A Synergistic Transcriptional Regulation of Olfactory Genes Drives Blood-Feeding Associated Complex Behavioral Responses in the Mosquito Anopheles culicifacies
Decoding the molecular basis of host seeking and blood feeding behavioral evolution/adaptation in the adult female mosquitoes may provide an opportunity to design new molecular strategy to disrupt human-mosquito interactions. Although there is a great progress in the field of mosquito olfaction and...
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Frontiers Media S.A.
2018-05-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fphys.2018.00577/full |
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| author | Tanwee Das De Tanwee Das De Tina Thomas Sonia Verma Deepak Singla Charu Chauhan Vartika Srivastava Punita Sharma Seena Kumari Sanjay Tevatiya Jyoti Rani Yasha Hasija Kailash C. Pandey Kailash C. Pandey Rajnikant Dixit |
| author_facet | Tanwee Das De Tanwee Das De Tina Thomas Sonia Verma Deepak Singla Charu Chauhan Vartika Srivastava Punita Sharma Seena Kumari Sanjay Tevatiya Jyoti Rani Yasha Hasija Kailash C. Pandey Kailash C. Pandey Rajnikant Dixit |
| author_sort | Tanwee Das De |
| collection | DOAJ |
| description | Decoding the molecular basis of host seeking and blood feeding behavioral evolution/adaptation in the adult female mosquitoes may provide an opportunity to design new molecular strategy to disrupt human-mosquito interactions. Although there is a great progress in the field of mosquito olfaction and chemo-detection, little is known about the sex-specific evolution of the specialized olfactory system of adult female mosquitoes that enables them to drive and manage the complex blood-feeding associated behavioral responses. A comprehensive RNA-Seq analysis of prior and post blood meal olfactory system of An. culicifacies mosquito revealed a minor but unique change in the nature and regulation of key olfactory genes that may play a pivotal role in managing diverse behavioral responses. Based on age-dependent transcriptional profiling, we further demonstrated that adult female mosquito's chemosensory system gradually learned and matured to drive the host-seeking and blood feeding behavior at the age of 5–6 days. A time scale expression analysis of Odorant Binding Proteins (OBPs) unravels unique association with a late evening to midnight peak biting time. Blood meal-induced switching of unique sets of OBP genes and Odorant Receptors (Ors) expression coincides with the change in the innate physiological status of the mosquitoes. Blood meal follows up experiments further provide enough evidence that how a synergistic and concurrent action of OBPs-Ors may drive “prior and post blood meal” associated complex behavioral events. A dominant expression of two sensory appendages proteins (SAP-1 & SAP2) in the legs of An. culicifacies suggests that this mosquito species may draw an extra advantage of having more sensitive appendages than An. stephensi, an urban malarial vector in the Indian subcontinents. Finally, our molecular modeling analysis predicts crucial amino acid residues for future functional characterization of the sensory appendages proteins which may play a central role in regulating multiple behaviors of An. culicifacies mosquito.SIGNIFICANCE Evolution and adaptation of blood feeding behavior not only favored the reproductive success of adult female mosquitoes but also make them important disease-transmitting vectors. An environmental exposure after emergence may favor the broadly tuned olfactory system of mosquitoes to drive complex behavioral responses. But, how these olfactory derived genetic factors manage female specific “pre and post” blood meal associated complex behavioral responses are not well known. Our findings suggest that a synergistic action of olfactory factors may govern an innate to prime learning strategy to facilitate rapid blood meal acquisition and downstream behavioral activities. A species-specific transcriptional profiling and an in-silico analysis predict that “sensory appendages protein” may be a unique target to design disorientation strategy against the mosquito Anopheles culicifacies. |
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| spelling | doaj.art-e255183f71c7460499d65a314e929e5c2022-12-21T17:32:28ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2018-05-01910.3389/fphys.2018.00577343596A Synergistic Transcriptional Regulation of Olfactory Genes Drives Blood-Feeding Associated Complex Behavioral Responses in the Mosquito Anopheles culicifaciesTanwee Das De0Tanwee Das De1Tina Thomas2Sonia Verma3Deepak Singla4Charu Chauhan5Vartika Srivastava6Punita Sharma7Seena Kumari8Sanjay Tevatiya9Jyoti Rani10Yasha Hasija11Kailash C. Pandey12Kailash C. Pandey13Rajnikant Dixit14Laboratory of Host-Parasite Interaction Studies, National Institute of Malaria Research, Dwarka, IndiaDepartment of Biotechnology, Delhi Technological University, Rohini, IndiaLaboratory of Host-Parasite Interaction Studies, National Institute of Malaria Research, Dwarka, IndiaLaboratory of Host-Parasite Interaction Studies, National Institute of Malaria Research, Dwarka, IndiaLaboratory of Host-Parasite Interaction Studies, National Institute of Malaria Research, Dwarka, IndiaLaboratory of Host-Parasite Interaction Studies, National Institute of Malaria Research, Dwarka, IndiaLaboratory of Host-Parasite Interaction Studies, National Institute of Malaria Research, Dwarka, IndiaLaboratory of Host-Parasite Interaction Studies, National Institute of Malaria Research, Dwarka, IndiaLaboratory of Host-Parasite Interaction Studies, National Institute of Malaria Research, Dwarka, IndiaLaboratory of Host-Parasite Interaction Studies, National Institute of Malaria Research, Dwarka, IndiaLaboratory of Host-Parasite Interaction Studies, National Institute of Malaria Research, Dwarka, IndiaDepartment of Biotechnology, Delhi Technological University, Rohini, IndiaLaboratory of Host-Parasite Interaction Studies, National Institute of Malaria Research, Dwarka, IndiaDepartment of Biochemistry, National Institute for Research in Environmental Health, Indian Council of Medical Research, Bhopal, IndiaLaboratory of Host-Parasite Interaction Studies, National Institute of Malaria Research, Dwarka, IndiaDecoding the molecular basis of host seeking and blood feeding behavioral evolution/adaptation in the adult female mosquitoes may provide an opportunity to design new molecular strategy to disrupt human-mosquito interactions. Although there is a great progress in the field of mosquito olfaction and chemo-detection, little is known about the sex-specific evolution of the specialized olfactory system of adult female mosquitoes that enables them to drive and manage the complex blood-feeding associated behavioral responses. A comprehensive RNA-Seq analysis of prior and post blood meal olfactory system of An. culicifacies mosquito revealed a minor but unique change in the nature and regulation of key olfactory genes that may play a pivotal role in managing diverse behavioral responses. Based on age-dependent transcriptional profiling, we further demonstrated that adult female mosquito's chemosensory system gradually learned and matured to drive the host-seeking and blood feeding behavior at the age of 5–6 days. A time scale expression analysis of Odorant Binding Proteins (OBPs) unravels unique association with a late evening to midnight peak biting time. Blood meal-induced switching of unique sets of OBP genes and Odorant Receptors (Ors) expression coincides with the change in the innate physiological status of the mosquitoes. Blood meal follows up experiments further provide enough evidence that how a synergistic and concurrent action of OBPs-Ors may drive “prior and post blood meal” associated complex behavioral events. A dominant expression of two sensory appendages proteins (SAP-1 & SAP2) in the legs of An. culicifacies suggests that this mosquito species may draw an extra advantage of having more sensitive appendages than An. stephensi, an urban malarial vector in the Indian subcontinents. Finally, our molecular modeling analysis predicts crucial amino acid residues for future functional characterization of the sensory appendages proteins which may play a central role in regulating multiple behaviors of An. culicifacies mosquito.SIGNIFICANCE Evolution and adaptation of blood feeding behavior not only favored the reproductive success of adult female mosquitoes but also make them important disease-transmitting vectors. An environmental exposure after emergence may favor the broadly tuned olfactory system of mosquitoes to drive complex behavioral responses. But, how these olfactory derived genetic factors manage female specific “pre and post” blood meal associated complex behavioral responses are not well known. Our findings suggest that a synergistic action of olfactory factors may govern an innate to prime learning strategy to facilitate rapid blood meal acquisition and downstream behavioral activities. A species-specific transcriptional profiling and an in-silico analysis predict that “sensory appendages protein” may be a unique target to design disorientation strategy against the mosquito Anopheles culicifacies.https://www.frontiersin.org/article/10.3389/fphys.2018.00577/fullmosquitohost-seekingblood feedingbehaviorolfaction |
| spellingShingle | Tanwee Das De Tanwee Das De Tina Thomas Sonia Verma Deepak Singla Charu Chauhan Vartika Srivastava Punita Sharma Seena Kumari Sanjay Tevatiya Jyoti Rani Yasha Hasija Kailash C. Pandey Kailash C. Pandey Rajnikant Dixit A Synergistic Transcriptional Regulation of Olfactory Genes Drives Blood-Feeding Associated Complex Behavioral Responses in the Mosquito Anopheles culicifacies Frontiers in Physiology mosquito host-seeking blood feeding behavior olfaction |
| title | A Synergistic Transcriptional Regulation of Olfactory Genes Drives Blood-Feeding Associated Complex Behavioral Responses in the Mosquito Anopheles culicifacies |
| title_full | A Synergistic Transcriptional Regulation of Olfactory Genes Drives Blood-Feeding Associated Complex Behavioral Responses in the Mosquito Anopheles culicifacies |
| title_fullStr | A Synergistic Transcriptional Regulation of Olfactory Genes Drives Blood-Feeding Associated Complex Behavioral Responses in the Mosquito Anopheles culicifacies |
| title_full_unstemmed | A Synergistic Transcriptional Regulation of Olfactory Genes Drives Blood-Feeding Associated Complex Behavioral Responses in the Mosquito Anopheles culicifacies |
| title_short | A Synergistic Transcriptional Regulation of Olfactory Genes Drives Blood-Feeding Associated Complex Behavioral Responses in the Mosquito Anopheles culicifacies |
| title_sort | synergistic transcriptional regulation of olfactory genes drives blood feeding associated complex behavioral responses in the mosquito anopheles culicifacies |
| topic | mosquito host-seeking blood feeding behavior olfaction |
| url | https://www.frontiersin.org/article/10.3389/fphys.2018.00577/full |
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