Abstract
Provisioning of sufficient lipids and vitellogenin to the oocytes is an indispensable process for fecundity of oviparous insects. Acute mobilization of lipid reserves in insects is controlled by the Brummer (Bmm), an orthologous of human adipose triglyceride lipase (ATGL). To investigate the functional roles of brummer-mediated lipolysis in the fecundity of the brown planthopper, Nilaparvata lugens, RNA interference (RNAi) analyses were performed with double-stranded RNA (dsRNA) against NlBmm in adult females. Knockdown of NlBmm expression resulted in obesity and blocked lipid mobilization in the fat body. In addition, NlBmm silencing led to retarded ovarian development with immature eggs and less ovarioles, decreased number of laid eggs, prolonged preoviposition period and egg duration. Furthermore, severe reductions of vitellogenin and its receptor abundance were observed upon NlBmm knockdown. The transcript levels of NlJHE (juvenile hormone esterase) which degrades JH were up-regulated, whereas the expression levels of JH receptors NlMet (Methoprene-tolerant) and NlTai (Taiman) and their downstream transcription factors NlKr-h1 (Krüppel-homolog 1) and NlBr (Broad-Complex) were down-regulated after suppression of NlBmm. JH-deficient females exhibited impaired vitellogenin expression, whereas JH exposure stimulated vitellogenin biosynthesis. Moreover, JH topical application partially rescued the decrease in vitellogenin expression in the NlBmm-deficient females. These results demonstrate that brummer-mediated lipolytic system is essential for lipid mobilization and energy homeostasis during reproduction in N. lugens. In addition to the classical view of brummer as a direct lipase with lipolysis activity, we propose here that brummer-mediated lipolysis works through JH signaling pathway to activate vitellogenesis and oocyte maturation that in turn regulates female fecundity.
Highlights
In oviparous insects, maturation of oocytes requires the accumulation of large amounts of proteins and lipids in the yolk bodies and lipid droplets (Roy et al, 2017)
We found that the fecundity of N. lugens was significantly decreased after brummer knockdown
Our results demonstrate that both lipid mobilization and Juvenile hormone (JH)-mediated vitellogenesis influenced by brummer are involved in the positive control of female fecundity
Summary
Maturation of oocytes requires the accumulation of large amounts of proteins and lipids in the yolk bodies and lipid droplets (Roy et al, 2017). Significant progress has been achieved to understand the process of yolk protein, vitellogenin uptake by developing oocytes via receptor-mediated endocytosis from biosynthesis to hormonal regulation of vitellogenin gene. Mostly triacylglycerol (TAG) stored in the oocytes are the main nutrient supply to provide energy for the development of embryo, to provide the precursors for the synthesis of cell membranes and to mediate cell signaling (Handela, 1993; Ziegler and Van Antwerpen, 2006; Santos et al, 2011). The enzymes accounting for TAG biosynthesis are active in insect oocytes, their ability to synthesize fatty acids (FAs) de novo is very limited (Van Hoof et al, 2005). It has been demonstrated that the site of lipophorin and vitellogenin synthesis is the fat body, an insect organ analogous to vertebrate liver and adipose tissue and functions as a major organ for energy storage and metabolism (Arrese and Soulages, 2010)
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