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Hidden genomic features of an invasive malaria vector, Anopheles stephensi

View ORCID ProfileMahul Chakraborty, View ORCID ProfileArunachalam Ramaiah, View ORCID ProfileAdriana Adolfi, Paige Halas, View ORCID ProfileBhagyashree Kaduskar, Luna Thanh Ngo, Suvratha Jayaprasad, Kiran Paul, Saurabh Whadgar, Subhashini Srinivasan, Suresh Subramani, View ORCID ProfileEthan Bier, Anthony A. James, View ORCID ProfileJ.J. Emerson
doi: https://doi.org/10.1101/2020.05.24.113019
Mahul Chakraborty
1Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA
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Arunachalam Ramaiah
1Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA
2Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, CA 92093-0335, USA
3Tata Institute for Genetics and Society, Center at inStem, Bangalore, KA 560065, India
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Adriana Adolfi
4Department of Microbiology & Molecular Genetics, University of California, Irvine, CA 92697, USA
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Paige Halas
4Department of Microbiology & Molecular Genetics, University of California, Irvine, CA 92697, USA
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Bhagyashree Kaduskar
2Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, CA 92093-0335, USA
3Tata Institute for Genetics and Society, Center at inStem, Bangalore, KA 560065, India
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Luna Thanh Ngo
1Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA
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Suvratha Jayaprasad
5Institute of Bioinformatics and Applied Biotechnology, Bangalore, KA 560100, India
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Kiran Paul
5Institute of Bioinformatics and Applied Biotechnology, Bangalore, KA 560100, India
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Saurabh Whadgar
5Institute of Bioinformatics and Applied Biotechnology, Bangalore, KA 560100, India
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Subhashini Srinivasan
3Tata Institute for Genetics and Society, Center at inStem, Bangalore, KA 560065, India
5Institute of Bioinformatics and Applied Biotechnology, Bangalore, KA 560100, India
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Suresh Subramani
3Tata Institute for Genetics and Society, Center at inStem, Bangalore, KA 560065, India
6Section of Molecular Biology, University of California, San Diego, La Jolla, CA 92093-0322, USA
7Tata Institute for Genetics and Society, University of California, San Diego, La Jolla, CA 92093-0335, USA
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Ethan Bier
2Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, CA 92093-0335, USA
7Tata Institute for Genetics and Society, University of California, San Diego, La Jolla, CA 92093-0335, USA
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Anthony A. James
4Department of Microbiology & Molecular Genetics, University of California, Irvine, CA 92697, USA
7Tata Institute for Genetics and Society, University of California, San Diego, La Jolla, CA 92093-0335, USA
8Department of Molecular Biology & Biochemistry, University of California, Irvine, CA 92697, USA
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J.J. Emerson
1Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA
9Center for Complex Biological Systems, University of California, Irvine, CA 92697, USA
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  • For correspondence: jje@uci.edu
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Abstract

Background The mosquito Anopheles stephensi is a vector of urban malaria in Asia that recently invaded Africa. Studying the genetic basis of vectorial capacity and engineering genetic interventions are both impeded by limitations of a vector’s genome assembly. The existing assemblies of An. stephensi are draft-quality and contain thousands of sequence gaps, potentially missing genetic elements important for its biology and evolution.

Results To access previously intractable genomic regions, we generated a reference-grade genome assembly and full transcript annotations that achieve a new standard for reference genomes of disease vectors. Here, we report novel species-specific transposable element families and insertions in functional genetic elements, demonstrating the widespread role of TEs in genome evolution and phenotypic variation. We discovered 29 previously hidden members of insecticide resistance genes, uncovering new candidate genetic elements for the widespread insecticide resistance observed in An. stephensi. We identified 2.4 Mb of the Y-chromosome and seven new male-linked gene candidates, representing the most extensive coverage of the Y-chromosome in any mosquito. By tracking full length mRNA for >15 days following blood feeding, we discover distinct roles of previously uncharacterized genes in blood metabolism and female reproduction. The Y-linked heterochromatin landscape reveals extensive accumulation of long-terminal repeat retrotransposons throughout the evolution and degeneration of this chromosome. Finally, we identify a novel Y-linked putative transcription factor that is expressed constitutively through male development and adulthood, suggesting an important role throughout male development.

Conclusion Collectively, these results and resources underscore the significance of previously hidden genomic elements in the biology of malaria mosquitoes and will accelerate development of genetic control strategies of malaria transmission.

Competing Interest Statement

EB has equity interest in two companies: Synbal Inc. and Agragene, Inc. These companies that may potentially benefit from the research results. E.B. also serves on the Synbal Inc. Board of Directors and Scientific Advisory Board and on Agragene Inc. Scientific Advisory Board. The terms of these arrangements have been reviewed and approved by the University of California, San Diego in accordance with its conflict of interest policies. All other authors declare no conflict of interest.

Footnotes

  • We have revised all figures, the assembly description, and Methods. We have also added a new paragraph on immune-gene function.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Hidden genomic features of an invasive malaria vector, Anopheles stephensi
Mahul Chakraborty, Arunachalam Ramaiah, Adriana Adolfi, Paige Halas, Bhagyashree Kaduskar, Luna Thanh Ngo, Suvratha Jayaprasad, Kiran Paul, Saurabh Whadgar, Subhashini Srinivasan, Suresh Subramani, Ethan Bier, Anthony A. James, J.J. Emerson
bioRxiv 2020.05.24.113019; doi: https://doi.org/10.1101/2020.05.24.113019
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Hidden genomic features of an invasive malaria vector, Anopheles stephensi
Mahul Chakraborty, Arunachalam Ramaiah, Adriana Adolfi, Paige Halas, Bhagyashree Kaduskar, Luna Thanh Ngo, Suvratha Jayaprasad, Kiran Paul, Saurabh Whadgar, Subhashini Srinivasan, Suresh Subramani, Ethan Bier, Anthony A. James, J.J. Emerson
bioRxiv 2020.05.24.113019; doi: https://doi.org/10.1101/2020.05.24.113019

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