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The antennal transcriptome of Triatoma infestans reveals substantial expression changes triggered by a blood meal

BACKGROUND: Triatoma infestans is the main vector of Chagas disease in the Americas, currently transmitting it in Argentina, Paraguay, and Bolivia. Many T. infestans populations present insecticide resistance, reducing the efficiency of control campaigns. Alternative vector control methods are neede...

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Autores principales: Latorre Estivalis, Jose Manuel, Traverso, Lucila, Pontes, Gina, Lorenzo, Marcelo Gustavo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9801554/
https://www.ncbi.nlm.nih.gov/pubmed/36585617
http://dx.doi.org/10.1186/s12864-022-09059-6
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author Latorre Estivalis, Jose Manuel
Traverso, Lucila
Pontes, Gina
Lorenzo, Marcelo Gustavo
author_facet Latorre Estivalis, Jose Manuel
Traverso, Lucila
Pontes, Gina
Lorenzo, Marcelo Gustavo
author_sort Latorre Estivalis, Jose Manuel
collection PubMed
description BACKGROUND: Triatoma infestans is the main vector of Chagas disease in the Americas, currently transmitting it in Argentina, Paraguay, and Bolivia. Many T. infestans populations present insecticide resistance, reducing the efficiency of control campaigns. Alternative vector control methods are needed, and molecular targets mediating fundamental physiological processes can be a promising option to manipulate kissing bug behavior. Therefore, it is necessary to characterize the main sensory targets, as well as to determine whether they are modulated by physiological factors. In order to identify gene candidates potentially mediating host cue detection, the antennal transcripts of T. infestans fifth instar larvae were sequenced and assembled. Besides, we evaluated whether a blood meal had an effect on transcriptional profiles, as responsiveness to host-emitted sensory cues depends on bug starvation. RESULTS: The sensory-related gene families of T. infestans were annotated (127 odorant receptors, 38 ionotropic receptors, 11 gustatory receptors, 41 odorant binding proteins, and 25 chemosensory proteins, among others) and compared to those of several other hemipterans, including four triatomine species. Several triatomine-specific lineages representing sensory adaptations developed through the evolution of these blood-feeding heteropterans were identified. As well, we report here various conserved sensory gene orthogroups shared by heteropterans. The absence of the thermosensor pyrexia, of pickpocket receptor subfamilies IV and VII, together with clearly expanded takeout repertoires, are revealed features of the molecular bases of heteropteran antennal physiology. Finally, out of 2,122 genes whose antennal expression was significantly altered by the ingestion of a blood meal, a set of 41 T. infestans sensory-related genes (9 up-regulated; 32 down-regulated) was detected. CONCLUSIONS: We propose that the set of genes presenting nutritionally-triggered modulation on their expression represent candidates to mediate triatomine host-seeking behavior. Besides, the triatomine-specific gene lineages found represent molecular adaptations to their risky natural history that involves stealing blood from an enormously diverse set of vertebrates. Heteropteran gene orthogroups identified may represent unknown features of the sensory specificities of this largest group of hemipteroids. Our work is the first molecular characterization of the peripheral modulation of sensory processes in a non-dipteran vector of human disease. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-09059-6.
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spelling pubmed-98015542022-12-31 The antennal transcriptome of Triatoma infestans reveals substantial expression changes triggered by a blood meal Latorre Estivalis, Jose Manuel Traverso, Lucila Pontes, Gina Lorenzo, Marcelo Gustavo BMC Genomics Research BACKGROUND: Triatoma infestans is the main vector of Chagas disease in the Americas, currently transmitting it in Argentina, Paraguay, and Bolivia. Many T. infestans populations present insecticide resistance, reducing the efficiency of control campaigns. Alternative vector control methods are needed, and molecular targets mediating fundamental physiological processes can be a promising option to manipulate kissing bug behavior. Therefore, it is necessary to characterize the main sensory targets, as well as to determine whether they are modulated by physiological factors. In order to identify gene candidates potentially mediating host cue detection, the antennal transcripts of T. infestans fifth instar larvae were sequenced and assembled. Besides, we evaluated whether a blood meal had an effect on transcriptional profiles, as responsiveness to host-emitted sensory cues depends on bug starvation. RESULTS: The sensory-related gene families of T. infestans were annotated (127 odorant receptors, 38 ionotropic receptors, 11 gustatory receptors, 41 odorant binding proteins, and 25 chemosensory proteins, among others) and compared to those of several other hemipterans, including four triatomine species. Several triatomine-specific lineages representing sensory adaptations developed through the evolution of these blood-feeding heteropterans were identified. As well, we report here various conserved sensory gene orthogroups shared by heteropterans. The absence of the thermosensor pyrexia, of pickpocket receptor subfamilies IV and VII, together with clearly expanded takeout repertoires, are revealed features of the molecular bases of heteropteran antennal physiology. Finally, out of 2,122 genes whose antennal expression was significantly altered by the ingestion of a blood meal, a set of 41 T. infestans sensory-related genes (9 up-regulated; 32 down-regulated) was detected. CONCLUSIONS: We propose that the set of genes presenting nutritionally-triggered modulation on their expression represent candidates to mediate triatomine host-seeking behavior. Besides, the triatomine-specific gene lineages found represent molecular adaptations to their risky natural history that involves stealing blood from an enormously diverse set of vertebrates. Heteropteran gene orthogroups identified may represent unknown features of the sensory specificities of this largest group of hemipteroids. Our work is the first molecular characterization of the peripheral modulation of sensory processes in a non-dipteran vector of human disease. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-09059-6. BioMed Central 2022-12-30 /pmc/articles/PMC9801554/ /pubmed/36585617 http://dx.doi.org/10.1186/s12864-022-09059-6 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Latorre Estivalis, Jose Manuel
Traverso, Lucila
Pontes, Gina
Lorenzo, Marcelo Gustavo
The antennal transcriptome of Triatoma infestans reveals substantial expression changes triggered by a blood meal
title The antennal transcriptome of Triatoma infestans reveals substantial expression changes triggered by a blood meal
title_full The antennal transcriptome of Triatoma infestans reveals substantial expression changes triggered by a blood meal
title_fullStr The antennal transcriptome of Triatoma infestans reveals substantial expression changes triggered by a blood meal
title_full_unstemmed The antennal transcriptome of Triatoma infestans reveals substantial expression changes triggered by a blood meal
title_short The antennal transcriptome of Triatoma infestans reveals substantial expression changes triggered by a blood meal
title_sort antennal transcriptome of triatoma infestans reveals substantial expression changes triggered by a blood meal
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9801554/
https://www.ncbi.nlm.nih.gov/pubmed/36585617
http://dx.doi.org/10.1186/s12864-022-09059-6
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