The neurotranscriptome of the Aedes aegypti mosquito

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Abstract

Background

A complete genome sequence and the advent of genome editing open up non-traditional model organisms to mechanistic genetic studies. The mosquito Aedes aegypti is an important vector of infectious diseases such as dengue, chikungunya, and yellow fever and has a large and complex genome, which has slowed annotation efforts. We used comprehensive transcriptomic analysis of adult gene expression to improve the genome annotation and to provide a detailed tissue-specific catalogue of neural gene expression at different adult behavioral states.

Results

We carried out deep RNA sequencing across all major peripheral male and female sensory tissues, the brain and (female) ovary. Furthermore, we examined gene expression across three important phases of the female reproductive cycle, a remarkable example of behavioral switching in which a female mosquito alternates between obtaining blood-meals from humans and laying eggs. Using genome-guided alignments and de novo transcriptome assembly, our re-annotation includes 572 new putative protein-coding genes and updates to 13.5 and 50.3 % of existing transcripts within coding sequences and untranslated regions, respectively. Using this updated annotation, we detail gene expression in each tissue, identifying large numbers of transcripts regulated by blood-feeding and sexually dimorphic transcripts that may provide clues to the biology of male- and female-specific behaviors, such as mating and blood-feeding, which are areas of intensive study for those interested in vector control.

Conclusions

This neurotranscriptome forms a strong foundation for the study of genes in the mosquito nervous system and investigation of sensory-driven behaviors and their regulation. Furthermore, understanding the molecular genetic basis of mosquito chemosensory behavior has important implications for vector control.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-2239-0) contains supplementary material, which is available to authorized users.

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Most cited references 69

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featureCounts: An efficient general-purpose program for assigning sequence reads to genomic features

, , (2013)

Next-generation sequencing technologies generate millions of short sequence reads, which are usually aligned to a reference genome. In many applications, the key information required for downstream analysis is the number of reads mapping to each genomic feature, for example to each exon or each gene. The process of counting reads is called read summarization. Read summarization is required for a great variety of genomic analyses but has so far received relatively little attention in the literature. We present featureCounts, a read summarization program suitable for counting reads generated from either RNA or genomic DNA sequencing experiments. featureCounts implements highly efficient chromosome hashing and feature blocking techniques. It is considerably faster than existing methods (by an order of magnitude for gene-level summarization) and requires far less computer memory. It works with either single or paired-end reads and provides a wide range of options appropriate for different sequencing applications. featureCounts is available under GNU General Public License as part of the Subread (http://subread.sourceforge.net) or Rsubread (http://www.bioconductor.org) software packages.

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orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET

Matthew DeGennaro, Carolyn S McBride, Laura Seeholzer … (2013)

Female mosquitoes of some species are generalists and will blood-feed on a variety of vertebrate hosts, whereas others display marked host preference. Anopheles gambiae and Aedes aegypti have evolved a strong preference for humans, making them dangerously efficient vectors of malaria and Dengue haemorrhagic fever 1 . Specific host odours likely drive this strong preference since other attractive cues, including body heat and exhaled carbon dioxide (CO2) are common to all warm-blooded hosts 2, 3 . Insects sense odours via several chemosensory receptor families, including the odorant receptors (ORs). ORs are membrane proteins that form heteromeric odour-gated ion channels 4, 5 comprised of a variable ligand-selective subunit and an obligate co-receptor called Orco 6 . Here we use zinc-finger nucleases to generate targeted mutations in the Ae. aegypti orco gene to examine the contribution of Orco and the OR pathway to mosquito host selection and sensitivity to the insect repellent DEET. orco mutant olfactory sensory neurons have greatly reduced spontaneous activity and lack odour-evoked responses. Behaviourally, orco mutant mosquitoes have severely reduced attraction to honey, an odour cue related to floral nectar, and do not respond to human scent in the absence of CO2. However, in the presence of CO2, female orco mutant mosquitoes retain strong attraction to both human and animal hosts, but no longer strongly prefer humans. orco mutant females are attracted to human hosts even in the presence of DEET, but are repelled upon contact, indicating that olfactory- and contact-mediated effects of DEET are mechanistically distinct. We conclude that the OR pathway is crucial for an anthropophilic vector mosquito to discriminate human from non-human hosts and to be effectively repelled by volatile DEET.

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Drosophila neuropeptides in regulation of physiology and behavior.

Dick Nässel, Asa M E Winther (2010)

Studies of neuropeptide and peptide hormone signaling are coming of age in Drosophila due to rapid developments in molecular genetics approaches that overcome the difficulties caused by the small size of the fly. In addition we have genome-wide information on genes involved in peptide signaling, and growing pools of peptidomics data. A large number of different neuropeptides has been identified in a huge variety of neuron types in different parts of the Drosophila nervous system and cells in other locations. This review addresses questions related to peptidergic signaling in the Drosophila nervous system, especially how peptides regulate physiology and behavior during development and in the mature fly. We first summarize novel findings on neuropeptide precursor genes, processed bioactive peptides and their cognate receptors. Thereafter we provide an overview of the physiological and behavioral roles of peptide signaling in Drosophila. These roles include regulation of development, growth, feeding, metabolism, reproduction, homeostasis, and longevity, as well as neuromodulation in learning and memory, olfaction and locomotor control. The substrate of this signaling is the peptide products of about 42 precursor genes expressed in different combinations in a variety of neuronal circuits or that act as circulating hormones. Approximately 45 G-protein-coupled peptide receptors are known in Drosophila and for most of these the ligands have been identified. Functions of some peptides are better understood than others, and much work remains to reveal the spectrum of roles neuropeptides and peptide hormones play in the daily life of a fly. Copyright 2010 Elsevier Ltd. All rights reserved.

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Author and article information

Contributors

Benjamin J. Matthews: Ben.Matthews@rockefeller.edu

Carolyn S. McBride: csm7@princeton.edu

Matthew DeGennaro: mdegenna@fiu.edu

Orion Despo: odespo@stanford.edu

Leslie B. Vosshall: Leslie.Vosshall@rockefeller.edu

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 6 January 2016

Publication date PMC-release: 6 January 2016

Publication date Collection: 2016

Volume: 17

Electronic Location Identifier: 32

Affiliations

[ ]Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY 10065 USA

[ ]Howard Hughes Medical Institute, New York, NY 10065 USA

[ ]Present Address: Department of Ecology and Evolutionary Biology, Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08544 USA

[ ]Present Address: Department of Biological Sciences, Biomolecular Sciences Institute, Florida International University, Miami, FL 33199 USA

[ ]Present address: Stanford University, Stanford, CA 94305 USA

Article

Publisher ID: 2239

DOI: 10.1186/s12864-015-2239-0

PMC ID: 4704297

PubMed ID: 26738925

SO-VID: 805fc3fe-a762-472f-908a-d285252811c3

License:

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.

History

Date received : 3 September 2015

Date accepted : 24 November 2015

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: mosquito,aedes aegypti,mrna-sequencing,de novo genome assembly,host-seeking behavior,neural genes,chemosensory receptors,ion channels,g protein-coupled receptors,gonotrophic cycle,neurogenetics

Data availability:

ScienceOpen disciplines: Genetics

Keywords: mosquito, aedes aegypti, mrna-sequencing, de novo genome assembly, host-seeking behavior, neural genes, chemosensory receptors, ion channels, g protein-coupled receptors, gonotrophic cycle, neurogenetics

The neurotranscriptome of the Aedes aegypti mosquito

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Arabidopsis genomics

Most cited references 69

featureCounts: An efficient general-purpose program for assigning sequence reads to genomic features

orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET

Drosophila neuropeptides in regulation of physiology and behavior.

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