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RNA-Seq analysis of blood meal induced gene-expression changes in Aedes aegypti ovaries

BACKGROUND: Transmission of pathogens by vector mosquitoes is intrinsically linked with mosquito’s reproductive strategy because anautogenous mosquitoes require vertebrate blood to develop a batch of eggs. Each cycle of egg maturation is tightly linked with the intake of a fresh blood meal for most...

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Autores principales: Nag, Dilip K., Dieme, Constentin, Lapierre, Pascal, Lasek-Nesselquist, Erica, Kramer, Laura D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8161926/
https://www.ncbi.nlm.nih.gov/pubmed/34044772
http://dx.doi.org/10.1186/s12864-021-07551-z
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author Nag, Dilip K.
Dieme, Constentin
Lapierre, Pascal
Lasek-Nesselquist, Erica
Kramer, Laura D.
author_facet Nag, Dilip K.
Dieme, Constentin
Lapierre, Pascal
Lasek-Nesselquist, Erica
Kramer, Laura D.
author_sort Nag, Dilip K.
collection PubMed
description BACKGROUND: Transmission of pathogens by vector mosquitoes is intrinsically linked with mosquito’s reproductive strategy because anautogenous mosquitoes require vertebrate blood to develop a batch of eggs. Each cycle of egg maturation is tightly linked with the intake of a fresh blood meal for most species. Mosquitoes that acquire pathogens during the first blood feeding can transmit the pathogens to susceptible hosts during subsequent blood feeding and also vertically to the next generation via infected eggs. Large-scale gene-expression changes occur following each blood meal in various tissues, including ovaries. Here we analyzed mosquito ovary transcriptome following a blood meal at three different time points to investigate blood-meal induced changes in gene expression in mosquito ovaries. RESULTS: We collected ovaries from Aedes aegypti that received a sugar meal or a blood meal on days 3, 10 and 20 post blood meal for transcriptome analysis. Over 4000 genes responded differentially following ingestion of a blood meal on day 3, and 660 and 780 genes on days 10 and 20, respectively. Proteins encoded by differentially expressed genes (DEGs) on day 3 include odorant binding proteins (OBPs), defense-specific proteins, and cytochrome P450 detoxification enzymes. In addition, we identified 580 long non-coding RNAs that are differentially expressed at three time points. Gene ontology analysis indicated that genes involved in peptidase activity, oxidoreductase activity, extracellular space, and hydrolase activity, among others were enriched on day 3. Although most of the DEGs returned to the nonsignificant level compared to the sugar-fed mosquito ovaries following oviposition on days 10 and 20, there remained differences in the gene expression pattern in sugar-fed and blood-fed mosquitoes. CONCLUSIONS: Enrichment of OBPs following blood meal ingestion suggests that these genes may have other functions besides being part of the olfactory system. The enrichment of immune-specific genes and cytochrome P450 genes indicates that ovaries become well prepared to protect their germ line from any pathogens that may accompany the blood meal or from environmental contamination during oviposition, and to deal with the detrimental effects of toxic metabolites. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07551-z.
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spelling pubmed-81619262021-06-01 RNA-Seq analysis of blood meal induced gene-expression changes in Aedes aegypti ovaries Nag, Dilip K. Dieme, Constentin Lapierre, Pascal Lasek-Nesselquist, Erica Kramer, Laura D. BMC Genomics Research Article BACKGROUND: Transmission of pathogens by vector mosquitoes is intrinsically linked with mosquito’s reproductive strategy because anautogenous mosquitoes require vertebrate blood to develop a batch of eggs. Each cycle of egg maturation is tightly linked with the intake of a fresh blood meal for most species. Mosquitoes that acquire pathogens during the first blood feeding can transmit the pathogens to susceptible hosts during subsequent blood feeding and also vertically to the next generation via infected eggs. Large-scale gene-expression changes occur following each blood meal in various tissues, including ovaries. Here we analyzed mosquito ovary transcriptome following a blood meal at three different time points to investigate blood-meal induced changes in gene expression in mosquito ovaries. RESULTS: We collected ovaries from Aedes aegypti that received a sugar meal or a blood meal on days 3, 10 and 20 post blood meal for transcriptome analysis. Over 4000 genes responded differentially following ingestion of a blood meal on day 3, and 660 and 780 genes on days 10 and 20, respectively. Proteins encoded by differentially expressed genes (DEGs) on day 3 include odorant binding proteins (OBPs), defense-specific proteins, and cytochrome P450 detoxification enzymes. In addition, we identified 580 long non-coding RNAs that are differentially expressed at three time points. Gene ontology analysis indicated that genes involved in peptidase activity, oxidoreductase activity, extracellular space, and hydrolase activity, among others were enriched on day 3. Although most of the DEGs returned to the nonsignificant level compared to the sugar-fed mosquito ovaries following oviposition on days 10 and 20, there remained differences in the gene expression pattern in sugar-fed and blood-fed mosquitoes. CONCLUSIONS: Enrichment of OBPs following blood meal ingestion suggests that these genes may have other functions besides being part of the olfactory system. The enrichment of immune-specific genes and cytochrome P450 genes indicates that ovaries become well prepared to protect their germ line from any pathogens that may accompany the blood meal or from environmental contamination during oviposition, and to deal with the detrimental effects of toxic metabolites. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07551-z. BioMed Central 2021-05-27 /pmc/articles/PMC8161926/ /pubmed/34044772 http://dx.doi.org/10.1186/s12864-021-07551-z Text en © The Author(s) 2021 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 Article
Nag, Dilip K.
Dieme, Constentin
Lapierre, Pascal
Lasek-Nesselquist, Erica
Kramer, Laura D.
RNA-Seq analysis of blood meal induced gene-expression changes in Aedes aegypti ovaries
title RNA-Seq analysis of blood meal induced gene-expression changes in Aedes aegypti ovaries
title_full RNA-Seq analysis of blood meal induced gene-expression changes in Aedes aegypti ovaries
title_fullStr RNA-Seq analysis of blood meal induced gene-expression changes in Aedes aegypti ovaries
title_full_unstemmed RNA-Seq analysis of blood meal induced gene-expression changes in Aedes aegypti ovaries
title_short RNA-Seq analysis of blood meal induced gene-expression changes in Aedes aegypti ovaries
title_sort rna-seq analysis of blood meal induced gene-expression changes in aedes aegypti ovaries
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8161926/
https://www.ncbi.nlm.nih.gov/pubmed/34044772
http://dx.doi.org/10.1186/s12864-021-07551-z
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