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

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 (St...

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Autores principales: Shi, Xiao-Xiao, Zhu, Mu-Fei, Wang, Ni, Huang, Yuan-Jie, Zhang, Min-Jing, Zhang, Chao, Ali, Soomro A., Zhou, Wen-Wu, Zhang, Chuanxi, Mao, Cungui, Zhu, Zeng-Rong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7943485/
https://www.ncbi.nlm.nih.gov/pubmed/33716775
http://dx.doi.org/10.3389/fphys.2021.629532
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author Shi, Xiao-Xiao
Zhu, Mu-Fei
Wang, Ni
Huang, Yuan-Jie
Zhang, Min-Jing
Zhang, Chao
Ali, Soomro A.
Zhou, Wen-Wu
Zhang, Chuanxi
Mao, Cungui
Zhu, Zeng-Rong
author_facet Shi, Xiao-Xiao
Zhu, Mu-Fei
Wang, Ni
Huang, Yuan-Jie
Zhang, Min-Jing
Zhang, Chao
Ali, Soomro A.
Zhou, Wen-Wu
Zhang, Chuanxi
Mao, Cungui
Zhu, Zeng-Rong
author_sort Shi, Xiao-Xiao
collection PubMed
description 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.
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spelling pubmed-79434852021-03-11 Neutral Ceramidase Is Required for the Reproduction of Brown Planthopper, Nilaparvata lugens (Stål) Shi, Xiao-Xiao Zhu, Mu-Fei Wang, Ni Huang, Yuan-Jie Zhang, Min-Jing Zhang, Chao Ali, Soomro A. Zhou, Wen-Wu Zhang, Chuanxi Mao, Cungui Zhu, Zeng-Rong Front Physiol Physiology 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. Frontiers Media S.A. 2021-02-24 /pmc/articles/PMC7943485/ /pubmed/33716775 http://dx.doi.org/10.3389/fphys.2021.629532 Text en Copyright © 2021 Shi, Zhu, Wang, Huang, Zhang, Zhang, Ali, Zhou, Zhang, Mao and Zhu. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Shi, Xiao-Xiao
Zhu, Mu-Fei
Wang, Ni
Huang, Yuan-Jie
Zhang, Min-Jing
Zhang, Chao
Ali, Soomro A.
Zhou, Wen-Wu
Zhang, Chuanxi
Mao, Cungui
Zhu, Zeng-Rong
Neutral Ceramidase Is Required for the Reproduction of Brown Planthopper, Nilaparvata lugens (Stål)
title Neutral Ceramidase Is Required for the Reproduction of Brown Planthopper, Nilaparvata lugens (Stål)
title_full Neutral Ceramidase Is Required for the Reproduction of Brown Planthopper, Nilaparvata lugens (Stål)
title_fullStr Neutral Ceramidase Is Required for the Reproduction of Brown Planthopper, Nilaparvata lugens (Stål)
title_full_unstemmed Neutral Ceramidase Is Required for the Reproduction of Brown Planthopper, Nilaparvata lugens (Stål)
title_short Neutral Ceramidase Is Required for the Reproduction of Brown Planthopper, Nilaparvata lugens (Stål)
title_sort neutral ceramidase is required for the reproduction of brown planthopper, nilaparvata lugens (stål)
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7943485/
https://www.ncbi.nlm.nih.gov/pubmed/33716775
http://dx.doi.org/10.3389/fphys.2021.629532
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