Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (20): 4022-4034.doi: 10.3864/j.issn.0578-1752.2024.20.008

• SPECIAL FOCUS: OCCURRENCE AND CONTROL OF MIGRATORY PESTS • Previous Articles     Next Articles

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. 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 Online:2024-10-16 Published:2024-10-24
  • Contact: ZHU ZengRong

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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

Table 1

The primers used in this study"

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

Fig. 1

Effect of silencing NlAgo1 on sphingolipid metabolic genes expression in N. lugens"

Fig. 2

Effect of silencing NlDicer1 on sphingolipid metabolic genes expression in N. lugens"

Fig. 3

Effect of silencing NlDrosha on sphingolipid metabolic genes expression in N. lugens"

Table 2

Predication of miRNAs targeting NlSPT1"

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

Table 3

Predication of miRNAs targeting NlSMase4"

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

Fig. 4

Silencing efficiency of NlSPT1 and NlSMase4"

Fig. 5

Cluster heat map of the differentially expressed miRNAs"

Fig. 6

GO (A) and KEGG (B) enrichment for the target genes of differentially expressed miRNAs in the dsNlSPT1 vs dsGFP"

Fig. 7

GO (A) and KEGG (B) enrichment for the target genes of differentially expressed miRNAs in the dsNlSMase4 vs dsGFP"

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