蜜蜂球囊菌中长链非编码RNA的调控作用

doi:10.3864/j.issn.0578-1752.2021.01.017

Abstract

Abstract:

【Objective】Long non-coding RNAs (lncRNAs), a kind of RNAs with highly conserved secondary and tertiary structures and a length of more than 200 nt, have no protein-coding potential. LncRNAs are widely involved in transcriptional and post-transcriptional regulations, such as dosage compensation, cell differentiation and growing development. The study aimed to perform analyses of cis regulation, antisense lncRNA regulation and competing endogenous RNA (ceRNA) regulation as well as related discussion based on previously obtained high-quality lncRNA omics dataset from mixed samples of Ascosphaera apis mycelia and spores, and further reveal the putative regulatory role of lncRNAs in A. apis.【Method】Protein-coding genes located at 100 kb upstream and downstream of A. apis lncRNAs were predicted on basis of the position of lncRNA genes; these upstream and downstream genes were annotated to GO and KEGG databases using Blast to gain function and pathway annotations. Target mRNAs of lncRNAs were identified using LncTar software and then annotated to KEGG and eggNOG databases. Target miRNAs of lncRNAs and target mRNAs of miRNAs were predicted using TargetFinder, followed by visualization of regulatory networks using Cytoscape v3.7.1. The expressions of partial lncRNAs, target miRNAs and target mRNAs within regulatory networks were validated using RT-PCR.【Result】A total of 5 852 upstream and downstream genes of A. apis lncRNAs were predicted. These upstream and downstream genes could be annotated to 48 functional terms such as cellular process, metabolic process and stress response, as well as 121 pathways including metabolic pathways, biosynthesis of secondary metabolites and biosynthesis of antibiotics, which indicated that part of A. apis lncRNAs could regulate the expression levels of upstream and downstream genes via cis-acting function, thus participating in regulation of basic cell activities including material and energy metabolisms. Seven lncRNAs were found to have sequence complementary pairing relationship with seven target mRNAs. Among them, five targets were annotated to hypothetical proteins in eggNOG database, while gene3444 could be annotated to nuclear pore complex protein An-Nup120 and hypothetical protein in KEGG database, suggesting that the aforementioned one antisense lncRNA might be involved in regulating biological processes including biosynthesis of nuclear pore complex protein. Additionally, 227 lncRNAs were predicted to have target binding relationship with 73 miRNAs; majority of these lncRNAs (79.02%) could only link to 1-2 miRNAs and partial miRNAs could be targeted by several lncRNAs. Furthermore, lncRNA-miRNA-mRNA regulatory networks associated with oxidative phosphorylation pathway and MAPK signaling pathway were constructed and analyzed, the results showed that 222 lncRNAs related to oxidative phosphorylation pathway could target 78 miRNAs and 50 mRNAs; as for MAPK signaling pathway, 222 associated lncRNAs could target 76 miRNAs and 46 mRNAs; the results suggested that part of A. apis lncRNAs were likely to regulate these two pathways via ceRNA mechanism, hence affecting energy synthesis, environmental adaptation as well as growth and development.【Conclusion】Partial lncRNAs may regulate a series of biological processes such as growth and development, material and energy mechanisms as well as environmental adaptation of A. apis; MSTRG.5393.1 as an antisense lncRNA may regulate biosynthesis of nuclear pore complex protein in A. apis.

Key words: Ascosphaera apis, long non-coding RNA (lncRNA), cis regulation, antisense lncRNA, competing endogenous RNA (ceRNA)

ZHOU DingDing, FAN YuanChan, WANG Jie, JIANG HaiBin, ZHU ZhiWei, FAN XiaoXue, CHEN HuaZhi, DU Yu, ZHOU ZiYu, XIONG CuiLing, ZHENG YanZhen, FU ZhongMin, CHEN DaFu, GUO Rui. Regulatory Function of Long Non-Coding RNAs in Ascosphaera apis[J].Scientia Agricultura Sinica, 2021, 54(1): 224-238.

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Figures/Tables 8

Table 1

Primers used in this study"

核酸ID Nucleic acid ID	引物名称 Primer name	引物序列 Primer sequence (5′-3′)	产物大小 Product size (bp)
MSTRG.6443.1	F	AAAATGAAAAGGCAAATC	210
MSTRG.6443.1	R	AAGGTCAAGAAGCACAAG	210
MSTRG.2135.1	F	AGAAGCAGCAAGGAAGTCG	128
MSTRG.2135.1	R	GGCAGGGCAATAACAAAAC	128
MSTRG.2134.1	F	ACTCACTCTCTGCCCCTC	238
MSTRG.2134.1	R	CCCATTTATTTGCTACCG	238
MSTRG.3422.1	F	AACCGAAAAACTCAAGGA	160
MSTRG.3422.1	R	TCGCAATCAGACATCAAA	160
MSTRG.2302.1	F	TGTCTGTCCGTTCGTCCTT	139
MSTRG.2302.1	R	CAGCGTAGCGTTGTGTAGT	139
MSTRG.5023.1	F	CAAACCCAGATTTATTCC	110
MSTRG.5023.1	R	TACCTTTCCTCCTTACGA	110
MSTRG.5584.1	F	GAAGACATTCAATCCAACAC	184
MSTRG.5584.1	R	AGCCACACACTTATCCACTA	184
MSTRG.1870.1	F	GCCTCTTTTCGGTTTGCT	158
MSTRG.1870.1	R	CGTTCTTGCTCGTGTCGT	158
MSTRG.1614.1	F	AAATCGGAACGGTGAGGGA	115
MSTRG.1614.1	R	GGCAGTGACCAAAGGCAAA	115
gene1602	F	AGCCCCGCTACCAAACTC	110
gene1602	R	CTGTCCCTCATCGCCATA	110
gene1970	F	AGTTCTCTTACTGGCGTCTTTG	100
gene1970	R	CTTTCACTTGCTGGGCTTTCTC	100
gene2674	F	TGGCTTCCTACACAAACCT	233
gene2674	R	TTCCTTATTCACCCGCTCC	233
gene4126	F	ATGAACAATGTCAAGGAAGC	320
gene4126	R	TCTGGAAAGAGTGTGGGGAG	320
gene4125	F	CCAAACAGACAAATGGCTAA	120
gene4125	R	TCGGGAAAGATGATTGAGAA	120
gene5384	F	TATGGTTATGCCTATGGTTT	122
gene5384	R	GATGTGGGGTATCTCGTGTT	122
gene1986	F	CATTGATACCGATACAGAGAC	237
gene1986	R	GAGATAACATTGACAACGCCT	237
gene989	F	CCTCTTCCCACACTCTCACT	236
gene989	R	AGACTCCAAAACCTGCTCCT	236
miR-281-y	L	CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGCAAAGAGA	72
miR-281-y	F	ACACTCCAGCTGGGTGTCATGGAGTTGC	72
miR-13-y	L	CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGAGCTCATC	73
miR-13-y	F	ACACTCCAGCTGGGTATCACAGCCATTTT	73
miR-11980-y	L	CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGTCTGCCAA	68
miR-11980-y	F	ACACTCCAGCTGGGGGGAACGGGC	68
miR-6057-y	L	CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGCATTTGTT	72
miR-6057-y	F	ACACTCCAGCTGGGTTTGTGACTGTAAC	72
miR-1-z	L	CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGATACATAC	72
miR-1-z	F	ACACTCCAGCTGGGTGGAATGTAAAGAA	72
miR-9-z	L	CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGTCATACAG	73
miR-9-z	F	ACACTCCAGCTGGGTCTTTGGTTATCTAG	73
miR-13-x	L	CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGCATTCCAC	72
miR-13-x	F	ACACTCCAGCTGGGACATCAAATTGGTT	72
actin (gene6001)	F	GCTACTTCCCATCATTCGTC	92
actin (gene6001)	R	CCCAATCTGTGACAATCCC	92
-	Universal R	CTCAACTGGTGTCGTGGA

Table 1

Fig. 1

Fig. 2

Table 2

Fig. 3

Table 3

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LncRNA ID	LncRNA大小 LncRNA size (bp)	靶mRNA ID Target mRNA ID	靶mRNA大小 Target mRNA size (bp)	eggNOG数据库注释 Annotation in eggNOG database
MSTRG.3576.1	285	gene1316	1851	保守性假定蛋白（土曲霉NIH2624） Conserved hypothetical protein (Aspergillus terreus NIH2624)
MSTRG.2795.1	253	gene548	1407	—
MSTRG.1238.1	294	gene1194	1569	保守性假定蛋白（土曲霉NIH2624） Conserved hypothetical protein (Aspergillus terreus NIH2624)
MSTRG.5393.1	238	gene3444	3831	核孔复合体蛋白An-Nup120（皮炎芽生菌ATCC 18188） Nuclear pore complex protein An-Nup120 (Blastomyces dermatitidis ATCC 18188)
MSTRG.1387.1	206	gene4650	3186	假定蛋白AN4929.2（构巢曲霉FGSC A4） Hypothetical protein AN4929.2 (Aspergillus nidulans FGSC A4)
MSTRG.1672.1	221	gene5233	7065	假定蛋白PABG_05261（巴西副球孢子菌Pb03） Hypothetical protein PABG_05261 (Paracoccidioides brasiliensis Pb03)
MSTRG.3829.1	296	gene1554	3036	假定蛋白CIMG_07970（粗球孢子菌RS） Hypothetical protein CIMG_07970 (Coccidioides immitis RS)

通路 Pathway	通路ID Pathway ID	mRNA数 Number of mRNAs	P值 P value
新陈代谢途径Metabolic pathway	ko01100	9	0.2834603
次生代谢物的生物合成Biosynthesis of secondary metabolite	ko01110	4	0.3784708
自噬-其他真核生物Autophagy-other eukaryote	ko04136	3	0.0012982
线粒体自噬-酵母Mitophagy-yeast	ko04139	3	0.0059399
自噬-酵母Autophagy-yeast	ko04138	3	0.0165266
抗生素生物合成Biosynthesis of antibiotics	ko01130	3	0.4179210
谷胱甘肽代谢Glutathione metabolism	ko00480	2	0.0271424
寿命调节途径-多物种Longevity regulating pathway-multiple species	ko04213	2	0.0302527
内质网蛋白加工Protein processing in endoplasmic reticulum	ko04141	2	0.1919356
减数分裂-酵母Meiosis-yeast	ko04113	2	0.2092014
嘌呤代谢Purine metabolism	ko00230	2	0.2678463
细胞周期-酵母Cell cycle-yeast	ko04111	2	0.3210316

Regulatory Function of Long Non-Coding RNAs in Ascosphaera apis

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