Skip to main content
SpringerLink
Log in

Integrated analysis of differentially expressed microRNAs and mRNAs to screen miRNAs and genes related to reproduction in Macrobrachium nipponense

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

Female Macrobrachium nipponense has the characteristic of short sexual maturity during the breeding season, which can increase breeding risk and lead to prevalent female individual miniaturization. In this study, we characterized micro (mi)RNA-seq data of the eyestalk (E) and cerebral ganglia (B) of female M. nipponense during breeding and non-breeding seasons. A total of 393 and 189 differentially expressed miRNAs (DE miRNAs) were identified in BSE vs. NBSE and BSB vs. NBSB, respectively. The most abundant up- and down-regulated DE miRNAs were miR-124, miR-14, and miR-7. Enrichment analysis showed that DE miRNA target genes were mainly involved in ‘metabolic process’ and ‘binding’, and were associated with ‘neurohormonal regulation’ and ‘photoreceptor activity’ signaling pathways. Integrated analysis of miRNA–mRNA expression showed that the most abundant DE miRNAs were miR-14 and miR-278 in BSE vs. NBSE and BSB vs. NBSB, respectively. Four pairs of DE miRNAs and their corresponding target annotated genes were selected from the DE miRNA–mRNA interaction network (bmo-miR-316-5p/opsin protein, ame-miR-125/skeletal muscle actin 8, dmo-miR-278/sugar transporter, and tca-miR-3885-5p/5-HT1 receptor). Gene expression analysis of these four pairs in different ovary development stages showed their potential regulatory roles in ovary maturation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Artigas GQ, Lapébie P, Leclère L, Takeda N, Deguchi R, Jékely G, Momose T, Houliston E (2018) A gonad-expressed opsin mediates light-induced spawning in the jellyfish Clytia. eLife 7:e29555

    Article  Google Scholar 

  • Baldwin SA, Henderson PJF (1989) Homologies between sugar transporters from eukaryotes and prokaryotes. Annu Rev Physiol 51:459–471

    Article  CAS  Google Scholar 

  • Bao CC, Yang YN, Huang HY, Ye HH (2015) Neuropeptides in the cerebral ganglia of the mud crab, Scylla paramamosain: transcriptomic analysis and expression profiles during vitellogenesis. Sci Rep 5:17055

    Article  CAS  Google Scholar 

  • Bolger AM, Lohse M, Usade IB (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  Google Scholar 

  • Brown MR, Sieglaf DH, Rees HH (2009) Gonadal ecdysteroidogenesis in Arthropoda: occurrence and regulation. Annu Rev Entomol 54:105–125

    Article  CAS  Google Scholar 

  • Bureau of Fishery (2017) Ministry of Agriculture, P.R.C. fisheries economic statistics. In: China fishery yearbook. China Agricultural Press, Beijing

    Google Scholar 

  • Bushati N, Cohen SM (2002) MicroRNA functions. Annu Rev Cell Dev Biol 2007(23):175–205

    Google Scholar 

  • Cai Y, Ng PKL (2002) The freshwater palaemonid prawns of Myanmar (Crustacea: Decapoda: Caridea). Hydrobiologia 487:59–83

    Article  Google Scholar 

  • Cai YM, Yu XM, Zhou Q, Yu CX, Hu HY, Liu JC, Lin HB, Yang J, Zhang B, Cui P (2010) Novel microRNAs in silkworm (Bombyx mori). Funct Integr Genom 10(405–415):1

    Google Scholar 

  • Caygill EE, Johnston LA (2008) Temporal regulation of metamorphic processes in Drosophila by the let-7 and miR-125 heterochronic microRNAs. Curr Biol 18:943–950

    Article  CAS  Google Scholar 

  • Coolen M, Katz S, Bally-Cuif L (2013) miR-9: a versatile regulator of neurogenesis. Front Cell Neurosci 7:220

    Article  Google Scholar 

  • Crawford K, Flick R, Close L, Shelly D, Paul R, Bove K, Kumar A, Lessard J (2002) Mice lacking skeletal muscle actin show reduced muscle strength and growth deficits and die during the neonatal period. Mol Cell Biol 22:5887–5896

    Article  CAS  Google Scholar 

  • Du JH, Niu XM, Wang Y, Kong LB, Wang RQ, Zhang YG, Zhao SX, Nan YM (2015) MiR-146a-5p suppresses activation and proliferation of hepatic stellate cells in nonalcoholic fibrosing steatohepatitis through directly targeting Wnt1 and Wnt5a. Sci Rep 5:16163

    Article  CAS  Google Scholar 

  • Friedländer MR, Mackowiak SD, Li N, Chen W, Rajewsky N (2012) miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res 40:37–52

    Article  Google Scholar 

  • Fu HT, Jiang SF, Xiong YW (2012) Current status and prospects of farming the giant river prawn (Macrobrachium rosenbergii) and the oriental river prawn (Macrobrachium nipponense) in China. Aquac Res 43:993–998

    Article  Google Scholar 

  • García-Fernández JM, Cernuda-Cernuda R, Davies WI, Rodgers J, Turton M, Peirson SN, Follett BK, Halforde S, Hughes S, Hankins MW, Foster RG (2015) The hypothalamic photoreceptors regulating seasonal reproduction in birds: a prime role for VA opsin. Front Neuroendocrinol 37:13–28

    Article  Google Scholar 

  • Ge LQ, Jiang YP, Xia T, Song QS, Stanley D, Kuai P, Lu XL, Yang GQ, Wu JC (2015) Silencing a sugar transporter gene reduces growth and fecundity in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Sci Rep 5:12194

    Article  CAS  Google Scholar 

  • He YD, Ju CY, Zhang XB (2015) Roles of small RNAs in the immune defense mechanisms of crustaceans. Mol Immunol 68:399–403

    Article  CAS  Google Scholar 

  • Ikeda KT, Hirose Y, Hiraoka K, Noro E, Fujishima K, Tomita M, Kanai A (2014) Identification, expression, and molecular evolution of microRNAs in the “living fossil” Triops cancriformis (tadpole shrimp). RNA 114:1–13

    Google Scholar 

  • Jiang HX, Li XL, Sun YH, Hou FJ, Zhang YF, Li F, Gu ZM, Liu XL (2016) Insights into sexual precocity of female oriental river prawn Macrobrachium nipponense through transcriptome analysis. PLoS One 11(6):e0157173

    Article  Google Scholar 

  • Jin SB, Fu HT, Zhou Q, Sun SM, Jiang SF, Xiong YW, Gong YS, Qiao H, Zhang WY (2013) Transcriptome analysis of androgenic gland for discovery of novel genes from the oriental river prawn, Macrobrachium nipponense, using Illumina Hiseq 2000. PLoS One 8:e76840

    Article  CAS  Google Scholar 

  • Jin SB, Fu HT, Jiang SF, Xiong YW, Qiao H, Zhang WY, Gong YS, Wu Y (2015) Identification of androgenic gland microRNA and their target genes to discover sex-related microRNA in the oriental river prawn, Macrobrachium nipponense. Genet Mol Res 14:18396–18406

    Article  CAS  Google Scholar 

  • Kenny NJ, Quah S, Holland PW, Tobe SS, Hui JH (2013) How are comparative genomics and the study of microRNAs changing our views on arthropod endocrinology and adaptations to the environment? Gen Comp Endocrinol 188:16–22

    Article  CAS  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  Google Scholar 

  • Li SK, Zhu S, Li CB, Zhang Z, Zhou LZ, Wang SJ, Wang SQ, Zhang YL, Wen XB (2013) Characterization of microRNAs in Mud Crab Scylla paramamosain under Vibrio parahaemolyticus Infection. PLoS One 8:e73392

    Article  CAS  Google Scholar 

  • Li F, Qiao H, Fu HT, Sun SM, Zhang WY, Jin SB, Jiang SF, Gong YS, Xiong YW, Wu Y (2018) Identification and characterization of opsin gene and its role in ovarian maturation in the oriental river prawn Macrobrachium nipponense. Comp Biochem Phys B 218:1–12

    Article  CAS  Google Scholar 

  • Liu W, Lin SK, Sun WJ, Liu T, Li YH, Zhong GH, Zhao DS, Zhang PS, Song JP, Jin XY (2015) Circulating microRNAs correlated with the level of coronary artery calcification in symptomatic patients. Sci Rep 5:16099

    Article  Google Scholar 

  • Lucas K, Raikhel AS (2013) Insect microRNAs: biogenesis, expression profiling and biological functions. Insect Biochem Mol 43:24–38

    Article  CAS  Google Scholar 

  • Marco A, Hooks K, Griffiths-Jones S (2012) Evolution and function of the extended miR-2 microRNA family. RNA Biol 9:242–248

    Article  CAS  Google Scholar 

  • Matsuda H, Takenouchi T, Yamakawa T (2002) Effects of photoperiod and temperature on ovarian development and spawning of the Japanese spiny lobster Panulirus japonicus. Aquaculture 205:385–398

    Article  Google Scholar 

  • Nagaraju GPC (2010) Reproductive regulators in decapod crustaceans: an overview. J Exp Biol 214:3–16

    Article  Google Scholar 

  • Nakane Y, Ikegami K, Ono H, Yamamoto N, Yoshida S, Hirunagi K, Shizufumi Ebihara S, Kubo Y, Yoshimura T (2010) A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds. Proc Natl Acad Sci 107:15264–15268

    Article  CAS  Google Scholar 

  • Ongvarrasopone C, Roshorm Y, Somyong S, Pothiratana C, Petchdee S, Tangkhabuanbutra J, Sophasan S, Panyim S (2006) Molecular cloning and functional expression of the Penaeus monodon 5-HT receptor. BBA Gene Struct Exp 1759:328–339

    Article  CAS  Google Scholar 

  • Ou JT, Li Y, Ding ZF, Xiu YZ, Wu T, Du J, Li WZ, Zhu HX, Ren Q, Gu W, Wang W (2013) Transcriptome-wide identification and characterization of the Procambarus clarkii microRNAs potentially related to immunity against Spiroplasma eriocheiris infection. Fish Shellfish Immunol 35:607–617

    Article  CAS  Google Scholar 

  • Qiao H, Fu HT, Jin SB, Wu Y, Jiang SF, Gong YS, Xiong YW (2012) Constructing and random sequencing analysis of normalized cDNA library of testis tissue from oriental river prawn (Macrobrachium nipponense). Comp Biochem Phys D 7:268–276

    CAS  Google Scholar 

  • Qiao H, Xiong YW, Zhang WY, Fu HT, Jiang SF, Sun SM, Bai HK, Jin SB, Gong YS (2015) Characterization, expression, and function analysis of gonad-inhibiting hormone in oriental river prawn, Macrobrachium nipponense and its induced expression by temperature. Comp Biochem Phys A 185:1–8

    Article  CAS  Google Scholar 

  • Qiao H, Fu HT, Xiong YW, Jiang SF, Zhang WY, Sun SM, Jin SB, Gong YS, Wang YB, Shan DY, Wu Y (2017) Molecular insights into reproduction regulation of female oriental river prawns Macrobrachium nipponense through comparative transcriptomic analysis. Sci Rep 7:12161

    Article  Google Scholar 

  • Quackenbush SL (1994) Lobster reproduction: a review. Crustaceana 67:82–94

    Article  Google Scholar 

  • Real FM, Sekido R, Lupiáñez DG, Lovell-Badge R, Jiménez R, Burgos M (2013) A microRNA (mmu-miR-124) prevents Sox9 expression in developing mouse ovarian cells. Biol Reprod 89:78–81

    Article  Google Scholar 

  • Rubio M, Belles X (2013) Subtle roles of microRNAs let-7, miR-100 and miR-125 on wing morphogenesis in hemimetabolan metamorphosis. J Insect Physiol 59:1089–1094

    Article  CAS  Google Scholar 

  • Rüdiger W, López-Figueroa F (1992) Photoreceptors in algae. Annu Rev Photochem Photobiol 55:949–954

    Article  Google Scholar 

  • Song YN, Shi LL, Liu ZQ, Qiu GF (2014) Global analysis of the ovarian microRNA transcriptome: implication for miR-2 and miR-133 regulation of oocyte meiosis in the Chinese mitten crab, Eriocheir sinensis (Crustacea: Decapoda). BMC Genom 15:547

    Article  Google Scholar 

  • Stefani G, Slack FJ (2008) Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 9:219–230

    Article  CAS  Google Scholar 

  • Sun SM, Fu HT, Ge XP, Zhu J, Gu ZM, Xuan FJ (2016) Identification and comparative analysis of the oriental river prawn (Macrobrachium nipponense) microRNA expression profile during hypoxia using a deep sequencing approach. Comp Biochem Phys D 17:41–47

    CAS  Google Scholar 

  • Suwansa-ard S, Thongbuakaew T, Wang T, Zhao M, Elizur A, Hanna PJ, Prapee Sretarugsa P, Cummins SF, Sobhon P (2015) In silico neuropeptidome of female Macrobrachium rosenbergii based on transcriptome and peptide mining of eyestalk, central nervous system and ovary. PLoS One 10:e0123848

    Article  Google Scholar 

  • Tan TT, Chen M, Harikrishna JA, Khairuddin N, Shamsudin MIM, Zhang G, Bhassu S (2013) Deep parallel sequencing reveals conserved and novel miRNAs in gill and hepatopancreas of giant fresh water prawn. Fish Shellfish Immunol 35:1061–1069

    Article  CAS  Google Scholar 

  • Tehler D, Høyland-Kroghsbo NM, Lund AH (2011) The miR-10 microRNA precursor family. RNA Biol 8:728–734

    Article  CAS  Google Scholar 

  • Tomy S, Saikrithi P, James N, Balasubramanian CP, Panigrahim A, Otta SK, Subramoniam T, Ponniah AG (2016) Serotonin induced changes in the expression of ovarian gene network in the Indian white shrimp, Penaeus indicus. Aquaculture 452:239–246

    Article  CAS  Google Scholar 

  • Varghese J, Lim SF, Cohen SM (2001) Drosophila miR-14 regulates insulin production and metabolism through its target, sugarbabe. Genes Dev 24:2748–2753

    Article  Google Scholar 

  • Varkonyi-Gasic E, Wu R, Wood M, Walton EF, Hellens RP (2007) Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3:12

    Article  Google Scholar 

  • Veenstra JA (2015) The power of next-generation sequencing as illustrated by the neuropeptidome of the crayfish Procambarus clarkii. Gen Comp Endocrinol 224:84–95

    Article  CAS  Google Scholar 

  • Xu ZQ, Zhao MZ, Li XG, Lu QP, Li YH, Ge JC, Pan JL (2015) Transcriptome profiling of the eyestalk of precocious juvenile Chinese mitten crab reveals putative neuropeptides and differentially expressed genes. Gene 569:280–286

    Article  CAS  Google Scholar 

  • Yoshimura T (2013) Thyroid hormone and seasonal regulation of reproduction. Front Neuroendocrinol 34:157–166

    Article  CAS  Google Scholar 

  • Yu JY, Reynolds SH, Hatfield SD, Shcherbata HR, Fischer KA, Ward EJ, Ruohola-Baker H (2009) Dicer-1-dependent Dacapo suppression acts downstream of Insulin receptor in regulating cell division of Drosophila germline stem cells. Development 136:1497–1507

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by grants by Central Public-Interest Scientific Institution Basal Research Fund CAFS (2017JBFM05); the National Natural Science Foundation of China (Grant No. 31572617), New varieties creation Major Project in Jiangsu province (PZCZ201745), the Science & Technology Supporting Program of Jiangsu Province (BE2016308), China Agriculture Research System-48 (CARS-48), Jiangsu Fisheries Research System-02 (JFRS-02).

Author information

Authors and Affiliations

  1. Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture, Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, 214081, People’s Republic of China

    Hui Qiao, Sufei Jiang, Yiwei Xiong, Hongtuo Fu, Wenyi Zhang, Yongsheng Gong, Shubo Jin & Yan Wu

  2. Wuxi Fisheries College, Nanjing Agricultural University, Wuxi, 214081, People’s Republic of China

    Hongtuo Fu & Yabing Wang

Authors
  1. Hui Qiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sufei Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yiwei Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hongtuo Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wenyi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yabing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yongsheng Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shubo Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hongtuo Fu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qiao, H., Jiang, S., Xiong, Y. et al. Integrated analysis of differentially expressed microRNAs and mRNAs to screen miRNAs and genes related to reproduction in Macrobrachium nipponense. 3 Biotech 9, 327 (2019). https://doi.org/10.1007/s13205-019-1847-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-019-1847-9

Keywords

Search

Navigation