Abstract
Although juvenile hormone (JH) is known to prevent insect larval metamorphosis and stimulate adult reproduction, the molecular mechanisms of JH action in insect reproduction remain largely unknown. Earlier, we reported that the JH-receptor complex, composed of methoprene-tolerant and steroid receptor co-activator, acts on mini-chromosome maintenance (Mcm) genes Mcm4 and Mcm7 to promote DNA replication and polyploidy for the massive vitellogenin (Vg) synthesis required for egg production in the migratory locust (Guo, W., Wu, Z., Song, J., Jiang, F., Wang, Z., Deng, S., Walker, V. K., and Zhou, S. (2014) PLoS Genet. 10, e1004702). In this study we have investigated the involvement of cell-division-cycle 6 (Cdc6) in JH-dependent vitellogenesis and oogenesis, as Cdc6 is essential for the formation of prereplication complex. We demonstrate here that Cdc6 is expressed in response to JH and methoprene-tolerant, and Cdc6 transcription is directly regulated by the JH-receptor complex. Knockdown of Cdc6 inhibits polyploidization of fat body and follicle cells, resulting in the substantial reduction of Vg expression in the fat body as well as severely impaired oocyte maturation and ovarian growth. Our data indicate the involvement of Cdc6 in JH pathway and a pivotal role of Cdc6 in JH-mediated polyploidization, vitellogenesis, and oogenesis.
Highlights
In addition to repressing insect larval metamorphosis, juvenile hormone (JH)2 has an essential role in stimulating adult reproduction [2, 3]
In a previous report we show that JH acts through its receptor complex Met-steroid receptor co-activator (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]
We first investigated the spatiotemporal expression patterns of locust cell-division-cycle 6 (Cdc6). qRT-PCR using total RNA from adult females collected at 8 days post adult eclosion (PAE) showed that Cdc6 was highly expressed in the ovary (Ov) followed by the fat body (Fb), whereas Cdc6 mRNA levels were much lower in the head (He), cuticle (Cu), midgut (Mg), thorax muscle (Tm), and back leg (Bl) (Fig. 1A)
Summary
At the onset of the G1 phase, recruitment of the replicative helicase Mcm onto origins of DNA replication to form the prereplication complex requires the loading factor cell-division-cycle 6 (Cdc6), a member of AAAϩ ATPase family (34 – 38). Along with the origin recognition complex and Cdt (Cdc protein-dependent transcript 1), Cdc loads Mcm proteins onto origins of replication to facilitate the formation of stable prereplication complex in G1 phase, thereby licensing these sites to initiate DNA replication in S phase (39 – 41). We wondered if JH and its receptor complex target Cdc for transcriptional regulation, which modulates locust polyploidy, vitellogenesis, and oogenesis. This work implicates a crucial role of Cdc in JH-dependent polyploidy, vitellogenesis, and oogenesis, which provides new insight into the mechanisms of JH regulation in insect reproduction
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