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Anatomy and evolution of a DNA replication origin

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Abstract

DNA amplification occurs at the DNA puff II/9A locus in the fungus fly Sciara coprophila. As a foundation to study the molecular mechanism for the initiating events of II/9A DNA re-replication, we have sequenced 14 kb spanning a DNase hypersensitive site (DHS) upstream of the 1 kb amplification origin and through transcription units II/9–1 and II/9–2 downstream of the origin. These elements are annotated as well as the ORC binding site at the origin and the transition point (TP) between continuous and discontinuous DNA syntheses that marks the origin of bidirectional replication at the nucleotide level. A 9 bp motif found at the TP is repeated near the other end of the 1 kb ORI and may identify a putative second TP. The steroid hormone ecdysone induces DNA amplification as well as transcription and puffing at locus II/9A. Within the 14 kb, several matches to the ecdysone response element (EcRE) consensus sequence were identified, including some in the amplification origin region. EcRE O-P is at a central axis of a remarkable symmetry, equidistant to the TPs that are themselves equidistant to EcRE O-1 and EcRE O-2. DNA sequence alterations have occurred throughout the II/9A region in a newly discovered polymorphism (#2). Polymorphism #2 is not specific to developmental stage, sex, or tissue, and it does not impair DNA amplification. The DHS, both 9 bp TP sequences, and EcREs O-1, O-P, and O-2 are conserved between the polymorphism #1 and #2 sequences, suggesting their functional importance and retention during evolutionary selection. Moreover, a 72 bp sequence in the Sciara DHS at DNA puff II/9A is conserved in DNA puff C-3 of Rhynchosciara americana. Comparisons are discussed between the Sciara II/9A amplicon and the chorion locus amplicon on the third chromosome of Drosophila.

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Data Availability

The 14 kb sequence from DNA puff II/9A polymorphism #1 has been submitted to GenBank (NCBI/NIH, Bethesda, MD) with the following accession number: BankIt2352620 Sciara MT582500. The 10 kb sequence from DNA puff II/9A polymorphism #2 has been submitted to GenBank (NCBI/NIH, Bethesda, MD) with the following accession number: BankIt2352636 Sciara MT582501.

Code availability

Not applicable.

References

  • Aggarwal BD, Calvi BR (2004) Chromatin regulates origin activity in Drosophila follicle cells. Nature 430:372–376

    Article  CAS  PubMed  Google Scholar 

  • Antoniewski C, Laval M, Lepesant J-A (1993) Structural features critical to the activity of an ecdysone receptor binding site. Insect Biochem Mol Biol 23:105–114

    Article  CAS  PubMed  Google Scholar 

  • Antoniewski C, Mugat B, Delbac F, Lepesant JA (1996) Direct repeats bind the EcR/USP receptor and mediate ecdysteroid responses in Drosophila melanogaster. Mol Cell Biol 16:2977–2986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Austin RJ, Orr-Weaver TL, Bell SP (1999) Drosophila ORC specifically binds to ACE3, an origin of DNA replication control element. Genes Dev 13:2639–2649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Badenhorst P, Xiao H, Cherbas L, Kwon SY, Voas M, Rebay I, Cherbas P, Wu C (2005) The Drosophila nucleosome remodeling factor NURF is required for ecdysteroid signaling and metamorphosis. Genes Dev 19:2540–2545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beall EL, Manak JR, Zhou S, Bell M, Lipsick JS, Botchan MR (2002) Role for a Drosophila Myb-containing protein complex in site-specific DNA replication. Nature 420:833–837

    Article  CAS  PubMed  Google Scholar 

  • Bell SP, Dutta A (2002) DNA replication in eukaryotic cells. Ann Rev Biochem 71:333–374

    Article  CAS  PubMed  Google Scholar 

  • Bernardi F, Romani P, Tzertzinis G, Gargiulo G, Cavaliere V (2009) EcR-B1 and Usp nuclear hormone receptors regulate expression of the VM32E eggshell gene during Drosophila oogenesis. Dev Biol 328:541–551

    Article  CAS  PubMed  Google Scholar 

  • Bielinsky A-K, Gerbi SA (1998) Discrete start sites for DNA synthesis in the yeast ARSI origin. Science 279:95–98

    Article  CAS  PubMed  Google Scholar 

  • Bielinsky A-K, Gerbi SA (1999) Chromosomal ARSI has a single leading strand start site. Mol Cell 3:477–486

    Article  CAS  PubMed  Google Scholar 

  • Bielinsky A-K, Blitzblau H, Beall EL, Ezrokhi M, Smith HS, Botchan MR, Gerbi SA (2001) Origin recognition complex binding to a metazoan replication origin. Current Biol 11:1427–1431

    Article  CAS  Google Scholar 

  • Bienz-Tadmor B, Smith HS, Gerbi SA (1991) The promoter of DNA puff gene II/9-1 of Sciara coprophila is inducible by ecdysone in late prepupal salivary glands of Drosophila melanogaster. Cell Regulation (Mol Biol Cell) 2:875–888

    Article  CAS  Google Scholar 

  • Blagoderov V, Grimaldi D (2004) Fossil Sciaroidea (Diptera) in Cretaceous ambers, exclusive of Cecidomyiidae, Sciaridae, and Keroplatidae. Am Museum Novit 3433:1–76

    Article  Google Scholar 

  • Breuer ME, Pavan C (1955) Behavior of polytene chromosomes of Rhynchosciara angelae at different stages of larval development. Chromosoma 7:371–386

    Article  Google Scholar 

  • Brewer BJ, Payen C, Di Rienzi SC, Higgins MM, Ong G, Dunham MJ, Raghuraman MK (2015) Origin-dependent inverted-repeat amplification: tests of a model for inverted DNA amplification. PLoS Genet 11:e1005699

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brodu V, Mugat B, Roignant J-Y, Lepesant J-A, Antoniewski C (1999) Dual requirement for the EcR/USP nuclear receptor and the dGATAb factor in an ecdysone response in Drosophila melanogaster. Mol Cell Biol 19:5732–5742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cakouros D, Daish TJ, Mills K, Kumar S (2004) An arginine histone methyltransferase, CARMER, coordinates ecdysone mediated apoptosis in Drosophila cells. J Biol Chem 279:18467–18471

    Article  CAS  PubMed  Google Scholar 

  • Calvi BR, Byrnes BA, Kolpakas AJ (2007) Conservation of epigenetic regulation, ORC binding and developmental timing of DNA replication origins in the genus Drosophila. Genetics 177:1291–1301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carbonell A, Mazo A, Serras F, Corominas M (2013) Ash2 acts as an ecdysone receptor coactivator by stabilizing the histone methyltransferase Trr. Mol Biol Cell 24:361–372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cherbas L, Lee K, Cherbas P (1991) Identification of ecdysone response elements by analysis of the Drosophila Eip28/29 gene. Genes Dev 5:120–131

    Article  CAS  PubMed  Google Scholar 

  • Christianson AM, King DL, Hatzivassiliou E, Casas JE, Hallenbeck PL, Nikodem VM, Mitsialis SA, Kafatos FC (1992) DNA binding and heteromerization of the Drosophila transcription factor chorion factor 1/ultraspiracle. Proc Natl Acad Sci 89:11503–11507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christianson AM, Kafatos FC (1993) Binding affinity of the Drosophila melanogaster CF1/USP protein to the chorion s15 promoter. Biochem Biophys Res Comm 193:1318–1323

    Article  CAS  PubMed  Google Scholar 

  • Claycomb JM, Orr-Weaver TL (2005) Developmental gene amplification: insights into DNA replication and gene expression. Trends Genet 21:149–162

    Article  CAS  PubMed  Google Scholar 

  • Claycomb JM, Benasutti M, Bosco G, Fenger DD, Orr-Weaver TL (2004) Gene amplification as a developmental strategy: isolation of two developmental amplicons in Drosophila. Dev Cell 6:145–155

    Article  CAS  PubMed  Google Scholar 

  • Clever U, Karlson P (1960) Induktion von Puff-Veränderungen in den Speicheldrüsenchromosomen von Chironomus tentans durch Ecdyson. Exp Cell Res 20:623–629

    Article  CAS  PubMed  Google Scholar 

  • Crouse HV (1968) The role of ecdysone on DNA-puff formation and DNA synthesis in the polytene chromosomes in Sciara coprophila. Proc Nat Acad Sci 61:971–978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crouse HV, Keyl H-G (1968) Extra replications in the “DNA puffs” of Sciara coprophila. Chromosoma 25:357–364

    Article  CAS  PubMed  Google Scholar 

  • D’Avino PP, Crispi S, Cherbas L, Cherbas P, Furia M (1995) The moulting hormone ecdysone is able to recognize target elements composed of direct repeats. Mol Cell Endocrinol 113:1–9

    Article  PubMed  Google Scholar 

  • Delidakis C, Kafatos FC (1989) Amplification enhancers and replication origins in the autosomal chorion gene cluster of Drosophila. EMBO J 8:891–901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DePamphilis ML (1999) Replication origins in metazoan chromosomes: fact or fiction? BioEssays 21:5–16

    Article  CAS  PubMed  Google Scholar 

  • DiBartolomeis SM, Gerbi SA (1989) Molecular characterization of DNA puff II/9A genes in Sciara coprophila. J Mol Biol 210:531–540

    Article  CAS  PubMed  Google Scholar 

  • Ficq A, Pavan C (1957) Autoradiography of polytene chromosomes of Rhynchosciara angelae at different stages of larval development. Nature 180:983–984

    Article  CAS  PubMed  Google Scholar 

  • Finn KJ, Li JJ (2013) Single-stranded annealing induced by re-initiation of replication origins provides a novel and efficient mechanism for generating copy number expansion via non-allelic homologous recombination. PLoS Genet 9:e1003192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foulk MS, Liang C, Wu N, Blitzblau HG, Smith H, Alam D, Batra M, Gerbi SA (2006) Ecdysone induces transcription and amplification in Sciara coprophila DNA puff II/9A. Dev Biol 299:151–163

    Article  CAS  PubMed  Google Scholar 

  • Foulk MS, Waggener JM, Johnson JM, Yamamoto Y, Liew GM, Urnov FD, Young Y, Lee G, Smith HS, Gerbi SA (2013) Isolation and characterization of the ecdysone receptor and its heterodimeric partner ultraspiracle through development in Sciara coprophila. Chromosoma 122:103–119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gerbi SA, Liang C, Wu N, Urnov FD, Smith HS, Spitzer JD (1993) Ecdysone regulation of DNA amplification and transcription in DNA puff II/9A of Sciara coprophila. Cold Spring Harbor Symp Quant Biol 58:487–494

    Article  CAS  PubMed  Google Scholar 

  • Gerbi SA, Strezoska Z, Waggener JM (2002) Initiation of DNA replication in multicellular eukaryotes. J Struct Biol 140:17–30

    Article  CAS  PubMed  Google Scholar 

  • Gilbert DM (2001) Making sense of eukaryotic DNA replication origins. Science 294:96–100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glover DM, Zaha A, Stocker AJ, Santelli RV, Pueyo MT, deToledo SM, Lara FJS (1982) Gene amplification in Rhynchosciara salivary gland chromosomes. Proc Nat Acad Sci 79:2947–2951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gopalakrishnan V, Simancek P, Houchens C, Snaith HA, Frattini MG, Sazer S, Kelly TJ (2001) Redundant control of rereplication in fission yeast. Proc Nat Acad Sci 98:13114–13119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green BM, Finn KJ, Li JJ (2010) Loss of DNA replication control is a potent inducer of gene amplification. Science 329:943–946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gauhar Z, Sun LV, Hua S, Mason CE, Fuchs F, Li T-R, Boutros M, White KP (2009) Genomic mapping of binding regions for the ecdysone receptor protein complex. Genome Res 19:1006–1013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hackney JF, Pucci C, Naes E, Dobens L (2007) Ras signaling modulates activity of the ecdysone receptor EcR during cell migration in the Drosophila ovary. Dev Dyn 236:1213–1226

    Article  CAS  PubMed  Google Scholar 

  • Hartl T, Boswell C, Orr-Weaver TL, Bosco G (2007) Developmentally regulated histone modifications in Drosophila follicle cells: initiation of gene amplification is associated with histone H3 and H4 hyperacetylation and H1 phosphorylation. Chromosoma 116:197–214

    Article  CAS  PubMed  Google Scholar 

  • Heck M, Spradling A (1990) Multiple replication origins are used during Drosophila chorion gene amplification. J Cell Biol 110:903–914

    Article  CAS  PubMed  Google Scholar 

  • Hua BL, Orr-Weaver TL (2017) DNA replication control during Drosophila development: insights into the onset of S phase, replication initiation, and fork progression. Genetics 207:29–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiang L, Heichinger C, Watt S, Bahler J, Nurse P (2010) Specific replication origins promote DNA amplification in fission yeast. J Cell Sci 123:3047–3051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JC, Nordman J, Xie F, Kashevsky H, Eng T, Li S, MacAlpine DM, Orr-Weaver TL (2011) Integrative analysis of gene amplification in Drosophila follicle cells: parameters of origin activation and repression. Genes Dev 25:1384–1398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohara Y, Tohdoh N, Jiang XW, Okazaki T (1985) The distribution and properties of RNA primed initiation sites of DNA synthesis at the replication origin of Escherichia coli chromosome. Nucleic Acids Res 13:6847–6866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohzaki H, Asano M (2016) Chromosome and genetic testing using ChIP assay. Front Bioscience (Scholar) 8:298–302

    Article  Google Scholar 

  • Kohzaki H, Asano M, Murakami Y, Mazo A (2020) Epigenetic regulation affects gene amplification in Drosophila development. Front Bioscience (Landmark Ed) 25:632–645

    Article  CAS  Google Scholar 

  • Kreher J, Kovač K, Bouazoune K, Mačinković I, Ernst AL, Engelen E, Pahl R, Finkernagel F, Murawska M, Ullah I, Brehm A (2017) EcR recruits dMi-2 and increases efficiency of dMi-2-mediated remodeling to constrain transcription of hormone-regulated genes. Nat Commun 8:14806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuo AJ, Song J, Cheung P, Ishibe-Murakami S, Yamazoe S, Chen JK, Patel DJ, Gozani O (2012) The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome. Nature 484:115–119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehmann M, Korge G (1995) Ecdysone regulation of the Drosophila Sgs-4 gene is mediated by the synergistic action of ecdysone receptor and SEBP 3. EMBO J 14:716–726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehmann M, Korge G (1996) The fork head product directly specifies the tissue-specific hormone responsiveness of the Drosophila Sgs-4 gene. EMBO J 15:4825–4834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis PW, Beall EL, Fleischer TC, Georlette D, Link AJ, Botchan MR (2004) Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex. Genes Dev 18:2929–2940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang C, Gerbi SA (1994) Analysis of an origin of DNA amplification in Sciara coprophila using a novel three-dimensional gel method. Mol Cell Biol 14:1520–1529

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liang C, Spitzer JD, Smith HS, Gerbi SA (1993) Replication initiates at a confined region during DNA amplification in Sciara DNA puff II/9A. Genes Dev 7:1072–1084

    Article  CAS  PubMed  Google Scholar 

  • Liew GM, Foulk MS, Gerbi SA (2013) The ecdysone receptor (ScEcR-A) binds DNA puffs at the start of DNA amplification in Sciara coprophila. Chromosome Res 21:345–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Zimmer K, Rusch DB, Paranjape N, Podicheti R, Tang H, Calvi BR (2015) DNA sequence templates adjacent nucleosome and ORC sites at gene amplification origins in Drosophila. Nucleic Acids Res 43:8746–8761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu L, Zhang H, Tower J (2001) Functionally distinct, sequence-specific replicator and origin elements are required for Drosophila chorion gene amplification. Genes Dev 15:134–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lunyak VV, Ezrokhi M, Smith HS, Gerbi SA (2002) Developmental changes in the Sciara II/9A initiation zone for DNA replication. Mol Cell Biol 22:8426–8437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mazina MY, Ziganshin RH, Magnitov MD, Golovnin AK, Vorobyeva NE (2020) Proximity-dependent biotin labelling reveals CP190 as an EcR/Usp molecular partner. Sci Rep 10:4793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDonald SI, Beachum AN, Hinnant TD, Blake AJ, Bynum T, Hickman EP, Barnes J, Churchill KL, Roberts TS, Zangwill DE, Ables ET (2019) Novel cis-regulatory regions in ecdysone responsive genes are sufficient to promote gene expression in Drosophila ovarian cells. Gene Expr Patterns 34:119074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menzel J, Tatman P, Black JC (2020) Isolation and analysis of rereplicated DNA by Rerep-Seq. Nucleic Acids Res 48:e58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitsialis SA, Kafatos FC (1985) Regulatory elements controlling chorion gene expression are conserved between flies and moths. Nature 317:453–456

    Article  CAS  PubMed  Google Scholar 

  • Mok EH, Smith HS, DiBartolomeis SM, Kerrebrock AW, Rothschild LJ, Lange TS, Gerbi SA (2000) Maintenance of the DNA puff expanded state is independent of active replication and transcription. Chromosoma 110:186–196

    Article  Google Scholar 

  • Newlon CS, Theis JF (1993) The structure and function of yeast ARS elements. Curr Opin Genet Dev 3:752–758

    Article  CAS  PubMed  Google Scholar 

  • Nguyen VQ, Co C, Li JJ (2001) Cyclin-dependent kinases prevent DNA re-replication through multiple mechanisms. Nature 411:1068–1073

    Article  CAS  PubMed  Google Scholar 

  • Orr-Weaver TL, Johnston CG, Spradling AC (1989) The role of ACE3 in Drosophila chorion gene amplification. EMBO J 8:4153–4162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ozyhar A, Pongs O (1993) Mutational analysis of the interaction between ecdysteroid receptor and its response element. J Steroid Biochem Mol Biol 46(135):145

    Google Scholar 

  • Ozyhar A, Strangrnann-Diekmann M, Kiltz HH, Pongs O (1991) Characterization of a specific ecdysteroid receptor-DNA complex reveals common properties for invertebrate and vertebrate hormone-receptor/DNA interactions. Eur J Biochem 200:329–335

    Article  CAS  Google Scholar 

  • Paçó-Larson ML, deAlmeida JC, Edström J-E, Sauaia H (1992) Cloning of a developmentally amplified gene sequence in the DNA puff C4 of Bradysia hygida (Diptera: Sciaridae) salivary glands. Insect Biochem Mol Biol 22:439–446

    Article  Google Scholar 

  • Penalva LO, Yokosawa J, Stocker AJ, Soares MA, Graessmann M, Orlando TC, Winter CE, Botella LM, Graessmann A, Lara FJ (1997) Molecular characterization of the C-3 DNA puff gene of Rhynchosciara americana. Gene 193:163–172

    Article  CAS  PubMed  Google Scholar 

  • Randell JCW, Bowers JL, Rodriguez HK, Bell SP (2006) Sequential ATP hydrolysis by Cdc6 and ORC directs loading of the Mcm2-7 helicase. Mol Cell 21:29–39

    Article  CAS  PubMed  Google Scholar 

  • Rasch EM (1970) Two-wavelength cytophotometry of Sciara salivary gland chromosomes. In: Wied GL, Bahr GF (eds) Introduction to quantitative cytochemistry, vol 2. Academic Press, New York, pp 335–355

    Google Scholar 

  • Remus D, Beall EL, Botchan MR (2004) DNA topology, not DNA sequence, is a critical determinant for Drosophila ORC-DNA binding. EMBO J 23:897–907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richardson CD, Li JJ (2014) Regulatory mechanisms that prevent re-initiation of DNA replication can be locally modulated at origins by nearby sequence elements. PLoS Genet 10:e1004358

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Riddiford LM, Cherbas P, Truman JW (2000) Ecdysone receptors and their biological actions. Vitam Horm 60:1–73

    Article  CAS  PubMed  Google Scholar 

  • Roschmann F, Morhig W (1995) Die trauermucken des sächsischen bernsteins aus dem untermiozän von Bitterfeld/Deutschland (Diptera, Sciaridae). Deutsche Entomol Zeitschrift 42:17–54

    Article  Google Scholar 

  • Rudkin G, Corlette SL (1957) Disproportionate synthesis of DNA in a polytene chromosome region. Proc Nat Acad Sci 43:964–968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schimke RT, Sherwood SW, Hill AB, Johnston RN (1986) Over-replication and recombination of DNA in higher eukaryotes: potential consequences and biological implications. Proc Nat Acad Sci 83:2157–2161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sedkov Y, Cho E, Petruk S, Cherbas L, Smith ST, Jones RS, Cherbas P, Canaani E, Jaynes JB, Mazo A (2003) Methylation at lysine 4 of histone H3 in ecdysone-dependent development of Drosophila. Nature 426:78–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shea M, King D, Conboy M, Mariani B, Kafatos F (1990) Proteins that bind to chorion cis-regulatory elements: a new C2H2 protein and a C2C2 steroid receptor-like component. Genes Dev 4:1128–1140

    Article  CAS  PubMed  Google Scholar 

  • Shlyueva D, Stelzer C, Gerlach D, Yanez-Cuna JO, Rath M, Boryn LM, Arnold CD, Stark A (2014) Hormone-responsive enhancer-activity maps reveal predictive motifs, indirect repression, and targeting of closed chromatin. Mol Cell 54:180–192

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui K, On KF, Diffley JF (2013) Regulating DNA replication in eukarya. Cold Spring Harb Perspect Biol. 5(9):a012930

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simon CR, Siviero F, Monesi N (2016) Beyond DNA puffs: what can we learn from studying Sciarids? Genesis 54:361–378

    Article  PubMed  Google Scholar 

  • Stark GR, Wahl GM (1984) Gene amplification. Ann Rev. Biochem 53:447–491

    CAS  Google Scholar 

  • Stinchcomb DT, Struhl K, Davis RW (1979) Isolation and characterisation of a yeast chromosomal replicator. Nature 282:39–43

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Smith L, Armento A, Deng WM (2008) Regulation of the endocycle/gene amplification switch by Notch and ecdysone signaling. J Cell Biol 182:885–896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swift HH (1962) Nucleic acids and cell morphology in dipteran salivary glands. In: Allen JM (ed) The molecular control of cellular activity. McGraw-Hill, New York, pp 73–125

    Google Scholar 

  • Swimmer C, Fenerjian MG, Martinez-Cruzado JC, Kafatos KC (1990) Evolution of the autosomal chorion gene cluster in Drosophila III. Comparison of the s18 gene in evolutionarily distant species and interspecific control of chorion gene amplification. J Mol Biol 215:225–235

    Article  CAS  PubMed  Google Scholar 

  • Tardat M, Brustel J, Kirsh O, Lefevbre C, Callanan M, Sardet C, Julien E (2010) The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat Cell Bio 12:1086–1093

    Article  CAS  Google Scholar 

  • Tower J (2004) Developmental gene amplification and origin regulation. Ann Rev Genet 38:273–304

    Article  CAS  PubMed  Google Scholar 

  • Urnov FD, Liang C, Blitzblau HG, Smith HS, Gerbi SA (2002) A DNase I hypersensitive site flanks an origin of replication and amplification in Sciara. Chromosoma 111:291–303

    Article  CAS  PubMed  Google Scholar 

  • Uyehara CM, McKay DJ (2019) Direct and widespread role for the nuclear receptor EcR in mediating the response to ecdysone in Drosophila. Proc Nat Acad Sci 116:9893–9902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vögtli M, Elke C, Imhof MO, Lezzi M (1998) High level transactivation by the ecdysone receptor complex at the core recognition motif. Nucleic Acids Res 26:2407–2414

    Article  PubMed  PubMed Central  Google Scholar 

  • Yokosawa J, Soares MA, Dijkwel PA, Stocker AJ, Hamlin JL, Lara FJ (1999) DNA replication during amplification of the C3 puff of Rhynchosciara americana initiates at multiple sites in a 6 kb region. Chromosoma 108:291–301

    Article  CAS  PubMed  Google Scholar 

  • Wang S-F, Miura K, Miksicek RJ, Segraves WA, Raikhel as, (1998) DNA binding and transactivation characteristics of the mosquito Ecdysone Receptor-Ultraspiracle complex. J Biol Chem 273:27531–27540

    Article  CAS  PubMed  Google Scholar 

  • Wiegmann BM, Trautwein MD, Winkler IS, Barr NB, Kim JW, Lambkin C, Bertone MA, Cassel BK, Bayless KM, Heimberg AM, Wheeler BM, Peterson KJ, Pape T, Sinclair BJ, Skevington JH, Blagoderov V, Caravas J, Kutty SN, Schmidt-Ott U, Kampmeier GE, Thompson FC, Grimaldi DA, Beckenbach AT, Courtney GW, Friedrich M, Meier R, Yeates DF (2011) Episodic radiations in the fly tree of life. Proc Nat Acad Sci 108:5690–5695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu N, Liang C, DiBartolomeis SM, Smith HS, Gerbi SA (1993) Developmental progression of DNA puffs in Sciara coprophila: amplification and transcription. Dev Biol 160:73–84

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Miiko Sokka for his help with some of the statistical analyses. We thank Jacob Bliss for maintenance of the Sciara fly stocks.

Funding

We received funding from NIH-GM121455 (currently) and NIH-GM35929 (previously).

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Author notes

  1. Eric A. Gustafson

    Present address: Zipher Medical Affairs Co., 380 Wareham Street, Marion, MA, 02738, USA

  2. Michael S. Foulk

    Present address: Department of Biology, Mercyhurst University, 501 East 38th Street, Erie, PA, 16546, USA

Authors and Affiliations

  1. Department of Molecular Biology, Cell Biology and Biochemistry, Brown University Division of Biology and Medicine, Box G – Sidney Frank Life Sciences Building room 260, Providence, RI, 02912, USA

    Yutaka Yamamoto, Eric A. Gustafson, Michael S. Foulk, Heidi S. Smith & Susan A. Gerbi

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Contributions

YY sequenced and analyzed 14 kb of the Sciara II/9A origin region, prepared the figures, and compiled the data and methods. EAG analyzed polymorphism #2 by PCR and sequencing 4 kb from the Sciara II/9A origin region; he also helped to prepare figures of the polymorphism results. MSF did the experiment with the Sciara 91S stock; he also did some initial work for Supplemental Table 1. HSS maintained the Sciara fly stocks and helped to select for the HoLo strain which has just polymorphism #1. SAG oversaw the project and wrote this paper.

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Correspondence to Susan A. Gerbi.

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Yamamoto, Y., Gustafson, E.A., Foulk, M.S. et al. Anatomy and evolution of a DNA replication origin. Chromosoma 130, 199–214 (2021). https://doi.org/10.1007/s00412-021-00756-x

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  • DOI: https://doi.org/10.1007/s00412-021-00756-x

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