Insulin signaling mediates previtellogenic development and enhances juvenile hormone-mediated vitellogenesis in a lepidopteran insect, Maruca vitrata

Abstract

Background Insulin/insulin-like growth peptide signaling (IIS) down-regulates hemolymph sugar level and facilitates larval growth in the soybean pod borer, Maruca vitrata . The objective of this study is to determine whether IIS of M. vitrata can mediate ovarian development of adult females. Results A pair of ovaries consists of 8 ovarioles, each of which is separated into distal germarium and proximal vitellarium in M. vitrata . In the germarium, oocyte development occurred with active mitotic activity which was visible by incorporating bromodeoxyribose uridine. Previtellogenic development and subsequent vitellogenesis began soon after adult emergence. They continued with increase of female age. Oocyte development was facilitated by up-regulation of vitellogenin (Vg) and Vg receptor (VgR) gene expression. Larval diets significantly influenced on ovarian development of M. vitrata because oocyte development varied with pupal size derived from larvae treated with different nutritional diets. Its ovarian development was dependent on endocrine signal(s) from the head because decapitation soon after adult emergence prevented oogenesis and subsequent vitellogenesis along with marked reduction of Vg and VgR expression. Topical application of juvenile hormone (JH) significantly recovered its ovarian development whereas farnesoic acid (a precursor of JH biosynthesis) or 20-hydroxyecdysone treatment did not. JH stimulated vitellogenesis and choriogenesis, but not previtellogenic development. In contrast, insulin injection to decapitated females stimulated oocyte differentiation and vitellogenesis along with increase of Vg and VgR expression. To further analyze the effect of insulin on ovarian development, expression of four IIS components (InR, FOXO, Akt, and TOR) genes was manipulated by RNA interference. Hemocoelic injection of gene-specific double stranded RNAs significantly reduced their target gene mRNA levels and interfered with ovarian development. An addition of insulin to JH treatment against decapitated females enhanced the gonadotropic effect of JH by stimulating oogenesis. Conclusions IIS plays crucial role in mediating previtellogenic development of M. vitrata in response to nutrient signal. It also enhances the gonadotropic effect of JH II on vitellogenesis. Electronic supplementary material The online version of this article (10.1186/s12861-019-0194-8) contains supplementary material, which is available to authorized users.

Juvenile hormone acts through FoxO to promote Cdc2 and Orc5 transcription for polyploidy-dependent vitellogenesis

“…aegypt, FoxO knockdown repressed Vg expression, resulting in low rate of reproduction(Hansen et al, 2007). Depletion of FoxO also suppressed Vg expression and reduced ovarian development in the soybean pod borer Maruca vitrata (AlBaki et al, 2019). These studies together support our observation that FoxO knockdown in vitellogenic female locusts led to significantly reduced Vg expression along with blocked oocyte maturation and arrested ovarian growth.…”

Regulatory Mechanisms of Vitellogenesis in Insects

“…Similarly, FoxO knockdown led to reduction of Vg transcript levels in fed adult females of T. castaneum, Ae. aegypti, L. migratoria and the soybean pod borer Maruca vitrata (Hansen et al, 2007 ; Parthasarathy and Palli, 2011 ; Abrisqueta et al, 2014 ; Al Baki et al, 2019 ; Wu et al, 2020 ). However, silencing of FoxO in the starved adult females of B. germanica caused significant increase of Vg expression due to elevated biosynthesis of JH (Suren-Castillo et al, 2012 ; Abrisqueta et al, 2014 ).…”

“…Similarly, knockdown of the Halloween genes coding for a group of enzymes involved in 20E synthesis remarkably reduced the levels of Vg and VgR expression, leading to defective egg development of the diamondback moth Plutella xylostella (Peng et al, 2019 ). In M. vitrata and the beet armyworm Spodoptera exigua , the expression of VgR is regulated by ILP/TOR signaling pathway (Zhao et al, 2018 ; Al Baki et al, 2019 ). Notably, two miRNAs, miR-2739 and miR-167 bind directly to the 3′UTR of B. mori VgR mRNA and coordinately inhibit VgR expression.…”

Physiological Alterations in Deletion Mutants of Two Insulin-Like Peptides Encoded in Maruca vitrata Using CRISPR/Cas9

“…Therefore, it is regulated by both ILPs in M. vitrata (Al Baki et al, 2018a). These two ILPs also mediate oocyte development by stimulating mitotic division of stem cells and promoting vitellogenin (Vg) synthesis in M. vitrata (Al Baki et al, 2019b). Moreover, these two ILPs are similarly expressed in most developmental stages and different tissues (Al Baki et al, 2020).…”