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Identification of sex-specific transcripts of the Anopheles gambiae doublesex gene.

ABSTRACT: The understanding of the molecular mechanisms of sex differentiation in the mosquito Anopheles gambiae could identify important candidate genes for inducing selective male sterility in transgenic lines or for sex-controlled expression of lethal genes. In many insects, doublesex (dsx) is the double-switch gene at the bottom of the somatic sex-determination cascade that determines the differentiation of sexually dimorphic traits. We report here on the identification of the dsx homologue in A. gambiae and on the characterization of its sex-specific transcripts. Agdsx consists of seven exons, distributed over an 85 kb region on chromosome 2R, which are sex-specifically spliced to produce the female and male AgdsxF and AgdsxM transcripts. AgdsxF contains a 795 bp ORF, coding for a protein of 265 amino acids, while AgdsxM comprises a much longer (1866 bp) ORF, coding for a 622 aa protein. Differences in the exon/intron organization suggest that Agdsx sex-specific splicing results from a different mechanism from Drosophila melanogaster dsx. These findings represent an important step towards the understanding of sex differentiation in Anopheles and will facilitate the use of gene transfer technologies to manipulate sex ratios for vector control programs based on the sterile insect technique.

SUBMITTER: Scali C

PROVIDER: S-EPMC1350936 | biostudies-literature | 2005 Oct

REPOSITORIES: biostudies-literature

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Identification of sex-specific transcripts of the Anopheles gambiae doublesex gene.

Scali Christina C Catteruccia Flaminia F Li Qiuxiang Q Crisanti Andrea A

The Journal of experimental biology 20051001 Pt 19

The understanding of the molecular mechanisms of sex differentiation in the mosquito Anopheles gambiae could identify important candidate genes for inducing selective male sterility in transgenic lines or for sex-controlled expression of lethal genes. In many insects, doublesex (dsx) is the double-switch gene at the bottom of the somatic sex-determination cascade that determines the differentiation of sexually dimorphic traits. We report here on the identification of the dsx homologue in A. gamb ...[more]

PMID: 16169947

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Project description:In many species, males and females display differences in their physiology that are not limited to the gonads. Sex differences in adult insects can comprise body size and feeding behaviour, as only female, but not male mosquitoes are blood-feeding in order to produce eggs. This is relevant since the malaria-causing parasite Plasmodium is transmitted by a female mosquito through a previous blood meal from an infected individual. The initiation of sex-specific developmental programs can be often linked to heteromorphic sex chromosomes (XX/XY in Anopheles). In males, the X-linked genes are only present in a single copy. To counteract this hemizygosity, Anopheles, like other species, exhibits dosage compensation (DC). Anopheles DC manifests by upregulation of the single male X ensuring the equal expression of sex-chromosomal genes between males and females. To date, the sex-specific differences at the transcriptome level related to the X/Y chromosomes and DC have been characterized at post-embryonic stages. Their onset during embryogenesis, especially during the early stages where the embryo switches from the maternal to the zygotic transcriptome, is largely uncharacterized to date. Here, we generate a sex-specific transcriptome atlas across Anopheles embryogenesis ending at the first larval stage. Along with the transition from the maternal to the zygotic transcriptome, many transcripts switch isoform, where the 3’ untranslated regions (UTR) of zygotic transcripts are significantly extended compared to their maternal counterpart. We also identify stage- and sex-specific splicing events. Comparing male and female embryos, we identify 120 sexually dimorphic protein coding genes and non-coding RNAs, indicating that sexually dimorphic gene expression is not widespread during embryogenesis. Furthermore, the imbalance of X-linked genes between males and females after zygotic genome activation is corrected shortly after, where the majority of genes exhibit DC around 9 hours of embryogenesis with further fine-tuning later in development. Our atlas provides a framework to explore sex differences in development and evolution and thereby, enables future functional analyses of sex-specific expression patterns and isoform usage.

Project description:BackgroundThe midgut of hematophagous insects, such as disease transmitting mosquitoes, carries out a variety of essential functions that mostly relate to blood feeding. The midgut of the female malaria vector mosquito Anopheles gambiae is a major site of interactions between the parasite and the vector. Distinct compartments and cell types of the midgut tissue carry out specific functions and vector borne pathogens interact and infect different parts of the midgut.ResultsA microarray based global gene expression approach was used to compare transcript abundance in the four major female midgut compartments (cardia, anterior, anterior part of posterior and posterior part of posterior midgut) and between the male and female Anopheles gambiae midgut. Major differences between the female and male midgut gene expression relate to digestive processes and immunity. Each compartment has a distinct gene function profile with the posterior midgut expressing digestive enzyme genes and the cardia and anterior midgut expressing high levels of antimicrobial peptide and other immune gene transcripts. Interestingly, the cardia expressed several known anti-Plasmodium factors. A parallel peptidomic analysis of the cardia identified known mosquito antimicrobial peptides as well as several putative short secreted peptides that are likely to represent novel antimicrobial factors.ConclusionThe A. gambiae sex specific midgut and female midgut compartment specific transcriptomes correlates with their known functions. The significantly greater functional diversity of the female midgut relate to hematophagy that is associated with digestion and nutrition uptake as well as exposes it to a variety of pathogens, and promotes growth of its endogenous microbial flora. The strikingly high proportion of immunity related factors in the cardia tissue most likely serves the function to increase sterility of ingested sugar and blood. A detailed characterization of the functional specificities of the female mosquito midgut and its various compartments can greatly contribute to our understanding of its role in disease transmission and generate the necessary tools for the development of malaria control strategies.

Dataset Information

Identification of sex-specific transcripts of the Anopheles gambiae doublesex gene.

Publications

Identification of sex-specific transcripts of the Anopheles gambiae doublesex gene.

Similar Datasets

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