Abstract
BackgroundThe 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.ResultsTo 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.ConclusionCollectively, 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.
Highlights
The mosquito Anopheles stephensi is a vector of urban malaria in Asia that recently invaded Africa
Chakraborty et al BMC Biology (2021) 19:28 (Continued from previous page). 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
In the new reference assembly, the major chromosomes are represented by just three sequences, making this assembly comparable to the Drosophila melanogaster reference assembly, widely considered a gold standard for metazoan genome assembly [22] (Fig. 1b, Table 1, Additional file 1: Figures S4 and S5, Additional file 1: Table S1)
Summary
The mosquito Anopheles stephensi is a vector of urban malaria in Asia that recently invaded Africa. Despite being a pioneering model for transgenics and CRISPR gene drive in malaria vectors [13, 17], the community studying An. stephensi still relies on draft genome assemblies that do not achieve the completeness and contiguity of reference-grade genomes to reveal all the hidden genetic features [7, 18, 19] This limitation obscures genes and repetitive genetic elements that are potentially relevant for understanding parasite transmission or for managing vector populations [20]. These resources facilitate characterization of regions of the genome less accessible to previous efforts, including gene families associated with insecticide resistance, targets for gene-drive interventions, and recalcitrant regions of the genome rich in repeats, including the Y chromosome
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