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Gene Review

fru  -  fruitless

Drosophila melanogaster

Synonyms: BTB-VI, BtbVI, CG14307, CG7688, CG7689, ...
 
 
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Disease relevance of fru

  • The MOL is shown to be dispensable for fertility and is therefore not the causative factor of fru-induced behavioral sterility [1].
  • Mutations in the tra target gene fruitless (fru), which is expressed in the antennal lobe as well as the suboesophageal ganglion (the gustatory inputs are processed here), also induce homosexual courtship in males [2].
  • The fruitless (fru) courtship mutant was dissected into three defects of male reproductive behavior, which were separable as to their genetic etiologies by application of existing and newly induced chromosomal aberrations. fru itself is a small inversion [In(3R) 90C; 91B] on genetic and cytological criteria [3].
 

Psychiatry related information on fru

  • This gene is known to influence courtship steps prior to mating, due to the absence of attempted copulation in the behavioral repertoire of most types of fru-mutant males [4].
 

High impact information on fru

  • Thus, we show that fru and dsx together act as a 'switch' system regulating behavior in the context of other developmental genes, such as retn [5].
  • The phenotypes of new fru mutants encompass nearly all aspects of male sexual behavior [6].
  • Sexual orientation and courtship behavior in Drosophila are regulated by fruitless (fru), the first gene in a branch of the sex-determination hierarchy functioning specifically in the central nervous system (CNS) [6].
  • Alternative splicing of fru transcripts produces sex-specific proteins belonging to the BTB-ZF family of transcriptional regulators [6].
  • A loss-of-function mutation in the takeout gene reduces male courtship and synergizes with fruitless mutations, suggesting that takeout plays a redundant role with other fru-dependent factors involved in male mating behavior [7].
 

Biological context of fru

  • It does this through sex-specific alternative splicing of the fru pre-mRNA, leading to the production of male-specific fru mRNAs capable of expressing male-specific fru proteins [8].
  • A female-specific mRNA from the fru locus has a putative Transformer (Tra) binding site in its 5' untranslated region, suggesting that fru is a direct target of Tra [9].
  • In Drosophila melanogaster, somatic sexual differentiation is regulated by a well characterized genetic hierarchy, by which the ratio of X chromosomes to autosomes (X:A) ultimately directs the deployment of sex-specific transcription factors encoded by doublesex (dsx) and fruitless (fru) [10].
  • In addition to the altered sexual orientation, the fru mutants displayed a range of defects in the formation of a male-specific muscle, the muscle of Lawrence [11].
  • Subsequent analyses revealed that all of these insertions were located at the same chromosomal division, 91B, where one of the inversion breakpoints responsible for the bisexual phenotype of the fruitless (fru) mutant has been mapped [11].
 

Anatomical context of fru

  • Finally, we describe Gal4 expression in neurites innervating male reproductive structures that are hypothesized to be targets of fru function [12].
  • Here we identify a subset of fru-expressing interneurons in the brain that show marked sexual dimorphism in their number and projection pattern [13].
  • Expression of fru in the nervous system specifies male sexual behavior and the muscle of Lawrence (MOL), an abdominal muscle that develops in males but not in females [14].
 

Associations of fru with chemical compounds

  • The s-Abg neurons and the proximal extents of their axons were unstained or absent in wild-type females and exhibited subnormal or no 5-HT immunoreactivity in certain fru-mutant males, indicating that fruitless controls the formation of these cells or 5-HT production in them [15].
 

Other interactions of fru

  • This rapid divergence contrasts with the apparently deep conservation of dsx, which in Drosophila controls virtually all aspects of somatic sex except for male courtship behavior (which is controlled by fru) [10].
  • The fru transcripts encode a set of proteins similar to the BTB (Bric à brac, Tramtrack and Broad-complex)-Zn finger family of transcription factors [9].
  • For fru, a social component is involved in the head-interaction phenotype, while increasing age is a modifying factor for the behavior of dsf males [16].
  • fruitless gene is required to maintain neuronal identity in evenskipped-expressing neurons in the embryonic CNS of Drosophila [17].
  • In this regard, certain mutant males that do not transfer SP nevertheless are able to transfer sperm: a fru-mated female possessing no GFP who was not fecund initially could produce progeny when seminal-fluid proteins were subsequently supplied by mating with a male that was spermless owing to the effects of a tudor mutation [18].
 

Analytical, diagnostic and therapeutic context of fru

  • Molecular cloning and analyses of the genomic and complementary DNAs indicated that transcription of the fru locus yields several different transcripts, one of which encodes a putative transcription regulator with a BTB domain and two zinc finger motifs [11].
  • Genetic dissection of the locus has shown that one of the fru gene's promoter, P1, controls the spatial and temporal expression of male-specific FruM proteins critical to determining stereotypical male sexual behavior [12].
  • In situ hybridization revealed no alterations in the locations of cells expressing the P1-fru-promoter-derived transcripts in fru(2), fru(3), fru(4), and fru(sat) pharate adults [19].
  • To further an understanding of this gene's behavioral role, we examined the central nervous system (CNS) for temporal, spatial, and sexually dimorphic expression patterns of sex-specific fru products by in situ hybridization and immunohistochemistry [20].

References

  1. Elements of the fruitless locus regulate development of the muscle of Lawrence, a male-specific structure in the abdomen of Drosophila melanogaster adults. Gailey, D.A., Taylor, B.J., Hall, J.C. Development (1991) [Pubmed]
  2. Sexual behavior mutants revisited: molecular and cellular basis of Drosophila mating. Yamamoto, D., Nakano, Y. Cell. Mol. Life Sci. (1999) [Pubmed]
  3. Behavior and cytogenetics of fruitless in Drosophila melanogaster: different courtship defects caused by separate, closely linked lesions. Gailey, D.A., Hall, J.C. Genetics (1989) [Pubmed]
  4. New reproductive anomalies in fruitless-mutant Drosophila males: extreme lengthening of mating durations and infertility correlated with defective serotonergic innervation of reproductive organs. Lee, G., Villella, A., Taylor, B.J., Hall, J.C. J. Neurobiol. (2001) [Pubmed]
  5. A double-switch system regulates male courtship behavior in male and female Drosophila melanogaster. Shirangi, T.R., Taylor, B.J., McKeown, M. Nat. Genet. (2006) [Pubmed]
  6. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Ryner, L.C., Goodwin, S.F., Castrillon, D.H., Anand, A., Villella, A., Baker, B.S., Hall, J.C., Taylor, B.J., Wasserman, S.A. Cell (1996) [Pubmed]
  7. The Drosophila takeout gene is regulated by the somatic sex-determination pathway and affects male courtship behavior. Dauwalder, B., Tsujimoto, S., Moss, J., Mattox, W. Genes Dev. (2002) [Pubmed]
  8. Regulation of sex-specific selection of fruitless 5' splice sites by transformer and transformer-2. Heinrichs, V., Ryner, L.C., Baker, B.S. Mol. Cell. Biol. (1998) [Pubmed]
  9. From behavior to development: genes for sexual behavior define the neuronal sexual switch in Drosophila. Yamamoto, D., Fujitani, K., Usui, K., Ito, H., Nakano, Y. Mech. Dev. (1998) [Pubmed]
  10. Functional conservation and divergence of intersex, a gene required for female differentiation in Drosophila melanogaster. Siegal, M.L., Baker, B.S. Dev. Genes Evol. (2005) [Pubmed]
  11. Genetic dissection of sexual orientation: behavioral, cellular, and molecular approaches in Drosophila melanogaster. Yamamoto, D., Ito, H., Fujitani, K. Neurosci. Res. (1996) [Pubmed]
  12. Characterization of Drosophila fruitless-gal4 transgenes reveals expression in male-specific fruitless neurons and innervation of male reproductive structures. Billeter, J.C., Goodwin, S.F. J. Comp. Neurol. (2004) [Pubmed]
  13. Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain. Kimura, K., Ote, M., Tazawa, T., Yamamoto, D. Nature (2005) [Pubmed]
  14. Functional conservation of the fruitless male sex-determination gene across 250 Myr of insect evolution. Gailey, D.A., Billeter, J.C., Liu, J.H., Bauzon, F., Allendorfer, J.B., Goodwin, S.F. Mol. Biol. Evol. (2006) [Pubmed]
  15. Abnormalities of male-specific FRU protein and serotonin expression in the CNS of fruitless mutants in Drosophila. Lee, G., Hall, J.C. J. Neurosci. (2001) [Pubmed]
  16. A newly uncovered phenotype associated with the fruitless gene of Drosophila melanogaster: aggression-like head interactions between mutant males. Lee, G., Hall, J.C. Behav. Genet. (2000) [Pubmed]
  17. fruitless gene is required to maintain neuronal identity in evenskipped-expressing neurons in the embryonic CNS of Drosophila. Song, H.J., Taylor, B.J. J. Neurobiol. (2003) [Pubmed]
  18. Defective transfer of seminal-fluid materials during matings of semi-fertile fruitless mutants in Drosophila. Villella, A., Peyre, J.B., Aigaki, T., Hall, J.C. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. (2006) [Pubmed]
  19. Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Goodwin, S.F., Taylor, B.J., Villella, A., Foss, M., Ryner, L.C., Baker, B.S., Hall, J.C. Genetics (2000) [Pubmed]
  20. Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. Lee, G., Foss, M., Goodwin, S.F., Carlo, T., Taylor, B.J., Hall, J.C. J. Neurobiol. (2000) [Pubmed]
 
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