Scientia Agricultura Sinica ›› 2020, Vol. 53 ›› Issue (12): 2512-2526.doi: 10.3864/j.issn.0578-1752.2020.12.017

• ANIMAL SCIENCE·VETERINARY SCIENCE·RESOURCE INSECT • Previous Articles    

The Potential Role of MicroRNAs and MicroRNA-Mediated Competing Endogenous Networks During the Developmental Process of Apis mellifera ligustica Worker’s Midgut

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   

  1. College of Animal Sciences (College of Bee Science), Fujian Agriculture and Forestry University, Fuzhou 350002
  • Received:2019-10-27 Online:2020-06-16 Published:2020-06-25

Abstract:

【Objective】 MicroRNA (miRNA) can lead to the inhibition or degradation of mRNA via target binding, thus performing negative regulation of gene expression. MiRNAs play a key role in regulating the growth, development, immunity and cellular activity of insects. This study aims to deeply investigate differentially expressed miRNAs (DEmiRNAs) and their regulatory networks, and to systematically parse differential expression pattern and competing endogenous RNA (ceRNA) mediated mechanism underlying the development of Apis mellifera ligustica worker’s midgut. 【Method】 Midguts of A. m. ligustica 7- and 10-day-old workers were sequenced using small RNA-seq technology. After quality control, the sequencing data were mapped to the genome of A. mellifera, followed by identification of known miRNAs via mapping the mapped tags to miRBase database. Expression levels of miRNAs were calculated and normalized using tags per million (TPM) algorithm. Significant DEmiRNAs were screened out following the criteria of |log2fold change|≥1 and P≤0.05. Prediction, GO database annotation and KEGG database annotation of target mRNAs were conducted using related software. Based on the target binding relationship and previous findings, DElncRNA/DEcircRNA-DEmiRNA-DEmRNA networks associated with 9 signaling pathways (AMPK, PI3K-Akt, Wnt, cAMP, Hippo, mTOR, Toll/Imd, TGF-beta and MAPK signaling pathways) were visualized using Cytoscape software. CeRNA regulatory network of miR-342-y was further constructed followed by KEGG pathway annotation of target mRNAs involved in the network. Stem-loop RT-qPCR was used to verify the reliability of our sequencing data and differential expression of miRNAs. 【Result】 A total of 112 significant DEmiRNAs were identified in Am7 vs Am10 comparison group, including 38 up-regulated miRNAs and 74 down-regulated miRNAs, which could respectively target 7 434 and 9 559 mRNAs. These target mRNAs could be annotated to 21 and 23 functional terms associated with biological process, 16 and 17 terms associated with cellular component, and 10 and 11 terms associated with molecular function. Additionally, the targets could be annotated to 83 and 86 pathways related to material metabolisms such as fructose and mannose metabolism, purine metabolism, glycine, serine and threonine metabolism; 10 and 10 pathways related to cellular immune such as endocytosis, ubiquitin mediated proteolysis and melanogenesis; 5 and 5 pathways related to humoral immune such as MAPK, Jak-STAT and NF-κB; 13 and 11 signaling pathways related to development such as Hippo, FoxO and Notch. Furthermore, ceRNA regulatory networks of aforementioned 9 signaling pathways were constructed and analyzed, the result showed the existence of complex relationship among DEmiRNAs, DElncRNAs, DEcircRNAs and DEmRNAs; DEmiRNAs were located in the center, while DElncRNAs, DEcircRNAs and DEmRNAs were around the network. Further investigation suggested that miR-342-y was significantly down-regulated in the developmental processes of both worker’s midgut and larval gut of A. m. ligustica; this miRNA could target 3 DEcircRNAs, 4 DElncRNAs and 327 mRNAs. Stem-loop RT-qPCR result indicated that the differential expression trend of 4 DEmiRNAs was in accordance of that in sequencing result, confirming the authenticity of the sequencing data and differential expression pattern of miRNAs. 【Conclusion】 DEmiRNAs are likely to affect the growth and development of A. m. ligustica worker’s midgut by participating in regulation of the expression of genes engaged in material and energy metabolism-associated pathways, signaling pathways such as Hippo and Wnt as well as cellular and humoral immune pathways; ceRNA regulatory networks mediated by several key DEmiRNAs including miR-182-x, miR-291-y, miR-342-y and ame-miR-6001-3p are likely to play pivotal regulatory parts during the developmental process of the midgut of A. m. ligustica.

Key words: Apis mellifera ligustica, midgut, microRNA (miRNA), long non-coding RNA (lncRNA), circular RNA (circRNA), competing endogenous RNA (ceRNA), developmental mechanism

Table 1

Information of primers for RT-qPCR"

引物名称Primer name 引物序列Primer sequence (5′-3′)
Loop-miR-210-z CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGACAGCCGC
F-miR-210-z ACACTCCAGCTGGGCTGTGCGTGTGACA
Loop-miR-342-y CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGACGGGTGC
F-miR-342-y ACACTCCAGCTGGGTCTCACACAGAAATC
Loop-miR-7975-y CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGTGGTGCCG
F-miR-7975-y ACACTCCAGCTGGGATCCTGGTCA
Loop-miR-155-x CTCAACTGGTGTCGTGGAGTCGGCAATTCAGTTGAGAACCCCTA
F-miR-155-x ACACTCCAGCTGGGTTAATGCTAATTGTGA
R CTCAACTGGTGTCGTGGA
U6-F GTTAGGCTTTGACGATTTCG
U6-R GGCATTTCTCCACCAGGTA

Table 2

Overview of sRNA-seq datasets"

样品
Sample
原始读段
Raw reads
有效读段
Clean reads
Am7-1 14021728 13619226 (97.13%)
Am7-2 13479635 13081146 (97.04%)
Am7-3 13033478 12656635 (97.11%)
Am10-1 13083648 12577875 (96.13%)
Am10-2 13544596 13137501 (96.99%)
Am10-3 13716280 13316876 (97.09%)

Fig. 1

Pearson correlation coefficients among different biological replicas within each A. m. ligustica worker’s midgut sample group"

Table 3

Top 10 significantly up-regulated miRNAs during the developmental process of A. m. ligustica worker’s midgut"

差异表达miRNA ID
DEmiRNA ID
以2为底miRNA的相对变化倍数的对数值
log2fold change
P
P value
miR-7132-y 13.27 8.68E-09
miR-2188-x 12.72 2.31E-06
miR-1388-x 12.43 6.78E-06
miR-1338-x 12.38 7.39E-06
miR-1388-y 11.76 4.20E-04
miR-1338-y 11.67 9.18E-04
miR-7132-x 11.16 9.01E-03
miR-3964-y 11.09 3.37E-03
miR-7935-y 11.01 4.31E-03
miR-6537-x 10.46 0.023

Table 4

Top 10 significantly down-regulated miRNAs during the developmental process of A. m. ligustica worker’s midgut"

差异表达miRNA ID
DEmiRNA ID
以2为底miRNA的相对变化倍数的对数值
log2fold change
P
P value
miR-8503-x -14.09 3.09E-04
miR-298-x -13.64 2.65E-08
miR-291-y -12.94 8.67E-05
miR-292-y -12.75 3.40E-04
miR-4700-x -12.55 0.015
miR-293-y -12.27 6.77E-04
miR-2965-y -12.13 0.030
miR-2518-y -12.13 6.13E-03
miR-300-y -12.03 2.96E-04
miR-4577-y -12.01 0.038

Fig. 2

GO database annotation of DEmiRNA target mRNAs involved in the developmental process of A. m. ligustica worker’s midgut"

Table 5

Top 15 pathways significantly enriched by target mRNAs of significantly up-regulated miRNAs in the midgut of A. m. ligustica worker"

通路
Pathway
通路ID
Pathway ID
靶mRNA富集数
Number of target mRNAs
P
P value
钙信号通道 Calcium signaling pathway ko04020 77 1.30E-14
催产素信号通路 Oxytocin signaling pathway ko04921 82 1.07E-14
坏死性凋亡 Necroptosis ko04217 58 5.72E-16
嗅觉传导 Olfactory transduction ko04740 50 3.01E-17
长时程增强 Long-term potentiation ko04720 70 3.98E-18
Hippo信号通路 Hippo signaling pathway ko04390 118 1.29E-18
促性腺激素释放激素信号通路 GnRH signaling pathway ko04912 79 4.76E-19
神经营养因子信号通路 Neurotrophin signaling pathway ko04722 89 3.17E-21
胆碱能突触 Cholinergic synapse ko04725 79 2.90E-21
胃酸分泌 Gastric acid secretion ko04971 69 2.05E-21
醛固酮合成与分泌 Aldosterone synthesis and secretion ko04925 74 1.94E-21
cAMP信号通路 cAMP signaling pathway ko04024 113 1.73E-21
昼夜节律调节 Circadian entrainment ko04713 75 2.93E-23
胰岛素分泌 Insulin secretion ko04911 78 2.53E-23
ErbB信号通路 ErbB signaling pathway ko04012 80 2.43E-25

Table 6

Top 15 pathways significantly enriched by target mRNAs of significantly down-regulated miRNAs in the midgut of A. m. ligustica worker"

通路
Pathway
通路ID
Pathway ID
靶mRNA富集数
Number of target mRNAs
P
P value
Hippo信号通路 Hippo signaling pathway ko04390 134 6.20E-17
醛固酮合成与分泌 Aldosterone synthesis and secretion ko04925 78 1.79E-17
胆碱能突触 Cholinergic synapse ko04725 84 1.71E-17
卵母细胞减数分裂 Oocyte meiosis ko04114 103 8.04E-19
昼夜节律调节 Circadian entrainment ko04713 79 3.12E-19
胃酸分泌 Gastric acid secretion ko04971 75 1.66E-19
神经营养因子信号通路 Neurotrophin signaling pathway ko04722 99 1.20E-19
胰岛素分泌 Insulin secretion ko04911 83 9.94E-20
促性腺激素释放激素信号通路 GnRH signaling pathway ko04912 91 9.12E-20
长时程增强 Long-term potentiation ko04720 82 4.72E-20
钙信号通道 Calcium signaling pathway ko04020 101 3.09E-22
ErbB信号通路 ErbB signaling pathway ko04012 87 3.11E-23
cAMP信号通路 cAMP signaling pathway ko04024 134 1.19E-23
炎症介质对TRP通道的调节Inflammatory mediator regulation of TRP channels ko04750 97 9.4E-26
黑色素生成 Melanogenesis ko04916 117 9.23E-28

Fig. 3

Relationship network of DElncRNA/DEcircRNA-DEmiRNA-DEmRNA associated with 9 signaling pathways in the midgut of A. m. ligustica worker"

Fig. 4

Relationship network of miR-342-y and its target DElncRNAs, target DEcircRNAs, target DEmRNAs associated with 10 signaling pathways in the midgut of A. m. ligustica worker"

Fig. 5

RT-qPCR validation of DEmiRNAs"

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