Drosophila OVO zinc-finger protein regulates ovo and ovarian tumor target promoters

Abstract

The ovo+ and ovarian tumor+ genes function in the germline sex determination pathway in Drosophila, but the hierarchical relationship between them is unknown. We found that increased ovo+ copy number resulted in increased ovarian tumor expression in the female germline and increased ovo expression in the male germline. The ovo locus encodes C2H2 zinc-finger proteins. Bacterially expressed OVO zinc-finger domain bound to multiple sites at or near the ovo and ovarian tumor promoters strongly suggesting that OVO is directly autoregulatory and that ovarian tumor is a direct downstream target of ovo in the germline sex determination hierarchy. Both positive and negative regulation by OVO proteins appears likely, depending on promoter context and on the sex of the fly. Our observation that two strong OVO-binding sites are at the initiator of the TATA-less ovo-B and ovarian tumor promoters raises the possibility that OVO proteins influence the nucleation of transcriptional pre-initiation complexes.

Suppression of distinct ovo phenotypes in the Drosophila female germline bymaleless− andSex-lethalM

“…Sxl M suppresses weak otu alleles to fertility, much like it does weak ovo alleles and suppresses only the tumor phenotype of strong otu mutations, again much like it does strong ovo alleles [Pauli et al, 1993;Nagoshi et al, 1995]. The similar suppression of ovo and otu by Sxl M and the indications that the otu ϩ locus is a direct target of ovo [Lü et al, 1998] makes it likely that Sxl ϩ is an indirect ovo target gene (ovo ϩ = otu ϩ =Sxl ϩ ). However, there also is a good potential OVO binding sites in a region that may be a germline Sxl promoter [Soper et al, 1998;J.…”

“…Though we saw no effect of Sxl M on the ovo germlinedeath phenotype, we expected Sxl gain-of-function alleles to have some effect on the ovo phenotype because of other evidence that ovo regulates Sxl ϩ either directly or indirectly [Oliver et al, 1990Lü et al, 1998]. We therefore tested the effect of Sxl gain-of-function alleles in ovo Ϫ ; mle Ϫ double mutants.…”

“…This phenotype indicates that ovo ϩ regulates genes required only in 2X female germ cells, not in 1X male germ cells (strangely, ovo ϩ has clear activity in the 1X male germline, but is not essential there [Hager and Cline, 1997;Lü et al, 1998]). In this paper, we have systematically examined the genetic interactions between amorphic ovo alleles and mutant alleles of the somatic dosage compensation loci that kill 1X somatic cells due to lowered X-linked gene expression [Lucchesi and Manning, 1987;Baker et al, 1994;Cline and Meyer, 1996].…”

“…The ovo ϩ locus is transcriptionally autoregulatory Mével-Ninio et al, 1996;Lü et al, 1998] and high level transcription of the ovarian tumor (otu) locus requires ovo ϩ [Lü et al, 1998]. At the molecular level, OVO binds to the TATA-less otu and ovo-B core promoters; as well as to several upstream sites in otu and ovo, suggesting that OVO directly regulates itself and otu [Lü et al, 1998]. In turn, the ovo ϩ locus helps to regulate the female-specific alternative splicing of SXL pre-mRNA [Bopp et al, 1993;Oliver et al, 1993;Pauli et al, 1993].…”

“…While no known ovo alleles result in male germline defects [Mével-Ninio et al, 1991;Garfinkel, 1992;Lü et al, 1998], the ovo ϩ locus encodes zinc-finger transcription factors required for germline-dependent female fertility (ovo) or non-sex-specific cuticular patterning (formerly known as shavenbaby). The ovo ϩ locus is transcriptionally autoregulatory Mével-Ninio et al, 1996;Lü et al, 1998] and high level transcription of the ovarian tumor (otu) locus requires ovo ϩ [Lü et al, 1998].…”