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Genomic sequence of a 320-kb segment of the Z chromosome of Bombyx mori containing a kettin ortholog

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Abstract

The sex chromosome constitution of the silkworm, Bombyx mori, is ZW in the female and ZZ in the male. Very little molecular information is available about the Z chromosome in Lepidoptera, although the topic is interesting because of the absence of gene dosage compensation in this chromosome. We constructed a 320-kb BAC contig around the Bmkettin gene on the Z chromosome in Bombyx and determined its nucleotide sequence by the shotgun method. We found 13 novel protein-coding sequences in addition to Bmkettin. All the transposable elements detected in the region were truncated, and no LTR retrotransposons were found, in stark contrast to the situation on the W chromosome. In this 320-kb region, four genes for muscle proteins (Bmkettin, Bmtitin1, Bmtitin2, and Bmprojectin) are clustered, together with another gene (Bmmiple) on the Z chromosome in B. mori; their orthologs are also closely linked on chromosome 3 in Drosophila, suggesting a partial synteny. Real-time RT-PCR experiments demonstrated that transcripts of 13 genes of the 14 Z-linked genes found accumulated in larger amounts in males than in female moths, indicating the absence of gene dosage compensation. The implications of these findings for the evolution and function of the Z chromosome in Lepidoptera are discussed.

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References

  • Abe H, Kanehara M, Terada T, Ohbayashi F, Shimada T, Kawai S, Suzuki M, Sugasaki T, Oshiki T (1998a) Identification of novel random amplified polymorphic DNAs (RAPDs) on the W chromosome of the domesticated silkworm, Bombyx mori, and the wild silkworm, B. mandarina, and their retrotransposable element-related nucleotide sequences. Genes Genet Syst 73:243–254

    Article  CAS  PubMed  Google Scholar 

  • Abe H, Ohbayashi F, Shimada T, Sugasaki T, Kawai S, Oshiki T (1998b) A complete full-length non-LTR retrotransposon, BMC1, on the W chromosome of the silkworm, Bombyx mori. Genes Genet Syst 73:353–358

    Article  CAS  PubMed  Google Scholar 

  • Abe H, Ohbayashi F, Shimada T, Sugasaki T, Kawai S, Mita K, Oshiki T (2000) Molecular structure of a novel gypsy - Ty3 -like retrotransposon ( Kabuki) and nested retrotransposable elements on the W chromosome of the silkworm Bombyx mori. Mol Gen Genet 263:916–924

    Article  CAS  PubMed  Google Scholar 

  • Abe H, Ohbayashi F, Sugasaki T, Kanehara M, Terada T, Shimada T, Kawai S, Mita K, Kanamori Y, Yamamoto MT, Oshiki T (2001) Two novel Pao-like retrotransposons ( Kamikaze and Yamato) from the silkworm species Bombyx mori and B. mandarina: common structural features of Pao-like elements. Mol Genet Genomics 265:375–385

    Article  CAS  PubMed  Google Scholar 

  • Adams DS, Eickbush TH, Herrera RJ, Lizardi PM (1986) A highly reiterated family of transcribed oligo(A)-terminated, interspersed DNA elements in the genome of Bombyx mori. J Mol Biol 187:465–478

    Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    PubMed  Google Scholar 

  • Baker BS, Gorman M, Marin I (1994) Dosage compensation in Drosophila. Annu Rev Genet 28:491–521

    Article  CAS  PubMed  Google Scholar 

  • Bateman A, Birney E, Durbin R, Eddy SR, Finn RD, Sonnhammer EL (1999) Pfam 3.1: 1313 multiple alignments and profile HMMs match the majority of proteins. Nucleic Acids Res. 27:260–262

    Google Scholar 

  • Baverstock PR, Adams M, Polkinghorne RW, Gelder M (1982) A sex-linked enzyme in birds—Z-chromosome conservation but no dosage compensation. Nature 296:763–766

    CAS  PubMed  Google Scholar 

  • Borsani T, Ballabio A (1993) X chromosome dosage compensation in female mammals. Semin Dev Biol 4:129–139

    Article  Google Scholar 

  • Bryant Z, Subrahmanyan L, Tworoger M, LaTray L, Liu CR, Li M, van den Engh G, Ruohola-Baker H (1999) Characterization of differentially expressed genes in purified Drosophila follicle cells: toward a general strategy for cell type-specific developmental analysis. Proc Natl Acad Sci USA 96:5559–5564

    PubMed  Google Scholar 

  • Carrel L, Cottle AA, Goglin KC, Willard HF (1999) A first-generation X-inactivation profile of the human X chromosome. Proc Natl Acad Sci USA 96:14440–14444

    PubMed  Google Scholar 

  • Catzeflis FM, Nevo E, Ahlquist JE, Sibley CG (1989) Relationships of the chromosomal species in the Eurasian mole rats of the Spalax ehrenbergi group as determined by DNA-DNA hybridization, and an estimate of the spalacid-murid divergence time. J Mol Evol 29:223–232

    Google Scholar 

  • Doira H, Fujii H, Kawaguchi Y, Kihara H, Banno Y (1998) Genetical stocks and mutation of Bombyx mori. In: Important genetic resources (2nd edn) Institute of Genetic Resources, Faculty of Agriculture, Kyusyu University

  • Ellegren H (2002) Dosage compensation: do birds do it as well? Trends Genet 18:25–28

    Article  CAS  PubMed  Google Scholar 

  • Frengen E, Weichenhan D, Zhao B, Osoegawa K, van Geel M, de Jong PJ (1999) A modular positive selection bacterial artificial chromosome vector with multiple cloning sites. Genomics 58:250–253

    CAS  PubMed  Google Scholar 

  • Gage LP (1974) The Bombyx mori genome: analysis by DNA reassociation kinetics. Chromosoma 45:27–42

    CAS  PubMed  Google Scholar 

  • Goberdhan DC, Paricio N, Goodman EC, Mlodzik M, Wilson C (1999) Drosophila tumor suppressor PTEN controls cell size and number by antagonizing the Chico/PI3-kinase signaling pathway. Genes Dev 13:3244–3258

    CAS  PubMed  Google Scholar 

  • Goldman MA, Stokes KR, Idzerda RL, McKnight GS, Hammer RE, Brinster RL, M. GS (1987) A chicken transferrin gene in transgenic mice escapes X-chromosome inactivation. Science 236:593–595

    CAS  PubMed  Google Scholar 

  • Gorman M, Kuroda MI, Baker BS (1993) Regulation of the sex-specific binding of the maleless dosage compensation protein to the male X chromosome in Drosophila. Cell 72:39–49

    CAS  PubMed  Google Scholar 

  • Gorman M, Franke A, Baker BS (1995) Molecular characterization of the male-specific lethal-3gene and investigations of the regulation of dosage compensation in Drosophila. Development 121:463–475

    CAS  PubMed  Google Scholar 

  • Gotter AL, Levine JD, Reppert SM (1999) Sex-linked period genes in the silkmoth, Antheraea pernyi: implications for circadian clock regulation and the evolution of sex chromosomes. Neuron 24:953–965

    CAS  PubMed  Google Scholar 

  • Grula J, Taylor ORJ (1980) The effect of X-chromosome inheritance on mate selection behaviour in the sulfur butterflies, Colias eurytheme and Colias philodice. Evolution 34:688–695

    Google Scholar 

  • Hakeda S, Endo S, Saigo K (2000) Requirements of Kettin, a giant muscle protein highly conserved in overall structure in evolution, for normal muscle function, viability, and flight activity of Drosophila. J Cell Biol 148:101–114

    Article  CAS  PubMed  Google Scholar 

  • Holt RA, et al (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129–149

    Article  CAS  PubMed  Google Scholar 

  • Hori T, Asakawa S, Itoh Y, Shimizu N, Mizuno S (2000) Wpkci, encoding an altered form of PKCI, is conserved widely on the avian W chromosome and expressed in early female embryos: implication of its role in female sex determination. Mol Biol Cell 11:3645–3660

    CAS  PubMed  Google Scholar 

  • Hoshino M, Matsuzaki F, Nabeshima Y, Hama C (1993) hikaru genki, a CNS-specific gene identified by abnormal locomotion in Drosophila, encodes a novel type of protein. Neuron 10:395–407

    CAS  PubMed  Google Scholar 

  • Hoshino M, Suzuki E, Nabeshima Y, Hama C (1996) Hikaru genki protein is secreted into synaptic clefts from an early stage of synapse formation in Drosophila. Development 122:589–597

    CAS  PubMed  Google Scholar 

  • Hoshino M, Suzuki E, Miyake T, Sone M, Komatsu A, Nabeshima Y, Hama C (1999) Neural expression of hikaru genki protein during embryonic and larval development of Drosophila melanogaster. Dev Genes Evol 209:1–9

    Article  CAS  PubMed  Google Scholar 

  • Hsu DR, Meyer BJ (1994) The dpy-30gene encodes an essential component of the Caenorhabditis elegans dosage compensation machinery. Genetics 137:999–1018

    CAS  PubMed  Google Scholar 

  • Huang H, Potter CJ, Tao W, Li DM, Brogiolo W, Hafen E, Sun H, Xu T (1999) PTEN affects cell size, cell proliferation and apoptosis during Drosophila eye development. Development 126:5365–5372

    CAS  PubMed  Google Scholar 

  • Ichimura S, Mita K, Zama M, Numata M (1985) Isolation of the giant ramified nuclei of the posterior silk glands of Bombyx mori. Insect Biochem 15:277–283

    CAS  Google Scholar 

  • Ichimura S, Mita, K., Sugaya, K. (1997) A major non–LTR retrotransposon of Bombyx mori, L1Bm. J Mol Evol 45:253–264

    Google Scholar 

  • Johnson MS, Turner JRG (1979) Absence of dosage compensation for a sex-linked enzyme in butterflies ( Heliconius). Heredity 43:71–77

    CAS  Google Scholar 

  • Kolmerer B, Clayton J, Benes V, Allen T, Ferguson C, Leonard K, Weber U, Knekt M, Ansorge W, Labeit S, Bullard B (2000) Sequence and expression of the kettin gene in Drosophila melanogaster and Caenorhabditis elegans. J Mol Biol 296:435–448

    Google Scholar 

  • Komoto N (2002) A deleted portion of one of the two xanthine dehydrogenase genes causes translucent larval skin in the oq mutant of the silkworm ( Bombyx mori). Insect Biochem Mol Biol 32:591–597

    Article  CAS  PubMed  Google Scholar 

  • Kulke M, Neagoe C, Kolmerer B, Minajeva A, Hinssen H, Bullard B, Linke WA (2001) Kettin, a major source of myofibrillar stiffness in Drosophila indirect flight muscle. J Cell Biol 154:1045–1057

    Article  CAS  PubMed  Google Scholar 

  • Littleton JT, Pallanck L, Ganetzky B (1999) Mechanisms of neurotransmitter release. Int Rev Neurobiol 43:139–161

    CAS  PubMed  Google Scholar 

  • Lloyd TE, Verstreken P, Ostrin EJ, Phillippi A, Lichtarge O, Bellen HJ (2000) A genome-wide search for synaptic vesicle cycle proteins in Drosophila. Neuron 26:45–50

    CAS  PubMed  Google Scholar 

  • Machado C, Andrew D (2000) D-Titin: a giant protein with dual roles in chromosomes and muscles. J Cell Biol 151:639–652

    CAS  PubMed  Google Scholar 

  • McQueen HA, McBride D, Miele G, Bird AP, Clinton M (2001) Dosage compensation in birds. Curr Biol 11:253–257

    Article  CAS  PubMed  Google Scholar 

  • Miller LM, Plenefisch JD, Casson LP, Meyer BJ (1988) xol-1: a gene that controls the male modes of both sex determination and X chromosome dosage compensation in C. elegans. Cell 55:167–183

    CAS  PubMed  Google Scholar 

  • Nanda I, Sick C, Munster U, Kaspers B, Schartl M, Staeheli P, Schmid M (1998) Sex chromosome linkage of chicken and duck type I interferon genes: further evidence of evolutionary conservation of the Z chromosome in birds. Chromosoma 107:204–210

    Article  CAS  PubMed  Google Scholar 

  • Nanda I, Zend-Ajusch E, Shan Z, Grutzner F, Schartl M, Burt DW, Koehler M, Fowler VM, Goodwin G, Schneider WJ, Mizuno S, Dechant G, Haaf T, Schmid M (2000) Conserved synteny between the chicken Z sex chromosome and human chromosome 9 includes the male regulatory gene DMRT1: a comparative (re)view on avian sex determination. Cytogenet Cell Genet 89:67–78

    Article  CAS  PubMed  Google Scholar 

  • Ogura T, Okano K, Tsuchida K, Miyajima N, Tanaka H, Takada N, Izumi S, Tomino S, Maekawa H (1994) A defective non-LTR retrotransposon is dispersed throughout the genome of the silkworm, Bombyx mori. Chromosoma 103:311–323

    Article  CAS  PubMed  Google Scholar 

  • Osoegawa K, Woon PY, Zhao B, Frengen E, Tateno M, Catanese JJ, deJong PJ (1998) An improved approach for construction of bacterial artificial chromosome libraries. Genomics 52:1–8

    CAS  PubMed  Google Scholar 

  • Osoegawa K, Tateno M, Woon PY, Frengen E, Mammoser AG, Catanese JJ, Hayashizaki Y, deJong PJ (2000) Bacterial artificial chromosome libraries for mouse sequencing and functional analysis. Genome Res 10:116–128

    CAS  PubMed  Google Scholar 

  • Quan GX, Kim I, Komoto N, Sezutsu H, Ote M, Shimada T, Kanda T, Mita K, Kobayashi M, Tamura, T (2002) Characterization of the kynurenine 3-monooxygenase gene corresponding to the white egg 1 mutant in the silkworm Bombyx mori. Mol Genet Genomics 267:1–9

    Article  CAS  PubMed  Google Scholar 

  • Quintana-Murci L, Jamain S, Fellous M (2001) Origin and evolution of mammalian sex chromosomes. C R Acad Sci III 324:1–11

    Article  CAS  PubMed  Google Scholar 

  • Ranz J, Casals F, Ruiz A (2001) How malleable is the eukaryotic genome? Extreme rate of chromosomal rearrangement in the genus Drosophila. Genome Res 11:230–239

    Article  CAS  PubMed  Google Scholar 

  • Robertson HM, Asplund ML (1996) Bmmar1: a basal lineage of the mariner family of transposable elements in the silkworm moth, Bombyx mori. Insect Biochem Mol Biol 26:945–954

    Article  CAS  PubMed  Google Scholar 

  • Saitoh Y, Ogawa A, Hori T, Kunita R, Mizuno S (1993) Identification and localization of two genes on the chicken Z chromosome: implication of evolutionary conservation of the Z chromosome among avian species. Chromosome Res 1:239–251

    CAS  PubMed  Google Scholar 

  • Schwartz A, Chan DC, Brown LG, Alagappan R, Pettay D, Disteche C, McGillivray B, de la Chapelle A, Page DC (1998) Reconstructing hominid Y evolution: X-homologous block, created by X-Y transposition, was disrupted by Yp inversion through LINE-LINE recombination. Hum Mol Genet 7:1–11

    Article  CAS  PubMed  Google Scholar 

  • Shan Z, Nanda I, Wang Y, Schmid M, Vortkamp A, Haaf T (2000) Sex-specific expression of an evolutionarily conserved male regulatory gene, DMRT1, in birds. Cytogenet Cell Genet 89:252–257

    Article  CAS  PubMed  Google Scholar 

  • Shizuya H, Birren B, Kim UJ, Mancino V, Slepak T, Tachiiri Y, Simon M (1992) Cloning and stable maintenance of 300-kilobase-pair fragments of human DNA in Escherichia coli using an F-factor-based vector. Proc Natl Acad Sci USA 89:8794–8797

    CAS  PubMed  Google Scholar 

  • Sperling FAH (1994) Sex-linked genes and species differences in Lepidoptera. Can Entomol 126:807–818

    Google Scholar 

  • Stehr G (1959) Haemolymph polymorphism in a moth and the nature of sex-controlled inheritance. Evolution 13:537–560

    Google Scholar 

  • Suzuki MG, Shimada T, Kobayashi M (1998) Absence of dosage compensation at the transcription level of a sex-linked gene in a female heterogametic insect, Bombyx mori. Heredity 81:275–283

    Article  CAS  PubMed  Google Scholar 

  • Suzuki MG, Shimada T, Kobayashi M (1999a) Bm kettin, a homologue of the Drosophila kettin gene, is located on the Z chromosome in Bombyx mori and is not dosage compensated. Heredity 82:170–179

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Kansaku N, Kurosaki T, Shimada K, Zadworny D, Koide M, Mano T, Namikawa T, Matsuda Y (1999b) Comparative FISH mapping on Z chromosomes of chicken and Japanese quail. Cytogenet Cell Genet 87:22–26

    Article  CAS  PubMed  Google Scholar 

  • Tomita S, Sohn BH, Tamura T (1997) Cloning and characterization of a mariner -like element in the silkworm, Bombyx mori. Genes Genet Syst 72:219–228

    Article  CAS  PubMed  Google Scholar 

  • Traut W (1976) Pachytene mapping in the female silkworm, Bombyx mori L. (Lepidoptera). Chromosoma 58:275–284

    CAS  PubMed  Google Scholar 

  • Traut W, Marec F (1996) Sex chromatin in Lepidoptera. Quart Rev Biol 71:239–256

    CAS  Google Scholar 

  • Uenoyama T, Uchida S, Fukunaga A, Oishi K (1982a) Studies on the sex-specific lethals of Drosophila melanogaster. IV. Gynandromorph analysis of three male-specific lethals, mle, msl-2 27 and mle(3)132. Genetics 102:223–231

    CAS  PubMed  Google Scholar 

  • Uenoyama T, Fukunaga, A., Ioshi, K (1982b) Studies on the sex-specific lethals of Drosophila melanogaster. V. Sex transformation caused by interactions between a female-specific lethal, Sxlf 1, and the male-specific lethals mle(3)132, msl-2 27, and mle. Genetics 102:233–243

    CAS  PubMed  Google Scholar 

  • Yasukochi Y (1998) A dense genetic map of the silkworm, Bombyx mori, covering all chromosomes based on 1018 molecular markers. Genetics 150:1513–1525

    CAS  PubMed  Google Scholar 

  • Zhou CZ, Confalonieri F, Medina N, Zivanovic Y, Esnault C, Yang T, Jacquet M, Janin J, Duguet M, Perasso R, Li ZG (2000) Fine organization of Bombyx mori fibroin heavy chain gene. Nucleic Acids Res 28:2413–2419

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Research for the Future Program, JSPS-MEXT (to T.S.), the Basic Research Program, BRAIN (to K.M. and T.S.), and the Animal Genome Research Program, MAFF (to K.M. and T.S.). We are grateful to Prof. M. Kobayashi for his continuous encouragement. We thank J. J. Catanese and B. Swiatkiewicz for helping with BAC library construction, and Y. Ishihara, J. Nohata, I. Matsumoto, M. Takahashi and S. Sasanuma for help with the shotgun sequencing

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Correspondence to T. Shimada.

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S. Maeda: Deceased

Communicated by G. Reuter

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Koike, Y., Mita, K., Suzuki, M.G. et al. Genomic sequence of a 320-kb segment of the Z chromosome of Bombyx mori containing a kettin ortholog. Mol Gen Genomics 269, 137–149 (2003). https://doi.org/10.1007/s00438-003-0822-6

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  • DOI: https://doi.org/10.1007/s00438-003-0822-6

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