Abstract
Major developmental transitions in multicellular organisms are driven by steroid hormones. In insects, these, together with juvenile hormone (JH), control development, metamorphosis, reproduction and aging, and are also suggested to play an important role in caste differentiation of social insects. Here, we aimed to determine how EcR transcription and ecdysteroid titers are related during honeybee postembryonic development and what may actually be the role of EcR in caste development of this social insect. In addition, we expected that knocking-down EcR gene expression would give us information on the participation of the respective protein in regulating downstream targets of EcR. We found that in Apis mellifera females, EcR-A is the predominantly expressed variant in postembryonic development, while EcR-B transcript levels are higher in embryos, indicating an early developmental switch in EcR function. During larval and pupal stages, EcR-B expression levels are very low, while EcR-A transcripts are more variable and abundant in workers compared to queens. Strikingly, these transcript levels are opposite to the ecdysteroid titer profile. 20-hydroxyecdysone (20E) application experiments revealed that low 20E levels induce EcR expression during development, whereas high ecdysteroid titers seem to be repressive. By means of RNAi-mediated knockdown (KD) of both EcR transcript variants we detected the differential expression of 234 poly-A+ transcripts encoding genes such as CYPs, MRJPs and certain hormone response genes (Kr-h1 and ftz-f1). EcR-KD also promoted the differential expression of 70 miRNAs, including highly conserved ones (e.g., miR-133 and miR-375), as well honeybee-specific ones (e.g., miR-3745 and miR-3761). Our results put in evidence a broad spectrum of EcR-controlled gene expression during postembryonic development of honeybees, revealing new facets of EcR biology in this social insect.
Highlights
Most multicellular organisms go through developmental transitions that enable them to cope with environmental changes and/or broaden their niche possibilities
Three major findings are worthy of note: (i) transcripts representing the EcRB variant are predominant in embryos (Mann–Whitney Test, P ≤ 0.05), but these transcript levels decline at the transition to the first larval instar, and it is the Ecdysone Receptor (EcR)-A variant which is predominantly expressed during the end of the larval stage and pupal stage; (ii) at several time-points, EcR expression is higher in workers than in queens (Mann–Whitney Test, P ≤ 0.05); and (iii) there is a clear discrepancy between circulating ecdysteroid levels and the developmental expression of EcR-A
A second group of overrepresented genes that called attention was the hormone response-related genes, as these may provide a link between juvenile hormone (JH) and ecdysteroid action during the pharate-adult to adult transition in honeybees. For this group we found three genes as overexpressed in the EcR knockdown (EcR-KD) group, viz. a JH-induced protein, kr-h1, and an Eclosion hormone-like (EH-like) gene. krh1 is certainly the most interesting gene in this set, as it represents a direct readout of the activity of the JH response in target tissues (Lozano and Belles, 2011; Bellés and Santos, 2014)
Summary
Most multicellular organisms go through developmental transitions that enable them to cope with environmental changes and/or broaden their niche possibilities. Such transitions are generally timed and synchronized by morphogenetic hormones in a broad range of species, including insects, amphibians, metamorphic fish, tunicates, echinoderms, and plants. Developmental transitions, such as larval and metamorphic molts, are driven by steroid hormones (ecdysteroids) acting in conjunction with juvenile hormone (JH). These hormones control reproduction and aging (Flatt et al, 2005; Gáliková et al, 2011), and, in social insects, play important roles in caste polyphenism (Hartfelder and Emlen, 2012). The mode of action of JH, which is a sesquiterpenoid morphogenetic molecule, has only recently become clear
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