Molecular genetic dissection of the sex-specific and vital functions of the Drosophila melanogaster sex determination gene fruitless

A multibranched hierarchy of regulatory genes controls all aspects of somat ic sexual development in Drosophila melanogaster. One branch of this hierar chy is headed by the fruitless (fru) gene and functions in the central nerv ous system, where it is necessary for male courtship behavior as well as th e differentiation of a male-specific abdominal structure, the muscle of Law rence (MOL). A preliminary investigation of several of the mutations descri bed here showed that the fru gene also has a sex-nonspecific vital function . The fru gene produces a complex set of transcripts through the use of fou r promoters and alternative splicing. Only the primary transcripts produced front the most distal (PI) promoter are sex specifically spliced under dir ection of the sex-determination hierarchy. We have analyzed eight new fi-it mutations, created by X-ray mutagenesis and P-element excision, to try to gain insight into the relationship of specific transcript classes to specif ic fru functions. Males that lack the Pl-derived fm transcript,, show a com plete absence of sexual behavior, but tic, Other defects besides the loss o f the MOL. Both males and females that have reduced levels of transcripts f rom the P3 promoter develop into adults but frequently die after failing to eclose. Analysis of the morphology and behavior of adult escapers showed t hat P3-encoded functions are required for the proper differentiation and ev ersion of imaginal discs. Furthermore, the reduction in the size of the neu romuscular junctions on abdominal muscles in these animals suggests that on e of fru's sex-nonspecific functions involves general aspects of neuronal d ifferentiation. In mutants that lack all fru transcripts as well its a smal l number of adjacent genes, animals die at all early pupal stage, indicatin g that fm's function is required only during late development. Thus, fru fu nctions both ill the sex-determination regulatory hierarch), to control mal e sexual behavior through sex-specific transcripts and sex-nonspecifically to control the development of imaginal discs and motorneuronal synapses dur ing adult development through sex-nonspecific transcript classes.