Juvenile Hormone-Receptor Complex Acts on Mcm4 and Mcm7 to Promote Polyploidy and Vitellogenesis in the Migratory Locust

Abstract

Juvenile hormone (JH), a sesquiterpenoid produced by the corpora allata, coordinates insect growth, metamorphosis, and reproduction. While JH action for the repression of larval metamorphosis has been well studied, the molecular basis of JH in promoting adult reproduction has not been fully elucidated. Methoprene-tolerant (Met), the JH receptor, has been recently shown to mediate JH action during metamorphosis as well as in vitellogenesis, but again, the precise mechanism underlying the latter has been lacking. We have now demonstrated using Met RNAi to phenocopy a JH-deprived condition in migratory locusts, that JH stimulates DNA replication and increases ploidy in preparation for vitellogenesis. Mcm4 and Mcm7, two genes in the DNA replication pathway were expressed in the presence of JH and Met. Depletion of Mcm4 or Mcm7 inhibited de novo DNA synthesis and polyploidization, and resulted in the substantial reduction of vitellogenin mRNA levels as well as severely impaired oocyte maturation and ovarian growth. By using luciferase reporter and electrophoretic mobility shift assays, we have shown that Met directly regulates the transcription of Mcm4 and Mcm7 by binding to upstream consensus sequences with E-box or E-box-like motifs. Our work suggests that the JH-receptor complex acts on Mcm4 and Mcm7 to regulate DNA replication and polyploidy for vitellogenesis and oocyte maturation.

Juvenile Hormone Activates the Transcription of Cell-division-cycle 6 (Cdc6) for Polyploidy-dependent Insect Vitellogenesis and Oogenesis

“…2B), indicating the dependence of Cdc6 expression on Met. Analysis of the upstream sequence of locust Cdc6 gene revealed an E-box-like motif (CACGCG, nt Ϫ1063 to Ϫ1058) that has been previously reported for Met binding as a JH-response element (1,8,48,52,53). To test the recognition of Cdc6 DNA element by Met, EMSA was conducted using nuclear extracts from dsMet-versus dsGFP-treated fat bodies.…”

“…The loading of Mcm helicase complex onto DNA at the origins of replication is central to DNA replication (42)(43)(44). In our RNA-seq-based gene expression profiling, Cdc6 together with Mcm2-7 were identified as the up-regulated genes in the fat body of JH-deprived adult female locusts further treated with methoprene (1). Given the functional importance of Cdc6 in loading Mcm2-7, we speculated that Cdc6, like Mcm, is a regulatory target of the JH pathway.…”

“…Cumulative studies have demonstrated that JH exerts the genomic actions through its receptor, methoprenetolerant (Met) (6). JH induces the heterodimerization of Met with steroid receptor co-activator (SRC) (also known as Taiman in Drosophila or FISC in the mosquito, Aedes aegypti) to form a transcriptionally active complex to regulate the transcription of target genes in several insect systems, including the beetle Tribolium castaneum, silkworm Bombyx mori, migratory locust Locusta migratoria, and mosquito A. aegypti (1,(7)(8)(9)(10)(11).…”

“…It has been reported that 20E regulates DNA replication and polyploidy during insect metamorphosis, but the underlying mechanisms have yet been defined (3, 28 -31). In locusts, polyploidization in the fat body and follicle cells of adult females during vitellogenesis and oocyte maturation is dependent on JH (1,32,33). In a previous report we show that JH acts through its receptor complex Met-SRC on two mini-chromosome maintenance (Mcm) genes, Mcm4 and Mcm7, to promote DNA replication and polyploidization for the massive Vg synthesis required for egg production in locusts (1).…”

Performance of reproductive system of Dichelops melacanthus (Hemiptera: Pentatomidae) subjected to buprofezin and pyriproxyfen: morphological analysis of ovarioles and testes

“…It is known that JH acts in lipid synthesis (ZIBAEE et al, 2011), which is important for formation of adult females, mainly for the production of vitellogenin (GUO et al, 2014;SMYKAL et al, 2014). Ecdysone is an important agent for the ecdysis of insects; in addition to controlling the biosynthesis of chitin, diapause and the immune system (LENAERTS et al, 2016), this hormone is also involved in the development of ovarian structure (ZERA; BOTTSFORD, 2001).…”