Abstract
Juvenile hormones (JH) are key endocrine regulators produced by the corpora allata (CA) of insects. Together with ecdysteroids, as well as nutritional cues, JH coordinates different aspects of insect postembryonic development and reproduction. The function of the recently characterized JH receptor, Methoprene-tolerant (Met), appears to be conserved in different processes regulated by JH. However, its functional interactions with other hormonal signalling pathways seem highly dependent on the feeding habits and on the developmental and reproductive strategies employed by the insect species investigated. Here we report on the effects of RNA interference (RNAi) mediated SgMet knockdown during the first gonadotrophic cycle in female desert locusts (Schistocerca gregaria). This voracious, phytophagous pest species can form migrating swarms that devastate field crops and harvests in several of the world’s poorest countries. A better knowledge of the JH signalling pathway may contribute to the development of novel, more target-specific insecticides to combat this very harmful swarming pest. Using RNAi, we show that the JH receptor Met is essential for ovarian maturation, vitellogenesis and associated ecdysteroid biosynthesis in adult female S. gregaria. Interestingly, knockdown of SgMet also resulted in a significant decrease of insulin-related peptide (SgIRP) and increase of neuroparsin (SgNP) 3 and 4 transcript levels in the fat body, illustrating the existence of an intricate regulatory interplay between different hormonal factors. In addition, SgMet knockdown in females resulted in delayed display of copulation behaviour with virgin males, when compared with dsGFP injected control animals. Moreover, we observed an incapacity of adult dsSgMet injected female locusts to oviposit during the time of the experimental setup. As such, SgMet is an essential gene playing crucial roles in the endocrine communication necessary for successful reproduction of the desert locust.
Highlights
The classic insect hormones, juvenile hormones (JH) and ecdysteroids, play critical roles in insect postembryonic development
Its expression in 10-day-old adult locusts is mainly observed in the male accessory glands (AGs), corpora allata (CA), fat body, prothoracic glands (PGs) and muscles (Supplementary Fig. S1)
SgMet transcript levels remain relatively stable in the fat body of adult female locusts throughout the first gonadotrophic cycle (Fig. 1A), a situation which is similar to what was reported on the expression of Met during the reproductive cycle of the pacific beetle cockroach, Diploptera punctata and the German cockroach, B. germanica[28,33]
Summary
The classic insect hormones, juvenile hormones (JH) and ecdysteroids, play critical roles in insect postembryonic development. The pleiotropic JH acts via Met and Kr-h1 to control different processes in adults, such as vitellogenesis in the fat body, lipid accumulation in the primary oocyte, regulation of mating and sex pheromone production[24,26–38] In another locust species, the migratory locust, L. migratoria, the molecular basis of JH action in reproduction is well established[20,39]. This same study showed that knockdown of the S. gregaria NPs (SgNPs) increases SgVg transcription, resulting in bigger oocytes This finding was in line with the initial discovery of the first locust NP, a peptide purified from the pars intercerebralis-corpora cardiaca (CC) neurohaemal complex, which was shown to act as an anti-gonadotrophic factor, contrary to the effects of JH48–50. Using RNAi, we demonstrate that the JH receptor Met is crucial for the initiation of ovarian maturation and vitellogenesis, and that its key role is situated within a complex hormonal network involved in the control of reproduction in S. gregaria
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