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

Xiao-Xiao Shi,Zeng-Rong Zhu,Soomro A Ali,Chao Zhang,Yuan-Jie Huang,Mu-Fei Zhu,Cungui Mao,Wen-Wu Zhou,Chuanxi Zhang,Min-Jing Zhang,Ni Wang

doi:10.3389/fphys.2021.629532

Xiao-Xiao Shi, Zeng-Rong Zhu + Show 9 more

Open Access

https://doi.org/10.3389/fphys.2021.629532

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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.

Highlights

The brown planthopper (BPH), Nilaparvata lugens (Stål), one of the most economically devastating rice pests in Asia, causes severe agricultural damages by sucking plant juice and spreading plant viruses
Before we investigated the role of sphingolipids for insect development, we first determined the levels of ceramides and dihydroceramides in BPH at different developmental stages
We found that the major individual ceramide species and total ceramides were more abundant than the major individual dihydroceramide species and total dihdyroceramides across the developmental stages (Figure 2C)

Summary

Introduction

The brown planthopper (BPH), Nilaparvata lugens (Stål), one of the most economically devastating rice pests in Asia, causes severe agricultural damages by sucking plant juice and spreading plant viruses. Identifying the internal signaling pathways that regulate BPH development and reproduction will facilitate novel approaches for containing the outbreak of BPH. Emerging evidence indicates that ceramides, a type of sphingolipid, are located in the central hub of the sphingolipid metabolic network and have a role in regulating the development and reproduction of mammals and insects. High levels of ceramides were detected in pregnancies complicated by preeclampsia (Melland-Smith et al, 2015). Ceramides and their derivatives, sphingosine-1-phosphates (S1P), can synergistically as well as antagonistically mediate embryonic stem (ES) cell differentiation in mice (Wang et al, 2018). Ceramides and S1Ps regulated the reproductive development of Drosophila (Phan et al, 2007). Mutations in the serine palmitoyl-transferase (SPT) enzyme subunit of Drosophila resulted in defective synaptic structure and function (West et al, 2018)

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