Analysis of the Doublesex female protein in Drosophila melanogaster: role in sexual differentiation and behavior and dependence on intersex

doublesex (dsx) is unusual among the known sex-determination genes of Drosophila melanogaster in that functional homologs are found in distantly related species. In flies, dsx occupies a position near the bottom of the sex determination hierarchy. It is expressed in male- and female-specific forms a...

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Published inGenetics (Austin) Vol. 152; no. 4; pp. 1653 - 1667
Main Authors Waterbury, J.A, Jackson, L.L, Schedl, P
Format Journal Article
LanguageEnglish
Published United States Genetics Soc America 01.08.1999
Genetics Society of America
Subjects
animal proteins
Animals
Animals, Genetically Modified
copulation
courtship behavior
Disorders of Sex Development - genetics
DNA-Binding Proteins - genetics
DNA-Binding Proteins - physiology
Drosophila melanogaster
Drosophila melanogaster - genetics
Drosophila Proteins
dsx gene
dsx protein
Egg Proteins - biosynthesis
Egg Proteins - genetics
egg yolk
enhancer sequences
Female
females
feminization
gene dosage
Gene Expression Regulation, Developmental - genetics
genes
genetic regulation
Genetics
Insect Proteins - genetics
Insect Proteins - physiology
intersexuality
Male
males
mating behavior
messenger RNA
Molecular biology
Pheromones - biosynthesis
Pheromones - genetics
Proteins
secondary sexual traits
Sex Characteristics
sex combs
Sex Differentiation - genetics
Sexes
Sexual Behavior, Animal
sexual development
transcription (genetics)
transcription factors
Transgenes
Vitellogenins - biosynthesis
Vitellogenins - genetics
yp gene
Online AccessGet full text

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Abstract doublesex (dsx) is unusual among the known sex-determination genes of Drosophila melanogaster in that functional homologs are found in distantly related species. In flies, dsx occupies a position near the bottom of the sex determination hierarchy. It is expressed in male- and female-specific forms and these proteins function as sex-specific transcription factors. In the studies reported here, we have ectopically expressed the female Dsx protein (Dsx(F)) from a constitutive promoter and examined its regulatory activities independent of other upstream factors involved in female sex determination. We show that it functions as a positive regulator of female differentiation and a negative regulator of male differentiation. As predicted by the DNA-binding properties of the Dsx protein, Dsx(F) and Dsx(M) compete with each other for the regulation of target genes. In addition to directing sex-specific differentiation, Dsx(F) plays an important role in sexual behavior. Wild-type males ectopically expressing Dsx(F) are actively courted by other males. This acquisition of feminine sex appeal is likely due to the induction of female pheromones by Dsx(F). More extreme behavioral abnormalities are observed when Dsx(F) is ectopically expressed in dsx(-) XY animals; these animals are not only courted by, but also copulate with, wild-type males. Finally, we provide evidence that intersex is required for the feminizing activities of Dsx(F) and that it is not regulated by the sex-specific splicing cascade.
AbstractList doublesex (dsx) is unusual among the known sex-determination genes of Drosophila melanogaster in that functional homologs are found in distantly related species. In flies, dsx occupies a position near the bottom of the sex determination hierarchy. It is expressed in male- and female-specific forms and these proteins function as sex-specific transcription factors. In the studies reported here, we have ectopically expressed the female Dsx protein (Dsx(F)) from a constitutive promoter and examined its regulatory activities independent of other upstream factors involved in female sex determination. We show that it functions as a positive regulator of female differentiation and a negative regulator of male differentiation. As predicted by the DNA-binding properties of the Dsx protein, Dsx(F) and Dsx(M) compete with each other for the regulation of target genes. In addition to directing sex-specific differentiation, Dsx(F) plays an important role in sexual behavior. Wild-type males ectopically expressing Dsx(F) are actively courted by other males. This acquisition of feminine sex appeal is likely due to the induction of female pheromones by Dsx(F). More extreme behavioral abnormalities are observed when Dsx(F) is ectopically expressed in dsx(-) XY animals; these animals are not only courted by, but also copulate with, wild-type males. Finally, we provide evidence that intersex is required for the feminizing activities of Dsx(F) and that it is not regulated by the sex-specific splicing cascade.
doublesex (dsx) is unusual among the known sex-determination genes of Drosophila melanogaster in that functional homologs are found in distantly related species. In flies, dsx occupies a position near the bottom of the sex determination hierarchy. It is expressed in male- and female-specific forms and these proteins function as sex-specific transcription factors. In the studies reported here, we have ectopically expressed the female Dsx protein (Dsx super(F)) from a constitutive promoter and examined its regulatory activities independent of other upstream factors involved in female sex determination. We show that it functions as a positive regulator of female differentiation and a negative regulator of male differentiation. As predicted by the DNA-binding properties of the Dsx protein, Dsx super(F) and Dsx super(M) compete with each other for the regulation of target genes. In addition to directing sex-specific differentiation, Dsx super(F) plays an important role in sexual behavior. Wild- type males ectopically expressing Dsx super(F) are actively courted by other males. This acquisition of feminine sex appeal is likely due to the induction of female pheromones by Dsx super(F). More extreme behavioral abnormalities are observed when Dsx super(F) is ectopically expressed in dsx- XY animals; these animals are not only courted by, but also copulate with, wild-type males. Finally, we provide evidence that intersex is required for the feminizing activities of Dsx super(F) and that it is not regulated by the sex-specific splicing cascade.
Abstract doublesex (dsx) is unusual among the known sex-determination genes of Drosophila melanogaster in that functional homologs are found in distantly related species. In flies, dsx occupies a position near the bottom of the sex determination hierarchy. It is expressed in male- and female-specific forms and these proteins function as sex-specific transcription factors. In the studies reported here, we have ectopically expressed the female Dsx protein (DsxF) from a constitutive promoter and examined its regulatory activities independent of other upstream factors involved in female sex determination. We show that it functions as a positive regulator of female differentiation and a negative regulator of male differentiation. As predicted by the DNA-binding properties of the Dsx protein, DsxF and DsxM compete with each other for the regulation of target genes. In addition to directing sex-specific differentiation, DsxF plays an important role in sexual behavior. Wild-type males ectopically expressing DsxF are actively courted by other males. This acquisition of feminine sex appeal is likely due to the induction of female pheromones by DsxF. More extreme behavioral abnormalities are observed when DsxF is ectopically expressed in dsx- XY animals; these animals are not only courted by, but also copulate with, wild-type males. Finally, we provide evidence that intersex is required for the feminizing activities of DsxF and that it is not regulated by the sex-specific splicing cascade.
Author Jackson, L.L
Waterbury, J.A
Schedl, P
AuthorAffiliation Department of Molecular Biology, Princeton University, Princeton, New Jersey, 08544, USA
AuthorAffiliation_xml – name: Department of Molecular Biology, Princeton University, Princeton, New Jersey, 08544, USA
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/10430590$$D View this record in MEDLINE/PubMed
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  ident: 2022011809362536800_R40
  article-title: Female pheromones in Drosophila melanogaster are controlled by the doublesex locus
  publication-title: Genet. Res.
  doi: 10.1017/S0016672300023892
  contributor:
    fullname: Jallon
– volume: 123
  start-page: 535
  year: 1989
  ident: 2022011809362536800_R57
  article-title: Regulation of behavioral and pheromonal aspects of sex determination in Drosophila melanogaster by the Sex-lethal gene
  publication-title: Genetics
  doi: 10.1093/genetics/123.3.535
  contributor:
    fullname: Tompkins
– volume: 56
  start-page: 997
  year: 1989
  ident: 2022011809362536800_R12
  article-title: Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides
  publication-title: Cell
  doi: 10.1016/0092-8674(89)90633-8
  contributor:
    fullname: Burtis
– volume: 139
  start-page: 1649
  year: 1995
  ident: 2022011809362536800_R16
  article-title: A genetic analysis of intersex, a gene regulating sexual differentiation in Drosophila melanogaster females
  publication-title: Genetics
  doi: 10.1093/genetics/139.4.1649
  contributor:
    fullname: Chase
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Snippet doublesex (dsx) is unusual among the known sex-determination genes of Drosophila melanogaster in that functional homologs are found in distantly related...
Abstract doublesex (dsx) is unusual among the known sex-determination genes of Drosophila melanogaster in that functional homologs are found in distantly...
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StartPage 1653
SubjectTerms animal proteins
Animals
Animals, Genetically Modified
copulation
courtship behavior
Disorders of Sex Development - genetics
DNA-Binding Proteins - genetics
DNA-Binding Proteins - physiology
Drosophila melanogaster
Drosophila melanogaster - genetics
Drosophila Proteins
dsx gene
dsx protein
Egg Proteins - biosynthesis
Egg Proteins - genetics
egg yolk
enhancer sequences
Female
females
feminization
gene dosage
Gene Expression Regulation, Developmental - genetics
genes
genetic regulation
Genetics
Insect Proteins - genetics
Insect Proteins - physiology
intersexuality
Male
males
mating behavior
messenger RNA
Molecular biology
Pheromones - biosynthesis
Pheromones - genetics
Proteins
secondary sexual traits
Sex Characteristics
sex combs
Sex Differentiation - genetics
Sexes
Sexual Behavior, Animal
sexual development
transcription (genetics)
transcription factors
Transgenes
Vitellogenins - biosynthesis
Vitellogenins - genetics
yp gene
Title Analysis of the Doublesex female protein in Drosophila melanogaster: role in sexual differentiation and behavior and dependence on intersex
URI http://www.genetics.org/cgi/content/abstract/152/4/1653
https://www.ncbi.nlm.nih.gov/pubmed/10430590
https://www.proquest.com/docview/214124019
https://search.proquest.com/docview/17269350
https://search.proquest.com/docview/69935811
https://pubmed.ncbi.nlm.nih.gov/PMC1460680
Volume 152
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