微小RNA介导意大利蜜蜂工蜂对东方蜜蜂微孢子虫的跨界调控

doi:10.3864/j.issn.0578-1752.2021.08.019

Abstract

Abstract:

【Objective】Nosema ceranae infects Apis mellifera ligustica and causes microsporidiosis. In this study, to reveal the mechanism of miRNA-mediated cross-kingdom regulation of A. m. ligustica worker to N. ceranae, prediction, GO and KEGG database annotation as well as regulatory network analysis of N. ceranae mRNAs and differentially expressed mRNAs (DEmRNAs) targeted by differentially expressed miRNAs (DEmiRNAs) of A. m. ligustica workers’ midguts were conducted by bioinformatic approaches based on previously gained miRNA and mRNA omics data. 【Method】Significant host DEmiRNAs were screened out by comparison of miRNA omics data from A. m. ligustica workers’ midguts at 7 d and 10 d post N. ceranae infection (AmT1, AmT2) and corresponding uninfected midguts (AmCK1, AmCK2). DEmRNAs of pathogen were screened out through comparison of mRNA omics data from N. ceranae infecting A. m. ligustica worker’s midgut (NcT1 and NcT2) and pure fungal spores (NcCK). mRNAs and DEmRNAs of N. ceranae targeted by significant host DEmiRNAs were predicted using TargetFinder software. GO and KEGG database annotations of aforementioned targets were conducted using related bioinformatics tools. On basis of our previous findings, pathogen DEmRNAs associated with spore wall protein, polar tube protein, ricin B lectin, ATP/ADP translocase, ABC transporters and glycolysis/gluconeogenesis, and their target significant DEmiRNAs of host were filtered out, followed by construction and investigation of regulatory network. 【Result】In AmCK1 vs AmT1 comparison group, 48 significantly up-regulated miRNAs and 36 significantly down-regulated miRNAs could respectively target 1 345 and 1 046 mRNAs of N. ceranae; additionally, 47 significantly up-regulated miRNAs and 34 significantly down-regulated miRNAs of host could target 584 significantly down-regulated mRNAs and 265 significantly up-regulated mRNAs in NcCK vs NcT1; these targets were involved in 19 and 22 functional terms as well as 66 and 64 pathways. In AmCK2 vs AmT2 comparison group, 56 significantly up-regulated miRNAs and 51 significantly down-regulated miRNAs could respectively target 1 260 and 1 317 mRNAs of N. ceranae, additionally, 52 significantly up-regulated miRNAs and 49 significantly down-regulated miRNAs could target 587 significantly down-regulated mRNAs and 336 significantly up-regulated mRNAs in NcCK vs NcT2, which were engaged in 20 and 23 functional terms as well as 64 and 65 pathways. Further, eight common significantly up-regulated miRNAs and one common significantly down-regulated miRNA in AmCK1 vs AmT1 and AmCK2 vs AmT2 comparison groups could respectively target 144 common significantly down-regulated mRNAs and 10 common significantly up-regulated mRNAs in NcCK vs NcT1 and NcCK vs NcT2 comparison groups, which could be annotated to 18 and 13 functional terms as well as 38 and seven pathways. Moreover, host significantly up-regulated miRNAs in AmCK1 vs AmT1 and AmCK2 vs AmT2 could target pathogen significantly down-regulated mRNAs in NcCK vs NcT1 and NcCK vs NcT2, associated with RNAi, virulence factors such as polar tube protein, spore wall protein and ricin B lectin, glycolysis/gluconeogenesis and MAPK signal pathway. 【Conclusion】Complex target binding relationship and potential cross-kingdom regulatory relationship exist between host DEmiRNAs and pathogen DEmRNAs during the infection of A. m. ligustica worker with N. ceranae; host DEmiRNAs are likely to inhibit or degrade pathogen DEmRNAs associated with RNAi, virulence factor/infection factor, glycolysis/gluconeogenesis pathway, ATP/ADP translocase, ABC transporters, and MAPK signal pathway to affect N. ceranae infection and proliferation.

Key words: Apis mellifera ligustica, Nosema ceranae, microRNA, cross-kingdom regulation, regulatory network, immune defense

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.

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Figures/Tables 7

Fig. 1

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Table 1

Summary of N. ceranae virulence factor/infection factor-associated down-regulated mRNAs in NcCK vs NcT1 targeted by significantly up-regulated miRNAs in AmCK1 vs AmT1"

差异表达miRNA DEmiRNA	差异表达mRNA DEmRNA	差异表达mRNA的log₂FC log₂FC of DEmRNA	差异表达mRNA的P值 P value of DEmRNA	Nr数据库描述 Description in Nr database
ame-miR-6052	XM_002996297.1	-10.4546	0.0802	蓖麻毒素B凝集素 Ricin B lectin
miR-196-x	XM_002996297.1	-10.4546	0.0802	蓖麻毒素B凝集素 Ricin B lectin
miR-16-y	XM_002995069.1	-1.7206	2.6275E-25	ABC转运蛋白 ABC transporter
miR-16-y	XM_002996253.1	-3.6539	1.2369E-118	ABC转运蛋白 ABC transporter
miR-20-x	XM_002996675.1	-1.9081	5.2746E-22	ABC转运蛋白 ABC transporter
miR-21-y	XM_002996253.1	-3.6539	1.2369E-118	ABC转运蛋白 ABC transporter
miR-28-y	XM_002996253.1	-3.6539	1.2369E-118	ABC转运蛋白 ABC transporter
miR-30-y	XM_002996675.1	-1.9081	5.2746E-22	ABC转运蛋白 ABC transporter
miR-374-y	XM_002995069.1	-1.7206	2.6275E-25	ABC转运蛋白 ABC transporter
miR-374-y	XM_002996253.1	-3.6539	1.2369E-118	ABC转运蛋白 ABC transporter
miR-590-y	XM_002996675.1	-1.9081	5.2746E-22	ABC转运蛋白 ABC transporter
miR-8212-y	XM_002996253.1	-3.6539	1.2369E-118	ABC转运蛋白 ABC transporter
novel-m0007-5p	XM_002996675.1	-1.9081	5.2746E-22	ABC转运蛋白 ABC transporter
miR-144-x	XM_002996538.1	-3.6489	8.2034E-116	ATP/ADP转位酶 ATP/ADP translocase
miR-454-y	XM_002996538.1	-3.6489	8.2034E-116	ATP/ADP转位酶 ATP/ADP translocase
ame-miR-193	XM_002996794.1	-1.1738	1.1394E-08	糖酵解/糖异生 Glycolysis/gluconeogenesis
miR-100-y	XM_002995703.1	-2.3880	1.2790E-52	糖酵解/糖异生 Glycolysis/gluconeogenesis
miR-144-x	XM_002996794.1	-1.1738	1.1394E-08	糖酵解/糖异生 Glycolysis/gluconeogenesis
miR-16-y	XM_002995703.1	-2.3880	1.2790E-52	糖酵解/糖异生 Glycolysis/gluconeogenesis
miR-193-y	XM_002996794.1	-1.1738	1.1394E-08	糖酵解/糖异生 Glycolysis/gluconeogenesis
miR-221-y	XM_002995703.1	-2.3880	1.2790E-52	糖酵解/糖异生 Glycolysis/gluconeogenesis
miR-222-y	XM_002995703.1	-2.3880	1.2790E-52	糖酵解/糖异生 Glycolysis/gluconeogenesis
miR-767-x	XM_002995703.1	-2.3880	1.2790E-52	糖酵解/糖异生 Glycolysis/gluconeogenesis
miR-8232-x	XM_002995703.1	-2.3880	1.2790E-52	糖酵解/糖异生 Glycolysis/gluconeogenesis
novel-m0007-5p	XM_002995703.1	-2.3880	1.2790E-52	糖酵解/糖异生 Glycolysis/gluconeogenesis
miR-16-y	XM_002996061.1	-5.8896	2.4289E-21	MAPK信号通路 MAPK signaling pathway
miR-29-y	XM_002995842.1	-2.6200	1.1211E-28	MAPK信号通路 MAPK signaling pathway
novel-m0007-5p	XM_002995842.1	-2.6200	1.1211E-28	MAPK信号通路 MAPK signaling pathway

Table 1

Table 2

Fig. 5

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差异表达miRNA ID DEmiRNA ID	差异表达miRNA的log₂FC log₂FC of DEmiRNA	差异表达miRNA的P值 P value of DEmiRNA	AmCK1组中的TPM值 TPM in AmCK1 group	AmT1组中的TPM值 TPM in AmT1 group
ame-miR-6052	11.7271	0.0021	0.0010	3.3900
miR-196-x	2.3757	0.0012	3.2800	17.0233
miR-16-y	2.7925	0.0421	0.5100	3.5333
miR-20-x	1.9111	0.0500	2.2733	8.5500
miR-21-y	2.2041	0.0000	12.6300	58.1967
miR-28-y	1.6298	0.0072	7.7467	23.9733
miR-30-y	2.1421	0.0034	6.3900	28.2067
miR-374-y	4.7301	0.0009	0.2033	5.3967
miR-590-y	3.6286	0.0325	0.1900	2.3500
miR-8212-y	11.4683	0.0036	0.0010	2.8333
novel-m0007-5p	2.9010	0.0223	0.4900	3.6600
miR-144-x	4.2291	0.0307	0.3933	7.3767
miR-454-y	3.5531	0.0306	0.2033	2.3867
ame-miR-193	3.1393	0.0039	0.9167	8.0767
miR-100-y	3.3495	0.0003	1.0367	10.5667
miR-193-y	2.8593	0.0049	0.8833	6.4100
miR-221-y	1.3376	0.0444	9.6667	24.4300
miR-222-y	1.8682	0.0000	100.1467	365.6167
miR-767-x	4.7167	0.0011	0.2033	5.3467
miR-8232-x	3.7159	0.0226	0.1900	2.4967
miR-29-y	1.5049	0.0014	29.6800	84.2333

MicroRNA-Mediated Cross-Kingdom Regulation of Apis mellifera ligustica Worker to Nosema ceranae

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