Neutral Ceramidase Is Required for the Reproduction of Brown Planthopper, Nilaparvata lugens (Stål)

Abstract

Ceramides are bioactive sphingolipids that have been implicated in insect development; however, their role in insect reproduction remains poorly understood. Here, we report the pivotal role of neutral ceramidase (NCER) in the female reproduction of the brown planthopper (BPH), Nilaparvata lugens (Stål), a significant pest in rice cultivation in Asia. LC-MS/MS demonstrated that, among different developmental stages of BPH, the levels of ceramides were highest in 1st instar nymphs and lowest in adults. The transcription of NCER was negatively correlated with the levels of ceramides at different developmental stages of BPH, in that the transcript levels of NCER were the highest, whereas ceramides levels were the lowest in BPH adults. Knocking down NCER through RNA interference (RNAi) increased the levels of ceramides in BPH females and ovaries, which resulted in a delay in oocyte maturation, a reduction in oviposition and egg hatching rate, as well as the production of vulnerable offspring. Transmission electron microscopy (TEM) analysis and TdT-mediated dUTP Nick-End Labeling (TUNEL) assays showed mitochondrial deficiency and apoptosis in NCER-deficient oocytes. Taken together, these results suggest that NCER plays a crucial role in female reproduction in BPH, likely by regulating the levels of ceramides.

Chromosome-Level Genome Assembly of Apoderus dimidiatus Voss (Coleoptera: Attelabidae): Insights into Evolution and Behavior

“…Ceramide is located at the center of sphingolipid metabolism [ 58 ]; studies have shown that abnormal accumulation of ceramide can negatively impact insect reproduction, particularly affecting female adults of N. lugens . This abnormal accumulation results in delayed maturation of oocytes, decreased oviposition, and diminished offspring survival rate [ 59 ]. Insects exhibit characteristics of being small, fast-growing, and short-lived, leading them to adopt the “r-selection” reproductive strategy emphasizing high fecundity to ensure population continuation and success through quantity rather than quality.…”

Alkaline ceramidase (ClAC) inhibition enhances heat stress response in Cyrtorhinus lividipennis (Reuter)

“…The alCDase of Drosophila ( Dacer ) was highly expressed in the pupal stage and significantly affected the longevity of Drosophila ( Yang et al, 2010 ; Zhang et al, 2019 ). The nCDase of Tribolium castaneum showed high expression in adults, but its biological functions had not been demonstrated ( Zhou et al, 2011 ).The nCDase of BPH was highly expressed in female adults and played essential roles in the reproduction of the insect ( Shi et al, 2018 ; Shi et al, 2021 ). Different from BPH or Tribolium castaneum , both ClNC and ClAC had high expression in the early nymph stages.…”

Characterization of MicroRNAs Associated with Reproduction in the Brown Planthopper, Nilaparvata lugens

“…Regarding the lipid biosynthetic process, sphingolipids are an important class of lipids that participate in crucial events of cell proliferation, differentiation, and apoptosis in various species [ 46 ]. Recently, evidence has accumulated to show that sphingolipids have roles in the signaling pathways involved in reproduction and oocyte development of N. lugens [ 47 , 48 , 49 ]. Cyclin-dependent kinase (CDK) is a serine/threonine protein kinase family that cooperates with cyclin and is required for embryo development and cell cycle progression [ 50 ].…”

“…The BPHs were reared on susceptible rice seedlings cv. Taichung Native 1 (TN1) at 27 ± 1 • C, 70% relative humidity, and a 16:8 h light: dark photoperiod as described in a previous study [47]. All samples were frozen in liquid nitrogen immediately and stored at −80 • C. Total RNA was extracted using TRIzol Reagent (Invitrogen, Carlsbad, CA, USA) according to the manufacturer's protocol.…”