Juvenile hormone biosynthesis in adult Blattella germanica requires nuclear receptors Seven-up and FTZ-F1

Ferran Borras-Castells,David Martín,Oscar Maestro,José L Maestro,Claudia Nieva,Xavier Belles

doi:10.1038/srep40234

Ferran Borras-Castells, David Martín + Show 4 more

Open Access

https://doi.org/10.1038/srep40234

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Abstract

In insects, the transition from juvenile development to the adult stage is controlled by juvenile hormone (JH) synthesized from the corpora allata (CA) glands. Whereas a JH-free period during the last juvenile instar triggers metamorphosis and the end of the growth period, the reappearance of this hormone after the imaginal molt marks the onset of reproductive adulthood. Despite the importance of such transition, the regulatory mechanism that controls it remains mostly unknown. Here, using the hemimetabolous insect Blattella germanica, we show that nuclear hormone receptors Seven-up-B (BgSvp-B) and Fushi tarazu-factor 1 (BgFTZ-F1) have essential roles in the tissue- and stage-specific activation of adult CA JH-biosynthetic activity. Both factors are highly expressed in adult CA cells. Moreover, RNAi-knockdown of either BgSvp-B or BgFTZ-F1 results in adult animals with a complete block in two critical JH-dependent reproductive processes, vitellogenesis and oogenesis. We show that this reproductive blockage is the result of a dramatic impairment of JH biosynthesis, due to the CA-specific reduction in the expression of two key JH biosynthetic enzymes, 3-hydroxy-3-methylglutaryl coenzyme A synthase-1 (BgHMG-S1) and HMG-reductase (BgHMG-R). Our findings provide insights into the regulatory mechanisms underlying the specific changes in the CA gland necessary for the proper transition to adulthood.

Highlights

Our findings reveal that nuclear hormone receptors Seven-up-B (BgSvp-B) and Fushi tarazu-factor 1 (BgFTZ-F1) provide tissue- and stage-specificity to the expression of two key Juvenile hormone (JH) biosynthetic enzyme genes, 3-hydroxy-3-methylglutaryl coenzyme A synthase-1 (BgHMG-S1) and 3-hydroxy-3-methylglutaryl coenzyme A reductase (BgHMG-R), in the corpora allata (CA) cells to control the massive production of JH during B. germanica adulthood
BgFTZ-F1 binding activity was only detected in the imaginal transition and during the entire adult stage (Fig. 10C and D). These findings show that BgFTZ-F1 protein competent to bind to the FTZ-F1 response element in the BgHMG-S1 gene is present in the CA cells during the transition from the last nymph to adult and along the adult stage of B. germanica females, suggesting that it could act as an adult-specific transcription factor required for JH biosynthesis during this period
Whereas the metamorphic stage is initiated by the inhibition of the JH biosynthetic activity of the CA cells, the onset of the reproductive adulthood is controlled by the precise re-induction of the CA activity at the imaginal molt[4,5,6,7,40]

Summary

Introduction

In the coleopteran Tribolium castaneum, the POU factor Ventral veins lacking/Drifter (vvl) activates JH synthesis during larval stages by activating JHAMT3 expression[15] In addition to these transcription factors, several peptide hormones (allatotropins, allatostatins and short neuropeptide F) and neurotransmitters (the biogenic amines octopamine, dopamine and glutamate) are involved in the regulation of CA activity[16]. We use the hemimetabolous insect Blattella germanica to elucidate the molecular mechanisms underlying the critical reactivation of JH production that marks the onset of the reproductive adulthood This cockroach provides an ideal opportunity to address JH biosynthesis regulation as patterns and functions of JH III, the only JH form detected in this species[17], have been intensively studied during the nymphal and adult stages[18,19].

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