Abstract
BackgroundThe Asian malaria mosquito, Anopheles stephensi, is a major urban malaria vector in the Middle East and on the Indian subcontinent. Early zygotic transcription, which marks the maternal-to-zygotic transition, has not been systematically studied in An. stephensi or any other Anopheles mosquitoes. Improved understanding of early embryonic gene expression in An. stephensi will facilitate genetic and evolutionary studies and help with the development of novel control strategies for this important disease vector.ResultsWe obtained RNA-seq data in biological triplicates from four early An. stephensi embryonic time points. Using these data, we identified 70 and 153 pure early zygotic genes (pEZGs) under stringent and relaxed conditions, respectively. We show that these pEZGs are enriched in functional groups related to DNA-binding transcription regulators, cell cycle modulators, proteases, transport, and cellular metabolism. On average these pEZGs are shorter and have less introns than other An. stephensi genes. Some of the pEZGs may arise de novo while others have clear non-pEZG paralogs. There is no or very limited overlap between An. stephensi pEZGs and Drosophila melanogaster or Aedes aegypti pEZGs. Interestingly, the upstream region of An. stephensi pEZGs lack significant enrichment of a previously reported TAGteam/VBRGGTA motif found in the regulatory region of pEZGs in D. melanogaster and Ae. aegypti. However, a GT-rich motif was found in An. stephensi pEZGs instead.ConclusionsWe have identified a number of pEZGs whose predicted functions and structures are consistent with their collective roles in the degradation of maternally deposited components, activation of the zygotic genome, cell division, and metabolism. The pEZGs appear to rapidly turn over within the Dipteran order and even within the Culicidae family. These pEZGs, and the shared regulatory motif, could provide the promoter or regulatory sequences to drive gene expression in the syncytial or early cellular blastoderm, a period when the developing embryo is accessible to genetic manipulation. In addition, these molecular resources may be used to achieve sex separation of mosquitoes for sterile insect technique.
Highlights
The genus Anopheles includes dozens of mosquito species that are important vectors of malaria, one of humankind’s most deadly and costly diseases [1]
We focused on the period of maternal-to-zygotic transition and obtained RNA-seq data in biological triplicates from early embryos at time points 0-1, 2-4, 4-8, and 8-12 h post-oviposition
To be consistent with previous analyses in Ae. aegypti [14] and D. melanogaster [15], we focused on the pure early zygotic genes, which are genes that have no maternally deposited transcripts but are initially transcribed during the maternalto-zygotic transition
Summary
The genus Anopheles includes dozens of mosquito species that are important vectors of malaria, one of humankind’s most deadly and costly diseases [1]. We are interested in the early embryonic stage when the maternal-to-zygotic transition (MZT) occurs in An. stephensi. The MZT includes the syncytial blastoderm and early cellular blastoderm stages, during which the developing embryo is more accessible to genetic. The MZT is of fundamental importance in embryonic development, it represents a stage where genetic manipulation could lead to novel mosquito control strategies. In Drosophila, the first 13 cycles of nuclear division are rapid and without the formation of new cellular membranes In these early embryos, up to thousands of nuclei share the same cytoplasm in a syncytial blastoderm [11]. Improved understanding of early embryonic gene expression in An. stephensi will facilitate genetic and evolutionary studies and help with the development of novel control strategies for this important disease vector
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