Abstract
In honeybees, the haplodiploid sex determination system promotes a unique embryogenesis process wherein females develop from fertilized eggs and males develop from unfertilized eggs. However, the developmental strategies of honeybees during early embryogenesis are virtually unknown. Similar to most animals, the honeybee oocytes are supplied with proteins and regulatory elements that support early embryogenesis. As the embryo develops, the zygotic genome is activated and zygotic products gradually replace the preloaded maternal material. The analysis of small RNA and mRNA libraries of mature oocytes and embryos originated from fertilized and unfertilized eggs has allowed us to explore the gene expression dynamics in the first steps of development and during the maternal-to-zygotic transition (MZT). We localized a short sequence motif identified as TAGteam motif and hypothesized to play a similar role in honeybees as in fruit flies, which includes the timing of early zygotic expression (MZT), a function sustained by the presence of the zelda ortholog, which is the main regulator of genome activation. Predicted microRNA (miRNA)-target interactions indicated that there were specific regulators of haploid and diploid embryonic development and an overlap of maternal and zygotic gene expression during the early steps of embryogenesis. Although a number of functions are highly conserved during the early steps of honeybee embryogenesis, the results showed that zygotic genome activation occurs earlier in honeybees than in Drosophila based on the presence of three primary miRNAs (pri-miRNAs) (ame-mir-375, ame-mir-34 and ame-mir-263b) during the cleavage stage in haploid and diploid embryonic development.
Highlights
Embryonic development is the result of a precisely controlled sequence of events modulated by environmental and intracellular signals [1]
Embryogenesis is characterized by maternal elements that are preloaded into eggs and act directly on egg activation, cleavage, and zygotic genome activation (ZGA) [2]
In Drosophila, zelda is described as a maternal transcript that is degraded in early embryogenesis, it is produced by zygotic machinery during blastoderm cellularization [15] when the number of transcribed mRNAs is high as demonstrated through genome-wide approaches [1,17,18,19]
Summary
Embryonic development is the result of a precisely controlled sequence of events modulated by environmental and intracellular signals [1]. The MZT is a dynamic process whereby the degradation of maternal protein and RNA occurs simultaneously with transcriptional reactivation for the synthesis of new molecules, ensuring the essential events of embryonic development [2]. The mRNAs expressed during the first wave are involved in sex determination, patterning, and cellularization [13] Transcription factors such as Zelda (vielfaltig-vlf) are involved in the two waves of ZGA by binding to cis-element conserved TAGteam motifs [13,15,16]. In Drosophila, zelda is described as a maternal transcript that is degraded in early embryogenesis, it is produced by zygotic machinery during blastoderm cellularization [15] when the number of transcribed mRNAs is high as demonstrated through genome-wide approaches [1,17,18,19]. Information on the dynamics of gene expression and the pathways and timing of honeybee development could provide insight into the early development of both types of embryos
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