Abstract
Currently, knowledge of circular RNAs (circRNAs) in insects including honeybee is extremely limited. Here, differential expression profiles and regulatory networks of circRNAs in the midguts of Apis cerana cerana workers were comprehensively investigated using transcriptome sequencing and bioinformatics. In total, 9589 circRNAs (201–800 nt in length) were identified from 8-day-old and 11-day-old workers’ midguts (Ac1 and Ac2); among them, 5916 (61.70%) A. cerana cerana circRNAs showed conservation with our previously indentified circRNAs in Apis mellifera ligucstica workers’ midguts (Xiong et al., Acta Entomologica Sinica 61:1363–1375, 2018). Five circRNAs were confirmed by RT-PCR and Sanger sequencing. Interestingly, novel_circ_003723, novel_circ_002714, novel_circ_002451, and novel_circ_001980 were highly expressed in both Ac1 and Ac2. In addition, the source genes of circRNAs were involved in 34 GO terms including organelle and cellular process and 141 pathways such as endocytosis and Wnt signaling pathway. Moreover, 55 DEcircRNAs including 34 upregulated and 21 downregulated circRNAs were identified in Ac2 compared with Ac1. circRNA-miRNA regulatory networks indicated that 1060 circRNAs can target 74 miRNAs; additionally, the DEcircRNA-miRNA-mRNA networks suggested that 13 downregulated circRNAs can bind to eight miRNAs and 29 miRNA-targeted mRNAs, while 16 upregulated circRNAs can link to 9 miRNAs and 29 miRNA-targeted mRNAs. These results indicated that DEcircRNAs as ceRNAs may play a comprehensive role in the growth, development, and metabolism of the worker’s midgut via regulating source genes and interacting with miRNAs. Notably, eight DEcircRNAs targeting miR-6001-y were likely to be key participants in the midgut development. Our findings not only offer a valuable resource for further studies on A. cerana cerana circRNA and novel insights into understanding the molecular mechanisms underlying the midgut development of eastern honeybee but also provide putative circRNA candidates for functional research in the near future and novel biomarkers for identification of eastern honeybee species including A. cerana cerana and honeybee diseases such as chalkbrood and microsporidiosis.
Similar content being viewed by others
References
Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121(2):207–221. https://doi.org/10.1016/j.cell.2005.04.004
Aronstein KA, Murray KD (2010) Chalkbrood disease in honey bees. J Invertebr Pathol 103(Suppl 1):S20–S29. https://doi.org/10.1016/j.jip.2009.06.018
Ashwal-Fluss R, Meyer M, Pamudurti NR, Ivanov A, Bartok O, Hanan M, Evantal N, Memczak S, Rajewsky N, Kadener S (2014) CircRNA biogenesis competes with pre-mRNA splicing. Mol Cell 56(1):55–66. https://doi.org/10.1016/j.molcel.2014.08.019
Camargo FD, Gokhale S, Johnnidis JB, Fu D, Bell GW, Jaenisch R, Brummelkamp TR (2007) YAP1 increases organ size and expands undifferentiated progenitor cells. Curr Biol 17(23):2054–2060. https://doi.org/10.1016/j.cub.2007.10.039
Chen DF, Guo R, Xu XJ, Xiong CL, Liang Q, Zheng YZ, Luo Q, Zhang ZN, Huang ZJ, Kumar D, Xi WJ, Zou X, Liu M (2017a) Uncovering the immune responses of Apis mellifera ligustica larval gut to Ascosphaera apis infection utilizing transcriptome sequencing. Gene 621:40–50. https://doi.org/10.1016/j.gene.2017.04.022
Chen J, Li Y, Zheng Q, Bao C, He J, Chen B, Lyu D, Zheng B, Xu Y, Long Z, Zhou Y, Zhu H, Wang Y, He X, Shi Y, Huang S (2017b) Circular RNA profile identifies circPVT1 as a proliferative factor and prognostic marker in gastric cancer. Cancer Lett 388:208–219. https://doi.org/10.1016/j.canlet.2016.12.006
Chen X, Shi W, Chen C (2018) Differential circular RNAs expression in ovary during oviposition in honey bees. Genomics 111(4):598–606. https://doi.org/10.1016/j.ygeno.2018.03.015
Cheng X, Zhang L, Zhang K, Zhang G, Hu Y, Sun X, Zhao C, Li H, Li YM, Zhao J (2018) Circular RNA VMA21 protects against intervertebral disc degeneration through targeting miR-200c and X linked inhibitor-of-apoptosis protein. Ann Rheum Dis 77(5):770–779. https://doi.org/10.1136/annrheumdis-2017-212056
Collins DH, Mohorianu I, Beckers M, Moulton V, Dalmay T, Bourke AF (2017) MicroRNAs associated with caste determination and differentiation in a primitively eusocial insect. Sci Rep 7:45674. https://doi.org/10.1038/srep45674
Cortes-Lopez M, Gruner MR, Cooper DA, Gruner HN, Voda AI, Vand LAM (2018) Global accumulation of circRNAs during aging in Caenorhabditis elegans. BMC Genomics 19(1):8. https://doi.org/10.1186/s12864-017-4386-y
Danan M, Schwartz S, Edelheit S, Sorek R (2012) Transcriptome-wide discovery of circular RNAs in Archaea. Nucleic Acids Res 40(7):3131–3142. https://doi.org/10.1093/nar/gkr1009
Darbani B, Noeparvar S, Borg S (2016) Identification of circular RNAs from the parental genes involved in multiple aspects of cellular metabolism in barley. Front Plant Sci 7:776. https://doi.org/10.3389/fpls.2016.00776
Diao Q, Sun L, Zheng H, Zeng Z, Wang S, Xu S, Zheng H, Chen Y, Shi Y, Wang Y, Meng F, Sang Q, Cao L, Liu F, Zhu Y, Li W, Li Z, Dai C, Yang M, Chen S, Chen R, Zhang S, Evans JD, Huang Q, Liu J, Hu F, Su S, Wu J (2018) Genomic and transcriptomic analysis of the Asian honeybee Apis cerana provides novel insights into honeybee biology. Sci Rep 8(1):822. https://doi.org/10.1038/s41598-017-17338-6
Du J, Yuan Z, Ma Z, Song J, Xie X, Chen Y (2014) KEGG-PATH: Kyoto encyclopedia of genes and genomes-based pathway analysis using a path analysis model. Mol BioSyst 10(9):2441–2447. https://doi.org/10.1039/c4mb00287c
Du WW, Yang W, Liu E, Yang Z, Dhaliwal P, Yang BB (2016) Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2. Nucleic Acids Res 44(6):2846–2858. https://doi.org/10.1093/nar/gkw027
Ellegaard KM, Tamarit D, Javelind E, Olofsson TC, Andersson SG, Vasquez A (2015) Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut. BMC Genomics 16:284. https://doi.org/10.1186/s12864-015-1476-6
Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M, Thompson GJ, Zou Z, Hultmark D (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 15(5):645–656. https://doi.org/10.1111/j.1365-2583.2006.00682.x
Fan X, Zhang X, Wu X, Guo H, Hu Y, Tang F, Huang Y (2015) Single-cell RNA-seq transcriptome analysis of linear and circular RNAs in mouse preimplantation embryos. Genome Biol 16:148. https://doi.org/10.1186/s13059-015-0706-1
Feng Y, Zhang L, Wu J, Khadka B, Fang Z, Gu J, Tang B, Xiao R, Pan G, Liu J (2019) CircRNA circ_0000190 inhibits the progression of multiple myeloma through modulating miR-767-5p/MAPK4 pathway. J Exp Clin Cancer Res 38(1):54. https://doi.org/10.1186/s13046-019-1071-9
Fevr T, Robine S, Louvard D, Huelsken J (2007) Wnt/beta-catenin is essential for intestinal homeostasis and maintenance of intestinal stem cells. Mol Cell Biol 27(21):7551–7559. https://doi.org/10.1128/MCB.01034-07
Gan H, Feng T, Wu Y, Liu C, Xia Q, Cheng T (2017) Identification of circular RNA in the Bombyx mori silk gland. Insect Biochem Mol Biol 89:97–106. https://doi.org/10.1016/j.ibmb.2017.09.003
Gao Y, Wang J, Zhao F (2015) CIRI: an efficient and unbiased algorithm for de novo circular RNA identification. Genome Biol 16:4. https://doi.org/10.1186/s13059-014-0571-3
Griffiths-Jones S (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34(suppl 1):140–144. https://doi.org/10.1093/nar/gkj112
Guo R, Chen DF, Chen HZ, Fu ZM, Xiong CL, Hou CS, Zheng YZ, Guo Y, Wang HP, Du Y, Diao QY (2018a) Systematic investigation of circular RNAs in Ascosphaera apis, a fungal pathogen of honeybee larvae. Gene 678:17–22. https://doi.org/10.1016/j.gene.2018.07.076
Guo R, Chen DF, Chen HZ, Xiong CL, Zheng YZ, Hou CS, Du Y, Geng SH, Wang HP, Zhou DD, Guo YL (2018b) Genome-wide identification of circular RNAs in fungal parasite Nosema ceranae. Curr Microbiol 75(12):1655–1660. https://doi.org/10.1007/s00284-018-1576-z
Guo R, Chen HZ, Xiong CL, Zheng YZ, Fu ZM, Xu GJ, Du Y, Wang HP, Geng SH, Zhou DD, Liu SY, Chen DF (2018c) Analysis of differentially expressed circular RNAs and their regulation networks during the developmental process of Apis mellifera ligustica worker’s midgut. Sci Agric Sin 51(23):4575–4590. https://doi.org/10.3864/j.issn.0578-1752.2018.23.015 (in Chinese)
Halder G, Johnson RL (2011) Hippo signaling: growth control and beyond. Development 138(1):9–22. https://doi.org/10.1242/dev.045500
Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495(7441):384–388. https://doi.org/10.1038/nature11993
He J, Xie Q, Xu H, Li J, Li Y (2017a) Circular RNAs and cancer. Cancer Lett 396:138–144. https://doi.org/10.1016/j.canlet.2017.03.027
He L, Zhang A, Xiong L, Li Y, Huang R, Liao L, Zhu Z, Wang AY (2017b) Deep circular RNA sequencing provides insights into the mechanism underlying grass carp reovirus infection. Int J Mol Sci 18(9):9. https://doi.org/10.3390/ijms18091977
Hedengren-Olcott M, Olcott MC, Mooney DT, Ekengren S, Geller BL, Taylor BJ (2004) Differential activation of the NF-kappaB-like factors Relish and Dif in Drosophila melanogaster by fungi and Gram-positive bacteria. J Biol Chem 279(20):21121–21127. https://doi.org/10.1074/jbc.M313856200
Hora ZA, Altaye SZ, Wubie AJ, Li J (2016) Proteomics improves the new understanding of honeybee biology. J Agric Food Chem 66(14):3605–3615. https://doi.org/10.1021/acs.jafc.8b00772
Hu X, Zhu M, Zhang X, Liu B, Liang Z, Huang L, Xu J, Yu L, Li K, Zar MS, Xue R, Cao G, Gong C (2018a) Identification and characterization of circular RNAs in the silkworm midgut following Bombyx mori cytoplasmic polyhedrosis virus infection. RNA Biol 15(2):292–301. https://doi.org/10.1080/15476286.2017.1411461
Hu X, Zhu M, Liu B, Liang Z, Huang L, Xu J, Yu L, Li K, Jiang M, Xue R, Cao G, Gong C (2018b) Circular RNA alterations in the Bombyx mori midgut following B. mori nucleopolyhedrovirus infection. Mol Immunol 101:461–470. https://doi.org/10.1016/j.molimm.2018.08.008
Huang DW, Sherman BT, Tan Q, Collins JR, Alvord WG, Roayaei J, Stephens R, Baseler MW, Lane HC, Lempicki RA (2007) The DAVID gene functional classification tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol 8(9):R183. https://doi.org/10.1186/gb-2007-8-9-r183
Huang M, Shen Y, Mao H, Chen L, Chen J, Guo X, Xu N (2018) Circular RNA expression profiles in the porcine liver of two distinct phenotype pig breeds. Asian-Australas J Anim Sci 31(6):812–819. https://doi.org/10.5713/ajas.17.0651
Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, Marzluff WF, Sharpless NE (2013) Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19(2):141–157. https://doi.org/10.1261/rna.035667.112
Jung SH (2014) Stratified Fisher's exact test and its sample size calculation. Biom J 56(1):129–140. https://doi.org/10.1002/bimj.201300048
Ke Y, Zhao W, Xiong J (2013) Cao R (2013) miR-149 inhibits non-small-cell lung cancer cells EMT by targeting FOXM1. Biochem Res Int 506731. https://doi.org/10.1155/2013/506731
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14(4):R36. https://doi.org/10.1186/gb-2013-14-4-r36
Kumar S, Molina-Cruz A, Gupta L, Rodrigues J, Barillas-Mury C (2010) A peroxidase/dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science 327(5973):1644–1648. https://doi.org/10.1126/science.1184008
Kwong WK, Moran NA (2015) Evolution of host specialization in gut microbes: the bee gut as a model. Gut Microbes 6(3):214–220. https://doi.org/10.1080/19490976.2015.1047129
Langdon WB (2015) Performance of genetic programming optimised Bowtie2 on genome comparison and analytic testing (GCAT) benchmarks. Biodata Min 8(1):1. https://doi.org/10.1186/s13040-014-0034-0
Lasda E, Parker R (2014) Circular RNAs: diversity of form and function. RNA 20(12):1829–1842. https://doi.org/10.1261/rna.047126.114
Legnini I, Di Timoteo G, Rossi F, Morlando M, Briganti F, Sthandier O, Fatica A, Santini T, Andronache A, Wade M, Laneve P, Rajewsky N, Bozzoni I (2017) Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell 66(1):22–37. https://doi.org/10.1016/j.molcel.2017.02.017
Li HL, Zhang YL, Gao QK, Cheng JA, Lou BG (2008) Molecular identification of cDNA, immunolocalization, and expression of a putative odorant-binding protein from an Asian honey bee, Apis cerana cerana. J Chem Ecol 34(12):1593–1601. https://doi.org/10.1007/s10886-008-9559-3
Li Z, Huang C, Bao C, Chen L, Lin M, Wang X, Zhong G, Yu B, Hu W, Dai L, Zhu P, Chang Z, Wu Q, Zhao Y, Jia Y, Xu P, Liu H, Shan G (2015) Exon-intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol 22(3):256–264. https://doi.org/10.1038/nsmb.2959
Li RC, Ke S, Meng FK, Lu J, Zou XJ, He ZG, Wang WF, Fang MH (2018) CiRS-7 promotes growth and metastasis of esophageal squamous cell carcinoma via regulation of miR-7/HOXB13. Cell Death Dis 9(8):838. https://doi.org/10.1038/s41419-018-0852-y
Li MZ, Xiao HM, He K, Li F (2019) Progress and prospects of noncoding RNAs in insects. J Integr Agric 18(4):729–747. https://doi.org/10.1016/S2095-3119(18)61976-8
Liu C, Teng ZQ, Santistevan NJ, Szulwach KE, Guo W, Jin P, Zhao X (2010) Epigenetic regulation of miR-184 by MBD1 governs neural stem cell proliferation and differentiation. Cell Stem Cell 6(5):433–444. https://doi.org/10.1016/j.stem.2010.02.017
Liu F, Peng W, Li Z, Li W, Li L, Pan J, Zhang S, Miao Y, Chen S, Su S (2012) Next-generation small RNA sequencing for microRNAs profiling in Apis mellifera: comparison between nurses and foragers. Insect Mol Biol 21(3):297–303. https://doi.org/10.1111/j.1365-2583.2012.01135.x
Lu T, Cui L, Zhou Y, Zhu C, Fan D, Gong H, Zhao Q, Zhou C, Zhao Y, Lu D, Luo J, Wang Y, Tian Q, Feng Q, Huang T, Han B (2015) Transcriptome-wide investigation of circular RNAs in rice. RNA 21(12):2076–2087. https://doi.org/10.1261/rna.052282.115
Ma HB, Yao YN, Yu JJ, Chen XX, Li HF (2018) Extensive profiling of circular RNAs and the potential regulatory role of circRNA-000284 in cell proliferation and invasion of cervical cancer via sponging miR-506. Am J Transl Res 10(2):592–604
Macedo LM, Nunes FM, Freitas FC, Pires CV, Tanaka ED, Martins JR, Piulachs MD, Cristino AS, Pinheiro DG, Simões ZL (2016) MicroRNA signatures characterizing caste-independent ovarian activity in queen and worker honeybees (Apis mellifera L.). Insect Mol Biol 25(3):216–226. https://doi.org/10.1111/imb.12214
McBride WH, Iwamoto KS, Syljuasen R, Pervan M, Pajonk F (2003) The role of the ubiquitin/proteasome system in cellular responses to radiation. Oncogene 22(37):5755–5773. https://doi.org/10.1038/sj.onc.1206676
Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, le Noble F, Rajewsky N (2013) Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495(7441):333–338. https://doi.org/10.1038/nature11928
Nishiura JT, Burgos C, Aya S, Goryacheva Y, Lo W (2007) Modulation of larval nutrition affects midgut neutral lipid storage and temporal pattern of transcription factor expression during mosquito metamorphosis. J Insect Physiol 53(1):47–58. https://doi.org/10.1016/j.jinsphys.2006.09.014
Otto C, Stadler PF, Hoffmann S (2014) Lacking alignments? The next-generation sequencing mapper segemehl revisited. Bioinformatics 30(13):1837–1843. https://doi.org/10.1093/bioinformatics/btu146
Park D, Jung JW, Choi BS, Jayakodi M, Lee J, Lim J, Yu Y, Choi YS, Lee ML, Park Y, Choi IY, Yang TJ, Edwards OR, Nah G, Kwon HW (2015) Uncovering the novel characteristics of Asian honey bee, Apis cerana, by whole genome sequencing. BMC Genomics 16:1. https://doi.org/10.1186/1471-2164-16-1
Perkel JM (2013) Assume nothing: the tale of circular RNA. Biotechniques 55(2):55–57. https://doi.org/10.2144/000114061
Qu S, Yang X, Li X, Wang J, Gao Y, Shang R, Sun W, Dou K, Li H (2015) Circular RNA: a new star of noncoding RNAs. Cancer Lett 365(2):141–148. https://doi.org/10.1016/j.canlet.2015.06.003
Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP (2011) A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146(3):353–358. https://doi.org/10.1016/j.cell.2011.07.014
Salzman J, Chen RE, Olsen MN, Wang PL, Brown PO (2013) Cell-type specific features of circular RNA expression. PLoS Genet 9(9):e1003777. https://doi.org/10.1371/journal.pgen.1003777
Saraav I, Singh S, Sharma S (2014) Outcome of Mycobacterium tuberculosis and Toll-like receptor interaction: immune response or immune evasion? Immunol Cell Biol 92(9):741–746. https://doi.org/10.1038/icb.2014.52
Shen Y, Guo X, Wang W (2017) Identification and characterization of circular RNAs in zebrafish. FEBS Lett 591(1):213–220. https://doi.org/10.1002/1873-3468.12500
Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27(3):431–432. https://doi.org/10.1093/bioinformatics/btq675
Stanley D, Miller J, Tunaz H (2009) Eicosanoid actions in insect immunity. J Innate Immun 1(4):282–290. https://doi.org/10.1159/000210371
Sun X, Wang L, Ding J, Wang Y, Wang J, Zhang X, Ye J, Wang J, Sablok G, Deng Z, Zhao H (2016) Integrative analysis of Arabidopsis thaliana transcriptomics reveals intuitive splicing mechanism for circular RNA. FEBS Lett 590(20):3510–3516. https://doi.org/10.1002/1873-3468.12440
Tan K, Dong S, Li X, Liu X, Wang C, Li J, Nieh JC (2016) Honey bee inhibitory signaling is tuned to threat severity and can act as a colony alarm signal. PLoS Biol 14(3):e1002423. https://doi.org/10.1371/journal.pbio.1002423
Tang H, Huang X, Wang J, Yang L, Kong Y, Gao G, Zhang L, Chen ZS, Xie X (2019) circKIF4A acts as a prognostic factor and mediator to regulate the progression of triple-negative breast cancer. Mol Cancer 18(1):23. https://doi.org/10.1186/s12943-019-0946-x
Teleman AA, Maitra S, Cohen SM (2006) Drosophila lacking microRNA miR-278 are defective in energy homeostasis. Genes Dev 20(4):417–422. https://doi.org/10.1101/gad.374406
Tholken C, Thamm M, Erbacher C, Lechner M (2019) Sequence and structural properties of circular RNAs in the brain of nurse and forager honeybees (Apis mellifera). BMC Genomics 20(1):88. https://doi.org/10.1186/s12864-018-5402-6
Toptan T, Abere B, Nalesnik MA, Swerdlow SH, Ranganathan S, Lee N, Shair KH, Moore PS, Chang Y (2018) Circular DNA tumor viruses make circular RNAs. Proc Natl Acad Sci U S A 115:e8737–e8745. https://doi.org/10.1073/pnas.1811728115
Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26(1):136–138. https://doi.org/10.1093/bioinformatics/btp612
Westholm JO, Miura P, Olson S, Shenker S, Joseph B, Sanfilippo P, Celniker SE, Graveley BR, Lai EC (2014) Genome-wide analysis of drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Rep 9(5):1966–1980. https://doi.org/10.1016/j.celrep.2014.10.062
Xiong CL, Chen HZ, Chen DF, Zheng YZ, Fu ZM, Xu GJ, Du Y, Wang HP, Geng SH, Zhou DD, Liu SY, Guo R (2018) Analysis of circular RNAs and their regulatory networks in the midguts of Apis mellifera ligustica workers. Acta Entomol Sin 61(12):1363–1375. https://doi.org/10.16380/j.kcxb.2018.12.001 (in Chinese)
Yang Y, Fan X, Mao M, Song X, Wu P, Zhang Y, Jin Y, Yang Y, Chen LL, Wang Y, Wong CC, Xiao X, Wang Z (2017) Extensive translation of circular RNAs driven by N(6)-methyladenosine. Cell Res 27(5):626–641. https://doi.org/10.1038/cr.2017.31
Yang L, Han B, Zhang Y, Bai Y, Chao J, Hu G, Yao H (2018) Engagement of circular RNA HECW2 in the nonautophagic role of ATG5 implicated in the endothelial-mesenchymal transition. Autophagy 14(3):404–418. https://doi.org/10.1080/15548627.2017.1414755
Yu X, Zhou Q, Li SC, Luo Q, Cai Y, Lin WC, Chen H, Yang Y, Hu S, Yu J (2008) The silkworm (Bombyx mori) microRNAs and their expressions in multiple developmental stages. PLoS One 3(8):e2997. https://doi.org/10.1371/journal.pone.0002997
Zhang C, Wu H, Wang Y, Zhu S, Liu J, Fang X, Chen H (2016) Circular RNA of cattle casein genes are highly expressed in bovine mammary gland. J Dairy Sci 99(6):4750–4760. https://doi.org/10.3168/jds.2015-10381
Zhang XH, Yan YM, Lei XY, Li AJ, Zhang HM, Dai ZK, Li X, Chen W, Lin W, Chen F, Ma J, Xie Q (2017) Circular RNA alterations are involved in resistance to avian leukosis virus subgroup-J-induced tumor formation in chickens. Oncotarget 8(21):34961–34970. https://doi.org/10.18632/oncotarget.16442
Zhao Z, Li X, Gao C, Jian D, Hao P, Rao L, Li M (2017) Peripheral blood circular RNA hsa_circ_0124644 can be used as a diagnostic biomarker of coronary artery disease. Sci Rep 7:39918. https://doi.org/10.1038/srep39918
Zhu Q, Lu G, Luo Z, Gui F, Wu J, Zhang D, Ni Y (2018) CircRNA circ_0067934 promotes tumor growth and metastasis in hepatocellular carcinoma through regulation of miR-1324/FZD5/Wnt/beta-catenin axis. Biochem Biophys Res Commun 497(2):626–632. https://doi.org/10.1016/j.bbrc.2018.02.119
Acknowledgments
We thank the editor and the anonymous reviewers for their valuable comments which helped us to improve our manuscript. We also thank Xiaoxue Fan (College of Animal Sciences (College of Bee Sciences), Fujian Agriculture and Forestry University, China) and Yuanchan Fan (College of Animal Sciences (College of Bee Science, Fujian), Agriculture and Forestry University, China) for their constructive contribution to the discussion during the revision process.
Funding
This work was founded by the National Natural Science Foundation of China (31702190) to RG, the Earmarked Fund for Modern Agro-industry Technology Research System (CARS-44-KXJ7) to DFC, the Science and Technology Planning Project of Fujian Province (2018J05042) to RG, the Education and Scientific Research Program Fujian Ministry of Education for Young Teachers (JAT170158) to RG, the Outstanding Scientific Research Manpower Fund of Fujian Agriculture and Forestry University (xjq201814) to RG, and the Science and Technology Innovation Fund of Fujian Agriculture and Forestry University (CXZX2017342, CXZX2017343) to RG and DFC.
Author information
Authors and Affiliations
Contributions
RG designed this study. DFC, HZC, YD, SHG, CLX, YZZ, and CSH carried out laboratory work. RG, DFC, QYD, and HZC performed bioinformatic analyses. RG, DFC, and HZC supervised the work and contributed to preparation of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Chen, D., Chen, H., Du, Y. et al. Systematic identification of circular RNAs and corresponding regulatory networks unveil their potential roles in the midguts of eastern honeybee workers. Appl Microbiol Biotechnol 104, 257–276 (2020). https://doi.org/10.1007/s00253-019-10159-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-019-10159-9