BackgroundIn the tephritids Ceratitis, Bactrocera and Anastrepha, the gene transformer provides the memory device for sex determination via its auto-regulation; only in females is functional Tra protein produced. To date, the isolation and characterisation of the gene transformer-2 in the tephritids has only been undertaken in Ceratitis, and it has been shown that its function is required for the female-specific splicing of doublesex and transformer pre-mRNA. It therefore participates in transformer auto-regulatory function. In this work, the characterisation of this gene in eleven tephritid species belonging to the less extensively analysed genus Anastrepha was undertaken in order to throw light on the evolution of transformer-2.ResultsThe gene transformer-2 produces a protein of 249 amino acids in both sexes, which shows the features of the SR protein family. No significant partially spliced mRNA isoform specific to the male germ line was detected, unlike in Drosophila. It is transcribed in both sexes during development and in adult life, in both the soma and germ line. The injection of Anastrepha transformer-2 dsRNA into Anastrepha embryos caused a change in the splicing pattern of the endogenous transformer and doublesex pre-mRNA of XX females from the female to the male mode. Consequently, these XX females were transformed into pseudomales. The comparison of the eleven Anastrepha Transformer-2 proteins among themselves, and with the Transformer-2 proteins of other insects, suggests the existence of negative selection acting at the protein level to maintain Transformer-2 structural features.ConclusionsThese results indicate that transformer-2 is required for sex determination in Anastrepha through its participation in the female-specific splicing of transformer and doublesex pre-mRNAs. It is therefore needed for the auto-regulation of the gene transformer. Thus, the transformer/transfomer-2 > doublesex elements at the bottom of the cascade, and their relationships, probably represent the ancestral state (which still exists in the Tephritidae, Calliphoridae and Muscidae lineages) of the extant cascade found in the Drosophilidae lineage (in which tra is just another component of the sex determination gene cascade regulated by Sex-lethal). In the phylogenetic lineage that gave rise to the drosophilids, evolution co-opted for Sex-lethal, modified it, and converted it into the key gene controlling sex determination.
The gene doublesex, which is placed at the bottom of the sex-determination gene cascade, plays the ultimate discriminatory role for sex determination in insects. In all insects where this gene has been characterized, the dsx premessenger RNA (premRNA) follows a sex-specific splicing pattern, producing male-and female-specific mRNAs encoding the male-DSXM and female-DSXF proteins, which determine male and female development, respectively. This article reports the isolation and characterization of the gene doublesex of dipteran Sciara insects. The Sciara doublesex gene is constitutively transcribed during development and adult life of males and females. Sciara had no sex-specific doublesex mRNAs but the same transcripts, produced by alternative splicing of its primary transcript, were present in both sexes, although their relative abundance is sex specific. However, only the female DSXF protein, but not the male DSXM protein, was produced at similar amounts in both sexes. An analysis of the expression of female and male Sciara DSX proteins in Drosophila showed that these proteins conserved female and male function, respectively, on the control of Drosophila yolk-protein genes. The molecular evolution of gene doublesex of all insects where this gene has been characterized revealed that Sciara doublesex displays a considerable degree of divergence in its molecular organization and its splicing pattern with respect to the rest of dipterans as suggested by its basal position within the doublesex phylogeny. It is suggested that the doublesex gene is involved in Sciara sex determination although it appears not to play the discriminatory role performed in other insects.KEYWORDS sex determination; molecular evolution; Sciara; gene doublesex; genetics of sex M ALES and females are different at the morphological, physiological, and behavioral levels. This sexual dimorphism results from the integration of two processes: sex determination and sexual differentiation. Sex determination refers to the developmental program that commits the embryo to either the male or the female pathway. The genes underlying this phenomenon are the sex-determination genes. Sexual differentiation refers to the expression of the sex cytodifferentiation genes (which are controlled by the sex-determination genes), the expression of which gives rise to the formation of the sexually dimorphic structures that characterize the male and female adults.The animal kingdom possesses a wealth of mechanisms by which sex is decided (Bull 1983;Beukeboom and Perrin 2014). These mechanisms can be classified into three main categories, depending on the origin of the primary sexdetermination signal, which can be zygotic, maternal, or environmental. These three primary signals occur and are concatenated in the dipteran Sciara (for details see Sánchez 2010). Briefly, in Sciara, sex determination follows the XX/X0 mechanism: XX zygotes will develop as females and X0 zygotes will develop as males. Yet, the final chromosome constitution of the zygote, which start...
The transformer-2 gene is involved in sex determination in tephritid flies (Tephritidae).It is required for the auto-regulation of the transformer gene (the memory device for sex determination in these insects) and for the female-specific splicing of doublesex pre-mRNA, the last gene in the sex determination gene cascade. The present manuscript addressed the question of the functional conservation of the tephritid Anastrepha Tra2 protein to direct sexual development in Drosophila (Drosophilidae). To express this protein in Drosophila, the GAL4-UAS system was used. The Anastrepha Tra2 protein supplies tra-2 function in Drosophila: this protein would form a complex with the endogenous Drosophila Tra protein to promote the female-specific splicing of the Drosophila doublesex pre-mRNA. The feminisation produced by the Anastrepha Tra2 protein was, however, partial.
BackgroundThe Drosophila SXL protein controls sex determination and dosage compensation. It is a sex-specific factor controlling splicing of its own Sxl pre-mRNA (auto-regulation), tra pre-mRNA (sex determination) and msl-2 pre-mRNA plus translation of msl-2 mRNA (dosage compensation). Outside the drosophilids, the same SXL protein has been found in both sexes so that, in the non-drosophilids, SXL does not appear to play the key discriminating role in sex determination and dosage compensation that it plays in Drosophila. Comparison of SXL proteins revealed that its spatial organisation is conserved, with the RNA-binding domains being highly conserved, whereas the N- and C-terminal domains showing significant variation. This manuscript focuses on the evolution of the SXL protein itself and not on regulation of its expression.Methodology Drosophila-Sciara chimeric SXL proteins were produced. Sciara SXL represents the non-sex-specific function of ancient SXL in the non-drosophilids from which presumably Drosophila SXL evolved. Two questions were addressed. Did the Drosophila SXL protein have affected their functions when their N- and C-terminal domains were replaced by the corresponding ones of Sciara? Did the Sciara SXL protein acquire Drosophila sex-specific functions when the Drosophila N- and C-terminal domains replaced those of Sciara? The chimeric SXL proteins were analysed in vitro to study their binding affinity and cooperative properties, and in vivo to analyse their effect on sex determination and dosage compensation by producing Drosophila flies that were transgenic for the chimeric SXL proteins.ConclusionsThe sex-specific properties of extant Drosophila SXL protein depend on its global structure rather than on a specific domain. This implies that the modifications, mainly in the N- and C-terminal domains, that occurred in the SXL protein during its evolution within the drosophilid lineage represent co-evolutionary changes that determine the appropriate folding of SXL to carry out its sex-specific functions.
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