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Genome analysis of a major urban malaria vector mosquito, Anopheles stephensi.

Jiang X, Peery A, Hall AB, Sharma A, Chen XG, Waterhouse RM, Komissarov A, Riehle MM, Shouche Y, Sharakhova MV, Lawson D, Pakpour N, Arensburger P, Davidson VL, Eiglmeier K, Emrich S, George P, Kennedy RC, Mane SP, Maslen G, Oringanje C, Qi Y, Settlage R, Tojo M, Tubio JM, Unger MF, Wang B, Vernick KD, Ribeiro JM, James AA, Michel K, Riehle MA, Luckhart S, Sharakhov IV, Tu Z - Genome Biol. (2014)

Bottom Line: RNA-seq analyses provide new insights into mosquito innate immunity, development, and sexual dimorphism.Chromosome-based investigations provide unique perspectives on Anopheles chromosome evolution.RNA-seq analysis and studies of immunity genes offer new insights into mosquito biology and mosquito-parasite interactions.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Anopheles stephensi is the key vector of malaria throughout the Indian subcontinent and Middle East and an emerging model for molecular and genetic studies of mosquito-parasite interactions. The type form of the species is responsible for the majority of urban malaria transmission across its range.

Results: Here, we report the genome sequence and annotation of the Indian strain of the type form of An. stephensi. The 221 Mb genome assembly represents more than 92% of the entire genome and was produced using a combination of 454, Illumina, and PacBio sequencing. Physical mapping assigned 62% of the genome onto chromosomes, enabling chromosome-based analysis. Comparisons between An. stephensi and An. gambiae reveal that the rate of gene order reshuffling on the X chromosome was three times higher than that on the autosomes. An. stephensi has more heterochromatin in pericentric regions but less repetitive DNA in chromosome arms than An. gambiae. We also identify a number of Y-chromosome contigs and BACs. Interspersed repeats constitute 7.1% of the assembled genome while LTR retrotransposons alone comprise more than 49% of the Y contigs. RNA-seq analyses provide new insights into mosquito innate immunity, development, and sexual dimorphism.

Conclusions: The genome analysis described in this manuscript provides a resource and platform for fundamental and translational research into a major urban malaria vector. Chromosome-based investigations provide unique perspectives on Anopheles chromosome evolution. RNA-seq analysis and studies of immunity genes offer new insights into mosquito biology and mosquito-parasite interactions.

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Molecular species phylogeny and orthology. (A) The maximum likelihood molecular species phylogeny estimated from universal single-copy orthologs supports the recognized species relationships with An. stephensi and An. gambiae in subgenus Cellia within the genus Anopheles. (B) Comparative analysis of orthologs from An. stephensi, An. gambiae, Ae. aegypti, and D. melanogaster. Orthologous genes were retrieved from OrthoDB. A total of 7,305 genes were shared among all four species, 1,297 genes were specific to An. stephensi, 653 genes were Anopheles-specific, and 1,863 genes were mosquito-specific.
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Fig2: Molecular species phylogeny and orthology. (A) The maximum likelihood molecular species phylogeny estimated from universal single-copy orthologs supports the recognized species relationships with An. stephensi and An. gambiae in subgenus Cellia within the genus Anopheles. (B) Comparative analysis of orthologs from An. stephensi, An. gambiae, Ae. aegypti, and D. melanogaster. Orthologous genes were retrieved from OrthoDB. A total of 7,305 genes were shared among all four species, 1,297 genes were specific to An. stephensi, 653 genes were Anopheles-specific, and 1,863 genes were mosquito-specific.

Mentions: A total of 11,789 protein-encoding genes were annotated using a combination of homology and de novo prediction. These gene models have been submitted to the NCBI (GCA_000300775.2) and are hosted in VectorBase [25]. The average transcript length was 3,666 bp and the average number of exons per transcript was 4.18. Evolutionary relationships among An. stephensi and other dipteran insects were evaluated by constructing a maximum likelihood molecular species phylogeny using universal single-copy orthologs (Figure 2A). An. stephensi and An. gambiae form a well-supported clade representing the subgenus Cellia within the genus Anopheles. This phylogeny provides the evolutionary context for current and future comparative genomics analysis. A total 10,492 (89.0%) of the 11,789 predicted An. stephensi protein-encoding genes had orthologs in An. gambiae, Aedes aegypti, and Drosophila melanogaster (Figure 2).Figure 2


Genome analysis of a major urban malaria vector mosquito, Anopheles stephensi.

Jiang X, Peery A, Hall AB, Sharma A, Chen XG, Waterhouse RM, Komissarov A, Riehle MM, Shouche Y, Sharakhova MV, Lawson D, Pakpour N, Arensburger P, Davidson VL, Eiglmeier K, Emrich S, George P, Kennedy RC, Mane SP, Maslen G, Oringanje C, Qi Y, Settlage R, Tojo M, Tubio JM, Unger MF, Wang B, Vernick KD, Ribeiro JM, James AA, Michel K, Riehle MA, Luckhart S, Sharakhov IV, Tu Z - Genome Biol. (2014)

Molecular species phylogeny and orthology. (A) The maximum likelihood molecular species phylogeny estimated from universal single-copy orthologs supports the recognized species relationships with An. stephensi and An. gambiae in subgenus Cellia within the genus Anopheles. (B) Comparative analysis of orthologs from An. stephensi, An. gambiae, Ae. aegypti, and D. melanogaster. Orthologous genes were retrieved from OrthoDB. A total of 7,305 genes were shared among all four species, 1,297 genes were specific to An. stephensi, 653 genes were Anopheles-specific, and 1,863 genes were mosquito-specific.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4195908&req=5

Fig2: Molecular species phylogeny and orthology. (A) The maximum likelihood molecular species phylogeny estimated from universal single-copy orthologs supports the recognized species relationships with An. stephensi and An. gambiae in subgenus Cellia within the genus Anopheles. (B) Comparative analysis of orthologs from An. stephensi, An. gambiae, Ae. aegypti, and D. melanogaster. Orthologous genes were retrieved from OrthoDB. A total of 7,305 genes were shared among all four species, 1,297 genes were specific to An. stephensi, 653 genes were Anopheles-specific, and 1,863 genes were mosquito-specific.
Mentions: A total of 11,789 protein-encoding genes were annotated using a combination of homology and de novo prediction. These gene models have been submitted to the NCBI (GCA_000300775.2) and are hosted in VectorBase [25]. The average transcript length was 3,666 bp and the average number of exons per transcript was 4.18. Evolutionary relationships among An. stephensi and other dipteran insects were evaluated by constructing a maximum likelihood molecular species phylogeny using universal single-copy orthologs (Figure 2A). An. stephensi and An. gambiae form a well-supported clade representing the subgenus Cellia within the genus Anopheles. This phylogeny provides the evolutionary context for current and future comparative genomics analysis. A total 10,492 (89.0%) of the 11,789 predicted An. stephensi protein-encoding genes had orthologs in An. gambiae, Aedes aegypti, and Drosophila melanogaster (Figure 2).Figure 2

Bottom Line: RNA-seq analyses provide new insights into mosquito innate immunity, development, and sexual dimorphism.Chromosome-based investigations provide unique perspectives on Anopheles chromosome evolution.RNA-seq analysis and studies of immunity genes offer new insights into mosquito biology and mosquito-parasite interactions.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Anopheles stephensi is the key vector of malaria throughout the Indian subcontinent and Middle East and an emerging model for molecular and genetic studies of mosquito-parasite interactions. The type form of the species is responsible for the majority of urban malaria transmission across its range.

Results: Here, we report the genome sequence and annotation of the Indian strain of the type form of An. stephensi. The 221 Mb genome assembly represents more than 92% of the entire genome and was produced using a combination of 454, Illumina, and PacBio sequencing. Physical mapping assigned 62% of the genome onto chromosomes, enabling chromosome-based analysis. Comparisons between An. stephensi and An. gambiae reveal that the rate of gene order reshuffling on the X chromosome was three times higher than that on the autosomes. An. stephensi has more heterochromatin in pericentric regions but less repetitive DNA in chromosome arms than An. gambiae. We also identify a number of Y-chromosome contigs and BACs. Interspersed repeats constitute 7.1% of the assembled genome while LTR retrotransposons alone comprise more than 49% of the Y contigs. RNA-seq analyses provide new insights into mosquito innate immunity, development, and sexual dimorphism.

Conclusions: The genome analysis described in this manuscript provides a resource and platform for fundamental and translational research into a major urban malaria vector. Chromosome-based investigations provide unique perspectives on Anopheles chromosome evolution. RNA-seq analysis and studies of immunity genes offer new insights into mosquito biology and mosquito-parasite interactions.

Show MeSH
Related in: MedlinePlus