Sex-specific transcriptome dynamics of Anopheles gambiae during embryonic development

Abstract

Malaria-transmitting mosquitoes are extremely sexually dimorphic in their anatomy and behavior. Sex-specific gene expression in Anopheles gambiae is well studied in adult stages, but its onset during embryogenesis, apart from sex determination factors like Yob, remains largely unknown. Here, we report a comprehensive single-embryo transcriptome atlas of A. gambiae males and females to understand the earliest stages of establishing the sex-specific expression networks. Our data set reveals embryonic RNA isoform diversity, including a global shift toward distal alternative polyadenylation (APA) event sites during the maternal-to-zygotic genome transition. Sex-biased gene expression and alternative splicing are limited during embryogenesis, with most sex-specific patterns emerging postembryonically. X-chromosome dosage compensation (DC) is established shortly after zygotic genome activation, concomitant with direct binding of the master regulator protein SOA to X-linked promoters. In contrast to known DC regulators in other species, we did not find evidence for early high-affinity sites or distance-dependent patterns in Anopheles. Instead, SOA binding and DC are dynamically specified on genes according to gene activity, where the most strongly expressed genes tend to show the strongest SOA binding. We propose that the Anopheles DC system represents an extreme case of a gene-by-gene regulatory mechanism that operates at the chromosome-wide level.