Skip to main content
SpringerLink
Log in

Sex determination: insights from the silkworm

  • Review Article
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

The sex-determining system differs considerably among organisms. Even among insect species, the genetic system for sexdetermination is highly diversified. In Drosophila melanogaster, somatic sexual differentiation is regulated by a well characterized genetic hierarchy X:A > Sxl > tra/tra2 > dsx and fru. This cascade seems to control sex determination in all Drosophila species and is partially conserved in another dipteran species, Ceratitis capitata: Cctra/Cctra-2 > Ccdsx and Ccfru. However, in the silkworm, Bombyx mori, femaleness is determined by the presence of a dominant feminizing factor on the W chromosome. Moreover, no sex-specific regulatory Sxl homolog has been isolated from B. mori. Also, no tra homolog has yet been found in the Bombyx genome. Despite such differences, dsx homolog of B. mori (Bmdsx) is implicated in the sex determination. Bmdsx produces alternatively spliced mRNA isoforms that encode sex specific transcription factors as observed in dsx. While the female-specific splicing of dsx is activated by splicing activators, Tra and Tra2, the female splicing of Bmdsx represents the default mode. Instead, a splicing inhibitor, BmPSI is involved in the regulation of male-specific splicing of Bmdsx. Since BmPSI does not exhibit any sequence relationship to known SR proteins, such as Tra and Tra2, the regulatory mechanism of sex-specific alternative splicing of Bmdsx is distinct from that of dsx.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adams M. D., Tarng R. S. and Rio D. C. 1997 The alternative splicing factor PSI regulates P-element third intron splicing in vivo. Genes Dev. 11, 129–138.

    Article  CAS  PubMed  Google Scholar 

  • Ajimura M., Sahara K., Abe H., Tamura T., Shimada T. and Mita K. 2006 Are the zinc-finger motif genes, zl and z20, located in the W chromosome involved in the sex-determination of the domesticated silkworm, Bombyx mori? Abstracts from Seventh International Workshop on the Molecular Biology and Genetics of the Lepidoptera. J. Insect Sci. 7, 4–5.

    Google Scholar 

  • Babic I., Jakymiw A. and Fujita D. J. 2004 The RNA binding proteen Sam68 is acetylated in tumos cell lines, and its acetylation correlates with enhanced RNA binding activity. Oncogene 23, 3781–3789.

    Article  CAS  PubMed  Google Scholar 

  • Baker R. H. and Sakai R. K. 1976 Male determining factor on chromosome 3 in the mosquito, Culex tritaeniorhynchus. J. Hered. 67, 289–294.

    CAS  PubMed  Google Scholar 

  • Bedo D. G. and Foster G. G. 1985 Cytogenetic mapping of the male-determining region of Lucilia cuprina (Diptera: Clliphoridae). Chromosoma 92, 344–350.

    Article  Google Scholar 

  • Berghammer A. J., Klingler M. and Wimmer E. A. 1999 A universal marker for transgenic insects. Nature 402, 370–371.

    Article  CAS  PubMed  Google Scholar 

  • Beukeboom L.W. 1995 Sex-determination in Hymenoptera: a need for genetic and molecular studies. BioEssays 17, 813–817.

    Article  CAS  PubMed  Google Scholar 

  • Carroll S. B., Grenier J. K. and Weatherbee S. D. 2001 From DNA to diversity: molecular genetics and the evolution of animal design. Blackwell, Malden, USA.

    Google Scholar 

  • Casper A. and Van Doren M. 2006 The control of sexual identity in the Drosophila germline. Development 133, 2783–2791.

    Article  CAS  PubMed  Google Scholar 

  • Cho S., Huang Z. Y. and Zhang J. 2007 Sex-specific splicing of the honeybee doublesex gene reveals 300 million years of evolution at the bottom of the insect sex-determination pathway. Genetics 177, 1733–1741.

    Article  CAS  PubMed  Google Scholar 

  • Christophides G. K., Livadaras I., Savakis C. and Komitopoulou K. 2000 Two medfly promoters that have originated by recent gene duplication drive distinct sex, tissue and temporal expression patterns. Genetics 156, 173–182.

    CAS  PubMed  Google Scholar 

  • Cline T. W. and Meyer B. J. 1996 Vive la difference: males vs. females in flies vs. worms. Annu. Rev. Genet. 30, 637–702

    Article  CAS  PubMed  Google Scholar 

  • Cristino A. S., Nascimento A. M., Costa Lda F. and Simões Z. L. 2006 A comparative analysis of highly conserved sexdetermining genes between Apis mellifera and Drosophila melanogaster. Genet. Mol. Res. 5, 154–168.

    CAS  PubMed  Google Scholar 

  • Erickson J. W. and Quintero J. J. 2007 Indirect effects of ploidy suggest X chromosome dose, not the X:A ratio, signals sex in Drosophila. PLoS Biol. 5, 2821–2830.

    Article  CAS  Google Scholar 

  • Funaguma S., Hashimoto S., Suzuki Y., Omuro N., Sugano S., Mita K. et al. 2007 SAGE analysis of early oogenesis in the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 37, 147–154.

    Article  CAS  PubMed  Google Scholar 

  • Grula J. W. and Taylor Jr O. R. 1980 The effect of X-chromosome inheritance on mate selection behavior in the sulfur butterflies, Colias eurytheme, Colias philodice. Evolution 34, 688–695.

    Article  Google Scholar 

  • Goldschmidt R. B. 1955 Theoretical genetics. University of California Press, Berkeley, USA.

    Google Scholar 

  • Haegebarth A., Heap D., Bie W., Derry J. J., Richard S. and Tyner A. L. 2004 The nuclear tyrosine kinase BRK/Sik phosphorylates and inhibits the RNA-binding activities of the Sam68-like mammalian proteins SLM-1 and SLM-2. J. Biol. Chem. 279, 54398–54404.

    Article  CAS  PubMed  Google Scholar 

  • Hägele K. 1985 Identification of a polytene chromosome band containing a male sex determiner of Chironomus thummi thummi. Chromosoma 91, 167–171.

    Article  PubMed  Google Scholar 

  • Hashimoto H. 1933 The role of the W chromosome for sexdetermination in the silkworm, Bombyx mori. Jap. J. Genet. 8, 245–258.

    Article  Google Scholar 

  • Hasselmann M., Gempe T., Schitt M., Nunes-Silva C. G., Otte M. and Beye M. 2008 Evidence for the evolutionary nascence of a novel sex-determination pathway in honeybees. Nature 454, 519–522.

    Article  CAS  PubMed  Google Scholar 

  • Hediger M., Burghardt G., Siegenthaler C., Buser N., Hilfiker-Kleiner D., Dübendorfer A. and Bopp D. 2004 Sexdetermination in Drosophila melanogaster and Musca domestica converges at the level of the terminal regulator doublesex. Dev. Genes Evol. 214, 29–42.

    Article  CAS  Google Scholar 

  • Johnson M. S. and Turner J. R. G. 1979 Absence of dosage compensation for a sex-linked enzyme in butterflies (Heliconius). Heredity 43, 71–77.

    Article  CAS  Google Scholar 

  • Kimura K., Harada C. and Aoki H. 1971 Studies on the Wtranslocation of yellow blood gene in the silkworm (Bombyx mori). Jap. J. Breed. 21, 199–203 (in Japanese with English summary).

    Google Scholar 

  • Koike Y., Mita K., Suzuki M. G., Maeda S., Abe H., Osoegawa K. et al. 2003 Genomic sequence of a 320-kb segment of the Z chromosome of Bombyx mori containing a kettin ortholog. Mol. Genet. Genomics 269, 137–149.

    CAS  Google Scholar 

  • Kuhn, S., Sievert, V. and Traut W. 2000 The sex-determining gene doublesex in the fly Megaselia scalaris: conserved structure and sex-specific splicing. Genome 43, 1011–1020.

    Article  CAS  PubMed  Google Scholar 

  • Kuwabara P. E. 1996 Interspecies comparison reveals evolution of control regions in the nematode sex-determining gene tra-2. Genetics 144, 597–607.

    CAS  PubMed  Google Scholar 

  • Lagos D., Ruiz M. F., Sánchez L. and Komitopoulou K. 2005 Isolation and characterization of the Bactrocera oleae genes orthologous to the sex determining Sex-lethal and doublesex genes of Drosophila melanogaster. Gene 348, 111–121.

    Article  CAS  PubMed  Google Scholar 

  • Lagos D., Koukidou M., Savakis C. and Komitopoulou K. 2007 The transformer gene in Bactrocera oleae: the genetic switch that determines its sex fate. Insect Mol. Biol. 16, 221–230.

    Article  CAS  PubMed  Google Scholar 

  • Marin I. and Baker B. S. 1998 The evolutionary dynamics of sexdetermination. Science 281, 1990–1994.

    Article  CAS  PubMed  Google Scholar 

  • Messias A. C., Harnisch C., Ostareck-Lederer A., Sattler M. and Ostareck D. H. 2006 The DICE-binding activity of KH domain 3 of hnRNP K is affected by c-Src-mediated tyrosine phosphorylation. J. Mol. Biol. 361, 470–481.

    Article  CAS  PubMed  Google Scholar 

  • Meise M., Hilfiker-Kleiner D., Dübendorfer A., Brunner C., Nöthiger R. and Bopp D. 1998 Sex-lethal, the master sexdetermining gene in Drosophila, is not sex-specifically regulated in Musca domestica. Development 125, 1487–1494.

    CAS  PubMed  Google Scholar 

  • Mita K., Morimyo M., Okano K., Koike Y., Nohata J., Kawasaki H. et al. 2003 The construction of an EST database for Bombyx mori and its application. Proc. Natl. Acad. Sci. USA 100, 14121–14126.

    Article  PubMed  Google Scholar 

  • Mita K., Kasahara M., Sasaki S., Nagayasu Y., Yamada T., Kanamori H. et al. 2004 The genome sequence of silkworm, Bombyx mori. DNA Res. 11, 27–35.

    Article  CAS  PubMed  Google Scholar 

  • Niimi T., Sahara K., Oshima H., Yasukochi Y., Ikeo K. and Traut W. 2006 Molecular cloning and chromosomal localization of the Bombyx Sex-lethal gene. Genome 49, 263–268.

    Article  CAS  PubMed  Google Scholar 

  • O’Neil M. T. and Belote J. M. 1992 Interspecific comparison of the transformer gene of Drosophila reveals an unusually high degree of evolutionary divergence. Genetics 131, 113–128.

    PubMed  Google Scholar 

  • Ohbayashi F., Suzuki M. G., Mita K., Okano K. and Shimada T. 2001 A homologue of the Drosophila doublesex gene is transcribed into sex-specific mRNA isoforms in the silkworm, Bombyx mori. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 128, 145–158.

    Article  CAS  Google Scholar 

  • Pane A., Salvemini M., Delli Bovi P., Polito C. and Saccone G. 2002 The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development 129, 3715–3725.

    CAS  PubMed  Google Scholar 

  • Ruiz M. F., Stefani R. N., Mascarenhas R. O., Perondini A. L., Selivon D. and Sánchez L. 2005 The gene doublesex of the fruit fly Anastrepha obliqua (Diptera, Tephritidae). Genetics 171, 849–854.

    Article  CAS  PubMed  Google Scholar 

  • Saccone G., Peluso I., Artiaco D., Giordano E., Bopp D. and Polito L. C. 1998 The Ceratitis capitata homologue of the Drosophila sex-determining gene sex-lethal is structurally conserved, but not sex-specifically regulated. Development 125, 1495–1500.

    CAS  PubMed  Google Scholar 

  • Satish V., Shukla J. N., and Nagaraju J. 2006 CCCH-type zinc finger genes: candidate regulators of sex-determination pathway in the silkworm, Bombyx mori. Abstracts from Seventh International Workshop on the Molecular Biology and Genetics of the Lepidoptera. J. Insect Sci. 7, 40.

    Google Scholar 

  • Scali C., Catteruccia F., Li Q. and Crisanti A. 2005 Identification of sex-specific transcripts of the Anopheles gambiae doublesex gene. J. Exp. Biol. 208, 3701–3709.

    Article  CAS  PubMed  Google Scholar 

  • Shearman D. C. A. and Formmer M. 1998 The Bactrocera tryoni homolog of the Drosophila melanogaster sex-determination gene doublesex. Insect Mol. Biol. 7, 355–366.

    Article  CAS  PubMed  Google Scholar 

  • Siebel C. W. and Rio D. C. 1990 Regulated splicing of the Drosophila P transposable element third intron in vitro: somatic repression Science 248, 1200–1208.

    Article  CAS  PubMed  Google Scholar 

  • Sievert V., Kuhn S., Paululat A. and Traut W. 2000 Sequence conservation and expression of the sex-lethal homologue in the fly Megaselia scalaris. Genome 43, 382–390.

    Article  CAS  PubMed  Google Scholar 

  • Sperling F. A. H. 1994 Sex-linked genes and species differences in Lepidoptera. Can. Entomol. 126, 807–818.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Suzuki M. G., Shimada T. and 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 M. G., Shimada T. and Kobayashi M. 1999 Bmkettin, 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 M. G., Ohbayashi F., Mita K. and Shimada T. 2001 The mechanism of sex-specific splicing at the doublesex gene is different between Drosophila melanogaster and Bombyx mori. Insect Biochem. Mol. Biol. 31, 1201–1211.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki M. G., Funaguma S., Kanda T., Tamura T. and Shimada T. 2003 Analysis of the biological functions of a doublesex homologue in Bombyx mori. Dev. Genes Evol. 213, 345–354.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki M. G., Funaguma S., Kanda T., Tamura T. and Shimada T. 2005 Role of the male BmDSX protein in the sexual differentiation of Bombyx mori. Evol. Dev. 7, 58–68.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki M. G., Imanishi S., Dohmae N., Nishimura T., Shimada T. and Matsumoto S. 2008 Establishment of a novel in vivo sexspecific splicing assay system to identify a trans-acting factor that negatively regulates splicing of Bombyx mori dsx female exons. Mol. Cell Biol. 28, 333–343.

    Article  CAS  PubMed  Google Scholar 

  • Tazima Y. 1954 Mechanisms of the sex-determination in the silkworm, Bombyx mori. In Proceedings of the 9th International Congress of Genetics 1953. Caryologia 6(suppl.) 958–960.

    Google Scholar 

  • Traut W. 1994 Sex-determination in the fly Megaselia scalaris, a model system for primary steps of sex chromosome evolution. Genetics 136, 1097–1104.

    CAS  PubMed  Google Scholar 

  • Traut W. and Marec F. 1996 Sex chromatin in lepidoptera. Quart. Rev. Biol. 71, 239–256.

    Article  CAS  PubMed  Google Scholar 

  • Traut W., Sahara K., Otto T. D. and Marec F. 1999 Molecular differentiation of sex chromosomes probed by comparative genomic hybridization. Chromosoma 108, 173–180.

    Article  CAS  PubMed  Google Scholar 

  • Wang L. L., Richard S. and Shaw A. S. 1995 p62 association with RNA is regulated by tyrosine phosphorylation. J. Biol. Chem. 270, 2010–2013.

    Article  CAS  PubMed  Google Scholar 

  • Willhoeft U. and Franz G. 1996 Identification of the sex-determining region of the Ceratitis capitata Y chromosome by deletion mapping. Genetics 144, 737–745.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Molecular Entomology, The Institute of Physical and Chemical Research (RIKEN) 2-1, Hirosawa, Wako, Saitama, 351-0198, Japan

    Masataka T. Suzuki

Authors
  1. Masataka T. Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Masataka T. Suzuki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suzuki, M.T. Sex determination: insights from the silkworm. J Genet 89, 357–363 (2010). https://doi.org/10.1007/s12041-010-0047-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12041-010-0047-5

Keywords

Search

Navigation