar 

  • Mahowald AP, Illmensee K, Turner FR (1976) Interspecific transplantation of polar plasm between Drosophila embryos. J Cell Biol 70:358–373

    PubMed  CAS  Google Scholar 

  • Malik HS, Burke WD, Eickbush TH (1999) The age and evolution of non-LTR retrotransposable elements. Mol Biol Evol 16:793–805

    PubMed  CAS  Google Scholar 

  • Marcus CH, Zitron AE, Wright DA, Hawley RS (1986) Autosomal modifiers of bobbed phenotype are a major component of the rDNA magnification paradox in Drosophila melanogaster. Genetics 113:305–319

    PubMed  CAS  Google Scholar 

  • McCain J, Danzy L, Hamdi A, Dellafosse O, DiMario P (2006) Tracking nucleolar dynamics with GFP-Nopp 140 during Drosophila oogenesis and embryogenesis. Cell Tissue Res 323:105–115

    PubMed  CAS  Google Scholar 

  • McClintock B (1934) The relationship of a particular chromosomal element to the development of the nucleoli in Zea mays. Zeitschr Zellf Mikr Anat 21:294–328

    Google Scholar 

  • McKee BD (1996) The license to pair: identification of meiotic pairing sites in Drosophila. Chromosoma 105:135–141

    PubMed  CAS  Google Scholar 

  • McKee BD (1997) Pairing sites and the role of chromosome pairing in meiosis and spermatogenesis in male Drosophila. Curr Top Dev Biol 37:77–115

    Google Scholar 

  • McKee BD (2004) Homologous pairing and chromosome dynamics in meiosis and mitosis. Biochim Biophys Acta Gene Struct Expr 1677:165–180

    CAS  Google Scholar 

  • McKee BD, Karpen GH (1990) Drosophila ribosomal RNA genes function as an X-Y pairing site during male meiosis. Cell 61:61–72

    PubMed  CAS  Google Scholar 

  • McKee BD, Lindsley DL (1987) Inseparability of X heterochromatic functions responsible for X:Y pairing, meiotic drive and male fertility in Drosophila melanogaster males. Genetics 116:399–407

    PubMed  CAS  Google Scholar 

  • McKee BD, Habera L, Vrana JA (1992) Evidence that intergenic spacer repeats of Drosophila melanogaster rRNA genes function as X-Y pairing sites in male meiosis, and a general model for achiasmatic pairing. Genetics 132:529–544

    PubMed  CAS  Google Scholar 

  • McKnight SL, Miller OL Jr (1976) Ultrastructural patterns of RNA synthesis during early embryogenesis of Drosophila melanogaster. Cell 8:305–319

    PubMed  CAS  Google Scholar 

  • McStay B (2006) Nucleolar dominance: a model for rRNA gene silencing. Genes Dev 20:1207–1214

    PubMed  CAS  Google Scholar 

  • McStay B, Grummt I (2008) The epigenetics of rRNA genes: from molecular to chromosome biology. Annu Rev Cell Dev Biol 24:131–157

    PubMed  CAS  Google Scholar 

  • Meier UT (1996) Comparison of the rat nucleolar protein Nopp 140 with its yeast homolog SRP40. J Biol Chem 271:19376–19384

    PubMed  CAS  Google Scholar 

  • Meier UT, Blobel G (1990) A nuclear localization signal binding protein in the nucleolus. J Cell Biol 111:2235–2245

    PubMed  CAS  Google Scholar 

  • Merrill CJ, Chakravarti D, Habera L, Das S, Eisenhour L, McKee BD (1992) Promoter-containing ribosomal DNA fragments function as X-Y meiotic pairing sites in D. melanogaster males. Dev Genet 13:468–484

    PubMed  CAS  Google Scholar 

  • Miller JR, Hayward DC, Glover DM (1983) Transcription of the ‘non-transcribed’ spacer of Drosophila melanogaster rDNA. Nucleic Acids Res 11:11–19

    PubMed  CAS  Google Scholar 

  • Minchiotti G, Di Nocera PP (1991) Convergent transcription initiates oppositely oriented promoters within the 5′ end regions of Drosophila melanogaster F elements. Mol Cell Biol 11:5171–5180

    PubMed  CAS  Google Scholar 

  • Mizrokhi LJ, Georgieva SG, Ilyin YV (1988) jockey, a mobile Drosophila element similar to mammalian LINEs, is transcribed from the internal promoter by RNA polymerase II. Cell 54:685–691

    PubMed  CAS  Google Scholar 

  • Morgan TH, Bridges CB, Sturtevant AH (1925) The genetics of Drosophila. Bibliographica Genetica 2:1–262

    Google Scholar 

  • Morgan TH, Sturtevant AH, Bridges CB (1927) The constitution of germ material in relation to heredity, vol 26. Carnegie Institution of Washington Year Book, Washington, DC, pp 284–288

    Google Scholar 

  • Mulder MP, van Duijn P, Gloor HJ (1968) The replicative organization of DNA in polytene chromosomes of Drosophila hydei. Genetica 39:385–428

    PubMed  CAS  Google Scholar 

  • Murtif VL, Rae PMM (1985) In vivo transcription of rDNA spacers in Drosophila. Nucleic Acids Res 13:3221–3239

    PubMed  CAS  Google Scholar 

  • Nakamura A, Seydoux G (2008) Less is more: specification of the germline by transcriptional repression. Development 35:3817–3827

    Google Scholar 

  • Ohlsson R, Bartkuhn M, Renkawitz R (2010) CTCF shapes chromatin by multiple mechanisms: the impact of 20 years of CTCF research on understanding the workings of chromatin. Chromosoma 119:351–360

    PubMed  CAS  Google Scholar 

  • Olson MOJ (2004) Sensing cellular stress: another new function for the nucleolus? Sci STKE 224:pe10

    Google Scholar 

  • Pardue ML, Gerbi SA, Eckhardt RA, Gall JG (1970) Cytological localization of DNA complementary to ribosomal RNA in polytene chromosomes of Diptera. Chromosoma 29:268–290

    Google Scholar 

  • Paredes S, Maggert KA (2009a) Expression of I-CreI endonuclease generates deletions within the rDNA of Drosophila. Genetics 181:1661–1671

    PubMed  CAS  Google Scholar 

  • Paredes S, Maggert KA (2009b) Ribosomal DNA contributes to global chromatin regulation. Proc Natl Acad Sci 106:17829–17834

    PubMed  CAS  Google Scholar 

  • Paredes S, Branco AT, Hartl DL, Maggert KA, Lemos B (2011) Ribosomal DNA deletions modulate genome-wide gene expression: “rDNA-sensitive” genes and natural variation. PLoS Genet 7:e1001376

    PubMed  CAS  Google Scholar 

  • Pavlakis GN, Jordan BR, Wurst RM, Vournalis JN (1979) Sequence and secondary structure of Drosophila melanogaster 5.8S and 2S rRNAs and of the processing site between them. Nucleic Acids Res 7:2213–2238

    PubMed  CAS  Google Scholar 

  • Peacock WJ, Appels R, Endow S, Glover D (1981) Chromosomal distribution of the major insert in Drosophila melanogaster 28S rRNA genes. Genet Res 37:209–214

    PubMed  CAS  Google Scholar 

  • Pederson T (1988) The plurifunctional nucleolus. Nucleic Acids Res 26:3871–3876

    Google Scholar 

  • Pellegrini M, Manning J, Davidson N (1977) Sequence arrangement of the rDNA of Drosophila melanogaster. Cell 10:213–224

    PubMed  CAS  Google Scholar 

  • Peng JC, Karpen GH (2007) H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability. Nat Cell Biol 9:25–35

    PubMed  CAS  Google Scholar 

  • Pikaard CS (2000) Nucleolar dominance: uniparental gene silencing on a multi-megabase scale in genetic hybrids. Plant Mol Biol 43:163–177

    PubMed  CAS  Google Scholar 

  • Pikaard C, Pontes O (2007) Heterochromatin: condense or excise. Nat Cell Biol 9:19–20

    PubMed  CAS  Google Scholar 

  • Pikaard CS, McStay B, Schultz MC, Bell SP, Reeder RH (1989) The Xenopus ribosomal gene enhancers bind an essential polymerase I transcription factor, xUBF. Genes Dev 3:1779–1788

    PubMed  CAS  Google Scholar 

  • Plata MP, Kang HJ, Zhang S, Kuruganti S, Hsu S-J, Labrador M (2009) Changes in chromatin structure correlate with transcriptional activity of nucleolar rDNA in polytene chromosomes. Chromosoma 118:303–322

    PubMed  CAS  Google Scholar 

  • Rabinowitz M (1941) Studies on the cytology and early embryology of the egg of Drosophila melanogaster. J Morphol 69:1–49

    Google Scholar 

  • Rae PMM (1970) Chromosomal distribution of rapidly reannealing DNA in Drosophila melanogaster. Proc Natl Acad Sci 67:1018–1025

    PubMed  CAS  Google Scholar 

  • Reeder RH (1984) Enhancers and ribosomal gene spacers. Cell 38:349–351

    PubMed  CAS  Google Scholar 

  • Reeder RH (1985) Mechanisms of nucleolar dominance in animals and plants. J Cell Biol 101:2013–2016

    PubMed  CAS  Google Scholar 

  • Ren X-j, Eisenhour L, Hong C-s, Lee Y, McKee BD (1997) Roles of rDNA spacer and transcription unit-sequences in X-Y meiotic chromosome pairing in Drosophila melanogaster males. Chromosoma 106:29–36

    PubMed  CAS  Google Scholar 

  • Ritossa FM (1968) Unstable redundancy of genes for ribosomal RNA. Proc Natl Acad Sci U S A 60:509–516

    PubMed  CAS  Google Scholar 

  • Ritossa F (1972) Procedure for magnification of lethal deletions of genes for ribosomal RNA. Nature 240:109–111

    CAS  Google Scholar 

  • Ritossa F (1976) The bobbed locus. In: Asburner M, Novitski E (eds) The genetics and biology of Drosophila, vol 1b. Academic, London

    Google Scholar 

  • Ritossa FM, Spiegelman S (1965) Localization of DNA complementary to ribosomal RNA in the nucleolus organizer region of Drosophila melanogaster. Proc Natl Acad Sci U S A 53:737–745

    PubMed  CAS  Google Scholar 

  • Ritossa FM, Atwood KC, Spiegelman S (1966) A molecular explanation of the bobbed mutants of Drosophila as partial deficiencies of “ribosomal” DNA. Genetics 54:819–834

    PubMed  CAS  Google Scholar 

  • Roiha H, Glover DM (1980) Characterization of complete type II insertions in cloned segments of ribosomal DNA from Drosophila melanogaster. J Mol Biol 140:341–355

    PubMed  CAS  Google Scholar 

  • Roiha H, Miller JR, Woods LC, Glover DM (1981) Arrangements and rearrangements of sequences flanking the two types of rDNA insertion in D. melanogaster. Nature 290:749–753

    PubMed  CAS  Google Scholar 

  • Rudkin GT (1969) Non replicating DNA in Drosophila. Genetics (Suppl.) 61:227–238

    Google Scholar 

  • Ruschak AM, Mathews DH, Bibillo A, Spinelli SL, Childs JL, Eickbush TH, Turner DH (2004) Secondary structure models of the 3′ untranslated regions of diverse R2 RNAs. RNA 10:978–987

    PubMed  CAS  Google Scholar 

  • Santoro R, Li J, Grummt I (2002) The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat Genet 32:393–396

    PubMed  CAS  Google Scholar 

  • Saumweber HP, Symmons P, Kabisch R, Will H, Bonhoeffer F (1980) Monoclonal antibodies against chromosomal proteins of Drosophila melanogaster. Chromosoma 80:253–275

    PubMed  CAS  Google Scholar 

  • Seleme MC, Disson O, Robin S, Brun C, Teninges D, Bucheton A (2005) In vivo RNA localization of I factor, a non-LTR retrotransposon, requires a cis-acting signal in ORF2 and ORF1 protein. Nucleic Acids Res 33:776–785

    PubMed  CAS  Google Scholar 

  • Shermoen AW, Kiefer BI (1975) Regulation in rDNA-deficient Drosophila melanogaster. Cell 4:275–280

    PubMed  CAS  Google Scholar 

  • Simeone A, La Volpe A, Boncinelli E (1985) Nucleotide sequence of a complete ribosomal spacer of D. melanogaster. Nucleic Acids Res 13:1089–1101

    PubMed  CAS  Google Scholar 

  • Sonnenblick BP (1950) The early embryology of Drosophila melanogaster. In: Demerec M (ed) Biology of Drosophila. Wiley, New York

    Google Scholar 

  • Spear BB (1974) The genes for ribosomal RNA in diploid and polytene chromosomes of Drosophila melanogaster. Chromosoma 48:159–179

    PubMed  CAS  Google Scholar 

  • Spear BB, Gall JG (1973) Independent control of ribosomal gene replication in polytene chromosomes of Drosophila melanogaster. Proc Natl Acad Sci U S A 70:1359–1363

    PubMed  CAS  Google Scholar 

  • Spofford JB, DeSalle R (1991) Nucleolus organizer-suppressed position-effect variegation in Drosophila melanogaster. Genet Res 57:245–255

    PubMed  CAS  Google Scholar 

  • Stage DE, Eickbush TH (2009) Origin of nascent lineages and the mechanisms used to prime second-strand DNA synthesis in the R1 and R2 retrotransposons of Drosophila. Genome Biol 10:R49, 1–17

    Google Scholar 

  • Stern C (1929) Uber die additive Wirckung multiplier allele. Biol Zbl 49:261–290

    Google Scholar 

  • Swergold GD (1990) Identification, characterization, and cell specificity of a human LINE-1 promoter. Mol Cell Biol 10:6718–6729

    PubMed  CAS  Google Scholar 

  • Tartof KD (1971) Increasing the multiplicity of ribosomal RNA genes in Drosophila melanogaster. Science 171:294–297

    PubMed  CAS  Google Scholar 

  • Tartof KD (1974a) Unequal mitotic sister chromatid exchange and disproportionate replication as mechanisms regulating ribosomal RNA gene redundancy. Cold Spring Harb Symp Quant Biol 38:491–500

    PubMed  CAS  Google Scholar 

  • Tartof KD (1974b) Unequal mitotic sister chromatid exchange as the mechanism of ribosomal RNA gene magnification. Proc Natl Acad Sci U S A 71:1272–1276

    PubMed  CAS  Google Scholar 

  • Tartof KD, Dawid IB (1976) Similarities and differences in the structure of X and Y chromosome rDNA genes of Drosophila. Nature 263:27–30

    PubMed  CAS  Google Scholar 

  • Tautz D, Tautz C, Webb D, Dover GA (1987) Evolutionary divergence of promoters and spacers in the rDNA family of four Drosophila species. Implications for molecular coevolution in multigene families. J Mol Biol 195:525–542

    PubMed  CAS  Google Scholar 

  • Thomas S, McKee BD (2007) Meiotic pairing and disjunction of mini-X chromosomes in Drosophila is mediated by 240-bp rDNA repeats and the homolog conjugation proteins SNM and MNM. Genetics 177:785–799

    PubMed  CAS  Google Scholar 

  • Thomas SE, Soltani-Bejnood M, Roth P, Dorn R, Logsdon JM Jr, McKee BD (2005) Identification of two proteins required for conjunction and regular segregation of achiasmate homologs in Drosophila male meiosis. Cell 123:555–568

    PubMed  CAS  Google Scholar 

  • Tsai J-H, McKee BD (2011) Homologous pairing and the role of pairing centers in meiosis. J Cell Sci 124:1955–1963

    PubMed  CAS  Google Scholar 

  • Vallet SM, Brudnak M, Pelligrini M, Weber HW (1993) In vivo regulation of rRNA transcription occurs rapidly in nondividing and dividing Drosophila cells in response to a phorbol ester and serum. Mol Cell Biol 13:928–933

    Google Scholar 

  • Waggener JM, DiMario PJ (2002) Two splice variants of Nopp 140 in Drosophila melanogaster. Mol Biol Cell 13:362–381

    PubMed  CAS  Google Scholar 

  • Wallace H, Birnstiel ML (1966) Ribosomal cistrons and the nucleolar organizer. Biochim Biophys Acta 114:296–310

    PubMed  CAS  Google Scholar 

  • Wang Z, Lindquist S (1998) Developmentally regulated nuclear transport of transcription factors in Drosophila embryos enable the heat shock response. Development 125:4841–4850

    PubMed  CAS  Google Scholar 

  • Wellauer PK, Dawid IB (1977) The structural organization of ribosomal DNA in Drosophila melanogaster. Cell 10:193–212

    PubMed  CAS  Google Scholar 

  • Wellauer PK, Dawid IB (1978) Ribosomal DNA in Drosophila melanogaster II. Heteroduplex mapping of cloned and uncloned rDNA. J Mol Biol 126:769–782

    PubMed  CAS  Google Scholar 

  • Wellauer PK, Dawid IG, Tartof KD (1978) X and Y chromosomal ribosomal DNA of Drosophila: comparison of spacers and insertions. Cell 14:269–278

    PubMed  CAS  Google Scholar 

  • White RL, Hogness DS (1977) R loop mapping of the 18S and 28S sequences in the long and short repeating units of Drosophila melanogaster rDNA. Cell 10:177–192

    PubMed  CAS  Google Scholar 

  • Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124:471–484

    PubMed  CAS  Google Scholar 

  • Xiong Y, Eickbush TH (1988a) The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons. Mol Cell Biol 8:114–123

    PubMed  CAS  Google Scholar 

  • Xiong Y, Eickbush TH (1988b) Functional expression of a sequence-specific endonuclease encoded by the retrotransposon R2Bm. Cell 55:235–246

    PubMed  CAS  Google Scholar 

  • Yang J, Malik H, Eickbush TH (1999) Identification of the endonuclease domain encoded by R2 and other site-specific, non-long terminal repeat retrotransposable elements. Proc Natl Acad Sci U S A 96:7847–7852

    PubMed  CAS  Google Scholar 

  • Ye J, Eickbush TH (2006) Chromatin structure and transcription of the R1- and R2-inserted rRNA genes of Drosophila melanogaster. Mol Cell Biol 26:8781–8790

    PubMed  CAS  Google Scholar 

  • Zalokar M (1976) Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. Dev Biol 49:425–437

    PubMed  CAS  Google Scholar 

  • Zhou J, Eickbush TH (2009) The pattern of R2 retrotransposon activity in natural populations of Drosophila simulans reflects the dynamic nature of the rDNA locus. PLoS Genet 5:e1000386

    PubMed  Google Scholar 

Download references

Acknowledgements

We thank Tom Eickbush for reading portions of this review and for offering many insights during his visit to LSU in October, 2011. Our work on R2 retrotransposon expression upon loss of Nopp140 as reported here for the first time was supported by the NSF award MCB-0919709.

Author information

Authors and Affiliations

  1. Institute of Biophysics, Academy of Sciences of the Czech Republic, v.v.i., Královopolská 135, Brno, CZ-612 65, Czech Republic

    Patrick DiMario, Allison James & Himanshu Raje

  2. Eva Bártová, Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803, USA

    Patrick DiMario

Authors
  1. Patrick DiMario
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Allison James
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Himanshu Raje
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patrick DiMario .

Editor information

Editors and Affiliations

  1. , Biology, University of Toronto at Mississauga, Mississauga Rd. N. 3359, Mississauga, L5L1C6, Ontario, Canada

    Danton H O'Day

  2. , Biology, University of Toronto at Mississauga, Mississauga Rd. 3359, Mississauga, L5L1C6, Ontario, Canada

    Andrew Catalano

Rights and permissions

Reprints and Permissions

Copyright information

© 2013 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

DiMario, P., James, A., Raje, H. (2013). rDNA and Nucleologenesis in Drosophila . In: O'Day, D., Catalano, A. (eds) Proteins of the Nucleolus. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5818-6_3

Download citation

search

Navigation