The Gene Sex-Lethal of the Sciaridae Family (Order Diptera, Suborder Nematocera) and Its Phylogeny in Dipteran Insects

By Serna, Esther; Gorab, Eduardo et al. | Genetics, October 2004 | Go to article overview

The Gene Sex-Lethal of the Sciaridae Family (Order Diptera, Suborder Nematocera) and Its Phylogeny in Dipteran Insects


Serna, Esther, Gorab, Eduardo, Ruiz, M. Fernanda, Goday, Clara, et al., Genetics


ABSTRACT

This article reports the cloning and characterization of the gene homologous to Sex-lethal (Sxl) of Drosophila melanogaster from Sciara coprophila, Rhynchosciara americana, and Trichosia pubescens. This gene plays the key role in controlling sex determination and dosage compensation in D. melanogaster. The Sxl gene of the three species studied produces a single transcript encoding a single protein in both males and females. Comparison of the Sxl proteins of these Nematocera insects with those of the Brachycera showed their two RNA-binding domains (RBD) to be highly conserved, whereas significant variation was observed in both the N- and C-terminal domains. The great majority of nucleotide changes in the RBDs were synonymous, indicating that purifying selection is acting on them. In both sexes of the three Nematocera insects, the Sxl protein colocalized with transcription-active regions dependent on RNA polymerase II but not on RNA polymerase I. Together, these results indicate that Sxl does not appear to play a discriminatory role in the control of sex determination and dosage compensation in nematocerans. Thus, in the phylogenetic lineage that gave rise to the drosophilids, evolution coopted for the Sxl gene, modified it, and converted it into the key gene controlling sex determination and dosage compensation. At the same time, however, certain properties of the recruited ancestral Sxl gene were beneficial, and these are maintained in the evolved Sxl gene, allowing it to exert its sex-determining and dose compensation functions in Drosophila.

IN Drosophila melanogaster, the gene Sex-lethal (Sxl) controls the processes of sex determination, sexual behavior, and dosage compensation (the products of the X-linked genes are present in equal amounts in males and females; reviewed in PENALVA and SÁNCHEZ 2003). Sxl regulates the expression of two independent sets of genes (LUCCHESI and SKRIPSKY 1981): the sex determination genes (mutations in which affect sex determination but have no effect on dosage compensation) and the male-specific lethal genes (msls; mutations in which affect dosage compensation but have no effect on sex determination).

Sxl produces two temporally distinct sets of transcripts corresponding to the function of the female-specific early and non-sex-specific late promoters, respectively (SALZ et al. 1989). The early set is produced as a response to the X/A signal, which controls Sxl expression at the transcriptional level (TORRES and SÁNCHEZ 1991; KEYES et al. 1992). Once the state of activity of Sxl is deter mined-an event that occurs at the blastoderm stage-the X/A signal is no longer needed and the gene's activity is fixed (SÁNCHEZ and NÖTHIGER 1983; BACHILLER and SÁNCHEZ 1991).

Three male-specific and three-female specific tran scripts form the late set of Sxl transcripts, which appear slightly after the blastoderm stage and persist through out development. The male transcripts are similar to their female counterparts, except for the presence of an additional exon (exon 3), which contains a transla tion stop codon. Consequently, male late transcripts give rise to presumably inactive truncated proteins. In fe males, this exon is spliced out and functional Sxl protein is produced (BELL et al. 1988; BOPP et al. 1991). Therefore, the control of Sxl expression throughout develop0 ment occurs by sex-specific splicing of its primary script. The ability of Sxl to function as a stable switch is due to the positive autoregulatory function of its own product (CLINE 1984), which is required for the femalespecific splicing of Sxl pre-mRNA (BELL et al. 1991).

The gene Sxl encodes an RNA-binding protein that regulates its own RNA splicing (SAKAMOTO et al. 1992; HORABIN and SCHEDL 1993). The Sxl protein controls sex determination and sexual behavior by inducing the use of a female-specific 3' splice site in the first intron of the transformer (tra) pre-mRNA. Use of the alternative, non-sex-specific 3' splice site results in a transcript that encodes a nonfunctional truncated protein, while use of the female-specific site allows the synthesis of full-length functional Tra polypeptide (BOGGS et al. …

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