Recruitment of the Proneural Gene scute to the Drosophila Sex-Determination Pathway

Corresponding author: Thomas W. Cline, University of California, 11 Koshland Hall, Mail Code 3204, Berkeley, CA 94720-3204., sxlcline{at}uclink.berkeley.edu (E-mail)

Communicating editor: T. C. KAUFMAN

In flies, scute (sc) works with its paralogs in the achaete-scute-complex (ASC) to direct neuronal development. However, in the family Drosophilidae, sc also acquired a role in the primary event of sex determination, X chromosome counting, by becoming an X chromosome signal element (XSE)—an evolutionary step shown here to have occurred after sc diverged from its closest paralog, achaete (ac). Two temperature-sensitive alleles, sc^sisB2 and sc^sisB3, which disrupt only sex determination, were recovered in a powerful F₁ genetic selection and used to investigate how sc was recruited to the sex-determination pathway. sc^sisB2 revealed 3' nontranscribed regulatory sequences likely to be involved. The sc^sisB2 lesion abolished XSE activity when combined with mutations engineered in a sequence upstream of all XSEs. In contrast, changes in Sc protein sequence seem not to have been important for recruitment. The observation that the other new allele, sc^sisB3, eliminates the C-terminal half of Sc without affecting neurogenesis and that sc^sisB1, the most XSE-specific allele previously available, is a nonsense mutant, would seem to suggest the opposite, but we show that housefly Sc can substitute for fruit fly Sc in sex determination, despite lacking Drosophilidae-specific conserved residues in its C-terminal half. Lack of synergistic lethality among mutations in sc, twist, and dorsal argue against a proposed role for sc in mesoderm formation that had seemed potentially relevant to sex-pathway recruitment. The screen that yielded new sc alleles also generated autosomal duplications that argue against the textbook view that fruit fly sex signal evolution recruited a set of autosomal signal elements comparable to the XSEs.

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