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Species-specific chemosensory gene expression in the olfactory organs of the malaria vector Anopheles gambiae

BACKGROUND: The malaria mosquito Anopheles gambiae has a high preference for human hosts, a characteristic that contributes greatly to its capacity for transmitting human malaria. A sibling species, An. quadriannulatus, has a quite different host preference and feeds mostly on bovids. For this reaso...

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Autores principales: Hodges, Theresa K, Cosme, Luciano V, Athrey, Giridhar, Pathikonda, Sharmila, Takken, Willem, Slotman, Michel A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4299676/
https://www.ncbi.nlm.nih.gov/pubmed/25495232
http://dx.doi.org/10.1186/1471-2164-15-1089
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author Hodges, Theresa K
Cosme, Luciano V
Athrey, Giridhar
Pathikonda, Sharmila
Takken, Willem
Slotman, Michel A
author_facet Hodges, Theresa K
Cosme, Luciano V
Athrey, Giridhar
Pathikonda, Sharmila
Takken, Willem
Slotman, Michel A
author_sort Hodges, Theresa K
collection PubMed
description BACKGROUND: The malaria mosquito Anopheles gambiae has a high preference for human hosts, a characteristic that contributes greatly to its capacity for transmitting human malaria. A sibling species, An. quadriannulatus, has a quite different host preference and feeds mostly on bovids. For this reason it does not contribute to human malaria transmission. Host seeking in mosquitoes is modulated by the olfactory system, which is primarily housed in the antennae and maxillary palps. Therefore, the detection of differing host odors by sibling species may be reflected in the expression level of the olfactory genes involved. Accordingly, we compared the transcriptomes of the antennae and maxillary palps of An. gambiae and An. quadriannulatus. RESULTS: We identified seven relatively abundant olfactory receptors, nine ionotropic receptors and three odorant binding proteins that are substantially up-regulated in An. gambiae antennae. Interestingly, we find that the maxillary palps of An. gambiae contain a species-specific olfactory receptor, Or52, and five An. gambiae-specific gustatory receptors (AgGr48-52) that are relatively abundant. These five gustatory receptors are also expressed in An. gambiae antennae, although at lower level, indicating a likely role in olfaction, rather than gustation. We also document an approximately three-fold higher overall expression of olfaction genes in the maxillary palps of An. quadriannulatus, indicating an important role of this organ in the olfaction system of this species. Finally, the expression of the CO(2) receptor genes is five to six-fold higher in the zoophilic An. quadriannulatus, implying a much higher sensitivity for detecting CO(2). CONCLUSIONS: These results identify potential human host preference genes in the malaria vector An. gambiae. Interestingly, species-specific expression of several gustatory receptors in the olfactory organs indicate a role in olfaction rather than gustation. Additionally, a more expansive role for maxillary palps in olfaction is implicated than previously thought, albeit more so in the zoophilic An. quadriannulatus. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-1089) contains supplementary material, which is available to authorized users.
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spelling pubmed-42996762015-01-21 Species-specific chemosensory gene expression in the olfactory organs of the malaria vector Anopheles gambiae Hodges, Theresa K Cosme, Luciano V Athrey, Giridhar Pathikonda, Sharmila Takken, Willem Slotman, Michel A BMC Genomics Research Article BACKGROUND: The malaria mosquito Anopheles gambiae has a high preference for human hosts, a characteristic that contributes greatly to its capacity for transmitting human malaria. A sibling species, An. quadriannulatus, has a quite different host preference and feeds mostly on bovids. For this reason it does not contribute to human malaria transmission. Host seeking in mosquitoes is modulated by the olfactory system, which is primarily housed in the antennae and maxillary palps. Therefore, the detection of differing host odors by sibling species may be reflected in the expression level of the olfactory genes involved. Accordingly, we compared the transcriptomes of the antennae and maxillary palps of An. gambiae and An. quadriannulatus. RESULTS: We identified seven relatively abundant olfactory receptors, nine ionotropic receptors and three odorant binding proteins that are substantially up-regulated in An. gambiae antennae. Interestingly, we find that the maxillary palps of An. gambiae contain a species-specific olfactory receptor, Or52, and five An. gambiae-specific gustatory receptors (AgGr48-52) that are relatively abundant. These five gustatory receptors are also expressed in An. gambiae antennae, although at lower level, indicating a likely role in olfaction, rather than gustation. We also document an approximately three-fold higher overall expression of olfaction genes in the maxillary palps of An. quadriannulatus, indicating an important role of this organ in the olfaction system of this species. Finally, the expression of the CO(2) receptor genes is five to six-fold higher in the zoophilic An. quadriannulatus, implying a much higher sensitivity for detecting CO(2). CONCLUSIONS: These results identify potential human host preference genes in the malaria vector An. gambiae. Interestingly, species-specific expression of several gustatory receptors in the olfactory organs indicate a role in olfaction rather than gustation. Additionally, a more expansive role for maxillary palps in olfaction is implicated than previously thought, albeit more so in the zoophilic An. quadriannulatus. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-1089) contains supplementary material, which is available to authorized users. BioMed Central 2014-12-11 /pmc/articles/PMC4299676/ /pubmed/25495232 http://dx.doi.org/10.1186/1471-2164-15-1089 Text en © Hodges et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Hodges, Theresa K
Cosme, Luciano V
Athrey, Giridhar
Pathikonda, Sharmila
Takken, Willem
Slotman, Michel A
Species-specific chemosensory gene expression in the olfactory organs of the malaria vector Anopheles gambiae
title Species-specific chemosensory gene expression in the olfactory organs of the malaria vector Anopheles gambiae
title_full Species-specific chemosensory gene expression in the olfactory organs of the malaria vector Anopheles gambiae
title_fullStr Species-specific chemosensory gene expression in the olfactory organs of the malaria vector Anopheles gambiae
title_full_unstemmed Species-specific chemosensory gene expression in the olfactory organs of the malaria vector Anopheles gambiae
title_short Species-specific chemosensory gene expression in the olfactory organs of the malaria vector Anopheles gambiae
title_sort species-specific chemosensory gene expression in the olfactory organs of the malaria vector anopheles gambiae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4299676/
https://www.ncbi.nlm.nih.gov/pubmed/25495232
http://dx.doi.org/10.1186/1471-2164-15-1089
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