Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene.

BACKGROUND: How the central nervous system (CNS) develops to implement innate behaviors remains largely unknown. Drosophila male sexual behavior has long been used as a model to address this question. The male-specific products of fruitless (fru) are pivotal to the emergence of this behavior. These...

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Main Authors: Billeter, J, Villella, A, Allendorfer, J, Dornan, A, Richardson, M, Gailey, D, Goodwin, S
Format: Journal article
Language:English
Published: 2006
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author Billeter, J
Villella, A
Allendorfer, J
Dornan, A
Richardson, M
Gailey, D
Goodwin, S
author_facet Billeter, J
Villella, A
Allendorfer, J
Dornan, A
Richardson, M
Gailey, D
Goodwin, S
author_sort Billeter, J
collection OXFORD
description BACKGROUND: How the central nervous system (CNS) develops to implement innate behaviors remains largely unknown. Drosophila male sexual behavior has long been used as a model to address this question. The male-specific products of fruitless (fru) are pivotal to the emergence of this behavior. These putative transcription factors, containing one of three alternative DNA binding domains, determine the neuronal substrates for sexual behavior in male CNS. RESULTS: We isolated the first fru coding mutation, resulting in complete loss of one isoform. At the neuronal level, this isoform alone controls differentiation of a male-specific muscle and its associated motorneuron. Conversely, a combination of isoforms is required for development of serotonergic neurons implicated in male copulatory behavior. Full development of these neurons requires the male-specific product of doublesex, a gene previously thought to act independently of fru. At the behavioral level, missing one isoform leads to diminished courtship behavior and infertility. We achieved the first rescue of a distinct fru behavioral phenotype, expressing a wild-type isoform in a defined subset of its normal expression pattern. CONCLUSION: This study exemplifies how complex behaviors can be controlled by a single locus through multiple isoforms regulating both developmental and physiological pathways in different neuronal substrates.
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spelling oxford-uuid:26d1ba61-a467-4430-a856-511a888fcf362022-03-26T12:03:19ZIsoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene.Journal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:26d1ba61-a467-4430-a856-511a888fcf36EnglishSymplectic Elements at Oxford2006Billeter, JVillella, AAllendorfer, JDornan, ARichardson, MGailey, DGoodwin, S BACKGROUND: How the central nervous system (CNS) develops to implement innate behaviors remains largely unknown. Drosophila male sexual behavior has long been used as a model to address this question. The male-specific products of fruitless (fru) are pivotal to the emergence of this behavior. These putative transcription factors, containing one of three alternative DNA binding domains, determine the neuronal substrates for sexual behavior in male CNS. RESULTS: We isolated the first fru coding mutation, resulting in complete loss of one isoform. At the neuronal level, this isoform alone controls differentiation of a male-specific muscle and its associated motorneuron. Conversely, a combination of isoforms is required for development of serotonergic neurons implicated in male copulatory behavior. Full development of these neurons requires the male-specific product of doublesex, a gene previously thought to act independently of fru. At the behavioral level, missing one isoform leads to diminished courtship behavior and infertility. We achieved the first rescue of a distinct fru behavioral phenotype, expressing a wild-type isoform in a defined subset of its normal expression pattern. CONCLUSION: This study exemplifies how complex behaviors can be controlled by a single locus through multiple isoforms regulating both developmental and physiological pathways in different neuronal substrates.
spellingShingle Billeter, J
Villella, A
Allendorfer, J
Dornan, A
Richardson, M
Gailey, D
Goodwin, S
Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene.
title Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene.
title_full Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene.
title_fullStr Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene.
title_full_unstemmed Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene.
title_short Isoform-specific control of male neuronal differentiation and behavior in Drosophila by the fruitless gene.
title_sort isoform specific control of male neuronal differentiation and behavior in drosophila by the fruitless gene
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