Advertisement
JOURNAL ARTICLES
Structure, function and evolution of sex-determining systems in Dipteran insects
C. Schutt, R. Nothiger
Development 2000 127: 667-677;

Summary

Nature has evolved an astonishing variety of genetic and epigenetic sex-determining systems which all achieve the same result, the generation of two sexes. Genetic and molecular analyses, mainly performed during the last 20 years, have gradually revealed the mechanisms that govern sexual differentiation in a few model organisms. In this review, we will introduce the sex-determining system of Drosophila and compare the fruitfly to the housefly Musca domestica and other Dipteran insects. Despite the ostensible variety, all these insects use the same basic strategy: a primary genetic signal that is different in males and females, a key gene that responds to the primary signal, and a double-switch gene that eventually selects between two alternative sexual programmes. These parallels, however, do not extend to the molecular level. Except for the double-switch gene doublesex at the end of the cascade, no functional homologies were found between more distantly related insects. In particular, Sex-lethal, the key gene that controls sexual differentiation in Drosophila, does not have a sex-determining function in any other genus studied so far. These results show that sex-determining cascades, in comparison to other regulatory pathways, evolve much more rapidly.

REFERENCES

    1. Albrecht E. B.,
    2. Salz H. K.
    (1993) The Drosophila sex determination gene snf is utilized for the establishment of the female-specific splicing pattern of Sex-lethal. Genetics 134, 801–807
    OpenUrlAbstract/FREE Full Text
    1. Amrein H.,
    2. Gorman M.,
    3. Nöthiger R.
    (1988) The sex-determining gene tra-2 of Drosophila encodes a putative RNA binding protein. Cell 55, 1025–1035
    OpenUrlCrossRefPubMedWeb of Science
    1. An W.,
    2. Wensink P. C.
    (1995) Integrating sex-and tissue-specific regulation within a single Drosophila enhancer. Genes Dev 9, 256–266
    OpenUrlAbstract/FREE Full Text
    1. Baker B. S.,
    2. Ridge K. A.
    (1980) Sex and the single cell. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics 94, 383–423
    OpenUrlAbstract/FREE Full Text
    1. Barbash D. A.,
    2. Cline T. W.
    (1995) Genetic and molecular analysis of the autosomal component of the primary sex determination signal of Drosophila melanogaster. Genetics 141, 1451–1471
    OpenUrlAbstract/FREE Full Text
    1. Bashaw G. J.,
    2. Baker B. S.
    (1995) The msl-2 dosage compensation gene of Drosophila encodes a putative DNA-binding protein whose expression is sex-specifically regulated by Sex-lethal. Development 121, 3245–3258
    OpenUrlAbstract
    1. Bashaw G. J.,
    2. Baker B. S.
    (1997) The regulation of the Drosophilamsl-2 gene reveals a function for Sex-lethal in translational control. Cell 89, 789–798
    OpenUrlCrossRefPubMedWeb of Science
    1. Bell L. R.,
    2. Maine E. M.,
    3. Schedl P.,
    4. Cline T. W.
    (1988) Sex-lethal, a Drosophila sex determination switch gene, exhibits sex-specific RNA splicing and sequence similarity to RNA binding proteins. Cell 55, 1037–1046
    OpenUrlCrossRefPubMedWeb of Science
    1. Bell L. R.,
    2. Horabin J. I.,
    3. Schedl P.,
    4. Cline T. W.
    (1991) Positive autoregulation of Sex-lethal by alternative splicing maintains the female determined state in Drosophila. Cell 65, 229–239
    OpenUrlCrossRefPubMedWeb of Science
    1. Belote J. M.,
    2. Baker B. S.
    (1982) Sex determination in Drosophila melanogaster: Analysis of transformer-2, a sex-transforming locus. Proc. Natl. Acad. Sci. USA 79, 1568–1572
    OpenUrlAbstract/FREE Full Text
    1. Belote J. M.,
    2. Handler A. M.,
    3. Wolfner M. F.,
    4. Livak K. L.,
    5. Baker B. S.
    (1985) Sex specific regulation of yolk protein gene expression in Drosophila. Cell 40, 339–348
    OpenUrlCrossRefPubMedWeb of Science
    1. Bernstein M.,
    2. Cline T. W.
    (1994) Differential effects of Sex-lethal mutations on dosage compensation early in Drosophila development. Genetics 136, 1051–1061
    OpenUrlAbstract/FREE Full Text
    1. Bone J. R.,
    2. Lavender J.,
    3. Richman R.,
    4. Palmer M. J.,
    5. Turner B. M.,
    6. Kuroda M. I.
    (1994) Acetylated histone H4 on the male X chromosome is associated with dosage compensation in Drosophila. Genes Dev 8, 96–104
    OpenUrlAbstract/FREE Full Text
    1. Bopp D.,
    2. Bell L. R.,
    3. Cline T. W.,
    4. Schedl P.
    (1991) Developmental distribution of female-specific Sex-lethal proteins in Drosophila melanogaster. Genes Dev 5, 403–415
    OpenUrlAbstract/FREE Full Text
    1. Bopp D.,
    2. Horabin J. I.,
    3. Lersch R. A.,
    4. Cline T. W.,
    5. Schedl P.
    (1993) Expression of the Sex-lethal gene is controlled at multiple levels during Drosophila oogenesis. Development 118, 797–812
    OpenUrlAbstract
    1. Bopp D.,
    2. Calhoun G.,
    3. Horabin J. I.,
    4. Samuels M.,
    5. Schedl P.
    (1996) Sex-specific control of Sex-lethal is a conserved mechanism for sex determination in the genus Drosophila. Development 122, 971–982
    OpenUrlAbstract
    1. Bopp D.,
    2. Schutt C.,
    3. Puro J.,
    4. Huang H.,
    5. Nöthiger R.
    (1999) Recombination and disjunction in female germ cells of Drosophila depend on the germline activity of the gene Sex-lethal. Development 126, 5785–5794
    OpenUrlAbstract
    1. Bownes M.,
    2. Steinmann-Zwicky M.,
    3. Nöthiger R.
    (1990) Differential control of yolk protein gene expression in fat bodies and gonads by the sex-determining gene tra-2 of Drosophila. EMBO J 9, 3975–3980
    OpenUrlPubMed
    1. Burtis K. C.,
    2. Baker B. S.
    (1989) Drosophiladoublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56, 997–1010
    OpenUrlCrossRefPubMedWeb of Science
    1. Cabrera C. V.,
    2. Alonso M. C.
    (1991) Transcriptional activation by heterodimers of the achaete-scute and daughterless gene products of Drosophila. EMBO J 10, 2965–2973
    OpenUrlPubMedWeb of Science
    1. Chandler D.,
    2. McGuffin M. E.,
    3. Piskur J.,
    4. Yao J.,
    5. Baker B. S.,
    6. Mattox W.
    (1997) Evolutionary conservation of regulatory strategies for the sex determination factor transformer-2. Mol. Cell. Biol 17, 2908–2919
    OpenUrlAbstract/FREE Full Text
    1. Chase B. A.,
    2. Baker B. S.
    (1995) A genetic analysis of intersex, a gene regulating sexual differeniation in Drosophila melanogaster females. Genetics 139, 1649–1661
    OpenUrlAbstract/FREE Full Text
    1. Cho S.,
    2. Wensink P. C.
    (1997) DNA binding by the male and female doublesex proteins of Drosophila melanogaster. J. Biol. Chem 272, 3185–3189
    OpenUrlAbstract/FREE Full Text
    1. Cho S.,
    2. Wensink P. C.
    (1998) Linkage between oligomerization and DNA binding in Drosophiladoublesex proteins. Biochemistry 37, 11301–11308
    OpenUrlCrossRefPubMedWeb of Science
    1. Cline T. W.
    (1988) Evidence that sisterless-a and sisterless-b are two of several discrete “numerator elements” of the X/A sex determination signal in Drosophila that switch Sxl between two alternative stable expression states. Genetics 119, 829–862
    OpenUrlAbstract/FREE Full Text
    1. Cline T. W.
    (1993) The Drosophila sex determination signal: how do flies count to two?. Trends Genet 9, 385–390
    OpenUrlCrossRefPubMedWeb of Science
    1. Cline T. W.,
    2. Meyer B. J.
    (1996) Vive la difference: males vs females in flies vs worms. Annu. Rev. Genet 30, 637–702
    OpenUrlCrossRefPubMedWeb of Science
    1. Coschigano K. T.,
    2. Wensink P. C.
    (1993) Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila. Genes Dev 7, 42–54
    OpenUrlAbstract/FREE Full Text
    1. Cronmiller C.,
    2. Schedl P.,
    3. Cline T. W.
    (1988) Molecular characterization of daughterless, a Drosophila sex determination gene with multiple roles in development. Genes Dev 2, 1666–1676
    OpenUrlAbstract/FREE Full Text
    1. Dauwalder B.,
    2. Amaya-Manzanares F.,
    3. Mattox W.
    (1996) A human homologue of the Drosophila sex determination factor transformer-2 has conserved splicing regulatory functions. Proc. Natl. Acad. Sci. USA 93, 9004–9009
    OpenUrlAbstract/FREE Full Text
    1. Deshpande G.,
    2. Stukey J.,
    3. Schedl P.
    (1995) scute (sis-b) function in Drosophila sex determination. Mol. Cell Biol 15, 4430–4440
    OpenUrlAbstract/FREE Full Text
    1. Deshpande G.,
    2. Samuels M. E.,
    3. Schedl P.
    (1996) Sex-lethal interacts with splicing factors in vitro and in vivo. Mol. Cell Biol 16, 5036–5047
    OpenUrlAbstract/FREE Full Text
    1. Duffy J. B.,
    2. Gergen J. P.
    (1991) The Drosophila segmentation gene runt acts as a position-specific numerator element necessary for the uniform expression of the sex-determining gene Sex-lethal. Genes Dev 5, 2176–2187
    OpenUrlAbstract/FREE Full Text
    1. Erickson J. W.,
    2. Cline T. W.
    (1993) A bZIP protein, sisterless-a, collaborates with bHLH transcription factors early in Drosophila development to determine sex. Genes Dev 7, 1688–1702
    OpenUrlAbstract/FREE Full Text
    1. Estes P. A.,
    2. Keyes L. N.,
    3. Schedl P.
    (1995) Multiple response elements in the Sex-lethal early promoter ensure its female-specific expression pattern. Mol. Cell. Biol 15, 904–917
    OpenUrlAbstract/FREE Full Text
    1. Finley K. D.,
    2. Taylor B. J.,
    3. Milstein M.,
    4. McKeown M.
    (1997) dissatisfaction, a gene involved in sex-specific behavior and neural development of Drosophila. Genetics 94, 913–918
    OpenUrl
    1. Flickinger T. W.,
    2. Salz H. K.
    (1994) The Drosophila sex determination gene snf encodes a nuclear protein with sequence and functional similarity to the mammalian U1A snRNP protein. Genes Dev 8, 914–925
    OpenUrlAbstract/FREE Full Text
    1. Granadino B.,
    2. Juán A. S.,
    3. Santamaria P.,
    4. Sánchez L.
    (1992) Evidence of a dual function in fl(2)d, a gene needed for Sex-lethal expression in Drosophila melanogaster. Genetics 130, 597–612
    OpenUrlAbstract/FREE Full Text
    1. Hager J. H.,
    2. Cline T. W.
    (1997) Induction of female Sex-lethal RNA splicing in male germ cells: implications for Drosophila germline sex determination. Development 124, 5033–5048
    OpenUrlAbstract
    1. Hilfiker A.,
    2. Amrein H.,
    3. Dubendorfer A.,
    4. Schneiter R.,
    5. Nöthiger R.
    (1995) The gene virilizer is required for female-specific splicing controlled by Sxl, the master gene for sexual development in Drosophila. Development 121, 4017–4026
    OpenUrlAbstract
    1. Hilfiker-Kleiner D.,
    2. Dubendorfer A.,
    3. Hilfiker A.,
    4. Nöthiger R.
    (1994) Genetic control of sex determination in the germ line and soma of the housefly, Musca domestica. Development 120, 2531–2538
    OpenUrlAbstract/FREE Full Text
    1. Hinson S.,
    2. Nagoshi R. N.
    (1999) Regulatory and functional interactions between the somatic sex regulatory gene transformer and the germline genes ovo and ovarian tumor. Development 126, 861–871
    OpenUrlAbstract
    1. Hodgkin J.
    (1990) Sex determination compared in Drosophila and Caenorhabditis. Nature 344, 721–728
    OpenUrlCrossRefPubMed
    1. Horabin J. I.,
    2. Schedl P.
    (1993) Regulated splicing of the Drosophila Sex-lethal male exon involves a blockage mechanism. Mol. Cell. Biol 13, 1408–1414
    OpenUrlAbstract/FREE Full Text
    1. Hoshijima K.,
    2. Inoue K.,
    3. Higuchi I.,
    4. Sakamoto H.,
    5. Shimura Y.
    (1991) Control of doublesex alternative splicing by transformer and transformer-2 in Drosophila. Science 252, 833–836
    OpenUrlAbstract/FREE Full Text
    1. Hoshijima K.,
    2. Kohyama A.,
    3. Watakabe I.,
    4. Inoue K.,
    5. Sakamoto H.,
    6. Shimura Y.
    (1995) Transcriptional regulation of the Sex-lethal gene by helix-loop-helix proteins. Nucleic Acids Res 23, 3441–3448
    OpenUrlAbstract/FREE Full Text
    1. Kelley R. L.,
    2. Solovyeva I.,
    3. Lyman L. M.,
    4. Richman R.,
    5. Solovyev V.,
    6. Kuroda M. I.
    (1995) Expression of msl-2 causes assembly of dosage compensation regulators on the X chromosomes and female lethality in Drosophila. Cell 81, 867–877
    OpenUrlCrossRefPubMedWeb of Science
    1. Kelley R. L.,
    2. Wang J.,
    3. Bell L.,
    4. Kuroda M. I.
    (1997) Sex lethal controls dosage compensation in Drosophila by a non-splicing mechanism. Nature 387, 195–199
    OpenUrlCrossRefPubMed
    1. Keyes L. N.,
    2. Cline T. W.,
    3. Schedl P.
    (1992) The primary sex determination signal of Drosophila acts at the level of transcription. Cell 68, 933–943
    OpenUrlCrossRefPubMedWeb of Science
    1. Kramer S. G.,
    2. Timothy M. J.,
    3. Schedl P.,
    4. Gergen J. P.
    (1999) Direct activation of Sex-lethal transcription by the Drosophila Runt protein. Development 126, 191–200
    OpenUrlAbstract
    1. Lopez A. J.
    (1998) Alternative splicing of pre-mRNA: Developmental consequences and mechanisms of regulation. Annu. Rev. Genet 32, 279–305
    OpenUrlCrossRefPubMedWeb of Science
    1. Loukeris T. G.,
    2. Livadaras I.,
    3. Arcà B.,
    4. Zabalou S.,
    5. Savakis C.
    (1995) Gene transfer into the Medfly, Ceratitis capitata with a Drosophilahydei transposable element. Science 270, 2002–2005
    OpenUrlAbstract/FREE Full Text
    1. Lucchesi J. C.
    (1996) Dosage compensation in Drosophila and the ‘complex’ world of transcriptional regulation. BioEssays 18, 541–547
    OpenUrlCrossRefPubMedWeb of Science
    1. Marín I.,
    2. Baker B. S.
    (1998) The evolutionary dynamics of sex determination. Science 281, 1990–1994
    OpenUrlAbstract/FREE Full Text
    1. Meise M.,
    2. Hilfiker-Kleiner D.,
    3. Dubendorfer A.,
    4. Brunner C.,
    5. Nöthiger R.,
    6. Bopp D.
    (1998) Sex-lethal, the master sex-determining gene in Drosophila, is not sex-specifically regulated in Musca domestica. Development 125, 1487–1494
    OpenUrlAbstract
    1. Misquitta L.,
    2. Paterson B. M.
    (1999) Targeted disruption of gene function in Drosophila by RNA interference (RNA-i): A role for nautilus in embryonic somatic muscle formation. Proc. Natl. Acad. Sci. USA 96, 1451–1456
    OpenUrlAbstract/FREE Full Text
    1. Mori L.,
    2. Perondini A. L. P.
    (1980) Errors in the elimination of X chromosomes in Sciara ocellaris. Genetics 94, 663–673
    OpenUrlAbstract/FREE Full Text
    1. Muller-Holtkamp F.
    (1995) The Sex-lethal gene homologue in Chrysomya rufifacies is highly conserved in sequence and exon-intron organization. J. Mol. Evol 41, 467–477
    OpenUrlCrossRefPubMedWeb of Science
    1. Nöthiger R.,
    2. Steinmann-Zwicky M.
    (1985) Sex determination in Drosophila. Trends Genet 1, 209–215
    1. Nöthiger R.,
    2. Steinmann-Zwicky M.
    (1992) Genetic control of sex determination. Semin. Dev. Biol. 3
    1. Oliver B.,
    2. Kim Y.-J.,
    3. Baker B. S.
    (1993). Sex-lethal, master and slave: a hierarchy of germ-line sex determination in Drosophila. Development 119, 897–908
    OpenUrlAbstract/FREE Full Text
    1. O'Neil M. T.,
    2. Belote J. M.
    (1992) Interspecific comparison of the transformer gene of Drosophila reveals an unusually high degree of evolutionary divergence. Genetics 131, 113–128
    OpenUrlCrossRefPubMedWeb of Science
    1. Parkhurst S. M.,
    2. Bopp D.,
    3. Ish-Horowicz D.
    (1990) X:A ratio, the primary sex-determining signal in Drosophila, is transduced by helix-loop-helix proteins. Cell 63, 1179–1191
    1. Parkhurst S. M.,
    2. Ish-Horowicz D.
    (1992) Common denominators for sex. Curr. Biol 2, 629–631
    OpenUrlCrossRefPubMedWeb of Science
    1. Paroush Z.,
    2. Finley R. L.,
    3. Kidd T.,
    4. Wainwright S. M.,
    5. Ingham P. W.,
    6. Brent R.,
    7. Ish-Horowicz D.
    (1994) groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy -related bHLH proteins. Cell 79, 805–815
    OpenUrlAbstract
    1. Pauli D.,
    2. Oliver B.,
    3. Mahowald A. P.
    (1993) The role of the ovarian tumor locus in Drosophila melanogaster germ line sex determination. Development 119, 123–134
    OpenUrlAbstract/FREE Full Text
    1. Pultz M. A.,
    2. Carson G. S.,
    3. Baker B. S.
    (1994) A genetic analysis of hermaphrodite, a pleiotropic sex determination gene in Drosophila melanogaster. Genetics 136, 195–207
    OpenUrlAbstract
    1. Pultz M. A.,
    2. Baker B. S.
    (1995) The dual role of hermaphrodite in the Drosophila sex determination regulatory hierarchy. Development 121, 99–111
    OpenUrlCrossRefPubMedWeb of Science
    1. Raymond C. S.,
    2. Shamu C. E.,
    3. Shen M. M.,
    4. Seifert K. J.,
    5. Hirsch B.,
    6. Hodgkin J.,
    7. Zarkower D.
    (1998) Evidence for evolutionary conservation of sex-determining genes. Nature 391, 691–695
    OpenUrlCrossRefPubMedWeb of Science
    1. Ryner L. C.,
    2. Goodwin S. F.,
    3. Castrillon D. H.,
    4. Anand A.,
    5. Villella A.,
    6. Baker B. S.,
    7. Hall J. C.,
    8. Taylor B. J.,
    9. Wasserman S. A.
    (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87, 1079–1089
    OpenUrlAbstract
    1. Saccone G.,
    2. Pelusio I.,
    3. Artiaco D.,
    4. Giordano E.,
    5. Bopp D.,
    6. 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
    OpenUrlAbstract/FREE Full Text
    1. Salz H. K.
    (1992) The genetic analysis of snf: a Drosophila sex determination gene required for activation of Sex-lethal in both the germline and the soma. Genetics 130, 547–554
    OpenUrlAbstract/FREE Full Text
    1. Schmidt R.,
    2. Hediger M.,
    3. Nöthiger R.,
    4. Dubendorfer A.
    (1997) The mutation masculinizer (man) defines a sex-determining gene with maternal and zygotic functions in Musca domestica L. Genetics 145, 173–183
    OpenUrlAbstract/FREE Full Text
    1. Schupbach T.
    (1985) Normal female germ cell differentiation requires the female X chromosome to autosome ratio and expression of Sex-lethal in Drosophila melanogaster. Genetics 109, 529–548
    OpenUrlAbstract
    1. Schutt C.,
    2. Hilfiker A.,
    3. Nöthiger R.
    (1998) virilizer regulates Sex-lethal in the germline of Drosophila melanogaster. Development 125, 1501–1507
    OpenUrlCrossRefPubMedWeb of Science
    1. Shearman D. C. A.,
    2. Frommer M.
    (1998) The Bactrocera tryoni homologue of the Drosophila melanogaster sex-determination gene doublesex. Insect Mol. Biol 7, 1–12
    1. Sievert V.,
    2. Kuhn S.,
    3. Traut W.
    (1997) Expression of the sex-determining cascade genes Sex-lethal and doublesex in the phorid fly Megaselia scalaris. Genome 40, 211–214
    OpenUrlCrossRefPubMedWeb of Science
    1. Sosnowski B. A.,
    2. Belote J. M.,
    3. McKeown M.
    (1989) Sex-specific alternative splicing of RNA from the transformer gene results from sequence-dependent splice site blockage. Cell 58, 449–459
    OpenUrlAbstract
    1. Staab S.,
    2. Heller A.,
    3. Steinmann-Zwicky M.
    (1996) Somatic sex-determining signals act on XX germ cells in Drosophila embryos. Development 122, 4065–4071
    OpenUrlCrossRefPubMedWeb of Science
    1. Steinmann-Zwicky M.,
    2. Schmid H.,
    3. Nöthiger R.
    (1989) Cell-autonomous and inductive signals can determine the sex of the germ line of Drosophila by regulating the gene Sxl. Cell 57, 157–166
    OpenUrlAbstract
    1. Steinmann-Zwicky M.
    (1993) Sex determination in Drosophila: sis-b, a major numerator element of the X:A ratio in the soma, does not contribute to the X:A ratio in the germ line. Development 117, 763–767
    OpenUrlCrossRefPubMedWeb of Science
    1. Steinmann-Zwicky M.
    (1994) Sxl in the germline of Drosophila: a target for somatic late induction. Dev. Genet 15, 265–274
    OpenUrlCrossRefPubMedWeb of Science
    1. Taylor B. J.,
    2. Villella A.,
    3. Ryner L. C.,
    4. Baker B. S.,
    5. Hall J. C.
    (1994) Behavioral and neurobiological implications of sex-determining factors in Drosophila. Dev. Genet 15, 275–296
    OpenUrlCrossRef
    1. Ullerich F.-H.
    (1984) Analysis of sex determination in the monogenic blowfly Chrysomya rufifacies by pole cell transplantation. Mol. Gen. Genet 193, 479–487
    OpenUrlAbstract
    1. Van Doren M.,
    2. Ellis H. M.,
    3. Posakony J. W.
    (1991) The Drosophila extramacrochaetae protein antagonizes sequence-specific DNA binding by daughterless/achaete-scute protein complexes. Development 113, 245–255
    OpenUrlCrossRefPubMedWeb of Science
    1. Wilkins A. S.
    (1995) Moving up the hierarchy: A hypothesis on the evolution of a genetic sex determination pathway. BioEssays 17, 71–77
    OpenUrlAbstract
    1. Yi W.,
    2. Zarkower D.
    (1999) Similarity of DNA binding and transcriptional regulation by Caenorhabditis elegans MAB-3 and Drosophila melanogaster DSX suggests conservation of sex determining mechanisms. Development 126, 873–881
    OpenUrlCrossRefPubMedWeb of Science
    1. Younger-Shepherd S.,
    2. Vaessin H.,
    3. Bier E.,
    4. Jan L. Y.,
    5. Jan Y. N.
    (1992) deadpan, an essential pan-neural gene encoding an HLH protein, acts as a denominator in Drosophila sex determination. Cell 70, 911–922
    OpenUrlPubMedWeb of Science
    1. Zhou S.,
    2. Yang Y.,
    3. Scott M. J.,
    4. Eisen A.,
    5. Koonin E. V.,
    6. Fouts D. L.,
    7. Wrightsman R.,
    8. Manning J. E.,
    9. Lucchesi J. C.
    (1995) Male-specific lethal 2, a dosage compensation gene of Drosophila, undergoes sex-specific regulation and encodes a protein with a RING finger and a metallothionein-like cystein cluster. EMBO J 14, 2884–2895
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Structure, function and evolution of sex-determining systems in Dipteran insects
C. Schutt, R. Nothiger
Development 2000 127: 667-677;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

A new society for regenerative biologists

Kenneth Poss and Elly Tanaka announce the launch of the International Society for Regenerative Biology (ISRB), which will promote research and education in the field of regenerative biology.

Upcoming special issue: call for papers

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

The special issue welcomes Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

An interview with Cagney Coomer

Over a virtual chat, we spoke to Cagney Coomer about her experiences in the lab, the classroom and the community centre, and why she thinks outreach and role models are vital to science.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Here, Michèle Romanos talks about her new preprint, which mixes experimentation in quail embryos and computational modelling to understand how heterogeneity in a tissue influences cell rate.

Save your spot at our next session:

10 March
Time: 9:00 (GMT)
Chaired by: Thomas Lecuit

Join our mailing list to receive news and updates on the series.