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Abstract
Although endocrine changes are known to modulate the timing of major developmental transitions, the genetic mechanisms underlying these changes remain poorly understood. In insects, two developmental hormones, juvenile hormone (JH) and ecdysteroids, are coordinated with each other to induce developmental changes associated with metamorphosis. However, the regulation underlying the coordination of JH and ecdysteroid synthesis remains elusive. Here, we examined the function of a homolog of the vertebrate POU domain protein, Ventral veins lacking (Vvl)/Drifter, in regulating both of these hormonal pathways in the red flour beetle, Tribolium castaneum (Tenebrionidae). RNA interference-mediated silencing of vvl expression led to both precocious metamorphosis and inhibition of molting in the larva. Ectopic application of a JH analog on vvl knockdown larvae delayed the onset of metamorphosis and led to a prolonged larval stage, indicating that Vvl acts upstream of JH signaling. Accordingly, vvl knockdown also reduced the expression of a JH biosynthesis gene, JH acid methyltransferase 3 (jhamt3). In addition, ecdysone titer and the expression of the ecdysone response gene, hormone receptor 3 (HR3), were reduced in vvl knockdown larvae. The expression of the ecdysone biosynthesis gene phantom (phm) and spook (spo) were reduced in vvl knockdown larvae in the anterior and posterior halves, respectively, indicating that Vvl might influence ecdysone biosynthesis in both the prothoracic gland and additional endocrine sources. Injection of 20-hydroxyecdysone (20E) into vvl knockdown larvae could restore the expression of HR3 although molting was never restored. These findings suggest that Vvl coordinates both JH and ecdysteroid biosynthesis as well as molting behavior to influence molting and the timing of metamorphosis. Thus, in both vertebrates and insects, POU factors modulate the production of major neuroendocrine regulators during sexual maturation.
Highlights
Many organisms, including amphibians, echinoderms, marine invertebrates, vertebrates, and insects, undergo dramatic morphological and behavioral changes when they enter metamorphosis or puberty
We show that silencing the POU domain transcription factor Ventral veins lacking (Vvl)/Drifter in the red flour beetle Tribolium castaneum leads to precocious metamorphosis and an inability to molt
We show that Vvl regulates the biosynthesis and signaling of two key insect developmental hormones, juvenile hormone (JH) and ecdysteroids
Summary
Many organisms, including amphibians, echinoderms, marine invertebrates, vertebrates, and insects, undergo dramatic morphological and behavioral changes when they enter metamorphosis or puberty. Puberty is associated with morphological changes and reproductive maturation. These dramatic transformations are orchestrated by neuroendocrine changes that occur during postembryonic development of an organism. Members of the POU family have been shown to influence the neuroendocrine system during puberty and early development of vertebrates [7,8,9,10,11,12,13]. POU factors regulate the onset of puberty in mammals [13,15]
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