miRNA对褐飞虱鞘脂质代谢基因表达的影响及沉默NlSPT1和NlSMase4的small RNA分析

doi:10.3864/j.issn.0578-1752.2024.20.008

中国农业科学 ›› 2024, Vol. 57 ›› Issue (20): 4022-4034.doi: 10.3864/j.issn.0578-1752.2024.20.008

• 专题：迁飞性害虫发生与防控 • 上一篇下一篇

miRNA对褐飞虱鞘脂质代谢基因表达的影响及沉默NlSPT1和NlSMase4的small RNA分析

王妮¹^,²^,³^,⁴(), 施哲逸¹^,²^,³, 尤元政¹^,²^,³, 张超¹^,²^,³, 周文武¹^,²^,³, 周瀛²^,³, 祝增荣¹^,²^,³()

¹ 浙江大学农业与生物技术学院昆虫科学研究所/水稻生物育种全国重点实验室/农业农村部作物病虫分子生物学重点实验室，杭州 310058
² 浙江大学海南研究院，海南三亚 572025
³ 浙江余杭稻米科技小院，浙江余杭 311121
⁴ 新疆农业大学农学院农业有害生物监测与安全防控重点实验室，乌鲁木齐 830052

收稿日期:2024-07-07 接受日期:2024-07-26 出版日期:2024-10-16 发布日期:2024-10-24
通信作者:
祝增荣，E-mail：zrzhu@zju.edu.cn
联系方式: 王妮，E-mail：niwang@xjau.edu.cn。
基金资助:
国家重点研发计划(2021YFD1401105); 国家自然科学基金面上项目(31871962); 浙江省“三农六方”科技协作项目(CTZB-F190625LWZ- SNY1)

Effects of miRNA on Gene Expression of Sphingolipids Metabolism and Small RNA Analysis of Silencing NlSPT1 and NlSMase4 in Nilaparvata lugens

WANG Ni¹^,²^,³^,⁴(), SHI ZheYi¹^,²^,³, YOU YuanZheng¹^,²^,³, ZHANG Chao¹^,²^,³, ZHOU WenWu¹^,²^,³, ZHOU Ying²^,³, ZHU ZengRong¹^,²^,³()

¹ Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University/State Key Laboratory of Rice Biology and Breeding/Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture and Rural Affairs, Hangzhou 310058
² Hainan Institute of Zhejiang University, Sanya 572025, Hainan
³ Zhejiang Yuhang Rice Science and Technology Institute, Yuhang 311121, Zhejiang
⁴ Key Laboratory of Monitoring and Safe Prevention and Control of Agricultural and Forestry Pests, College of Agriculture, Xinjiang Agricultural University, Urumqi 830052

Received:2024-07-07 Accepted:2024-07-26 Published:2024-10-16 Online:2024-10-24

摘要/Abstract

摘要：

【背景】鞘脂质是第二大类膜脂，作为信号转导物质参与细胞生长发育、繁殖及凋亡等过程。鞘脂质代谢酶调控鞘脂质代谢以维持生物体内代谢的稳态。【目的】以重要水稻害虫褐飞虱（Nilaparvata lugens）为研究对象，通过RNA干扰（RNA interference，RNAi）技术检测微小RNA（microRNA，miRNA）生物合成通路核心组分NlAgo1、NlDicer1和NlDrosha沉默后褐飞虱鞘脂质代谢通路相关基因的相对转录水平，结合small RNA测序分析沉默丝氨酸棕榈酰转移酶1（serine palmitoyltransferase 1，SPT1）和鞘磷脂酶4（sphingomyelinase 4，SMase4）基因的差异miRNA，探究miRNA在褐飞虱鞘脂质代谢中的作用，为害虫防治提供新的分子靶标。【方法】利用RNAi技术，分别对羽化后第1天（1 PAE，post adult eclosion）的雌成虫NlAgo1、NlDicer1和NlDrosha进行dsRNA注射，以dsGFP为对照；分别解剖羽化后第5天的卵巢组织，以β-actin作为内参基因，采用实时荧光定量PCR（qRT-PCR）方法检测NlAgo1、NlDicer1和NlDrosha沉默后鞘脂质代谢通路相关基因的表达量变化；根据已有的小RNA文库联合miRNA-靶基因预测软件对可能调控NlSPT1和NlSMase4表达的miRNA进行预测；通过small RNA测序技术对沉默NlSPT1和NlSMase4的差异miRNA进行鉴定和靶基因富集性分析。【结果】与对照组相比，沉默NlAgo1、NlDicer1或NlDrosha显著上调卵巢中NlSPT1和NlSMase4等鞘脂质代谢通路相关基因的表达；靶基因预测结果显示，有6条miRNA能与NlSPT1结合，13条miRNA能与NlSMase4结合；沉默NlSPT1和NlSMase4的差异miRNA的靶基因显著富集在细胞核和蛋白质结合等生物学过程以及内吞作用、内质网加工、MAPK信号通路、TOR信号通路、凋亡、脂质代谢等代谢通路。【结论】NlAgo1、NlDicer1和NlDrosha依赖性的miRNA通过影响鞘脂质代谢相关基因的表达影响鞘脂质代谢。NlSPT1和NlSMase4沉默引起褐飞虱卵巢miRNA表达水平的改变。研究结果可为基于鞘脂质代谢基因为靶标的害虫防治提供理论依据。

关键词: 褐飞虱, 微小RNA, 鞘脂质, RNA干扰, small RNA测序

Abstract:

【Background】Sphingolipids are the second major type of membrane lipids and mediate various biological processes as signal transducers, including cell growth, development, reproduction and apoptosis. Sphingolipid metabolism is tightly regulated by sphingolipid metabolizing enzymes to maintain the homeostasis of metabolism in vivo.aaaaa【Objective】The objectives of this study are to investigate the relative transcript levels of genes related to the sphingolipid metabolism pathway after silencing of the core components of microRNA (miRNA) biosynthesis pathway, NlAgo1, NlDicer1 and NlDrosha by RNA interference (RNAi), and analyze the differentially expressed miRNAs after silencing of serine palmitoyltransferase 1 (SPT1) and sphingomyelinase 4 (SMase4) gene combined with small RNA sequencing of Nilaparvata lugens, explore the role of miRNAs in the sphingolipid metabolism of N. lugens, and to provide a new molecular target for pest control.【Method】RNAi was performed with double stranded RNAs (dsRNAs) targeting NlAgo1, NlDicer1 and NlDrosha at 1 day post adult eclosion (1 PAE), respectively, and dsGFP was used as control. The ovaries at 5 PAE were dissected and β-actin was used as internal reference gene, the transcript levels of genes related to the sphingolipid metabolism pathway were detected by reverse-transcription quantitative PCR (qRT-PCR). miRNAs that may regulate the expression of NlSPT1 and NlSMase4 were predicated based on small RNA libraries combined with miRNA-target prediction software. Differentially expressed miRNAs after the silencing of NlSPT1 and NlSMase4 were identified and the target gene enrichment was analyzed by small RNA sequencing.【Result】RNAi-mediated silencing of NlAgo1, NlDicer1 or NlDrosha significantly up-regulated the expression of genes related to the sphingolipid metabolism pathway, including NlSPT1 and NlSMase4 in ovaries. Target gene prediction revealed 6 miRNAs and 13 miRNAs that could bind NlSPT1 and NlSMase4. The target genes of differentially expressed miRNAs that silencing NlSPT1 and NlSMase4 were significantly enriched in biological processes, including nuclear and protein binding, as well as metabolic pathways such as endocytosis, endoplasmic reticulum processing, MAPK signaling pathway, TOR signaling pathway, apoptosis, and lipid metabolism.【Conclusion】NlAgo1, NlDicer1, and NlDrosha-dependent miRNAs affect sphingolipid metabolism by influencing the expression of genes encoding sphingolipid metabolizing enzymes. The silencing of NlSPT1 and NlSMase4 induced changes in miRNA expression levels in N. lugens ovaries. These research results can provide a theoretical basis for pest control based on sphingolipid metabolism genes.

Key words: Nilaparvata lugens, microRNA (miRNA), sphingolipid, RNA interference (RNAi), small RNA sequencing

王妮, 施哲逸, 尤元政, 张超, 周文武, 周瀛, 祝增荣. miRNA对褐飞虱鞘脂质代谢基因表达的影响及沉默NlSPT1和NlSMase4的small RNA分析[J]. 中国农业科学, 2024, 57(20): 4022-4034.

WANG Ni, SHI ZheYi, YOU YuanZheng, ZHANG Chao, ZHOU WenWu, ZHOU Ying, ZHU ZengRong. Effects of miRNA on Gene Expression of Sphingolipids Metabolism and Small RNA Analysis of Silencing NlSPT1 and NlSMase4 in Nilaparvata lugens[J]. Scientia Agricultura Sinica, 2024, 57(20): 4022-4034.

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目的Purpose	引物名称Primer name	引物序列Primer sequence (5°‒3°)
dsRNA合成 dsRNA synthesis	dsNlAgo-1_F	T7-GTTTTGCGAGCCAATCATTT
	dsNlAgo-1_R	T7-CCTCCGAGCGGATGATAATA
	dsNlDicer-1_F	T7-GCAAGAAATATGGAGAGGCG
	dsNlDicer-1_R	T7-GTAGGTGGTGATGGCGAACT
	dsNlDrosha_F	T7-GCACACCCTCCAACGGATTA
	dsNlDrosha_R	T7-ATTTCGGCCTCGGCTTCTAC
	dsGFP_F	T7-AAGTTCAGCGTGTCCGGCGA
	dsGFP_R	T7-CACCTTGATGCCGTTCTTCT
实时荧光定量PCR分析 qRT-PCR analysis	qNlAgo-1_F	GAAAGCCGTTGACTGACTCC
	qNlAgo-1_R	ACTCCACAGTTTGCCCATTC
	qNlDicer-1_F	CACGCCTCCTATCACACCAA
	qNlDicer-1_R	TCCATGTCGAACGGCTAATG
	qNlDrosha_F	GAAGCTTTTCTGGGCGCTTT
	qNlDrosha_R	CGTTGGCCCTATGCACTCTA
	qNlSPT1_F	CGGCTCCTGTACCAAATAG
	qNlSPT1_R	GTAGATCACGTCCCGCTTGT
	qNlSPT2_F	TGCCTATCAGCGGCACATAC
	qNlSPT2_R	CAGATCCATAGACGACCGGC
	qNlSMase4_F	TGGACACCTCGTTCCGATTG
	qNlSMase4_R	GTTCCACAACCATGGGGCTA
	qNlKDR_F	GCGACGGCTACATTGTGTTC
	qNlKDR_R	GCTTCAGCCACACCTCTGAT
	qNlDES_F	GTTACCTATCCGAAGCCCCC
	qNlDES_R	CCCAGCATGTAAGCAAGCAC
	qNlCerS_F	ACCATGGCTGTGGCGAATTA
	qNlCerS_R	TCCTTGCGAATCACGTCGAA
	qNlCDase_F	ACTGGACCAAGTGCCAAACA
	qNlCDase_R	GATCGCGAACTGCCCTATGA
	qNlSMSL1_F	TACCACACACTCGCCAACAA
	qNlSMSL1_R	ACAGCGTGTCGTACTCGTTT
	qNlSMSL2_F	GTGTCGTTCGCATCGACTTG
	qNlSMSL2_R	GCCAGAGACAGTGTCGTGAT
	qNlGBA1_F	GGTCCCAACTGGGTCAACAA
	qNlGBA1_R	GCAACTGCCGATGAACTTGG
	qNlGBA2_F	GAACAACGTGCGGTAACGAG
	qNlGBA2_R	TACTGGGCTACCCACTCTCC
	qNlSPPase_F	GGCAGATGAGTGAACCCCAA
	qNlSPPase_R	AGCGCATAGGACACCGATTT
	β-actin_F	GTGCGTGACATCAAGGAGAAGC
	β-actin_R	GGAAGGAAGGCTGGAACAGAG

miRNA名称 miRNA name	miRNA序列 miRNA sequence (5°‒3°)
bmo-miR-316-5p_1ss23GT	TGTCTTTTTCCGCTTTGCTGCTT
tca-miR-316-5p_R+2	TGTCTTTTTCCGCTTTGCTGCCG
bmo-miR-9a-5p_L+2R-2	AATCTTTGGTTATCTAGCTGTAT
tca-miR-14-3p_L-4R+1	TCTTTTTCTCTCTCCTATT
tca-miR-277-3p	TAAATGCACTATCTGGTACGACA
tca-miR-92b-3p_L-1R+1	TTGCACTTGTCCCGGCCTGT

miRNA名称 miRNA name	miRNA序列 miRNA sequence (5°‒3°)
aae-miR-33_R-1	GTGCATTGTAGTTGCATTGC
dme-miR-276a-5p_L-1R-1_1ss22CT	AGCGAGGTATAGAGTTCCTAT
pca-miR-276-5p_R+4	AGCGAGGTATAGAGTTCCTACGAA
tca-miR-276-5p_R-2	AGCGAGGTATAGAGTTCCTACG
tca-miR-14-3p	TCAGTCTTTTTCTCTCTCCTAT
tca-miR-14-3p_R+1_1ss22TC	TCAGTCTTTTTCTCTCTCCTACT
tca-miR-14-3p_R-2_1ss15TC	TCAGTCTTTTTCTCCCTCCT
tca-miR-14-3p_R-2_1ss8TC	TCAGTCTCTTTCTCTCTCCT
tca-miR-14-3p_R-3_1ss19CA	TCAGTCTTTTTCTCTCTCA
tca-miR-14-3p_R-4	TCAGTCTTTTTCTCTCTC
tca-miR-14-3p_R-2_1ss1TC	CCAGTCTTTTTCTCTCTCCT
tca-miR-210-5p_R+1_1ss12GA	AGCTGCTGGACACTGCACAAGA
tca-miR-307-3p_R+2	TCACAACCTCCTTGAGTGAGCG

miRNA对褐飞虱鞘脂质代谢基因表达的影响及沉默NlSPT1和NlSMase4的small RNA分析

Effects of miRNA on Gene Expression of Sphingolipids Metabolism and Small RNA Analysis of Silencing NlSPT1 and NlSMase4 in Nilaparvata lugens

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