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A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior.

ABSTRACT: The male accessory glands (MAGs) of many insect species produce and secrete a number of reproductive proteins collectively named Acps. These proteins, many of which are rapidly evolving, are essential for male fertility and represent formidable modulators of female postmating behavior. Upon copulation, the transfer of Acps has been shown in Drosophila and other insects to trigger profound physiological and behavioral changes in females, including enhanced ovulation/oviposition and reduced mating receptivity. In Anopheles gambiae mosquitoes, the principal vectors of human malaria, experimental evidence clearly demonstrates a key role of MAG products in inducing female responses. However, no Acp has been experimentally identified to date in this or in any other mosquito species. In this study we report on the identification of 46 MAG genes from An. gambiae, 25 of which are male reproductive tract-specific. This was achieved through a combination of bioinformatics searches and manual annotation confirmed by transcriptional profiling. Among these genes are the homologues of 40% of the Drosophila Acps analyzed, including Acp70A, or sex peptide, which in the fruit fly is the principal modulator of female postmating behavior. Although many Anopheles Acps belong to the same functional classes reported for Drosophila, suggesting a conserved role for these proteins in mosquitoes, some represent novel lineage-specific Acps that may have evolved to perform functions relevant to Anopheles reproductive behavior. Our findings imply that the molecular basis of Anopheles female postmating responses can now be studied, opening novel avenues for the field control of these important vectors of human disease.

SUBMITTER: Dottorini T

PROVIDER: S-EPMC2042187 | biostudies-literature | 2007 Oct

REPOSITORIES: biostudies-literature

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A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior.

Dottorini Tania T Nicolaides Lietta L Ranson Hilary H Rogers David W DW Crisanti Andrea A Catteruccia Flaminia F

Proceedings of the National Academy of Sciences of the United States of America 20070927 41

The male accessory glands (MAGs) of many insect species produce and secrete a number of reproductive proteins collectively named Acps. These proteins, many of which are rapidly evolving, are essential for male fertility and represent formidable modulators of female postmating behavior. Upon copulation, the transfer of Acps has been shown in Drosophila and other insects to trigger profound physiological and behavioral changes in females, including enhanced ovulation/oviposition and reduced mating ...[more]

PMID: 17901209

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Project description:In Drosophila, the accessory gland proteins (Acps) secreted from the male accessory glands (MAGs) and transferred along with sperm into the female reproductive tract have been implicated in triggering postmating behavioral changes, including refractoriness to subsequent mating and propensity to egg laying. Recently, Acps have been found also in Anopheles, suggesting similar functions. Understanding the mechanisms underlying transcriptional regulation of Acps and their functional role in modulating Anopheles postmating behavior may lead to the identification of novel vector control strategies to reduce mosquito populations. We identified heat-shock factor (HSF) binding sites within the Acp promoters of male Anopheles gambiae and discovered three distinct Hsf isoforms; one being significantly up-regulated in the MAGs after mating. Through genome-wide transcription analysis of Hsf-silenced males, we observed significant down-regulation in 50% of the Acp genes if compared to control males treated with a construct directed against an unrelated bacterial sequence. Treated males retained normal life span and reproductive behavior compared to control males. However, mated wild-type females showed a ?46% reduction of egg deposition rate and a ?23% reduction of hatching rate (?58% combined reduction of progeny). Our results highlight an unsuspected role of HSF in regulating Acp transcription in A. gambiae and provide evidence that Acp down-regulation in males leads a significant reduction of progeny, thus opening new avenues toward the development of novel vector control strategies. Total RNA from 4-d-old dsLacZ-treated controls and HSF-silenced males was extracted using TRIzol reagent (Life Technologies), following protocols set according to manufacturer’s instructions. RNA preparation, labelling, hybridization and data analysis were performed by the Oxford Gene Technology (OGT) company. In particular, RNA was further cleaned up using the RNeasy Mini Kit (Qiagen) followed by ethanol precipitation. Sample passing the purity metrics (260/280 and 260/230 ratio) were considered for labeling and hybridization procedures. Labeling was done with cyanine 3 (dsHSF1 and dsHSF123) and cyanine 5 (control dsLacZ). Samples and controls were hybridized in triplicates to the Agilent Mosquito Gene expression arrays (4x44,000, Agilent Technologies, Santa Clara, CA, USA). Data analysis was performed by OGT according to a standardized procedure, as implemented by the software applications Feature Extraction (version 9.5.3.1.), and Genespring GX (version 11.0). Expression data was first normalised using linear and loess normalization in Feature Extraction, then it was imported into Genespring where it was converted into normalised log ratios. The distribution of the data between and within the treatments was checked via boxplots and hierarchical clustering to confirm consistency. Intensity measures from spots flagged as being of poor quality were excluded. Then, the control probes were removed for the statistical analysis: t-tests were carried out for each condition with null hypothesis of log ratio being equal to zero. This was done on the normalised log ratios from the 3 technical replicates. Probes meeting a cut-off of p<0.05 with Benjamini-Hochberg multiple testing correction and with a fold change cutoff greater than 2 were considered statistically and biologically relevant and were used to generate lists of differentially expressed targets.

Project description:In order to find a blood host and to select appropriate oviposition sites female Anopheles gambiae mosquitoes rely on olfactory cues which are sensed by olfactory sensory neurons (OSNs) located within morphologically different sensilla hairs. While the sharp type trichoid sensilla are most abundant and intensely studied, the striking blunt type trichoid sensilla exist only in small numbers and their specific function is unknown. It has been suggested that they may play a role in the detection of chemical cues indicating oviposition sites. With the aim of identifying molecular elements in blunt type trichoid sensilla, which may be relevant for chemosensory function of this sensillum type, experiments were performed which include whole mount fluorescence in situ hybridization (WM-FISH) and fluorescence immunohistochemistry (WM-FIHC). The studies were concentrated on odorant binding proteins (AgOBPs) and odorant receptors (AgORs). WM-FISH approaches using a probe for the plus-C class AgOBP47 led to the labeling of cells, which resembled in number and antennal distribution pattern the blunt type trichoid sensilla. Moreover, WM-FIHC with an antiserum for AgOBP47 allowed to assign the AgOBP47-expressing cells to blunt type trichoid sensilla and to allocate the protein within the sensillum hair shafts. The result of double WM-FISH-experiments and combined WM-FIHC/FISH approaches indicated that the AgOBP47-expressing cells are co-localized with cells, which express AgOR11, AgOR13 and AgOR55. In addition, it turned out that the two receptor types AgOR13 and AgOR55 are co-expressed in the same cells. Together, the results indicate that the blunt type trichoid sensilla contain a characteristic binding protein, plus-C AgOBP47, in the sensillum lymph and two sensory neurons, one cell which express the odorant receptor AgOR11 and a second cell which express the receptor types AgOR13 and AgOR55. The expression of characteristic chemosensory elements in blunt type trichoid sensilla supports the notion that this sensillum type is involved in sensing distinct odorous compounds.

Dataset Information

A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior.

Publications

A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior.

Similar Datasets

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