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

中国农业科学 ›› 2021, Vol. 54 ›› Issue (8): 1805-1820.doi: 10.3864/j.issn.0578-1752.2021.08.019

• 畜牧·兽医·资源昆虫 • 上一篇

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

杜宇¹(),范小雪¹(),蒋海宾¹,王杰¹,冯睿蓉¹,张文德¹,余岢骏¹,隆琦¹,蔡宗兵¹,熊翠玲¹,郑燕珍^1,²,陈大福^1,²,付中民^1,²,徐国钧^1,²,郭睿^1,²()

¹福建农林大学动物科学学院（蜂学学院）,福州 350002
²福建农林大学蜂疗研究所,福州 350002

收稿日期:2020-06-02 接受日期:2020-06-22 出版日期:2021-04-16 发布日期:2021-04-25
通讯作者: 郭睿
作者简介:杜宇,E-mail： m18505700830@163.com。|范小雪,E-mail： imfanxx@163.com。
基金资助:
国家现代农业产业技术体系建设专项(CARS-44-KXJ7);福建农林大学杰出青年科研人才计划(xjq201814);福建农林大学科技创新专项(CXZX2017342,CXZX2017343);福建农林大学优秀硕士学位论文资助基金(杜宇);福建省大学生创新创业训练计划(202010389016);福建省大学生创新创业训练计划(202010389158)

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

DU Yu¹(),FAN XiaoXue¹(),JIANG HaiBin¹,WANG Jie¹,FENG RuiRong¹,ZHANG WenDe¹,YU KeJun¹,LONG Qi¹,CAI ZongBing¹,XIONG CuiLing¹,ZHENG YanZhen^1,²,CHEN DaFu^1,²,FU ZhongMin^1,²,XU GuoJun^1,²,GUO Rui^1,²()

¹College of Animal Sciences (College of Bee Science), Fujian Agriculture and Forestry University, Fuzhou 350002
²Apitherapy Research Institute, Fujian Agriculture and Forestry University, Fuzhou 350002

Received:2020-06-02 Accepted:2020-06-22 Online:2021-04-16 Published:2021-04-25
Contact: Rui GUO

摘要/Abstract

摘要：

【目的】东方蜜蜂微孢子虫（Nosema ceranae）感染意大利蜜蜂（Apis mellifera ligustica,简称意蜂）导致蜜蜂微孢子虫病。本研究结合前期已获得的miRNA和mRNA组学数据,通过生物信息学方法对意蜂工蜂中肠的差异表达miRNA（differentially expressed miRNA,DEmiRNA）靶向结合的东方蜜蜂微孢子虫的mRNA和差异表达mRNA（DEmRNA）进行预测、数据库注释和调控网络分析,以期在组学水平解析miRNA介导意蜂工蜂对东方蜜蜂微孢子虫的跨界调控机制。【方法】通过比较东方蜜蜂微孢子虫侵染7 d和10 d的意蜂工蜂中肠（AmT1、AmT2）和未受侵染的工蜂中肠（AmCK1、AmCK2）的miRNA组学数据筛选出宿主的显著性DEmiRNA,通过比较侵染意蜂工蜂中肠的东方蜜蜂微孢子虫（NcT1、NcT2）和东方蜜蜂微孢子虫纯净孢子（NcCK）的mRNA数据筛选出病原的DEmRNA。利用TargetFinder软件预测宿主显著性DEmiRNA靶向结合的病原mRNA和DEmRNA。利用相关生物信息学工具对上述靶DEmRNA进行GO和KEGG数据库注释。结合前期研究结果筛选出孢壁蛋白、极管蛋白、蓖麻毒素B凝集素、ABC转运蛋白、ATP/ADP移位酶和糖酵解/糖异生途径等毒力因子和能量代谢通路相关的病原DEmRNA及与其存在靶向结合关系的宿主显著性DEmiRNA,并构建和分析二者的调控网络。【结果】AmCK1 vs AmT1比较组中宿主的48条显著上调miRNA和36条显著下调miRNA分别靶向病原的1 345和1 046条mRNA;进一步分析发现,宿主的47条显著上调miRNA和34条显著下调miRNA可分别靶向NcCK vs NcT1比较组中病原的584条显著下调mRNA和265条显著上调mRNA,它们可分别注释到19和22个功能条目以及66和64条通路。AmCK2 vs AmT2比较组中宿主的56条显著上调miRNA和51条显著下调miRNA分别靶向病原的1 260和1 317条mRNA;进一步分析发现,宿主的52条显著上调miRNA和49条显著下调miRNA可分别靶向NcCK vs NcT2比较组中病原的587条显著下调mRNA和336条显著上调mRNA,它们可分别注释到20和23个功能条目以及64和65条通路。AmCK1 vs AmT1和AmCK2 vs AmT2比较组的8条共同显著上调miRNA和1条共同显著下调miRNA分别靶向NcCK vs NcT1和NcCK vs NcT2比较组中的144条共同显著下调和10条共同显著上调mRNA,可分别注释到18和13个功能条目以及38和7条通路。此外,AmCK1 vs AmT1和AmCK2 vs AmT2比较组中宿主的显著上调miRNA可靶向结合NcCK vs NcT1和NcCK vs NcT2比较组中与RNAi途径,孢壁蛋白和蓖麻毒素B凝集素等毒力因子,糖酵解/糖异生途径以及MAPK信号通路相关的病原下调表达mRNA。【结论】在东方蜜蜂微孢子虫的侵染过程中,意蜂工蜂中肠的DEmiRNA与病原的DEmRNA之间存在复杂的靶向结合关系以及潜在的跨界调控关系;宿主的DEmiRNA可能通过抑制或降解病原的RNAi途径、毒力因子、糖酵解/糖异生通路、ATP/ADP移位酶、ABC转运蛋白及MAPK信号通路相关靶DEmRNA影响病原的侵染和增殖。

关键词: 意大利蜜蜂, 东方蜜蜂微孢子虫, 微小RNA, 跨界调控, 调控网络, 免疫防御

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

杜宇,范小雪,蒋海宾,王杰,冯睿蓉,张文德,余岢骏,隆琦,蔡宗兵,熊翠玲,郑燕珍,陈大福,付中民,徐国钧,郭睿. 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[J]. 中国农业科学, 2021, 54(8): 1805-1820.

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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链接本文: https://www.chinaagrisci.com/CN/10.3864/j.issn.0578-1752.2021.08.019

https://www.chinaagrisci.com/CN/Y2021/V54/I8/1805

图/表 7

图1

图2

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图4

表1

AmCK1 vs AmT1中显著上调miRNA靶向NcCK vs NcT1中东方蜜蜂微孢子虫的毒力因子/侵染因子相关下调mRNA的信息概要"

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

表1

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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

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

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

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