Mahul Chakraborty1, Arunachalam Ramaiah1,2,3, Adriana Adolfi4, Paige Halas4, Bhagyashree Kaduskar2,3, Luna Thanh Ngo1, Suvratha Jayaprasad5, Kiran Paul5, Saurabh Whadgar5, Subhashini Srinivasan3,5, Suresh Subramani3,6,7, Ethan Bier2,7, Anthony A James4,7,8, J J Emerson9,10. 1. Department of Ecology and Evolutionary Biology, University of California, Irvine, CA, 92697, USA. 2. Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, CA, 92093-0335, USA. 3. Tata Institute for Genetics and Society, Center at inStem, Bangalore, Karnataka, 560065, India. 4. Department of Microbiology & Molecular Genetics, University of California, Irvine, CA, 92697, USA. 5. Institute of Bioinformatics and Applied Biotechnology, Bangalore, KA, 560100, India. 6. Section of Molecular Biology, University of California, San Diego, La Jolla, CA, 92093-0322, USA. 7. Tata Institute for Genetics and Society, University of California, San Diego, La Jolla, CA, 92093-0335, USA. 8. Department of Molecular Biology & Biochemistry, University of California, Irvine, CA, 92697, USA. 9. Department of Ecology and Evolutionary Biology, University of California, Irvine, CA, 92697, USA. jje@uci.edu. 10. Center for Complex Biological Systems, University of California, Irvine, CA, 92697, USA. jje@uci.edu.
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 (TE) 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 throughout male development and adulthood, suggesting an important role. CONCLUSION: Collectively, these results and resources underscore the significance of previously hidden genomic elements in the biology of malaria mosquitoes and will accelerate the development of genetic control strategies of malaria transmission.
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 (TE) 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 throughout male development and adulthood, suggesting an important role. CONCLUSION: Collectively, these results and resources underscore the significance of previously hidden genomic elements in the biology of malaria mosquitoes and will accelerate the development of genetic control strategies of malaria transmission.
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