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. 2011;6(6):e21572.
doi: 10.1371/journal.pone.0021572. Epub 2011 Jun 30.

Transcription regulation of sex-biased genes during ontogeny in the malaria vector Anopheles gambiae

Kalle Magnusson  1 , Antonio M Mendes, Nikolai Windbichler, Philippos-Aris Papathanos, Tony Nolan, Tania Dottorini, Ermanno Rizzi, George K Christophides, Andrea Crisanti
Affiliations

Transcription regulation of sex-biased genes during ontogeny in the malaria vector Anopheles gambiae

Kalle Magnusson et al. PLoS One. 2011.

Abstract

In Anopheles gambiae, sex-regulated genes are responsible for controlling gender dimorphism and are therefore crucial in determining the ability of female mosquitoes to transmit human malaria. The identification and functional characterization of these genes will shed light on the sexual development and maturation of mosquitoes and provide useful targets for genetic control measures aimed at reducing mosquito fertility and/or distorting the sex ratio.We conducted a genome wide transcriptional analysis of sex-regulated genes from early developmental stages through adulthood combined with functional screening of novel gonadal genes. Our results demonstrate that the male-biased genes undergo a major transcription turnover starting from larval stages to adulthood. The male biased genes at the adult stage include a significant high number of unique sequences compared to the rest of the genome. This is in contrast to female-biased genes that are much more conserved and are mainly activated during late developmental stages.The high frequency of unique sequences would indicate that male-biased genes evolve more rapidly than the rest of the genome. This finding is particularly intriguing because A. gambiae is a strictly female monogamous species suggesting that driving forces in addition to sperm competition must account for the rapid evolution of male-biased genes. We have also identified and functionally characterized a number of previously unknown A. gambiae testis- and ovary-specific genes. Two of these genes, zero population growth and a suppressor of defective silencing 3 domain of the histone deacetylase co-repressor complex, were shown to play a key role in gonad development.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Developmentally regulated A. gambiae sex-biased genes.
(A) Number of female- (pink) and male- (blue) biased genes transcribed at the larval, pupal and adult stages. The bars are split in light and dark colours to arrange sex-biased genes according to two different thresholds of male:female log2 expression ratios +/− 0.8 and +/− 1.6 respectively. (B) Venn diagram showing the relationship between sex-biased transcription and development. Larval stages were pooled together to simplify their visualization. The relative percentage of sex-biased genes respect to a total of 1544 genes with transcription values at all stages examined is shown in parenthesis. (C) Variance of gene expression across different developmental stages at increasing male:female expression ratios. The average male:female expression ratio of each gene at all stage examined is plotted against the standard deviation of its expression. The male-biased expression is the most relevant turnover of sex-linked expression across mosquito development though at the adult stage female-biased genes are more numerous than the male-biased ones. See also Figure S1 and Tables S1, S2, S3.
Figure 2
Figure 2. Sex-biased developmental transcription programmes of co-expressed genes.
The sex-biased genes with transcription values for at least three of the five developmental stages analysed (1st instar larvae (L1), 2nd/3rd instar larvae (L2-3), 4th instar larvae (L4), pupae (P), adults (A)) are arranged in co expression K-means clusters. The number of genes included in each cluster is indicated in brackets. The clusters are arranged in three groups according to the average sex-bias profile at the adult stage. Group A (M1-M4) and B (F1-F4) contain genes that have distinct developmental transcription profiles but have a male- and female-bias respectively at the adult stage. Group C (E1-E3) contains genes that are sex-biased (either male or female) at early developmental stages but not sex-biased in adult mosquitoes. See also Figure S6 and Tables S4, S7.
Figure 3
Figure 3. Tissue transcription analysis of M3 cluster components.
(A) The genes of cluster M3 transcribed exclusively in the testis and (B) in both testis and ovaries are arranged on the basis of their transcription profile during ontogeny (1st instar larvae, 2nd/3rd instar larvae, 4th instar larvae, pupae (P) and adults (A)) and analyzed for the presence of identifiable A. gambiae (An) orthologues in the genomes of D. melanogaster (Dm) and Ae. aegypti (Ae). The male:female transcription ratio values are translated into a colour code eisengram ranging from blue (top at 3.0 log2) to pink (bottom at -3.0 log2) showing different levels of male- and female-biased transcription intensity respectively. For each gene RT-PCR experiments were performed on the testes (Tt), carcass of adult males (Mc), ovaries (Ov) and carcass of adult females (Fc). See also Tables S5, S6, S8.
Figure 4
Figure 4. Phylogenomic analysis of A. gambiae sex-biased genes.
Percentages of male- (blue) and female-biased (pink) genes identified at the stage of larvae, pupae and adults that are either unique (left panels) or have identifiable orthologues (right panels) when comparing the genomes of A. gambiae with D. melanogaster (An:Dm), A. gambiae with Ae. Aegypti (An:Ae) and A. gambiae with Ae agypti and D. melanogaster (An:Ae:Dm). Differences in the percentage of either unique sequences or orthologues compared to those observed in the subset of all genes transcribed at a particular stage (grey) were statistically evaluated by Bonferroni corrected hypergeometric distribution (P<0.05, one asterisk). See also Tables S9, S10.
Figure 5
Figure 5. Transcription of sex-biased genes in A. gambiae and D. melanogaster.
The transcription profile of a total of 118 male- (M), 334 female- (F) and 1343 non sex-biased (N) A. gambiae genes was compared to that of their one-to-one D. melanogaster orthologues. The bars show the proportion of A. gambiae sex-biased genes with D. melanogaster orthologues showing either a conserved male (blue), female (pink) sex-bias or a reversed (light gray) transcription pattern (i.e. male-biased genes becoming female-biased and vice versa). The proportion of A. gambiae non sex-biased genes with sex-biased D. melanogaster orthologues is also shown (dark grey). See also Table S11.
Figure 6
Figure 6. Development of internal reproductive organs in dsRNA injected mosquitoes.
Micrographs of dissected male (upper panels) and female reproductive tracts (lower panels) of adult individuals that had developed from lacZ dsRNA, AGAP006241-dsRNA -and AGAPP006449 –dsRNA injected embryos.
See this image and copyright information in PMC

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