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Male-specific fruitless isoforms target neurodevelopmental genes to specify a sexually dimorphic nervous system

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Date
03/02/2014
Author
Neville, Megan C.
Nojima, Tetsuya
Ashley, Elizabeth
Parker, Darren J.
Walker, John
Southall, Tony
Van de Sande, Bram
Marques, Ana C.
Fischer, Bettina
Brand, Andrea H.
Russell, Steven
Ritchie, Michael G.
Aerts, Stein
Goodwin, Stephen F.
Funder
NERC
Grant ID
NE/J020818/1
Keywords
Antagonistic chromatin factors
Zinc-finger protein
Drosophila-melanogaster
Courtship song
Transcription factors
Neural circuitry
Behavior
Differentiation
Brain
Orientation
QH426 Genetics
BDC
R2C
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Abstract
Background In Drosophila, male courtship behavior is regulated in large part by the gene fruitless (fru). fru encodes a set of putative transcription factors that promote male sexual behavior by controlling the development of sexually dimorphic neuronal circuitry. Little is known about how Fru proteins function at the level of transcriptional regulation or the role that isoform diversity plays in the formation of a male-specific nervous system. Results To characterize the roles of sex-specific Fru isoforms in specifying male behavior, we generated novel isoform-specific mutants and used a genomic approach to identify direct Fru isoform targets during development. We demonstrate that all Fru isoforms directly target genes involved in the development of the nervous system, with individual isoforms exhibiting unique binding specificities. We observe that fru behavioral phenotypes are specified by either a single isoform or a combination of isoforms. Finally, we illustrate the utility of these data for the identification of novel sexually dimorphic genomic enhancers and novel downstream regulators of male sexual behavior. Conclusions These findings suggest that Fru isoform diversity facilitates both redundancy and specificity in gene expression, and that the regulation of neuronal developmental genes may be the most ancient and conserved role of fru in the specification of a male-specific nervous system.
Citation
Neville , M C , Nojima , T , Ashley , E , Parker , D J , Walker , J , Southall , T , Van de Sande , B , Marques , A C , Fischer , B , Brand , A H , Russell , S , Ritchie , M G , Aerts , S & Goodwin , S F 2014 , ' Male-specific fruitless isoforms target neurodevelopmental genes to specify a sexually dimorphic nervous system ' , Current Biology , vol. 24 , no. 3 , pp. 229-241 . https://doi.org/10.1016/j.cub.2013.11.035
Publication
Current Biology
Status
Peer reviewed
DOI
https://doi.org/10.1016/j.cub.2013.11.035
ISSN
0960-9822
Type
Journal article
Rights
Copyright © 2014 The Authors. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-No Derivative Works License, which permits non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
Description
This work was supported by grants from the Wellcome Trust to S.F.G. (WT085521MA and WT082987MF) and the Natural Environment Research Council to S.F.G and M.G.R. (NE/J023647/1). J.W. and E.A were supported by Biotechnology and Biological Sciences Research Council Committee studentships.
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  • University of St Andrews Research
URI
http://hdl.handle.net/10023/4790

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