Sequencing of
            <i>Culex quinquefasciatus</i>
            Establishes a Platform for Mosquito Comparative Genomics

Arensburger, Peter; Mégy, Karyn; Waterhouse, Robert M.; Abrudan, Jenica; Amedeo, Paolo; Antelo, Beatriz; Bartholomay, Lyric C.; Bidwell, Shelby L.; Caler, Elisabet; Câmara, Francisco; Campbell, Corey L.; Campbell, Kathryn S.; Casola, Claudio; Castro, Marta T; Chandramouliswaran, Ishwar; Chapman, Sinéad B.; Christley, Scott; Costas, Javier; Eisenstadt, Eric; Feschotte, Cédric; Fraser, Claire M.; Guigó, Roderic; Haas, Brian J.; Hammond, Martin; Hansson, Bill S.; Hemingway, Janet; Hill, Sharon R.; Howarth, Clint; Ignell, Rickard; Kennedy, Ryan; Kodira, Chinnappa D.; Lobo, Neil F.; Mao, Chunhong; Mayhew, George F.; Michel, Kristin; Mori, Akio; Liu, Nannan; Naveira, Horacio; Nene, Vishvanath; Nguyen, Nam Q.; Pearson, Matthew D.; Pritham, Ellen J.; Puiu, Daniela; Qi, Yumin; Ranson, Hilary; Ribeiro, José M. C.; Roberston, Hugh M; Severson, David W.; Shumway, Martin; Stanke, Mario; Strausberg, Robert L.; Sun, C. Jung; Sutton, Granger; Tu, Zhijian; Tubío, José M. C.; Unger, Maria; Vanlandingham, Dana L.; Vilella, Albert J.; White, Owen; White, Jared; Wondji, Charles S.; Wortman, Jennifer; Zdobnov, Evgeny M.; Birren, Bruce W.; Christensen, Bruce M.; Collins, Frank H.; Cornel, Anthony J.; Dimopoulos, George; Hannick, Linda I.; Higgs, Stephen; Lanzaro, Gregory C.; Lawson, Daniel; Lee, Norman H.; Muskavitch, Marc A. T.; Raikhel, Alexander S.; Atkinson, Peter W.

doi:10.1126/science.1191864

Cited by 438 publications

(472 citation statements)

References 10 publications

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“…Deep targeted sequencing for studying insecticide resistance Screening for genomic changes associated with insecticide resistance remained challenging until the sequencing of mosquito genomes (Holt et al 2002;Nene et al 2007;Arensburger et al 2010). Afterward, the development of mosquito DNA microarrays allowed screening for resistance genes based on their differential transcription, leading to the identification of detoxification genes conferring resistance (David et al 2005Strode et al 2008;Vontas et al 2010;Edi et al 2014).…”

Section: Discussionmentioning

confidence: 99%

Identifying genomic changes associated with insecticide resistance in the dengue mosquito Aedes aegypti by deep targeted sequencing

et al. 2015

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The capacity of mosquitoes to resist insecticides threatens the control of diseases such as dengue and malaria. Until alternative control tools are implemented, characterizing resistance mechanisms is crucial for managing resistance in natural populations. Insecticide biodegradation by detoxification enzymes is a common resistance mechanism; however, the genomic changes underlying this mechanism have rarely been identified, precluding individual resistance genotyping. In particular, the role of copy number variations (CNVs) and polymorphisms of detoxification enzymes have never been investigated at the genome level, although they can represent robust markers of metabolic resistance. In this context, we combined target enrichment with high-throughput sequencing for conducting the first comprehensive screening of gene amplifications and polymorphisms associated with insecticide resistance in mosquitoes. More than 760 candidate genes were captured and deep sequenced in several populations of the dengue mosquito Ae. aegypti displaying distinct genetic backgrounds and contrasted resistance levels to the insecticide deltamethrin. CNV analysis identified 41 gene amplifications associated with resistance, most affecting cytochrome P450s overtranscribed in resistant populations. Polymorphism analysis detected more than 30,000 variants and strong selection footprints in specific genomic regions. Combining Bayesian and allele frequency filtering approaches identified 55 nonsynonymous variants strongly associated with resistance. Both CNVs and polymorphisms were conserved within regions but differed across continents, confirming that genomic changes underlying metabolic resistance to insecticides are not universal. By identifying novel DNA markers of insecticide resistance, this study opens the way for tracking down metabolic changes developed by mosquitoes to resist insecticides within and among populations.

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Section: Discussionmentioning

confidence: 99%

Identifying genomic changes associated with insecticide resistance in the dengue mosquito Aedes aegypti by deep targeted sequencing

et al. 2015

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“…We compared the An. gambiae genome with Culex quinquefasciatus, a distantly related species that is estimated to have last shared a common ancestor ∼145 million years ago (15,16), to find conserved chromosomal domains. Our approach differs from previous studies in vector competence, in which candidate genes were identified on the basis of changes in transcription profiles after parasite challenges.…”

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confidence: 99%

Genome-block expression-assisted association studies discover malaria resistance genes in Anopheles gambiae

Wang

Zhang

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The malaria parasite-resistance island (PRI) of the African mosquito vector, Anopheles gambiae, was mapped to five genomic regions containing 80 genes, using coexpression patterns of genomic blocks. High-throughput sequencing identified 347 nonsynonymous single-nucleotide polymorphisms within these genes in mosquitoes from malaria-endemic areas in Kenya. Direct association studies between nonsynonymous single-nucleotide polymorphisms and Plasmodium falciparum infection identified three naturally occurring genetic variations in each of three genes (An. gambiae adenosine deaminase, fibrinogen-related protein 30, and fibrinogenrelated protein 1) that were associated significantly with parasite infection. A role for these genes in the resistance phenotype was confirmed by RNA interference knockdown assays. Silencing fibrinogen-related protein 30 increased parasite infection significantly, whereas ablation of fibrinogen-related protein 1 transcripts resulted in mosquitoes nearly free of parasites. The discovered genes and single-nucleotide polymorphisms are anticipated to be useful in the development of tools for malaria control in endemic areas in Africa.synteny | genomics | traits | chromosomal domains | gene expression

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“…In culicines, such as Aedes and Culex, chromosomes are homomorphic and each pair, traditionally referred to as chromosomes 1, 2 and 3, undergoes recombination. In Culex and Aedes, chromosome 1 is sex determining; its p and q arms are largely syntenic to, respectively, the X chromosome and chromosomal arm 2R of Anopheles gambiae (Nene et al, 2007;Arensburger et al, 2010). In Aedes aegypti males, one chromosome of the chromosome 1 pair (hereafter called the M-chromosome, as opposed to the non-sex-specific m-chromosome) carries the SDR that does not recombine and harbors a dominant male-determining gene Nix (Hall et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

The sex locus is tightly linked to factors conferring sex-specific lethal effects in the mosquito Aedes aegypti

et al. 2016

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In many taxa, sex chromosomes are heteromorphic and largely non-recombining. Evolutionary models predict that spread of recombination suppression on the Y chromosome is fueled by the accumulation of sexually antagonistic alleles in close linkage to the sex determination region. However, empirical evidence for the existence of sexually antagonistic alleles is scarce. In the mosquito Aedes aegypti, the sex-determining chromosomes are homomorphic. The region of suppressed recombination, which surrounds the male-specific sex-determining gene, remains very small, despite ancient origin of the sex chromosomes in the Aedes lineage. We conducted a genetic analysis of the A. aegypti chromosome region tightly linked to the sex locus. We used a strain with an enhanced green fluorescent protein (EGFP)-tagged transgene inserted near the male-determining gene to monitor crossing-over events close to the boundary of the sex-determining region (SDR), and to trace the inheritance pattern of the transgene in relation to sex. In a series of crossing experiments involving individuals with a recombinant sex chromosome we found developmental abnormalities leading to 1:2 sex biases, caused by lethality of half of the male or female progeny. Our results suggest that various factors causing sex-specific lethal effects are clustered within the neighborhood of the SDR, which in the affected sex are likely lost or gained through recombination, leading to death. These may include genes that are recessive lethal, vital for development and/or sexually antagonistic. The sex chromosome fragment in question represents a fascinating test case for the analysis of processes that shape stable boundaries of a non-recombining region.

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Sequencing of Culex quinquefasciatus Establishes a Platform for Mosquito Comparative Genomics

Cited by 438 publications

References 10 publications

Identifying genomic changes associated with insecticide resistance in the dengue mosquito Aedes aegypti by deep targeted sequencing

Identifying genomic changes associated with insecticide resistance in the dengue mosquito Aedes aegypti by deep targeted sequencing

Genome-block expression-assisted association studies discover malaria resistance genes in Anopheles gambiae

The sex locus is tightly linked to factors conferring sex-specific lethal effects in the mosquito Aedes aegypti

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