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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Frontiers Media S.A.
2021-02-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fphys.2021.629532/full |
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| author | Xiao-Xiao Shi Mu-Fei Zhu Ni Wang Yuan-Jie Huang Yuan-Jie Huang Min-Jing Zhang Chao Zhang Soomro A. Ali Wen-Wu Zhou Chuanxi Zhang Cungui Mao Zeng-Rong Zhu Zeng-Rong Zhu |
| author_facet | Xiao-Xiao Shi Mu-Fei Zhu Ni Wang Yuan-Jie Huang Yuan-Jie Huang Min-Jing Zhang Chao Zhang Soomro A. Ali Wen-Wu Zhou Chuanxi Zhang Cungui Mao Zeng-Rong Zhu Zeng-Rong Zhu |
| author_sort | Xiao-Xiao Shi |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-14T17:44:16Z |
| format | Article |
| id | doaj.art-eae2389e62d048919739d23782a8eb88 |
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| issn | 1664-042X |
| language | English |
| last_indexed | 2024-12-14T17:44:16Z |
| publishDate | 2021-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-eae2389e62d048919739d23782a8eb882022-12-21T22:52:46ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2021-02-011210.3389/fphys.2021.629532629532Neutral Ceramidase Is Required for the Reproduction of Brown Planthopper, Nilaparvata lugens (Stål)Xiao-Xiao Shi0Mu-Fei Zhu1Ni Wang2Yuan-Jie Huang3Yuan-Jie Huang4Min-Jing Zhang5Chao Zhang6Soomro A. Ali7Wen-Wu Zhou8Chuanxi Zhang9Cungui Mao10Zeng-Rong Zhu11Zeng-Rong Zhu12State Key Laboratory of Rice Biology, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Institute of Insect Sciences, Zhejiang University, Hangzhou, ChinaState Key Laboratory of Rice Biology, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Institute of Insect Sciences, Zhejiang University, Hangzhou, ChinaState Key Laboratory of Rice Biology, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Institute of Insect Sciences, Zhejiang University, Hangzhou, ChinaState Key Laboratory of Rice Biology, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Institute of Insect Sciences, Zhejiang University, Hangzhou, ChinaPeople’s Government of Fenshui Town, Tonglu County, Hangzhou, ChinaState Key Laboratory of Rice Biology, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Institute of Insect Sciences, Zhejiang University, Hangzhou, ChinaState Key Laboratory of Rice Biology, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Institute of Insect Sciences, Zhejiang University, Hangzhou, ChinaState Key Laboratory of Rice Biology, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Institute of Insect Sciences, Zhejiang University, Hangzhou, ChinaState Key Laboratory of Rice Biology, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Institute of Insect Sciences, Zhejiang University, Hangzhou, ChinaState Key Laboratory of Rice Biology, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Institute of Insect Sciences, Zhejiang University, Hangzhou, ChinaDepartment of Medicine and Stony Brook Cancer Center, The State University of New York at Stony Brook, Stony Brook, NY, United StatesState Key Laboratory of Rice Biology, Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture, Institute of Insect Sciences, Zhejiang University, Hangzhou, ChinaHainan Research Institute, Zhejiang University, Sanya, ChinaCeramides 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.https://www.frontiersin.org/articles/10.3389/fphys.2021.629532/fullneutral ceramidasebrown planthopperreproductionapoptosisceramide |
| spellingShingle | Xiao-Xiao Shi Mu-Fei Zhu Ni Wang Yuan-Jie Huang Yuan-Jie Huang Min-Jing Zhang Chao Zhang Soomro A. Ali Wen-Wu Zhou Chuanxi Zhang Cungui Mao Zeng-Rong Zhu Zeng-Rong Zhu Neutral Ceramidase Is Required for the Reproduction of Brown Planthopper, Nilaparvata lugens (Stål) Frontiers in Physiology neutral ceramidase brown planthopper reproduction apoptosis ceramide |
| 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 stal |
| topic | neutral ceramidase brown planthopper reproduction apoptosis ceramide |
| url | https://www.frontiersin.org/articles/10.3389/fphys.2021.629532/full |
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