Abstract

Krüppel-homolog 1 (Kr-h1) is a zinc finger transcription factor maintaining the status quo in immature insect stages and promoting reproduction in adult insects through the transduction of the Juvenile Hormone (JH) signal. Knockdown studies have shown that precocious silencing of Kr-h1 in the immature stages results in the premature development of adult features. However, the molecular characteristics and reproductive potential of these premature adult insect stages are still poorly understood. Here we report on an adult-like or ‘adultoid’ phenotype of the migratory locust, Locusta migratoria, obtained after a premature metamorphosis induced by the silencing of LmKr-h1 in the penultimate instar. The freshly molted adultoid shows precocious development of adult features, corresponding with increased transcript levels of the adult specifier gene LmE93. Furthermore, accelerated ovarian maturation and vitellogenesis were observed in female adultoids, coinciding with elevated expression of LmCYP15A1 in corpora allata (CA) and LmKr-h1 and vitellogenin genes (LmVg) in fat body, whereas LmE93 and Methoprene-tolerant (LmMet) transcript levels decreased in fat body. In adultoid ovaries, expression of the Halloween genes, Spook (LmSpo) and Phantom (LmPhm), was elevated as well. In addition, the processes of mating and oviposition were severely disturbed in these females. L. migratoria is a well-known, swarm-forming pest insect that can destroy crops and harvests in some of the world’s poorest countries. As such, a better understanding of factors that are capable of significantly reducing the reproductive potential of this pest may be of crucial importance for the development of novel locust control strategies.

Highlights

  • The transition from immature insect stages to fully reproductive adults is dependent on two hormones, i.e., Juvenile Hormone (JH) and ecdysteroids

  • Our study describes a premature adult-like L. migratoria phenotype, the result of a reprogrammed development caused by the precocious RNA interference (RNAi)-mediated silencing of LmKr-h1 during the fourth nymphal stage

  • In female locusts (double-stranded green fluorescent protein-injected control), we investigated the temporal profiles of the MEKRE93 pathway transcripts LmKr-h1, LmE93 and LmE93 and Methoprene-tolerant (LmMet), as well as these of LmJHAMT and LmCYP15A1, the enzymes catalyzing the two final steps in JH biosynthesis, by qRT-PCR analyses at different time points from day 4 of the fourth nymphal (N4 D4) until day 12 of the adult (Ad D12) stage (Figure S1)

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Summary

Introduction

The transition from immature insect stages to fully reproductive adults is dependent on two hormones, i.e., Juvenile Hormone (JH) and ecdysteroids. JH is a sesquiterpenoid hormone synthesized in the corpora allata (CA), which are part of the retrocerebral complex of insects In addition to their role in immature insect stages, both ecdysteroids and JH are endocrine regulators of reproduction in adult insects. Ecdysteroids induce their effects by binding to a heterodimeric complex of two nuclear receptors, the ecdysone receptor (EcR) and the retinoid-X-receptor/ultraspiracle (RXR/USP), as reviewed by Hill et al (2013) [2]. External genitals were found in dsKr-h1-injected N. lugens and P. apterus [10,16,18], while an aberrant ovipositor morphology was described in adultoid crickets of the species G. bimaculatus [15]

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