微小RNA介导东方蜜蜂微孢子虫侵染意大利蜜蜂工蜂的分子机制

doi:10.3864/j.issn.0578-1752.2020.15.018

Abstract

Abstract:

【Objective】Differentially expressed miRNAs (DEmiRNAs) and their target mRNAs in purified spores of Nosema ceranae and N. ceranae infecting Apis mellifera ligustica worker were systematically analyzed, followed by screening, investigation and exploration of DEmiRNAs and corresponding regulatory networks associated with pathogenic virulence factors and infection factors to reveal the mechanism of N. ceranae infection to A. m. ligustica worker.【Method】A. m. ligustica workers' midguts at 7 d and 10 d post infection (dpi) with N. ceranae and purified spores of N. ceranae (NcCK) were deeply sequenced using small RNA-seq (sRNA-seq), followed by screening out datasets of N. ceranae during the infection process (NcT1 and NcT2) and purified spores through sequential mapping to rRNA database, Apis mellifera genome and N. ceranae genome. Based on the criteria of P≤0.05, |log₂ fold change|≥1, DEmiRNAs in each comparison group were filtered out by comparative analysis. Expression profiling of DEmiRNAs, prediction of target mRNAs, function and pathway annotations of target mRNAs, and construction and survey of regulatory networks were performed by relevant bioinformatic software. The differential expression trend of DEmiRNAs and the reliability of sequencing data were verified by RT-qPCR.【Result】There were 164, 122 and 60 DEmiRNAs in NcCK vs NcT1, NcCK vs NcT2 and NcT1 vs NcT2 comparison groups. Venn analysis showed that 5 up-regulated miRNAs and 6 down-regulated ones were shared by these three comparison groups. In total, 1 885, 1 733 and 1 524 target mRNAs of DEmiRNAs were respectively predicted. These targets were annotated to 27, 25, and 26 functional terms, respectively, with the most abundant annotations being metabolic processes, catalytic activity, cellular processes, binding and cell. These targets were as well respectively annotated to 84, 84, and 84 pathways, among them the largest groups were metabolic pathway, ribosome, and secondary metabolite biosynthesis. In addition, 35, 26 and 12 target mRNAs associated with MAPK signaling pathway were targeted by DEmiRNAs in NcCK vs NcT1, NcCK vs NcT2 and NcT1 vs NcT2, while 49, 40 and 17 target mRNAs related to glycolysis/gluconeogenesis pathway were targeted by DEmiRNAs in the aforementioned three comparison groups. Further analysis revealed that DEmiRNAs of N. ceranae were involved in regulating the expression of genes encoding virulence factors such as ricin B lectin, apoptosis inhibitor, polar tube protein and spore wall protein; and genes encoding infection factors such as hexokinase and ATP/ADP transferase, ABC transporter and transcription factor ste12.【Conclusion】The differential expression profile of miRNAs in N. ceranae infecting A. m. ligustica worker was parsed via in-depth and detailed investigation and exploration. N. ceranae may regulate the expression level of genes encoding virulence factors including ricin B lectin, apoptosis inhibitor, polar tube protein and spore wall protein, as well as genes encoding infection factors such as hexokinase, ATP/ADP transferase, ABC transporter and transcription factor ste12 corresponding miRNAs, by controlling the expression of corresponding miRNAs, thus adapting to the environment within the host cell and promoting its proliferation and infection.

Key words: Nosema ceranae, Apis mellifera ligustica, microRNA (miRNA), infection mechanism, regulatory network

GENG SiHai,SHI CaiYun,FAN XiaoXue,WANG Jie,ZHU ZhiWei,JIANG HaiBin,FAN YuanChan,CHEN HuaZhi,DU Yu,WANG XinRui,XIONG CuiLing,ZHENG YanZhen,FU ZhongMin,CHEN DaFu,GUO Rui. The Mechanism Underlying MicroRNAs-Mediated Nosema ceranae Infection to Apis mellifera ligustica Worker[J].Scientia Agricultura Sinica, 2020, 53(15): 3187-3204.

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References 51

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引物ID Primer ID	引物序列 Primer sequence
miR-2478-y	Loop: GTCGTATCCAGTGCGTGTCGTGGAGTCGGCAATTGCACTGGATACGACTGGTGTC F: GCGCGCGTCGAATCCCACT
novel-m0017-5p	Loop: GTCGTATCCAGTGCGTGTCGTGGAGTCGGCAATTGCACTGGATACGACGGGCATA F: GCGCGCGTGGACCAGTGGC
novel-m0010-5p	Loop: GTCGTATCCAGTGCGTGTCGTGGAGTCGGCAATTGCACTGGATACGACGCTCGCT F: GCGCGCGTTTAGTTTGGCT
miR-3968-y	Loop: GTCGTATCCAGTGCGTGTCGTGGAGTCGGCAATTGCACTGGATACGACTGGTGTC F: GCGCGCGTCGAATCCCACT
miR-146-x	Loop: GTCGTATCCAGTGCGTGTCGTGGAGTCGGCAATTGCACTGGATACGACAACCCAT R: GCGCGCGTGAGAACTGAAT
miR-24-y	Loop: GTCGTATCCAGTGCGTGTCGTGGAGTCGGCAATTGCACTGGATACGACGTTCCTG F: GCGCGCGTGGCTCAGTTCA
miR-2965-y	Loop: GTCGTATCCAGTGCGTGTCGTGGAGTCGGCAATTGCACTGGATACGACTGCTCTC F: GCGCCGGAGGACTGCT
miR-318-y	Loop: GTCGTATCCAGTGCGTGTCGTGGAGTCGGCAATTGCACTGGATACGACGACCAAC F: CGGCCGCTCACTGGGC
	R: CAGTGCGTGTCGTGGAGT
5S rRNA	F: CGAGCGGTTTCCCATCTCAGTA R: AAAACACCGGAACTCGTCAGCT

样品Sample	原始读段Raw reads	有效标签Clean tags	映射读段Mapped reads	映射率Mapping ratio (%)
NcCK1	16506662	13466818	7560765	56.14
NcCK2	15368310	11938692	7655068	64.12
NcCK3	12180663	10160918	6349388	62.49
NcT1-1	13345686	6950844	1865571	26.84
NcT1-2	12837034	7324633	2510215	34.27
NcT1-3	13943680	7249967	1934012	26.68
NcT2-1	13820326	10605224	5503089	51.89
NcT2-2	14311818	9988951	4763103	47.68
NcT2-3	14013040	9722581	4513943	46.43

The Mechanism Underlying MicroRNAs-Mediated Nosema ceranae Infection to Apis mellifera ligustica Worker

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通路 Pathway	NcCK vs NcT1比较组 NcCK vs NcT1 group	NcCK vs NcT2比较组 NcCK vs NcT2 group	NcT1 vs NcT2比较组 NcT1 vs NcT2 group
新陈代谢途径 Metabolic pathways	119	113	103
核糖体 Ribosome	56	50	41
次生代谢产物合成 Biosynthesis of secondary metabolites	48	47	42
真菌生物核糖体的生物合成 Ribosome biogenesis in eukaryotes	37	38	29
抗生素的生物合成 Biosynthesis of antibiotics	36	35	31
内质网蛋白质加工 Protein processing in endoplasmic reticulum	35	32	29
嘌呤代谢 Purine metabolism	33	28	26
嘧啶代谢 Pyrimidine metabolism	32	28	25
细胞周期 Cell cycle	31	30	28
RNA转运 RNA transport	30	26	24
蛋白酶体 Proteasome	28	25	24
减数分裂 Meiosis	26	24	24
mRNA监督通路 mRNA surveillance pathway	24	21	22
DNA复制 DNA replication	24	24	22
泛素蛋白水解 Ubiquitin mediated proteolysis	24	24	20

[1]	DU Yu,FAN XiaoXue,JIANG HaiBin,WANG Jie,FENG RuiRong,ZHANG WenDe,YU KeJun,LONG Qi,CAI ZongBing,XIONG CuiLing,ZHENG YanZhen,CHEN DaFu,FU ZhongMin,XU GuoJun,GUO Rui. MicroRNA-Mediated Cross-Kingdom Regulation of Apis mellifera ligustica Worker to Nosema ceranae [J]. Scientia Agricultura Sinica, 2021, 54(8): 1805-1820.
[2]	HuaZhi CHEN,YuanChan FAN,HaiBin JIANG,Jie WANG,XiaoXue FAN,ZhiWei ZHU,Qi LONG,ZongBing CAI,YanZhen ZHENG,ZhongMin FU,GuoJun XU,DaFu CHEN,Rui GUO. Improvement of Nosema ceranae Genome Annotation Based on Nanopore Full-Length Transcriptome Data [J]. Scientia Agricultura Sinica, 2021, 54(6): 1288-1300.
[3]	GAO Yan,ZHU YaNan,LI QiuFang,SU SongKun,NIE HongYi. Transcriptomic Analysis of Genes Related to Nursing Behavior in the Brains of Apis mellifera ligustica [J]. Scientia Agricultura Sinica, 2020, 53(19): 4092-4102.
[4]	DU Yu,FAN XiaoXue,JIANG HaiBin,WANG Jie,FAN YuanChan,ZHU ZhiWei,ZHOU DingDing,WAN JieQi,LU JiaXuan,XIONG CuiLing,ZHENG YanZhen,CHEN DaFu,GUO Rui. The Potential Role of MicroRNAs and MicroRNA-Mediated Competing Endogenous Networks During the Developmental Process of Apis mellifera ligustica Worker’s Midgut [J]. Scientia Agricultura Sinica, 2020, 53(12): 2512-2526.
[5]	ZHOU DingDing,SHI XiaoYu,WANG Jie,FAN YuanChan,ZHU ZhiWei,JIANG HaiBin,FAN XiaoXue,XIONG CuiLing,ZHENG YanZhen,FU ZhongMin,XU GuoJun,CHEN DaFu,GUO Rui. Investigation of Competing Endogenous RNA Regulatory Network and Putative Function of Long Non-Coding RNAs in Nosema ceranae Spore [J]. Scientia Agricultura Sinica, 2020, 53(10): 2122-2136.
[6]	Yu DU,DingDing ZHOU,JieQi WAN,JiaXuan LU,XiaoXue FAN,YuanChan FAN,Heng CHEN,CuiLing XIONG,YanZhen ZHENG,ZhongMin FU,GuoJun XU,DaFu CHEN,Rui GUO. Profiling and Regulation Network of Differentially Expressed Genes During the Development Process of Apis mellifera ligustica Worker’s Midgut [J]. Scientia Agricultura Sinica, 2020, 53(1): 201-212.
[7]	FU ZhongMin,CHEN HuaZhi,LIU SiYa,ZHU ZhiWei,FAN XiaoXue,FAN YuanChan,WAN JieQi,ZHANG Lu,XIONG CuiLing,XU GuoJun,CHEN DaFu,GUO Rui. Immune Responses of Apis mellifera ligustia to Nosema ceranae Stress [J]. Scientia Agricultura Sinica, 2019, 52(17): 3069-3082.
[8]	YU Jing,ZHANG WeiXing,MA LanTing,XU BaoHua. Effect of Dietary α-Linolenic Acid Levels on Physiological Function of Apis mellifera ligustica Worker Bee Larvae [J]. Scientia Agricultura Sinica, 2019, 52(13): 2368-2378.
[9]	GUO Rui,DU Yu,TONG XinYu,XIONG CuiLing,ZHENG YanZhen,XU GuoJun,WANG HaiPeng,GENG SiHai,ZHOU DingDing,GUO YiLong,WU SuZhen,CHEN DaFu. Differentially Expressed MicroRNAs and Their Regulation Networks in Apis mellifera ligustica Larval Gut During the Early Stage of Ascosphaera apis Infection [J]. Scientia Agricultura Sinica, 2019, 52(1): 166-180.
[10]	GUO Rui,CHEN HuaZhi,XIONG CuiLing,ZHENG YanZhen,FU ZhongMin,XU GuoJun,DU Yu,WANG HaiPeng,GENG SiHai,ZHOU DingDing,LIU SiYa,CHEN DaFu. Analysis of Differentially Expressed Circular RNAs and Their Regulation Networks During the Developmental Process of Apis mellifera ligustica Worker’s Midgut [J]. Scientia Agricultura Sinica, 2018, 51(23): 4575-4590.
[11]	Rui GUO,Yu DU,CuiLing XIONG,YanZhen ZHENG,ZhongMin FU,GuoJun XU,HaiPeng WANG,HuaZhi CHEN,SiHai GENG,DingDing ZHOU,CaiYun SHI,HongXia ZHAO,DaFu CHEN. Differentially Expressed MicroRNA and Their Regulation Networks During the Developmental Process of Apis mellifera ligustica Larval Gut [J]. Scientia Agricultura Sinica, 2018, 51(21): 4197-4209.
[12]	Rui GUO, SiHai GENG, CuiLing XIONG, YanZhen ZHENG, ZhongMin FU, HaiPeng WANG, Yu DU, XinYu TONG, HongXia ZHAO, DaFu CHEN. Differential Expression Analysis of Long Non-Coding RNAs During the Developmental Process of Apis mellifera ligustica Worker’s Midgut [J]. Scientia Agricultura Sinica, 2018, 51(18): 3600-3613.