Abstract
Non-ATPase regulatory subunits (Rpns) are components of the 26S proteasome involved in polyubiquitinated substrate recognition and deubiquitination in eukaryotes. Here, we identified 15 homologues sequences of Rpn and associated genes by searching the genome and transcriptome databases of the brown planthopper, Nilaparvata lugens, a hemipteran rice pest. Temporospatial analysis showed that NlRpn genes were significantly highly expressed in eggs and ovaries but were less-highly expressed in males. RNA interference-mediated depletion of NlRpn genes decreased the proteolytic activity of proteasome and impeded the transcription of lipase and vitellogenin genes in the fat bodies and ovaries in adult females, and reduced the triglyceride content in the ovaries. Decrease of the proteolytic activity of the proteasome via knockdown of NlRpns also inhibited the transcription of halloween genes, including NlCYP307A2, NlCYP306A2 and NlCYP314A1, in the 20-hydroxyecdysone (20E) biosynthetic pathway in the ovaries, reduced 20E production in adult females, and impaired ovarian development and oocyte maturation, resulting in reduced fecundity. These novel findings indicate that the proteolytic activity of the proteasome is required for female reproductive processes in N. lugens, thus furthering our understanding of the reproductive and developmental strategies in insects.
Highlights
The brown planthopper, Nilaparvata lugens Stål (Hemiptera: Delphacidae), is one of the most threatening pests of rice crops in tropical Asia and southern China [1,2]
We investigated the effects of N. lugens proteasome subunit β5 (NlPSMB5) knockdown on the transcript level variations of Vg, Vg receptor (VgR) and lipase genes in fat bodies and ovaries of adult females. quantitative realtime polymerase chain reaction (qRT-PCR) analysis confirmed that transcript levels of NlPSMB5 gene were notably reduced in dsNlPSMB5-injected fat bodies and ovaries compared with those in double strand green fluorescent protein (dsGFP)-injected controls
NlBicC knockdown did not significantly alter the expression of lipid-metabolizing genes (NlATGL, NlPNLIP1, NlLPL2 and NlLIPF1), 20E biosynthetic enzymes (NlCYP307A2 and NlCYP314A1) and Vg genes (NlVg and NlVg-like2). These results indicate that knockdown of N. lugens Bicaudal-C (NlBic-C), which is necessary for the late stages of oogenesis, did not affect the levels of lipid-metabolizing genes, 20E biosynthetic enzymes and the Vg gene, whereas knockdown of NlRpns affected the expression of these genes in adult females
Summary
The brown planthopper, Nilaparvata lugens Stål (Hemiptera: Delphacidae), is one of the most threatening pests of rice crops in tropical Asia and southern China [1,2]. The mechanisms regulating fecundity in insects have attracted interest for decades, and many genes, including vitellogenin (Vg) and insulin associated with nutritional metabolism, and halloween genes involved in ecdysteroid biosynthesis, are known to play important roles in the regulation of oocyte maturation and embryonic development in most insect species [1,5,6,7,8,9,10,11,12]. The DICER1 gene, which is mostly responsible for microRNA precursor processing, was demonstrated to be important for oocyte maturation in the telotrophic ovary [13], while the female-specific gene for bicaudal-C was essential for oogenesis [14]. We conducted a genome- and transcriptome-wide search and identified a group of genes encoding non-ATPase regulatory subunits and associated proteins of the 26S proteasome, which were highly expressed in the ovaries of adult females and in eggs laid in rice leaf sheaths
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