~ Dept. of Biology, Brandeis University, Waltham, MA, § Dept. of Biological Sciences, Stanford University, Stanford, CA, # Dept. of Zoology, Oregon State University, Corvallis, OR, % Dept. of Biochemistry, University of Texas, S.W.Medical Center, Dallas, TX,
fruitless (fru) mutations have profound effects on male courtship behavior: mutant males expressing the original allele (fru1) initiate courtship of males and females indiscriminately and do not copulate. Moreover, fru males fail to develop a male-specific muscle called the Muscle of Lawrence (MOL). Development of the MOL depends on innervation by male-specific motorneurons, consistent with the notion that fru functions within the nervous system. Behavioral studies of new fru alleles extend the view that fru specifically effects male-specific nervous system functions; as some of these alleles cause more severe courtship impairments, such as elimination of courtship song while other motor functions are normal.
We have suggested that fru may be a new member of the somatic sex determination hierarchy in addition to governing many aspects of male sexual behavior. Specifically, development of the MOL does not depend on the function of doublesex (dsx) but does depend on the function of genes upstream of dsx in the regulatory hierarchy, suggesting that there is a fru-containing branch in the hierarchy just after transformer (tra) and transformer-2 (tra-2).
The fru locus spans at least 140 kb based on the locations of behavioral and MOL disrupting chromosomal breakpoints and transposon-insert sites, as well as hybridization to the walk of several overlapping classes of cDNAs. Sequence analysis of the cDNAs reveal that fru is a member of a class of transcription factors (such as those encoded by Broad-Complex, tramtrack, and bric a brac) that contain a conserved N-terminal domain and alternative C-terminal zinc fingers.
Analysis of RNAs and cDNAs complementary to fru probes has revealed that the gene is transcriptionally complex, with at least 3 promoters. In addition there is alternative splicing at both the 3' and 5' ends of the gene. Moreover, consistent with fru's role as a new member/branch of the sex determination hierarchy, several of these fru transcripts are sex-specifically spliced under the control of tra and tra-2, but not dsx. Analysis of the gene's in situ expression revealed fru products in a subset of cells in the adult CNS (enriched in adult head as opposed to body tissue).