Involvement of Two Paralogous Methoprene-Tolerant Genes in the Regulation of Vitellogenin and Vitellogenin Receptor Expression in the Rice Stem Borer, Chilo suppressalis

Abstract

Besides the function of preventing metamorphosis in insects, the juvenile hormone (JH) plays a role in female reproduction; however, the underlying mechanism is largely unknown. The methoprene-tolerant (Met) protein belongs to a family of basic helix-loophelix-Per-Arnt-Sim (bHLH-PAS) transcription factors and functions as the JH intracellular receptor. In this study, two full length cDNAs encoding Met (CsMet1 and CsMet2) were isolated from the rice stem borer, Chilo suppressalis. Structural analysis revealed that both CsMet1 and CsMet2 exhibited typical bHLH, PAS-A, PAS-B, and PAC (PAS C terminal motif) domains. Comparative analysis of transcript level using reverse transcription-quantitative PCR (RT-qPCR) revealed that CsMet1 was predominant in almost all examined developmental stages and tissues. Treatment with methoprene in vivo induces the transcription of both CsMet1 and CsMet2. Notably, injection of dsCsMet1 and dsCsMet2 suppressed the expression levels of vitellogenin (CsVg) and Vg receptor (CsVgR). These findings revealed the potential JH signaling mechanism regulating C. suppressalis reproduction, and provided evidence that RNAi-mediated knockdown of Met holds great potential as a control strategy of C. suppressalis.

CRISPR/Cas9‐mediated methoprene‐tolerant 1 knockout results in precocious metamorphosis of beet armyworm (Spodoptera exigua) only at the late larval stage

“…The identification of the transcription factor Met as a critical intracellular receptor for JH is a major breakthrough, which has prompted JH signalling studies (Charles et al, 2011). Up to now, Met has been identified from a broad range of insect species (Daimon et al, 2015; Miao et al, 2020; Villalobos‐Sambucaro et al, 2015). Most insects like mosquitoes and beetles possess only a single gene while two Met paralogs were present across 12 Drosophila species and found in several Lepidopteran insects including D. plexippus , O. brumata , B. mori and C. suppressalis (Baumann et al, 2010; Derks et al, 2015; Kayukawa & Shinoda, 2015; Miao et al, 2020; Zhan et al, 2011).…”

“…Subsequently, studies in multiple insects demonstrated that Met and its partners upregulate downstream genes to transduce JH signals and play an essential role in insect metamorphosis and reproduction (He et al, 2014; Kayukawa et al, 2017; Konopova et al, 2011; Ma et al, 2018; Song et al, 2014). While beetles and mosquitoes possess only a single gene, two Met paralogs have also been identified in 12 Drosophila species and several Lepidopteran insects (Baumann et al, 2010; Miao et al, 2020). Krüppel‐homologue 1 ( Kr‐h1 ) represents a primary JH response gene encoding a zinc‐finger transcription factor which is regulated by Met to control metamorphosis and reproduction while Broad Complex ( BR‐C ) is a transcription factor that directs pupal development.…”

Effect of Insulin Receptor on Juvenile Hormone Signal and Fecundity in Spodoptera litura (F.)

“…The reproductive success of insects depends on vitellogenin (Vg) biosynthesis and uptake of Vg into developing oocytes mediated by the vitellogenin receptor [ 4 ]. Vg synthesis can be induced by JH in many insects [ 17 , 19 , 55 ].…”

“…Vg is primarily synthesized in insect body fat, then secreted into the haemolymph and utilized by oocytes through a complicated physiological process [ 3 ]. The reproductive success of insects depends on Vg biosynthesis and uptake by developing oocytes [ 4 ]. Therefore, Vg can be used as a molecular marker of fecundity [ 5 ].…”

“…JH is synthesized by the corpora allata (CA), which are known as another important factor to regulate a large array of physiological processes, such as embryonic development [ 9 ], metamorphosis [ 10 ], energy homeostasis [ 11 ], reproduction [ 12 ] behaviors [ 13 , 14 ], etc. JH binds to intracellular receptor Methoprene (Met), a member of the family of the basic helix-loop-helix (bHLH)-Per-Arnt-Sim (PAS) transcription factors, and then the JH signaling pathway is activated [ 4 ]. In the adult stage, nutrition is used to stimulate the production of the major gonadotropin JH [ 15 ].…”