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Isolation and characterization of sex chromosome rearrangements generating male muscle dystrophy and female abnormal oogenesis in the silkworm, Bombyx mori

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Abstract

In deletion-mapping of W-specific RAPD (W-RAPD) markers and putative female determinant gene (Fem), we used X-ray irradiation to break the translocation-carrying W chromosome (WZe). We succeeded in obtaining a fragment of the WZe chromosome designated as Ze W, having 3 of 12 W-RAPD markers (W-Bonsai, W-Yukemuri-S, W-Yukemuri-L). Inheritance of the Ze W fragment by males indicates that it does not include the Fem gene. On the basis of these results, we determined the relative positions of W-Yukemuri-S and W-Yukemuri-L, and we narrowed down the region where Fem gene is located. In addition to the Ze W fragment, the Z chromosome was also broken into a large fragment (Z1) having the +sch (1-21.5) and a small fragment (Z2) having the +od (1-49.6). Moreover, a new chromosomal fragment (Ze WZ2) was generated by a fusion event between the Ze W and the Z2 fragments. We analyzed the genetic behavior of the Z1 fragment and the Ze WZ2 fragment during male (Z/Z1 Ze WZ2) and female (Z1 Ze WZ2/W) meiosis using phenotypic markers. It was observed that the Z1 fragment and the Z or the W chromosomes separate without fail. On the other hand, non-disjunction between the Ze WZ2 fragment and the Z chromosome and also between the Ze WZ2 fragment and the W chromosome occurred. Furthermore, the females (2A: Z/Ze WZ2/W) and males (2A: Z/Z1) resulting from non-disjunction between the Ze WZ2 fragment and the W chromosome had phenotypic defects: namely, females exhibited abnormal oogenesis and males were flapless due to abnormal indirect flight muscle structure. These results suggest that Z2 region of the Z chromosome contains dose-sensitive gene(s), which are involved in oogenesis and indirect flight muscle development.

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References

  • Abe H, Ohbayashi F, Harada T, Shimada T, Yokoyama T, Kobayashi M, Oshiki T (1996) An application of DNA diagnosis method for preservation of the susceptible strain to densonucleosis virus type-1 of the silkworm, Bombyx mori. J Sericult Sci Jpn 65:196–200 (in Japanese with English summary)

    CAS  Google Scholar 

  • Abe H, Kanehara M, Terada T, Ohbayashi F, Shimada T, Kawai S, Suzuki M, Sugasaki T, Oshiki T (1998) 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  PubMed  CAS  Google Scholar 

  • Abe H, Seki M, Ohbayashi F, Tanaka N, Yamashita J, Fujii T, Yokoyama T, Takahashi M, Banno Y, Sahara K, Yoshido A, Ihara J, Yasukochi Y, Mita K, Ajimura M, Suzuki MG, Oshiki T, Shimada T (2005a) Partial deletions of the W chromosome due to reciprocal translocation in the silkworm Bombyx mori. Insect Mol Biol 14:339–352

    Article  CAS  Google Scholar 

  • Abe H, Mita K, Yasukochi Y, Oshiki T, Shimada T (2005b) Retrotransposable elements on the W chromosome of the silkworm, Bombyx mori. Cytogenet Genome Res 110:144–151

    Article  CAS  Google Scholar 

  • Bainbridge D (2003) The X in Sex. Harvard University Press, London

    Google Scholar 

  • Ball E, Ball SP, Sparrow JC (1985) A mutation affecting larval muscle development in Drosophila melanogaster. Dev Genet 6:77–92

    Article  Google Scholar 

  • Bernstein AI, Mogami K, Donady JJ, Emerson CP (1983) Drosophila muscle myosin heavy chain encoded by a single gene in a cluster of muscle mutations. Nature 302:393–397

    Article  PubMed  CAS  Google Scholar 

  • Bortoluzzi S, Rampoldi L, Simionati B, Zimbello R, Barbon A, d’Alessi F, Tiso N, Pallavicini A, Toppo S, Cannata N, Valle G, Lanfranchi G, Danieli GA (1998) A comprehensive, high-resolution genomic transcript map of human skeletal muscle. Genome Res 8:817–825

    PubMed  CAS  Google Scholar 

  • Cripps RM, Ball E, Stark M, Lawn A, Sparrow JC (1994) Recovery of dominant, autosomal flightless mutants of Drosophila melanogaster and identification of a new gene required for normal muscle structure and function. Genetics 137:151–164

    PubMed  CAS  Google Scholar 

  • Doira H (1978) Genetic stocks of the silkworm: In: Tazima Y (ed), The silkworm, an important laboratory tool. Kodansha Ltd., Japan

    Google Scholar 

  • Eric JV, Bruce TL (2004) How mammalian sex chromosome acquired their peculiar gene content. BioEssays 26:159–169

    Article  CAS  Google Scholar 

  • Fujii H, Banno Y, Doira H, Kihara H, Kawaguchi Y (1998) Genetical stocks and mutations of Bombyx mori: important genetic resources. 2nd edn. Institute of Genetic Resources, Faculty of Agriculture, Kyushu University, Fukuoka, p54

    Google Scholar 

  • Fujii T, Tanaka N, Yokoyama T, Ninagi O, Oshiki T, Ohnuma A, Tazima Y, Banno Y, Ajimura M, Mita K, Seki M, Ohbayashi F, Shimada T, Abe H (2006) The female-killing chromosome of the silkworm, Bombyx mori, was generated by translocation between Z and W chromosomes. Genetica 127:253–265

    Article  PubMed  CAS  Google Scholar 

  • Fujiwara H, Ninaki O, Kobayashi M, Kusuda J, Maekawa H (1991) Chromosomal fragment responsible for genetic mosaicism in larval body marking of the silkworm, Bombyx mori. Genet Res 57:11–16

    CAS  Google Scholar 

  • Fujiwara H, Maekawa H (1994) RFLP analysis of chromosomal fragments in genetic mosaic strain of Bombyx mori. Chromosoma 103:468–474

    PubMed  CAS  Google Scholar 

  • Hasimoto H (1933) The role of the W-chromosome in the sex determination of Bombyx mori. Jpn J Genet 8:245–247 (in Japanese)

    Google Scholar 

  • Hasimoto H (1948) Sex-limited zebra, an X-ray mutation in the silkworm. J Sericult Sci Jpn 16:62–64 (in Japanese with English summary)

    Google Scholar 

  • Hurst LD, Randerson JP (1999) An exceptional chromosome. Trends Genet 15:383–385

    Article  PubMed  CAS  Google Scholar 

  • Kawamura N (1988) The egg size determining gene, Esd, is a unique morphological marker on the W chromosome of Bombyx mori. Genetica 76:195–201

    Article  Google Scholar 

  • Kawaguchi Y (1995) Genetic analysis of the soft and elongated trunk mutant in Bombyx mori. J Sericult Sci Jpn 64:31–34

    CAS  Google Scholar 

  • Koike Y, Mita K, Suzuki MG, Maeda S, Abe H, Osoegawa K, deJong PJ, Shimada T (2003) Genomic sequence of a 320-kb segment of the Z chromosome of Bombyx mori containing a kettin ortholog. Mol Gen Genomics 269:137–149

    CAS  Google Scholar 

  • Kondoh Y, Obara Y (1982) Anatomy of motoneurones innervating mesothoracic indirect flight muscles in the silkworm, Bombyx mori. J Exp Biol 98:23–27

    Google Scholar 

  • Marec F, Mirchi R (1990) Genetic control of the pest Lepidoptera: gamma-ray induction of translocations between sex chromosomes of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). J Stored Prod Res 26:109–116

    Article  Google Scholar 

  • Marec F (1996) Synaptonemal complex in insects. Int J Insect Morphol Embryol 25:205–233

    Article  Google Scholar 

  • Marec F, Neven LG, Robinson AS, Vreysen M, Goldsmith MR, Nagaraju J, Franz G (2005) Development of Genetic sexing strains in Lepidoptera: from traditional to transgenic approaches. J Econ Entomol 98:248–259

    Article  PubMed  Google Scholar 

  • Marec F, Tothova A, Sahara K, Traut W (2001) Meiotic pairing of sex chromosome fragments and its relation to atypical transmission of a sex-linked marker in Ephestia kuehniella (Insecta: Lepidoptera). Heredity 87:659–671

    Article  PubMed  CAS  Google Scholar 

  • Mogami K, O’Donnell PT, Bernstein SI, Wright TRF, Emerson CP (1986) Mutations of the Drosophila myosin heavy-chain gene: effects on transcription, myosin accumulation, and muscle function. Proc Natl Acad Sci USA 83:1393–1397

    Article  PubMed  CAS  Google Scholar 

  • Mogami K, Hotta Y (1981) Isolation of Drosophila flightless mutants which affect myofibrillar proteins of indirect flight muscle. Mol Gen Genet 183:409–417

    Article  PubMed  CAS  Google Scholar 

  • Murakami A, Imai HT (1974) Cytological evidence for holocentric chromosomes of the silkwoms, Bombyx mori and B. mandarina (Bombycidae, Lepidoptera). Chromosoma 47:167–178

    Article  PubMed  CAS  Google Scholar 

  • Nagaraja GM, Mahesh G, Satish V, Madhu M, Muthulakshmi M, Nagaraju J (2005) Genetic mapping of Z chromosome and identification of W chromosome-specific markers in the silkworm, Bombyx mori. Heredity 95:148–157

    Article  PubMed  CAS  Google Scholar 

  • Newman SM, Wright TRF (1983) lethal(1)fibrillardysgenesis. A mutation affecting muscle development in the embryo of Drosophila melanogaster. Dev Genet 4:329–345

    Google Scholar 

  • Ohnuma A (1988) Synthesis of balanced sex-linked lethal strain in the silkworm. Rep Silk Sci Res Inst (Tokyo, Japan) 36:17–25 (in Japanese with English summary)

    Google Scholar 

  • Sahara K, Yoshido A, Kawamura N, Ohnuma A, Abe H, Mita K, Oshiki T, Shimada T, Asano S-I, Bando H, Yasukochi Y (2003) W-derived BAC probes as a new tool for identification of the W chromosome and its aberrations in Bombyx mori. Chromosoma 112:48–55

    Article  PubMed  CAS  Google Scholar 

  • Saifi GM, Chandra HS (1999) An apparent excess of sex- and reproduction-related genes on the human X chromosome. Proc R Soc Lond B Biol Sci 266:203–209

    Article  CAS  Google Scholar 

  • Strunnikov VA (1975) Sex control in silkworms. Nature 255:111–113

    Article  PubMed  CAS  Google Scholar 

  • Sturtevant AH (1915) No crossing over in the female of the silkworm moth. Am Nat 49:42–44

    Article  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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y (1913a) A study of mendelian factors in the silkworm, Bombyx mori. J Coll Agric Sapporo 5:61–113

    Google Scholar 

  • Tanaka Y (1913b) Gametic coupling and repulsion in silkworms. J Coll Agric Sapporo 5:115–148

    Google Scholar 

  • Tanaka Y (1916) Genetic studies in the silkworm. J Coll Agric Sapporo 6:1–33

    Google Scholar 

  • Tanaka Y (1923) Inheritance of elongate (a preliminary note). Sanshikaiho 32:21–23

    Google Scholar 

  • Traut W, Sahara K, Otto TD, Marec F (1999) Molecular differentiation of sex chromosome probed by comparative genomic hybridization. Chromosoma 108:173–180

    Article  PubMed  CAS  Google Scholar 

  • Warmke JW, Kreuz AJ, Falkenthal S (1989) Co-localization to chromosome bands 99E1-3 of the Drosophila melanpgaster myosin light chain-2 gene and a haplo-insufficient locus that affects flight behavior. Genetics 122:139–151

    PubMed  CAS  Google Scholar 

  • Yokoyama T, sugai E, Oshiki T, Pan Q (1990) Induction of the triploid silkworm, Bombyx mori, by the hot-water treatment to the inseminated eggs immediately after oviposition. J Sericult Sci Jpn 59:281–224

    Google Scholar 

  • Yoshido A, Bando H, Yasukochi Y, Sahara K (2005) The Bombyx mori karyotype and the assignment of linkage groups. Genetics 170(2):675–685

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from BRAIN (to. K. M.), Grants-in-Aid for Scientific Research, MEXT (Nos. 17052006, 16011263, and 17018007) and JSPS (No. 16208006), the Insect Technology Project, MAFF/NIAS (No. 1216), and the National Bioresource Project, MEXT.

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Fujii, T., Yokoyama, T., Ninagi, O. et al. Isolation and characterization of sex chromosome rearrangements generating male muscle dystrophy and female abnormal oogenesis in the silkworm, Bombyx mori . Genetica 130, 267–280 (2007). https://doi.org/10.1007/s10709-006-9104-7

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  • DOI: https://doi.org/10.1007/s10709-006-9104-7

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