东方蜜蜂微孢子虫孢子中长链非编码RNA的竞争性内源RNA调控网络及潜在功能

doi:10.3864/j.issn.0578-1752.2020.10.018

Abstract

Abstract:

【Background】Long non-coding RNAs (lncRNAs) are a kind of non-coding transcripts with a length of more than 200 nt. LncRNAs can regulate gene expression at transcriptional level and post-transcriptional level via cis effect, trans effect or competing endogenous RNA (ceRNA) mechanism. LncRNAs have been proved to play pivotal roles in many biological processes such as growth and development.【Objective】The objective of this study is to perform detailed investigation and discussion of the regulatory manner of lncRNAs by combining small RNA (sRNA) omics dataset obtained in this work and previously gained lncRNA omics dataset, and to reveal the putative function of lncRNAs in Nosema ceranae spores.【Method】Here, purified spores of N. ceranae were sequenced using small RNA-seq (sRNA-seq), related bioinformatics software was used to conduct quality control of sequencing data. The upstream and downstream genes of N. ceranae lncRNAs were predicted based on the positional relationship between lncRNAs and mRNAs. Annotations of these upstream and downstream genes in GO and KEGG databases were carried out using Blast software. The lncRNA-miRNA and lncRNA-miRNA-mRNA regulatory networks were predicted using Target Finder software and then visualized with Cytoscape v3.7.2 software. The expression of partial lncRNAs, miRNAs and mRNAs within regulatory networks was validated with RT-PCR.【Result】In total, 16 597 883, 15 451 791 and 12 248 316 raw reads were obtained from sRNA-seq of N. ceranae spore samples, respectively, and after quality control, 15 608 370, 14 249 255 and 11 440 684 clean reads with a mean Q30 above 98.58% were gained, respectively. A total of 310 upstream and downstream genes of lncRNAs were predicted. These genes could be annotated to 35 functional terms associated with metabolic process, cell process, catalytic activity, binding and cells, etc. Additionally, these genes could be annotated to 56 metabolic pathways, including material metabolic pathways such as purine metabolism, carbon metabolism, pyruvate metabolism; and energy metabolic pathways including methane metabolism, oxidative phosphorylation, glycolysis/gluconeogenesis and so forth. The results indicated that corresponding lncRNAs could regulate the expression level of upstream and downstream genes through cis effect, thus participating in regulation of material and energy metabolisms as well as cell activities in N. ceranae spore. Furthermore, lncRNA-miRNA regulatory networks were constructed and analyzed, the result showed that MSTRG.3636.1, MSTRG.4498.1 and MSTRG.4883.1 could bind to four miRNAs including nce-miR-7729, nce-miR-7502, nce-miR-8639 and nce-miR-8565, suggesting that these three lncRNAs as ceRNAs could exert potential function in N. ceranae spore. LncRNA-miRNA-mRNA regulatory network analysis demonstrated that complex networks existed among them, miRNAs were located in the center, connecting lncRNAs and mRNAs, nce-miR-7502 and nce-miR-8639 could bind to the most mRNAs (28). MiRNAs targeting MSTRG.3636.1, MSTRG.4498.1 and MSTRG.4883.1 could target several mRNAs, indicating that these three lncRNAs might play a role via ceRNA mechanism, thus affecting the mechanism and vital activity in N. ceranae spore.【Conclusion】LncRNAs are likely to regulate the expression of upstream and downstream genes via cis effect, and indirectly affect the expression of target genes by absorbing miRNAs as ceRNAs, thus controlling basic activities in N. ceranae spore such as material metabolism and energy metabolism.

Key words: Nosema ceranae, non-coding RNA (ncRNA), long non-coding RNA (lncRNA), upstream and downstream genes, competing endogenous RNA (ceRNA), regulatory network

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.

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Figures/Tables 9

Table 1

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Table 3

Fig. 1

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Table 4

Swissprot and Nr database annotations of target mRNAs of miRNAs targeted by lncRNAs in N. ceranae spore"

核酸ID Nucleotide ID	Swissprot 数据库注释 Swissprot database annotation	Nr数据库注释 Nr database annotation
gene986	液泡氨基酸转运体5 Vacuolar amino acid transporter 5	假定蛋白NCER_101697 Hypothetical protein NCER_101697
gene783	负辅因子2复合亚基 Negative cofactor 2 complex subunit beta	假定蛋白NCER_101896 Hypothetical protein NCER_101896
gene565	丝氨酸/苏氨酸多聚蛋白激酶1 Serine/threonine-protein kinase plo1	假定蛋白NCER__102113 Hypothetical protein NCER_102113
gene2596	含C1778.09蛋白的TBC结构域 TBC domain-containing protein C1778.09	假定蛋白NCER_100108 Hypothetical protein NCER_100108
gene2543	TATA结合蛋白相关因子MOT1 TATA-binding protein-associated factor MOT1	假定蛋白NCER_100152 Hypothetical protein NCER_100152
gene2397	丝氨酸/苏氨酸蛋白激酶CDC5同源物 Cell cycle serine/threonine-protein kinase CDC5 homolog	假定蛋白NCER_100270 Hypothetical protein NCER_100270
gene2312	ERAD-相关E3泛素蛋白连接酶doa10 ERAD-associated E3 ubiquitin-protein ligase doa10	假定蛋白NCER_100375 Hypothetical protein NCER_100375
gene2178	转运蛋白sec24 Transport protein sec24	假定蛋白NCER_100510 Hypothetical protein NCER_100510
gene2014	转录相关蛋白1 Transcription-associated protein 1	假定蛋白NCER_100665 Hypothetical protein NCER_100665
gene1870	ERAD-相关E3泛素蛋白连接酶doa10 ERAD-associated E3 ubiquitin-protein ligase doa10	假定蛋白NCER_100805 Hypothetical protein NCER_100805
gene1766	赖氨酸- tRNA连接酶 Lysine-tRNA ligase	假定蛋白NCER_100909 Hypothetical protein NCER_100909
gene1719	T-复合体蛋白1亚基 T-complex protein 1 subunit alpha	假定蛋白NCER_100958 Hypothetical protein NCER_100958
gene1687	DNA-锚定 RNA 聚合酶 II 亚基RPB2 DNA-directed RNA polymerase II subunit RPB2	假定蛋白NCER_100983 Hypothetical protein NCER_100983
gene1678	锰-ATP转运酶4 Manganese-transporting ATPase 4	假定蛋白NCER_101005 Hypothetical protein NCER_101005
gene1677	3型蛋白酶体亚基 Probable proteasome subunit beta type-3	假定蛋白NCER_101004 Hypothetical protein NCER_101004
gene1662	微管蛋白γ链 Tubulin gamma chain	假定蛋白NCER_101024 Hypothetical protein NCER_101024
gene1563	核输出蛋白BRL1 Nucleus export protein BRL1	假定蛋白NCER_101114 Hypothetical protein NCER_101114
gene1383	V型质子ATP酶催化亚基A V-type proton ATPase catalytic subunit A	假定蛋白NCER_101294 Hypothetical protein NCER_101294
gene1366	长链脂肪酸CoA链2 Long chain fatty acid CoA ligase 2	假定蛋白NCER_101315 Hypothetical protein NCER_101315
gene1360	热休克蛋白hsp98 Heat shock protein hsp98	假定蛋白NCER_101322 Hypothetical protein NCER_101322
gene1348	丝氨酸/苏氨酸蛋白激酶MEC1同源物 Serine/threonine-protein kinase MEC1 homolog	假定蛋白NCER_101332 Hypothetical protein NCER_101332
gene1190	泛素羧基末端水解酶5 Ubiquitin carboxyl-terminal hydrolase 5	假定蛋白NCER_101487 Hypothetical protein NCER_101487
gene1180	苯丙氨酸-tRNA连接酶亚基 Phenylalanine-tRNA ligase beta subunit	假定蛋白NCER_101490 Hypothetical protein NCER_101490
gene1134	二磷酸异戊基丁二醇异构酶 Isopentenyl-diphosphate Delta-isomerase	假定蛋白NCER_101544 Hypothetical protein NCER_101544
newGene_142	60S核糖体蛋白L40（前体） 60S ribosomal protein L40 (precursor)	假定蛋白NCER_102067 Hypothetical protein NCER_102067

Table 4

Fig. 5

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核酸ID Nucleotide ID	引物名称 Primer name	引物序列 Primer sequence (5′-3′)	预期目的片段 Product size (bp)
gene1439	1-F	ATGTATCTTATGCCAACGC	382
gene1439	1-R	TGAATCTTTCCTACACCCT	382
gene565	2-F	TCAAGCCTGTTAAGATGAC	499
gene565	2-R	ACTACTTCTGGCGGTTTAT	499
gene1719	3-F	ATAGGAGGTAAACATCAG	438
gene1719	3-R	ATAGTAAAGTTCAGTGCC	438
gene1366	4-F	TTGAAGAAGGTGTCGCAGAAC	182
gene1366	4-R	AGCAGAGCCACATAAACAAGC	182
gene1360	5-F	AAGAAGCCGAAACAACCC	101
gene1360	5-R	GTTAGCCGCATCCATAGC	101
gene1134	6-F	TGTACGGTCTGGCTGCTTC	352
gene1134	6-R	GGACTTGGCTTTCCACTAA	352
gene1695	7-F	GATACAGCCTCTTTGG	138
gene1695	7-R	GGAACAATAACCCTAAA	138
gene1563	8-F	TGCCTACAATCAACTCTAAT	384
gene1563	8-R	CACCCAATACTTCAAATAAC	384
MSTRG.3636.1	9-F	TAACTAGCCTACTCTATCCC	257
MSTRG.3636.1	9-R	TAAAAGCACTAACTACAACC	257
MSTRG.4883.1	10-F	CTGACAGACCATAGTCGGCATA	128
MSTRG.4883.1	10-R	TCTACAATGATGGGCACAGGA	128
nce-miR-8565	11-L	CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGCCTAAAGA	67
nce-miR-8565	11-F	CGCGCCTTTAATTGTGAAACATG	67
nce-miR-7502	12-L	CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGAACTTGTC	66
nce-miR-7502	12-F	CGCGCCTAAAAACAAAAATGTA	66
nce-miR-7729	13-L	CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGTCTAGGCC	62
nce-miR-7729	13-F	CGCGCCTAGTGATGGCTGT	62
-	R	CTCAACTGGTGTCGTGGA

样品 Sample	原始读段 Raw reads	有效读段 Clean reads	99.9%的碱基正确率 Q30 (%)
NcS-1	16597883	15608370	98.61
NcS-2	15451791	14249255	98.65
NcS-2	12248316	11440684	98.58

样品 Sample	未注释的有效读段 Unannotated clean reads	比对上的有效读段 Mapped clean reads	比对率 Mapping ratio (%)
NcS-1	14596118	7717280	52.87
NcS-2	12924265	7801135	60.36
NcS-3	10842971	6482422	59.78

Investigation of Competing Endogenous RNA Regulatory Network and Putative Function of Long Non-Coding RNAs in Nosema ceranae Spore

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