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

Xiaofang Jiang, Ashley Peery, A. Brantley Hall, Atashi Sharma, Xiao Guang Chen, Robert M. Waterhouse, Aleksey Komissarov, Michelle M. Riehle, Yogesh Shouche, Maria V. Sharakhova, Dan Lawson, Nazzy Pakpour, Peter Arensburger, Victoria L M Davidson, Karin Eiglmeier, Scott Emrich, Phillip George, Ryan C. Kennedy, Shrinivasrao P. Mane, Gareth Maslen & 15 others Chioma Oringanje, Yumin Qi, Robert Settlage, Marta Tojo, Jose M C Tubio, Maria F. Unger, Bo Wang, Kenneth D. Vernick, Jose M C Ribeiro, Anthony A. James, Kristin Michel, Michael A. Riehle, Shirley Luckhart, Igor V. Sharakhov, Zhijian Tu

Research output: Contribution to journalArticle

49 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)459
Number of pages1
JournalGenome Biology
Volume15
Issue number9
DOIs
StatePublished - 2014
Externally publishedYes

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Anopheles stephensi
Anopheles
malaria
mosquito
Malaria
chromosome
Culicidae
genome
Genome
chromosomes
Chromosomes
immunity
RNA
Parasites
genome assembly
parasites
molecular models
parasite
physical chromosome mapping
autosomes

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Cell Biology

Cite this

Jiang, X., Peery, A., Hall, A. B., Sharma, A., Chen, X. G., Waterhouse, R. M., ... Tu, Z. (2014). Genome analysis of a major urban malaria vector mosquito, Anopheles stephensi. Genome Biology, 15(9), 459. https://doi.org/10.1186/s13059-014-0459-2

Genome analysis of a major urban malaria vector mosquito, Anopheles stephensi. / Jiang, Xiaofang; Peery, Ashley; Hall, A. Brantley; Sharma, Atashi; Chen, Xiao Guang; Waterhouse, Robert M.; Komissarov, Aleksey; Riehle, Michelle M.; Shouche, Yogesh; Sharakhova, Maria V.; Lawson, Dan; Pakpour, Nazzy; Arensburger, Peter; Davidson, Victoria L M; Eiglmeier, Karin; Emrich, Scott; George, Phillip; Kennedy, Ryan C.; Mane, Shrinivasrao P.; Maslen, Gareth; Oringanje, Chioma; Qi, Yumin; Settlage, Robert; Tojo, Marta; Tubio, Jose M C; Unger, Maria F.; Wang, Bo; Vernick, Kenneth D.; Ribeiro, Jose M C; James, Anthony A.; Michel, Kristin; Riehle, Michael A.; Luckhart, Shirley; Sharakhov, Igor V.; Tu, Zhijian.

In: Genome Biology, Vol. 15, No. 9, 2014, p. 459.

Research output: Contribution to journalArticle

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, VLM, Eiglmeier, K, Emrich, S, George, P, Kennedy, RC, Mane, SP, Maslen, G, Oringanje, C, Qi, Y, Settlage, R, Tojo, M, Tubio, JMC, Unger, MF, Wang, B, Vernick, KD, Ribeiro, JMC, James, AA, Michel, K, Riehle, MA, Luckhart, S, Sharakhov, IV & Tu, Z 2014, 'Genome analysis of a major urban malaria vector mosquito, Anopheles stephensi', Genome Biology, vol. 15, no. 9, pp. 459. https://doi.org/10.1186/s13059-014-0459-2
Jiang, Xiaofang ; Peery, Ashley ; Hall, A. Brantley ; Sharma, Atashi ; Chen, Xiao Guang ; Waterhouse, Robert M. ; Komissarov, Aleksey ; Riehle, Michelle M. ; Shouche, Yogesh ; Sharakhova, Maria V. ; Lawson, Dan ; Pakpour, Nazzy ; Arensburger, Peter ; Davidson, Victoria L M ; Eiglmeier, Karin ; Emrich, Scott ; George, Phillip ; Kennedy, Ryan C. ; Mane, Shrinivasrao P. ; Maslen, Gareth ; Oringanje, Chioma ; Qi, Yumin ; Settlage, Robert ; Tojo, Marta ; Tubio, Jose M C ; Unger, Maria F. ; Wang, Bo ; Vernick, Kenneth D. ; Ribeiro, Jose M C ; James, Anthony A. ; Michel, Kristin ; Riehle, Michael A. ; Luckhart, Shirley ; Sharakhov, Igor V. ; Tu, Zhijian. / Genome analysis of a major urban malaria vector mosquito, Anopheles stephensi. In: Genome Biology. 2014 ; Vol. 15, No. 9. pp. 459.
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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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T1 - Genome analysis of a major urban malaria vector mosquito, Anopheles stephensi

AU - Jiang, Xiaofang

AU - Peery, Ashley

AU - Hall, A. Brantley

AU - Sharma, Atashi

AU - Chen, Xiao Guang

AU - Waterhouse, Robert M.

AU - Komissarov, Aleksey

AU - Riehle, Michelle M.

AU - Shouche, Yogesh

AU - Sharakhova, Maria V.

AU - Lawson, Dan

AU - Pakpour, Nazzy

AU - Arensburger, Peter

AU - Davidson, Victoria L M

AU - Eiglmeier, Karin

AU - Emrich, Scott

AU - George, Phillip

AU - Kennedy, Ryan C.

AU - Mane, Shrinivasrao P.

AU - Maslen, Gareth

AU - Oringanje, Chioma

AU - Qi, Yumin

AU - Settlage, Robert

AU - Tojo, Marta

AU - Tubio, Jose M C

AU - Unger, Maria F.

AU - Wang, Bo

AU - Vernick, Kenneth D.

AU - Ribeiro, Jose M C

AU - James, Anthony A.

AU - Michel, Kristin

AU - Riehle, Michael A.

AU - Luckhart, Shirley

AU - Sharakhov, Igor V.

AU - Tu, Zhijian

PY - 2014

Y1 - 2014

N2 - 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.

AB - 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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DO - 10.1186/s13059-014-0459-2

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JO - Genome Biology

JF - Genome Biology

SN - 1465-6914

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