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Anciently duplicated Broad Complex exons have distinct temporal functions during tissue morphogenesis

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Abstract

Broad Complex (BRC) is an essential ecdysone-pathway gene required for entry into and progression through metamorphosis in Drosophila melanogaster. Mutations of three BRC complementation groups cause numerous phenotypes, including a common suite of morphogenesis defects involving central nervous system (CNS), adult salivary glands (aSG), and male genitalia. These defects are phenocopied by the juvenile hormone mimic methoprene. Four BRC isoforms are produced by alternative splicing of a protein-binding BTB/POZ-encoding exon (BTB BRC ) to one of four tandemly duplicated, DNA-binding zinc-finger-encoding exons (Z1 BRC , Z2 BRC , Z3 BRC , Z4 BRC ). Highly conserved orthologs of BTB BRC and all four Z BRC were found among published cDNA sequences or genome databases from Diptera, Lepidoptera, Hymenoptera, and Coleoptera, indicating that BRC arose and underwent internal exon duplication before the split of holometabolous orders. Tramtrack subfamily members, abrupt, tramtrack, fruitless, longitudinals lacking (lola), and CG31666 were characterized throughout Holometabola and used to root phylogenetic analyses of Z BRC exons, which revealed that the Z BRC clade includes Z abrupt . All four Z BRC domains, including Z4 BRC , which has no known essential function, are evolving in a manner consistent with selective constraint. We used transgenic rescue to explore how different BRC isoforms contribute to shared tissue-morphogenesis functions. As predicted from earlier studies, the common CNS and aSG phenotypes were rescued by BRC-Z1 in rbp mutants, BRC-Z2 in br mutants, and BRC-Z3 in 2Bc mutants. However, the isoforms are required at two different developmental stages, with BRC-Z2 and -Z3 required earlier than BRC-Z1. The sequential action of BRC isoforms indicates subfunctionalization of duplicated Z BRC exons even when they contribute to common developmental processes.

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References

  • Aguinaldo AM, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493

    Article  PubMed  CAS  Google Scholar 

  • Albagli O, Dhordain P, Deweindt C, Lecocq G, Leprince D (1995) The BTB/POZ domain: a new protein–protein interaction motif common to DNA- and actin-binding proteins. Cell Growth Differ 6:1193–1198

    PubMed  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Andres AJ, Thummel CS (1994) Methods for quantitative analysis of transcription in larvae and prepupae. In: Goldstein LSB, Fyrberg EA (eds) Drosophila melanogaster: practical uses in cell and molecular biology. Methods in cell biology, vol. 44. Academic Press, San Diego, pp 565–573

    Google Scholar 

  • Ashburner M (1970) Effects of juvenile hormone on adult differentiation of Drosophila melanogaster. Nature 227:187–189

    Article  PubMed  CAS  Google Scholar 

  • Bainbridge SP, Bownes M (1981) Staging the metamorphosis of Drosophila melanogaster. J Embryol Exp Morphol 66:57–80

    PubMed  CAS  Google Scholar 

  • Bardwell VJ, Treisman R (1994) The POZ domain: a conserved protein–protein interaction motif. Genes Dev 8:1664–1677

    Article  PubMed  CAS  Google Scholar 

  • Bayer CA, Holley B, Fristrom JW (1996) A switch in Broad-Complex zinc-finger isoform expression is regulated posttranscriptionally during the metamorphosis of Drosophila imaginal discs. Dev Biol 177:1–14

    Article  PubMed  CAS  Google Scholar 

  • Bayer CA, von Kalm L, Fristrom JW (1997) Relationships between protein isoforms and genetic functions demonstrate functional redundancy at the Broad-Complex during Drosophila metamorphosis. Dev Biol 187:267–282

    Article  PubMed  CAS  Google Scholar 

  • Bayer C, Zhou XF, Zhou BH, Riddiford LM, von Kalm L (2003) Evolution of the Drosophila broad locus: the Manduca sexta broad Z4 isoform has biological activity in Drosophila. Dev Genes Evol 213:471–476

    Article  PubMed  Google Scholar 

  • Belyaeva ES, Aizenzon MG, Semeshin VF, Kiss I, Koczka K, Baritcheva EM, Gorelova TD, Zhimulev IF (1980) Cytogenetic analysis of the 2B3-4-2B11 region of the X-chromosome of Drosophila melanogaster. I. Cytology of the region and mutant complementation groups. Chromosoma 81:281–306

    Article  PubMed  CAS  Google Scholar 

  • Brennan CA, Li TR, Bender M, Hsiung F, Moses K (2001) Broad-complex, but not Ecdysone receptor, is required for progression of the morphogenetic furrow in the Drosophila eye. Development 128:1–11

    PubMed  CAS  Google Scholar 

  • Bryant PJ, Sang JH (1968) Drosophila: lethal derangements of metamorphosis and modifications of gene expression caused by juvenile hormone mimics. Nature 220:393–394

    Article  PubMed  CAS  Google Scholar 

  • Chang ES, O’Connor JD (1978) In vitro secretion and hydroxylation of alpha-ecdysone as a function of crustacean molt cycle. Gen Comp Endocrinol 36:151–160

    Article  PubMed  CAS  Google Scholar 

  • Chen L, Zhu J, Sun G, Raikhel AS (2004) The early gene Broad is involved in the ecdysteroid hierarchy governing vitellogenesis of the mosquito Aedes aegypti. J Mol Endocrinol 33:743–761

    Article  PubMed  CAS  Google Scholar 

  • Chung ACK, Durica DS, Hopkins PM (1998) Tissue-specific patterns and steady-state concentrations of ecdysteroid receptor and retinoid-X-receptor mRNA during the molt cycle of the fiddler crab, Uca pugilator. Gen Comp Endocrinol 109:375–389

    Article  PubMed  CAS  Google Scholar 

  • Clark AG (1994) Invasion and maintenance of a gene duplication. Proc Natl Acad Sci USA 91:2950–2954

    Article  PubMed  CAS  Google Scholar 

  • Colbourne JK, Singan VR, Gilbert DG (2005) wFleaBase: the Daphnia genome database. BMC Bioinformatics 6:45

    Article  PubMed  CAS  Google Scholar 

  • Consoulas C, Levine RB, Restifo LL (2005) The steroid hormone-regulated gene Broad Complex is required for dendritic growth of motoneurons during metamorphosis of Drosophila. J Comp Neurol 485:321–337

    Article  PubMed  CAS  Google Scholar 

  • Crossgrove K, Bayer CA, Fristrom JW, Guild GM (1996) The Drosophila Broad-Complex early gene directly regulates late gene transcription during the ecdysone-induced puffing cascade. Dev Biol 180:745–758

    Article  PubMed  CAS  Google Scholar 

  • Davis CA, Holmyard DP, Millen KJ, Joyner AL (1991) Examining pattern formation in mouse, chicken and frog embryos with an En-specific antiserum. Development 111:287–298

    PubMed  CAS  Google Scholar 

  • DiBello PR, Withers DA, Bayer CA, Fristrom JW, Guild GM (1991) The Drosophila Broad-Complex encodes a family of related, zinc finger-containing proteins. Genetics 129:385–397

    PubMed  CAS  Google Scholar 

  • Elgin SR, Miller DW (1978) Mass rearing of flies and mass production and harvesting of eggs. In: Ashburner M, Wright TRF (eds) The Genetics and Biology of Drosophila, vol. 2a. Academic Press, New York, pp 112–121

    Google Scholar 

  • Emery IF, Bedian V, Guild GM (1994) Differential expression of Broad-Complex transcription factors may forecast tissue-specific developmental fates during Drosophila metamorphosis. Development 120:3275–3287

    PubMed  CAS  Google Scholar 

  • Erezyilmaz DF, Riddiford LM, Truman JW (2006) The pupal specifier broad directs progressive morphogenesis in a direct-developing insect. Proc Natl Acad Sci USA 103:6925–6930

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27:401–410

    Article  Google Scholar 

  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545

    PubMed  CAS  Google Scholar 

  • Force A, Cresko WA, Pickett FB, Proulx SR, Amemiya C, Lynch M (2005) The origin of subfunctions and modular gene regulation. Genetics 170:433–446

    Article  PubMed  CAS  Google Scholar 

  • Gailey DA, Billeter JC, Liu JH, Bauzon F, Allendorfer JB, Goodwin SF (2006) Functional conservation of the fruitless male sex-determination gene across 250 Myr of insect evolution. Mol Biol Evol 23:633–643

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Machado E, Pempera M, Dennebouy N, Oliva-Suarez M, Mounolou JC, Monnerot M (1999) Mitochondrial genes collectively suggest the paraphyly of Crustacea with respect to Insecta. J Mol Evol 49:142–149

    Article  PubMed  CAS  Google Scholar 

  • Giniger E, Tietje K, Jan LY, Jan YN (1994) lola encodes a putative transcription factor required for axon growth and guidance in Drosophila. Development 120:1385–1398

    PubMed  CAS  Google Scholar 

  • Goeke S, Greene EA, Grant PK, Gates MA, Crowner D, Aigaki T, Giniger E (2003) Alternative splicing of lola generates 19 transcription factors controlling axon guidance in Drosophila. Nat Neurosci 6:917–924

    Article  PubMed  CAS  Google Scholar 

  • Gonzy G, Pokholkova GV, Peronnet F, Mugat B, Demakova OV, Kotlikova IV, Lepesant JA, Zhimulev IF (2002) Isolation and characterization of novel mutations of the Broad-Complex, a key regulatory gene of ecdysone induction in Drosophila melanogaster. Insect Biochem Mol Biol 32:121–132

    Article  PubMed  CAS  Google Scholar 

  • Harrison SD, Travers AA (1990) The tramtrack gene encodes a Drosophila finger protein that interacts with the ftz transcriptional regulatory region and shows a novel embryonic expression pattern. EMBO J 9:207–216

    PubMed  CAS  Google Scholar 

  • Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JM, Wides R, Salzberg SL, Loftus B, Yandell M, Majoros WH, Rusch DB, Lai Z, Kraft CL, Abril JF, Anthouard V, Arensburger P, Atkinson PW, Baden H, de Berardinis V, Baldwin D, Benes V, Biedler J, Blass C, Bolanos R, Boscus D, Barnstead M, Cai S, Center A, Chaturverdi K, Christophides GK, Chrystal MA, Clamp M, Cravchik A, Curwen V, Dana A, Delcher A, Dew I, Evans CA, Flanigan M, Grundschober-Freimoser A, Friedli L, Gu Z, Guan P, Guigo R, Hillenmeyer ME, Hladun SL, Hogan JR, Hong YS, Hoover J, Jaillon O, Ke Z, Kodira C, Kokoza E, Koutsos A, Letunic I, Levitsky A, Liang Y, Lin JJ, Lobo NF, Lopez JR, Malek JA, McIntosh TC, Meister S, Miller J, Mobarry C, Mongin E, Murphy SD, O’Brochta DA, Pfannkoch C, Qi R, Regier MA, Remington K, Shao H, Sharakhova MV, Sitter CD, Shetty J, Smith TJ, Strong R, Sun J, Thomasova D, Ton LQ, Topalis P, Tu Z, Unger MF, Walenz B, Wang A, Wang J, Wang M, Wang X, Woodford KJ, Wortman JR, Wu M, Yao A, Zdobnov EM, Zhang H, Zhao Q et al (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129–149

    Article  PubMed  CAS  Google Scholar 

  • Huang R-Y, Orr WC (1992) Broad-Complex function during oogenesis in Drosophila melanogaster. Dev Genet 13:277–288

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP (1997) Is the Felsenstein zone a fly trap? Syst Biol 46:69–74

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Huet F, Ruiz C, Richards G (1993) Puffs and PCR: the in vivo dynamics of early gene expression during ecdysone responses in Drosophila. Development 118:613–627

    PubMed  CAS  Google Scholar 

  • Hwang UW, Friedrich M, Tautz D, Park CJ, Kim W (2001) Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413:154–157

    Article  PubMed  CAS  Google Scholar 

  • Ijiro T, Urakawa H, Yasukochi Y, Takeda M, Fujiwara Y (2004) cDNA cloning, gene structure, and expression of Broad-Complex (BR-C) genes in the silkworm, Bombyx mori. Insect Biochem Mol Biol 34:963–969

    Article  PubMed  CAS  Google Scholar 

  • Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, Yamamoto D (1996) Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc Natl Acad Sci USA 93:9687–9692

    Article  PubMed  CAS  Google Scholar 

  • Joyner AL, Martin GR (1987) En-1 and En-2, two mouse genes with sequence homology to the Drosophila engrailed gene: expression during embryogenesis. Genes Dev 1:29–38

    Article  PubMed  CAS  Google Scholar 

  • Karim FD, Guild GM, Thummel CS (1993) The Drosophila Broad-Complex plays a key role in controlling ecdysone-regulated gene expression at the onset of metamorphosis. Development 118:977–988

    PubMed  CAS  Google Scholar 

  • Kim HW, Lee SG, Mykles DL (2005) Ecdysteroid-responsive genes, RXR and E75, in the tropical land crab, Gecarcinus lateralis: differential tissue expression of multiple RXR isoforms generated at three alternative splicing sites in the hinge and ligand-binding domains. Mol Cell Endocrinol 242:80–95

    Article  PubMed  CAS  Google Scholar 

  • Kiss I, Bencze G, Fekete E, Fodor A, Gausz J, Maroy P, Szabad J, Szidonya J (1976) Isolation and characterization of X-linked lethal mutants affecting differentiation of the imaginal discs in Drosophila melanogaster. Theor Appl Genet 48:217–226

    Google Scholar 

  • Kiss I, Beaton AH, Tardiff J, Fristrom D, Fristrom JW (1988) Interactions and developmental effects of mutations in the Broad-Complex of Drosophila melanogaster. Genetics 118:247–259

    PubMed  CAS  Google Scholar 

  • Kondrashov FA, Koonin EV (2001) Origin of alternative splicing by tandem exon duplication. Hum Mol Genet 10:2661–2669

    Article  PubMed  CAS  Google Scholar 

  • Kopelman NM, Lancet D, Yanai I (2005) Alternative splicing and gene duplication are inversely correlated evolutionary mechanisms. Nat Genet 37:588–589

    Article  PubMed  CAS  Google Scholar 

  • Krebs RA, Feder ME (1997) Tissue-specific variation in Hsp70 expression and thermal damage in Drosophila melanogaster larvae. J Exp Biol 200:2007–2015

    PubMed  CAS  Google Scholar 

  • Kristensen NP (1999) Phylogeny of endopterygote insects, the most successful lineage of living organisms. Eur J Entomol 96:237–253

    Google Scholar 

  • Letunic I, Copley RR, Bork P (2002) Common exon duplication in animals and its role in alternative splicing. Hum Mol Genet 11:1561–1567

    Article  PubMed  CAS  Google Scholar 

  • Liu E, Restifo LL (1998) Identification of a Broad Complex-regulated enhancer in the developing visual system of Drosophila. J Neurobiol 34:253–270

    Article  PubMed  CAS  Google Scholar 

  • Maddison WP, Maddison DR (1992) MacClade: analysis of phylogeny and character evolution, version 3.0. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Madhavan K (1973) Morphogenetic effects of juvenile hormone and juvenile hormone mimics on adult development of Drosophila. J Insect Physiol 19:441–453

    Article  PubMed  CAS  Google Scholar 

  • Maroni G, Stamey SC (1983) Use of blue food to select synchronous, late third instar larvae. Drosoph Inf Serv 59:142–143

    Google Scholar 

  • Mu XY, LeBlanc GA (2004) Cross communication between signaling pathways: juvenoid hormones modulate ecdysteroid activity in a crustacean. J Exp Zool Part A Comp Exp Biol 301A:793–801

    Article  CAS  Google Scholar 

  • Mugat B, Brodu V, Kejzlarova-Lepesant J, Antoniewski C, Bayer CA, Fristrom JW, Lepesant JA (2000) Dynamic expression of Broad-Complex isoforms mediates temporal control of an ecdysteroid target gene at the onset of Drosophila metamorphosis. Dev Biol 227:104–117

    Article  PubMed  CAS  Google Scholar 

  • Nardi F, Spinsanti G, Boore JL, Carapelli A, Dallai R, Frati F (2003) Hexapod origins: monophyletic or paraphyletic? Science 299:1887–1889

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426

    PubMed  CAS  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, NY

    Google Scholar 

  • Nishita Y, Takiya S (2004) Structure and expression of the gene encoding a Broad-Complex homolog in the silkworm, Bombyx mori. Gene 339:161–172

    Article  PubMed  CAS  Google Scholar 

  • Ohsako T, Horiuchi T, Matsuo T, Komaya S, Aigaki T (2003) Drosophila lola encodes a family of BTB-transcription regulators with highly variable C-terminal domains containing zinc finger motifs. Gene 311:59–69

    Article  PubMed  CAS  Google Scholar 

  • O’Keefe S, Schouls M, Hodgetts R (1995) Epidermal cell-specific quantitation of dopa decarboxylase mRNA in Drosophila by competitive RT-PCR: an effect of Broad-Complex mutants. Dev Genet 16:77–84

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808

    Article  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Syst Biol 50:580–601

    Article  Google Scholar 

  • Postlethwait JH (1974) Juvenile hormone and the adult development of Drosophila. Biol Bull 147:119–135

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2005) R: a language and environment for statistical computing. Vienna, Austria

    Google Scholar 

  • Read D, Manley JL (1992) Alternatively spliced transcripts of the Drosophila tramtrack gene encode zinc finger proteins with distinct DNA binding specificities. EMBO J 11:1035–1044

    PubMed  CAS  Google Scholar 

  • Regier JC, Shultz JW, Kambic RE (2005) Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proc Biol Sci 272:395–401

    Article  PubMed  Google Scholar 

  • Renault N, King-Jones K, Lehmann M (2001) Downregulation of the tissue-specific transcription factor Fork head by Broad-Complex mediates a stage-specific hormone response. Development 128:3729–3737

    PubMed  CAS  Google Scholar 

  • Restifo LL, Hauglum W (1998) Parallel molecular genetic pathways operate during CNS metamorphosis in Drosophila. Mol Cell Neurosci 11:134–148

    Article  PubMed  CAS  Google Scholar 

  • Restifo LL, Merrill VKL (1994) Two Drosophila regulatory genes, Deformed and the Broad-Complex, share common functions in development of adult CNS, head, and salivary glands. Dev Biol 162:465–485

    Article  PubMed  CAS  Google Scholar 

  • Restifo LL, White K (1991) Mutations in a steroid hormone-regulated gene disrupt the metamorphosis of the central nervous system in Drosophila. Dev Biol 148:174–194

    Article  PubMed  CAS  Google Scholar 

  • Restifo LL, White K (1992) Mutations in a steroid hormone-regulated gene disrupt the metamorphosis of internal tissues in Drosophila: salivary glands, muscle, and gut. Roux’s Arch Dev Biol 201:221–234

    Article  CAS  Google Scholar 

  • Restifo LL, Wilson TG (1998) A juvenile hormone agonist reveals distinct developmental pathways mediated by ecdysone-inducible Broad Complex transcription factors. Dev Genet 22:141–159

    Article  PubMed  CAS  Google Scholar 

  • Restifo LL, Estes PS, DelloRusso C (1995) Genetics of ecdysteroid-regulated central nervous system metamorphosis in Drosophila. Eur J Entomol 92:169–187

    CAS  Google Scholar 

  • Reza AM, Kanamori Y, Shinoda T, Shimura S, Mita K, Nakahara Y, Kiuchi M, Kamimura M (2004) Hormonal control of a metamorphosis-specific transcriptional factor Broad-Complex in silkworm. Comp Biochem Physiol B Biochem Mol Biol 139:753–761

    Article  PubMed  CAS  Google Scholar 

  • Richards S, Liu Y, Bettencourt BR, Hradecky P, Letovsky S, Nielsen R, Thornton K, Hubisz MJ, Chen R, Meisel RP, Couronne O, Hua S, Smith MA, Zhang P, Liu J, Bussemaker HJ, van Batenburg MF, Howells SL, Scherer SE, Sodergren E, Matthews BB, Crosby MA, Schroeder AJ, Ortiz-Barrientos D, Rives CM, Metzker ML, Muzny DM, Scott G, Steffen D, Wheeler DA, Worley KC, Havlak P, Durbin KJ, Egan A, Gill R, Hume J, Morgan MB, Miner G, Hamilton C, Huang Y, Waldron L, Verduzco D, Clerc-Blankenburg KP, Dubchak I, Noor MA, Anderson W, White KP, Clark AG, Schaeffer SW, Gelbart W, Weinstock GM, Gibbs RA (2005) Comparative genome sequencing of Drosophila pseudoobscura: chromosomal, gene, and cis-element evolution. Genome Res 15:1–18

    Article  PubMed  CAS  Google Scholar 

  • Riddiford LM, Ashburner M (1991) Effects of juvenile hormone mimics on larval development and metamorphosis of Drosophila melanogaster. Gen Comp Endocrinol 82:172–183

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, Hall JC, Taylor BJ, Wasserman SA (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87:1079–1089

    Article  PubMed  CAS  Google Scholar 

  • Sanderson MJ, Kim J (2000) Parametric phylogenetics? Syst Biol 49:817–829

    Article  PubMed  CAS  Google Scholar 

  • Sandstrom DJ, Bayer CA, Fristrom JW, Restifo LL (1997) Broad-Complex transcription factors regulate thoracic muscle attachment in Drosophila. Dev Biol 181:168–185

    Article  PubMed  CAS  Google Scholar 

  • Sehnal F, Zdárek J (1976) Action of juvenoids on the metamorphosis of cyclorrhaphous Diptera. J Insect Physiol 22:673–682

    Article  CAS  Google Scholar 

  • Stewart M, Murphy C, Fristrom JW (1972) The recovery and preliminary characterization of X chromosome mutants affecting imaginal discs of Drosophila melanogaster. Dev Biol 27:71–83

    Article  PubMed  CAS  Google Scholar 

  • Stogios PJ, Downs GS, Jauhal JJS, Nandra SK, Prive GG (2005) Sequence and structural analysis of BTB domain proteins. Genome Biol 6:R82

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (1998) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  • Tavare S (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. In: Miura RM (ed) Some mathematical questions in biology-DNA sequence analysis. Amer Math Soc, Providence, RI, pp 57–86

    Google Scholar 

  • Thain D, Tannenbaum T, Livny M (2005) Distributed computing in practice: the Condor experience. Concurrency and Computation: Practice and Experience 17:323–356

    Article  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Towle DW, Smith CM (2006) Gene discovery in Carcinus maenas and Homarus americanus via expressed sequence tags. Integr Comp Biol 46:912–918

    Article  CAS  Google Scholar 

  • Uhlirova M, Foy BD, Beaty BJ, Olson KE, Riddiford LM, Jindra M (2003) Use of Sindbis virus-mediated RNA interference to demonstrate a conserved role of Broad-Complex in insect metamorphosis. Proc Natl Acad Sci USA 100:15607–15612

    Article  PubMed  CAS  Google Scholar 

  • Wagner A (1999) Redundant gene functions and natural selection. J Evol Biol 12:1–16

    Article  Google Scholar 

  • Whitfield CW, Band MR, Bonaldo MF, Kumar CG, Liu L, Pardinas JR, Robertson HM, Soares MB, Robinson GE (2002) Annotated expressed sequence tags and cDNA microarrays for studies of brain and behavior in the honey bee. Genome Res 12:555–566

    Article  PubMed  Google Scholar 

  • Wilson TG, Fabian J (1986) A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Dev Biol 118:190–201

    Article  PubMed  CAS  Google Scholar 

  • Wilson K, Cahill V, Ballment E, Benzie J (2000) The complete sequence of the mitochondrial genome of the crustacean Penaeus monodon: are malacostracan crustaceans more closely related to insects than to branchiopods? Mol Biol Evol 17:863–874

    PubMed  CAS  Google Scholar 

  • Wilson TG, Yerushalmi Y, Donnell DM, Restifo LL (2006) Interaction between hormonal signaling pathways in Drosophila melanogaster as revealed by genetic interaction between Methoprene-tolerant and Broad-Complex. Genetics 172:253–264

    Article  PubMed  CAS  Google Scholar 

  • Xia Q, Zhou Z, Lu C, Cheng D, Dai F, Li B, Zhao P, Zha X, Cheng T, Chai C, Pan G, Xu J, Liu C, Lin Y, Qian J, Hou Y, Wu Z, Li G, Pan M, Li C, Shen Y, Lan X, Yuan L, Li T, Xu H, Yang G, Wan Y, Zhu Y, Yu M, Shen W, Wu D, Xiang Z, Yu J, Wang J, Li R, Shi J, Li H, Li G, Su J, Wang X, Li G, Zhang Z, Wu Q, Li J, Zhang Q, Wei N, Xu J, Sun H, Dong L, Liu D, Zhao S, Zhao X, Meng Q, Lan F, Huang X, Li Y, Fang L, Li C, Li D, Sun Y, Zhang Z, Yang Z, Huang Y, Xi Y, Qi Q, He D, Huang H, Zhang X, Wang Z, Li W, Cao Y, Yu Y, Yu H, Li J, Ye J, Chen H, Zhou Y, Liu B, Wang J, Ye J, Ji H, Li S, Ni P, Zhang J, Zhang Y, Zheng H, Mao B, Wang W, Ye C, Li S, Wang J, Wong GK, Yang H (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306:1937–1940

    Article  PubMed  Google Scholar 

  • Yang ZH (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556

    PubMed  CAS  Google Scholar 

  • Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298

    Article  Google Scholar 

  • Zhou X, Riddiford LM (2002) Broad specifies pupal development and mediates the “status quo” action of juvenile hormone on the pupal-adult transformation in Drosophila and Manduca. Development 129:2259–2269

    PubMed  CAS  Google Scholar 

  • Zhou B, Hiruma K, Shinoda T, Riddiford LM (1998) Juvenile hormone prevents ecdysteroid-induced expression of Broad Complex RNAs in the epidermis of the tobacco hornworm, Manduca sexta. Dev Biol 203:233–244

    Article  PubMed  CAS  Google Scholar 

  • Zhu S, Lin S, Kao CF, Awasaki T, Chiang AS, Lee T (2006) Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell 127:409–422

    Article  PubMed  CAS  Google Scholar 

  • Zollman S, Godt D, Privé GG, Couderc J-L, Laski FA (1994) The BTB domain, found primarily in zinc-finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. Proc Natl Acad Sci USA 91:10717–10721

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank C. Michel for making fly food, C. Hedgcock for help with computer graphics, L. Tank and M. Kinney for assistance with histology, T. Yuhas and J. Bailey for network and computer support, and S. Miller (ARL Biotechnology Computing Facility) for help using the University of Arizona’s grid system to run the phylogenetic analysis software. We are grateful to colleagues who provided valuable advice on phylogenetic analysis methods (D. Maddison, C. Schmidt, M. Cordes, L. Nagy, and an anonymous reviewer) and statistics (B. Walsh). This work was funded by NIH (HD38363 to LLR); RFS was partially supported by an NSF IGERT training grant (DGE 0114420).

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  1. Rebecca F. Spokony

    Present address: Department of Human Genetics, The University of Chicago, 920 E 58th St, Chicago, IL, 60637, USA

Authors and Affiliations

  1. Graduate Interdisciplinary Program in Insect Science, University of Arizona, Tucson, AZ, 85721-0108, USA

    Rebecca F. Spokony & Linda L. Restifo

  2. ARL Division of Neurobiology, University of Arizona, Tucson, AZ, 85721-0077, USA

    Rebecca F. Spokony & Linda L. Restifo

  3. Department of Neurology, Arizona Health Sciences Center, Tucson, AZ, 85724, USA

    Linda L. Restifo

Authors
  1. Rebecca F. Spokony
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  2. Linda L. Restifo
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Corresponding author

Correspondence to Linda L. Restifo.

Additional information

Communicated by P. Simpson

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Supplement 5

Chromosomal organization of Zlola exons in various holometabolous insects (GIF 38.5 kb)

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Spokony, R.F., Restifo, L.L. Anciently duplicated Broad Complex exons have distinct temporal functions during tissue morphogenesis. Dev Genes Evol 217, 499–513 (2007). https://doi.org/10.1007/s00427-007-0159-y

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  • DOI: https://doi.org/10.1007/s00427-007-0159-y

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