Juvenile Hormone receptor Met is essential for ovarian maturation in the Desert Locust, Schistocerca gregaria

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.

Precocious Downregulation of Krüppel-Homolog 1 in the Migratory Locust, Locusta migratoria, Gives Rise to An Adultoid Phenotype with Accelerated Ovarian Development but Disturbed Mating and Oviposition

“…A study by Song et al (2014) described reduced Vg gene expression in the fat body, lipid accumulation in the primary oocytes, as well as a strong inhibition of oocyte maturation upon silencing LmMet and LmKr-h1 [ 6 ]. These observations are corroborated by multiple other studies performed in numerous insect species [ 13 , 23 , 24 , 25 , 27 , 29 , 31 , 32 , 33 , 34 , 38 , 62 , 63 , 64 ]. In addition to the higher LmKr-h1 transcript levels detected in fat body of adultoid females ( Figure S5A ), lower LmE93 transcript levels were observed ( Figure S5B ), which may refer to the inhibitory effect of Kr-h1 on E93 expression [ 21 , 65 ].…”

“…A recent study in the desert locust, Schistocerca gregaria , confirmed these findings, since a knockdown of Met in female adult locusts resulted in a failure to initiate Vg expression in the fat body, as well as basal oocyte growth in the ovaries. Moreover, these ds Met -treated locusts showed delayed mating behavior and were unable to oviposit [ 38 ]. In female locusts, JH is known to stimulate Vg production by inducing Vg gene transcription in the fat body [ 39 ].…”

Knockdown of Methoprene-Tolerant Arrests Ovarian Development in the Sogatella furcifera (Hemiptera: Delphacidae)

“…These results indicate that the JH-Met-Kr-h1 signaling pathway is involved in reproduction in L. migratoria (Song et al 2014). Other studies suggest that the JH-Met-Kr-h1 signaling pathway is conserved in insects, presumably because of its universal role in regulating female reproductive development (Marchal et al 2014, Yue et al 2018, Gijbels et al 2019).…”

Crucial role of Juvenile Hormone receptor components Methoprene-tolerant and Taiman in sexual maturation of adult male desert locusts (Schistocerca gregaria)

“…In the females of several insect species, a stimulatory role of the JH signaling system on vitellogenin production by the fat body and on oocyte development in the ovary is evidenced (Badisco et al, 2013). Also in adult S. gregaria females, we recently described that the JH receptor Met is necessary for ovarian maturation, vitellogenesis and associated ecdysteroid biosynthesis, making it a crucial gene in female locust reproductive physiology (Gijbels et al, 2019). In the current study, we report on the effects of an RNAi-mediated knockdown of Scg-Met and Scg-Tai on the reproductive development of adult male desert locusts.…”

“…Previous studies revealed that Scg -IRP expression is regulated during the reproductive cycle and there is evidence for a stimulatory role of Scg -IRP on vitellogenesis and ovarian development in adult female desert locusts (Badisco et al, 2011). In several other insect species, complex functional interactions have been observed between the ISP and JH signaling (Badisco et al, 2013; Gijbels et al, 2019; Roy et al, 2018; Van Wielendaele et al, 2012). In the fruit fly, D. melanogaster , the expression of the insulin receptor (IR) was detected in the CA, indicating the ability of the CA to respond to changing insulin-like peptide levels.…”