Sex-Specific Development in Haplodiploid Honeybee is Controlled by the Female-Embryo-Specific Activation of Thousands of Intronic lncRNAs

Abstract

Embryonic development depends on a highly coordinated shift in transcription programs known as the maternal-to-zygotic transition, and sex chromosome silencing occurs during early embryonic development. Here, we applied a single-embryo RNA-seq approach to characterize the embryonic transcriptome dynamics in haploid males vs. diploid females of the happlodiploid insect honeybee (Apis mellifera). We observed typical zygotic genome activation (ZGA) occurred in three major waves specifically in female honeybee embryos; haploid genome activation was much weaker and occurred later. Strikingly, we also observed three waves of transcriptional activation for thousands of long noncoding transcripts (lncRNA), 73% of which are transcribed from intronic regions and 65% were specific to female honeybee embryos. These findings support a model in which introns encode thousands of lncRNAs that are expressed in a diploid-embryo-specific and ZGA-triggered manner that function to silence gene expression from the entire set of extra chromosomes in the females of these haplodiploid animals.