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Chemosensory gene expression in olfactory organs of the anthropophilic Anopheles coluzzii and zoophilic Anopheles quadriannulatus

BACKGROUND: Anopheles (An.) coluzzii, one of Africa’s primary malaria vectors, is highly anthropophilic. This human host preference contributes greatly to its ability to transmit malaria. In contrast, the closely related An. quadriannulatus prefers to feed on bovids and is not thought to contribute...

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Autores principales: Athrey, G., Cosme, L. V., Popkin-Hall, Z., Pathikonda, S., Takken, W., Slotman, M. A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5610455/
https://www.ncbi.nlm.nih.gov/pubmed/28938869
http://dx.doi.org/10.1186/s12864-017-4122-7
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author Athrey, G.
Cosme, L. V.
Popkin-Hall, Z.
Pathikonda, S.
Takken, W.
Slotman, M. A.
author_facet Athrey, G.
Cosme, L. V.
Popkin-Hall, Z.
Pathikonda, S.
Takken, W.
Slotman, M. A.
author_sort Athrey, G.
collection PubMed
description BACKGROUND: Anopheles (An.) coluzzii, one of Africa’s primary malaria vectors, is highly anthropophilic. This human host preference contributes greatly to its ability to transmit malaria. In contrast, the closely related An. quadriannulatus prefers to feed on bovids and is not thought to contribute to malaria transmission. The diverged preference for host odor profiles between these sibling species is likely reflected in chemosensory gene expression levels in the olfactory organs. Therefore, we compared the transcriptomes of the antennae and maxillary palps between An. coluzzii and An. quadriannulatus, focusing on the major chemosensory gene families. RESULTS: While chemosensory gene expression is strongly correlated between the two species, various chemosensory genes show significantly enhanced expression in one of the species. In the antennae of An. coluzzii the expression of six olfactory receptors (Ors) and seven ionotropic receptors (Irs) is considerably enhanced, whereas 11 Ors and 3 Irs are upregulated in An. quadriannulatus. In the maxillary palps, leaving aside Irs with very low level of expression, one Ir is strongly enhanced in each species. In addition, we find divergence in odorant binding protein (Obp) gene expression, with several highly expressed Obps being enhanced in the antennae and palps of An. coluzzii. Finally, the expression of several gustatory receptors (Grs) in the palps appears to be species-specific, including a homolog of a sugar-sensing Drosophila Gr. CONCLUSIONS: A considerable number of Ors and Irs are differentially expressed between these two closely related species with diverging host preference. These chemosensory genes could play a role in the human host preference of the malaria vector An. coluzzii. Additionally, divergence in Obp expression between the two species suggests a possible role of these odor carrier proteins in determining host preference. Finally, divergence in chemosensory expression in the palps may point towards a possible role for the maxillary palps in host differentiation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-017-4122-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-56104552017-10-10 Chemosensory gene expression in olfactory organs of the anthropophilic Anopheles coluzzii and zoophilic Anopheles quadriannulatus Athrey, G. Cosme, L. V. Popkin-Hall, Z. Pathikonda, S. Takken, W. Slotman, M. A. BMC Genomics Research Article BACKGROUND: Anopheles (An.) coluzzii, one of Africa’s primary malaria vectors, is highly anthropophilic. This human host preference contributes greatly to its ability to transmit malaria. In contrast, the closely related An. quadriannulatus prefers to feed on bovids and is not thought to contribute to malaria transmission. The diverged preference for host odor profiles between these sibling species is likely reflected in chemosensory gene expression levels in the olfactory organs. Therefore, we compared the transcriptomes of the antennae and maxillary palps between An. coluzzii and An. quadriannulatus, focusing on the major chemosensory gene families. RESULTS: While chemosensory gene expression is strongly correlated between the two species, various chemosensory genes show significantly enhanced expression in one of the species. In the antennae of An. coluzzii the expression of six olfactory receptors (Ors) and seven ionotropic receptors (Irs) is considerably enhanced, whereas 11 Ors and 3 Irs are upregulated in An. quadriannulatus. In the maxillary palps, leaving aside Irs with very low level of expression, one Ir is strongly enhanced in each species. In addition, we find divergence in odorant binding protein (Obp) gene expression, with several highly expressed Obps being enhanced in the antennae and palps of An. coluzzii. Finally, the expression of several gustatory receptors (Grs) in the palps appears to be species-specific, including a homolog of a sugar-sensing Drosophila Gr. CONCLUSIONS: A considerable number of Ors and Irs are differentially expressed between these two closely related species with diverging host preference. These chemosensory genes could play a role in the human host preference of the malaria vector An. coluzzii. Additionally, divergence in Obp expression between the two species suggests a possible role of these odor carrier proteins in determining host preference. Finally, divergence in chemosensory expression in the palps may point towards a possible role for the maxillary palps in host differentiation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-017-4122-7) contains supplementary material, which is available to authorized users. BioMed Central 2017-09-22 /pmc/articles/PMC5610455/ /pubmed/28938869 http://dx.doi.org/10.1186/s12864-017-4122-7 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Athrey, G.
Cosme, L. V.
Popkin-Hall, Z.
Pathikonda, S.
Takken, W.
Slotman, M. A.
Chemosensory gene expression in olfactory organs of the anthropophilic Anopheles coluzzii and zoophilic Anopheles quadriannulatus
title Chemosensory gene expression in olfactory organs of the anthropophilic Anopheles coluzzii and zoophilic Anopheles quadriannulatus
title_full Chemosensory gene expression in olfactory organs of the anthropophilic Anopheles coluzzii and zoophilic Anopheles quadriannulatus
title_fullStr Chemosensory gene expression in olfactory organs of the anthropophilic Anopheles coluzzii and zoophilic Anopheles quadriannulatus
title_full_unstemmed Chemosensory gene expression in olfactory organs of the anthropophilic Anopheles coluzzii and zoophilic Anopheles quadriannulatus
title_short Chemosensory gene expression in olfactory organs of the anthropophilic Anopheles coluzzii and zoophilic Anopheles quadriannulatus
title_sort chemosensory gene expression in olfactory organs of the anthropophilic anopheles coluzzii and zoophilic anopheles quadriannulatus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5610455/
https://www.ncbi.nlm.nih.gov/pubmed/28938869
http://dx.doi.org/10.1186/s12864-017-4122-7
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