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Identification of Mitochondrial Genome-Encoded Small RNAs Related to Egg Deterioration Caused by Postovulatory Aging in Rainbow Trout

Marine Biotechnology volume 18, pages 584–597 (2016)Cite this article

Abstract

Many factors have been reported to affect rainbow trout egg quality, among which, postovulatory aging is one of the most significant causes as reared rainbow trout do not usually volitionally oviposit the ovulated eggs. In order to uncover the genetic regulation underling egg deterioration caused by postovulatory aging in rainbow trout, mitochondrial genome-encoded small RNA (mitosRNAs) were analyzed from unfertilized eggs on Days 1, 7, and 14 postovulation with fertilization rates of 91.8, 73.4, and less than 50 %, respectively. A total of 248 mitosRNAs were identified from Illumina high-throughput sequencing of the small RNA libraries derived from the eggs of ten females. Ninety-eight of the small RNAs exhibited more than a threefold difference in expression between eggs from females exhibiting high fertilization rates at Day 1 and low fertilization rates at Day 14. The differentially expressed mitosRNAs were predominantly derived from mitochondrial D-loop, tRNA, rRNA, COII, and Cytb gene regions. Real-time quantitative PCR analysis was carried out for 14 differentially expressed mitosRNAs, of which, 12 were confirmed to be consistent with the sequencing reads. Further characterization of the differentially expressed mitosRNAs may lead to the development of new biomarkers for egg quality in rainbow trout.

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References

  • Aegerter S, Jalabert B (2004) Effects of post-ovulatory oocyte ageing and temperature on egg quality and on the occurrence of triploid fry in rainbow trout, Oncorhynchus mykiss. Aquaculture 231:59–71

    Article  Google Scholar 

  • Aegerter S, Jalabert B, Bobe J (2005) Large scale real-time PCR analysis of mRNA abundance in rainbow trout eggs in relationship with egg quality and post-ovulatory ageing. Mol Reprod Dev 72:377–385

    Article  CAS  PubMed  Google Scholar 

  • Bandiera S, Ruberg S, Girard M, Cagnard N, Hanein S, Chretien D, Munnich A, Lyonnet S, Henrion-Caude A (2011) Nuclear outsourcing of RNA interference components to human mitochondria. PLoS One 6:e20746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barrey E, Saint-Auret G, Bonnamy B, Damas D, Boyer O, Gidrol X (2011) Pre-microRNA and mature microRNA in human mitochondria. PLoS One 6:e20220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blanco S, Dietmann S, Flores JV, Hussain S, Kutter C, Humphreys P, Lukk M, Lombard P, Treps L, Popis M, Kellner S, Holter SM, Garrett L, Wurst W, Becker L, Klopstock T, Fuchs H, Gailus-Durner V, Hrabe de Angelis M, Karadottir RT, Helm M, Ule J, Gleeson JG, Odom DT, Frye M (2014) Aberrant methylation of tRNAs links cellular stress to neuro-developmental disorders. EMBO J 33:2020–2039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bobe J, Labbe C (2010) Egg and sperm quality in fish. Gen Comp Endocrinol 165:535–548

    Article  CAS  PubMed  Google Scholar 

  • Bonnet E, Fostier A, Bobe J (2007) Microarray-based analysis of fish egg quality after natural or controlled ovulation. BMC Genomics 8:55

    Article  PubMed  PubMed Central  Google Scholar 

  • Bras M, Queenan B, Susin SA (2005) Programmed cell death via mitochondria: different modes of dying. Biochemistry (Mosc) 70:231–239

    Article  CAS  Google Scholar 

  • Brazert M, Pawelczyk LA (2015) Insulin-like growth factor-1 isoforms in human ovary. Preliminary report on the expression of the IGF-1 gene in PCOS patients and healthy controls. Ginekol Pol 86:890–895

    Article  PubMed  Google Scholar 

  • Brooks S, Tyler CR, Sumpter JP (1997) Egg quality in fish: what makes a good egg? Rev Fish Biol Fish 7:387–416

    Article  Google Scholar 

  • Brooks MJ, Rajasimha HK, Roger JE, Swaroop A (2011) Next-generation sequencing facilitates quantitative analysis of wild-type and Nrl(−/−) retinal transcriptomes. Mol Vis 17:3034–3054

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burns KH, Viveiros MM, Ren Y, Wang P, Demayo FJ, Frail DE, Eppig JJ, Matzuk MM (2003) Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science 300:633–636

    Article  CAS  PubMed  Google Scholar 

  • Burroughs AM, Ando Y, de Hoon MJ, Tomaru Y, Suzuki H, Hayashizaki Y, Daub CO (2011) Deep-sequencing of human Argonaute-associated small RNAs provides insight into miRNA sorting and reveals Argonaute association with RNA fragments of diverse origin. RNA Biol 8:158–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chinnery PF, Elliott HR, Hudson G, Samuels DC, Relton CL (2012) Epigenetics, epidemiology and mitochondrial DNA diseases. Int J Epidemiol 41:177–187

    Article  PubMed  PubMed Central  Google Scholar 

  • Cole C, Sobala A, Lu C, Thatcher SR, Bowman A, Brown JWS, Green PJ, Barton GJ, Hutvagner G (2009) Filtering of deep sequencing data reveals the existence of abundant dicer-dependent small RNAs derived from tRNAs. RNA 15:2147–2160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Craik JCA, Harvey SM (1984) Egg quality in rainbow-trout - the relation between egg viability, selected aspects of egg composition, and time of stripping. Aquaculture 40:115–134

    Article  CAS  Google Scholar 

  • Feng L, Liu H, Liu Y, Lu Z, Guo G, Guo S, Zheng H, Gao Y, Cheng S, Wang J, Zhang K, Zhang Y (2010) Power of deep sequencing and agilent microarray for gene expression profiling study. Mol Biotechnol 45:101–110

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Silva MR, Cabrera-Cabrera F, Guida MC, Cayota A (2012) Hints of tRNA-derived small RNAs role in RNA silencing mechanisms. Genes (Basel) 3:603–614

    Google Scholar 

  • Garmire LX, Subramaniam S (2012) Evaluation of normalization methods in mammalian microRNA-seq data. RNA 18:1279–1288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodarzi H, Liu X, Nguyen HC, Zhang S, Fish L, Tavazoie SF (2015) Endogenous tRNA-derived fragments suppress breast cancer progression via YBX1 displacement. Cell 161:790–802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanada T, Weitzer S, Mair B, Bernreuther C, Wainger BJ, Ichida J, Hanada R, Orthofer M, Cronin SJ, Komnenovic V, Minis A, Sato F, Mimata H, Yoshimura A, Tamir I, Rainer J, Kofler R, Yaron A, Eggan KC, Woolf CJ, Glatzel M, Herbst R, Martinez J, Penninger JM (2013) CLP1 links tRNA metabolism to progressive motor-neuron loss. Nature 495:474–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haussecker D, Huang Y, Lau A, Parameswaran P, Fire AZ, Kay MA (2010) Human tRNA-derived small RNAs in the global regulation of RNA silencing. RNA 16:673–695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hershberger WK, Hostuttler MA (2005) Variation in time to first cleavage in rainbow trout Oncorhynchus mykiss embryos: a major factor in induction of tetraploids. J World Aquacult Soc 36:96–102

    Article  Google Scholar 

  • Hirose Y, Ikeda KT, Noro E, Hiraoka K, Tomita M, Kanai A (2015) Precise mapping and dynamics of tRNA-derived fragments (tRFs) in the development of Triops cancriformis (tadpole shrimp). BMC Genet 16:83

    Article  PubMed  PubMed Central  Google Scholar 

  • Honda S, Loher P, Shigematsu M, Palazzo JP, Suzuki R, Imoto I, Rigoutsos I, Kirino Y (2015) Sex hormone-dependent tRNA halves enhance cell proliferation in breast and prostate cancers. Proc Natl Acad Sci U S A 112:E3816–E3825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Igarashi H, Takahashi T, Takahashi E, Tezuka N, Nakahara K, Takahashi K, Kurachi H (2005) Aged mouse oocytes fail to readjust intracellular adenosine triphosphates at fertilization. Biol Reprod 72:1256–1261

    Article  CAS  PubMed  Google Scholar 

  • Juanchich A, Le Cam A, Montfort J, Guiguen Y, Bobe J (2013) Identification of differentially expressed miRNAs and their potential targets during fish ovarian development. Biol Reprod 88:128

    Article  PubMed  Google Scholar 

  • Kal AJ, van Zonneveld AJ, Benes V, van den Berg M, Koerkamp MG, Albermann K, Strack N, Ruijter JM, Richter A, Dujon B, Ansorge W, Tabak HF (1999) Dynamics of gene expression revealed by comparison of serial analysis of gene expression transcript profiles from yeast grown on two different carbon sources. Mol Biol Cell 10:1859–1872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kala R, Peek GW, Hardy TM, Tollefsbol TO (2013) MicroRNAs: an emerging science in cancer epigenetics. J Clin Bioinforma 3:6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kren BT, Wong PY, Sarver A, Zhang X, Zeng Y, Steer CJ (2009) MicroRNAs identified in highly purified liver-derived mitochondria may play a role in apoptosis. RNA Biol 6:65–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: An information aesthetic for comparative genomics. Genome Research, 19:1639–1645

  • Kulshreshtha R, Davuluri RV, Calin GA, Ivan M (2008) A microRNA component of the hypoxic response. Cell Death Differ 15:667–671

    Article  CAS  PubMed  Google Scholar 

  • Kumar P, Anaya J, Mudunuri SB, Dutta A (2014) Meta-analysis of tRNA derived RNA fragments reveals that they are evolutionarily conserved and associate with AGO proteins to recognize specific RNA targets. BMC Biol 12:78

    Article  PubMed  PubMed Central  Google Scholar 

  • Lahnsteiner F (2000) Morphological, physiological and biochemical parameters characterizing the over-ripening of rainbow trout eggs. Fish Physiol Biochem 23:107–118

    Article  CAS  Google Scholar 

  • Latham KE, Sapienza C, Engel N (2012) The epigenetic lorax: gene-environment interactions in human health. Epigenomics 4:383–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee HC, Chang SS, Choudhary S, Aalto AP, Maiti M, Bamford DH, Liu Y (2009a) qiRNA is a new type of small interfering RNA induced by DNA damage. Nature 459:274–277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee YS, Shibata Y, Malhotra A, Dutta A (2009b) A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev 23:2639–2649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing, S (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Lord T, Aitken RJ (2013) Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction 146:R217–R227

    Article  CAS  PubMed  Google Scholar 

  • Ma H, Hostuttler M, Wei H, Rexroad CE 3rd, Yao J (2012) Characterization of the rainbow trout egg MicroRNA transcriptome. PLoS One 7:e39649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma H, Weber GM, Hostuttler MA, Wei H, Wang L, Yao J (2015) MicroRNA expression profiles from eggs of different qualities associated with post-ovulatory ageing in rainbow trout (Oncorhynchus mykiss). BMC Genomics 16:201

    Article  PubMed  PubMed Central  Google Scholar 

  • Mercer TR, Neph S, Dinger ME, Crawford J, Smith MA, Shearwood AM, Haugen E, Bracken CP, Rackham O, Stamatoyannopoulos JA, Filipovska A, Mattick JS (2011) The human mitochondrial transcriptome. Cell 146:645–658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320:1344–1349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petit PX, Susin SA, Zamzami N, Mignotte B, Kroemer G (1996) Mitochondria and programmed cell death: back to the future. FEBS Lett 396:7–13

    Article  CAS  PubMed  Google Scholar 

  • Ramachandra RK, Salem M, Gahr S, Rexroad CE, Yao J (2008) Cloning and characterization of microRNAs from rainbow trout (Oncorhynchus mykiss): their expression during early embryonic development. BMC Dev Biol 8:41

    Article  PubMed  PubMed Central  Google Scholar 

  • Ro S, Ma HY, Park C, Ortogero N, Song R, Hennig GW, Zheng H, Lin YM, Moro L, Hsieh JT, Yan W (2013) The mitochondrial genome encodes abundant small noncoding RNAs. Cell Res 23:759–774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saikia M, Jobava R, Parisien M, Putnam A, Krokowski D, Gao XH, Guan BJ, Yuan Y, Jankowsky E, Feng Z, Hu GF, Pusztai-Carey M, Gorla M, Sepuri NB, Pan T, Hatzoglou M (2014) Angiogenin-cleaved tRNA halves interact with cytochrome c, protecting cells from apoptosis during osmotic stress. Mol Cell Biol 34:2450–2463

    Article  PubMed  PubMed Central  Google Scholar 

  • Sattler FR (2013) Growth hormone in the aging male. Best Pract Res Clin Endocrinol Metab 27:541–555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shigematsu M, Honda S, Kirino Y (2014) Transfer RNA as a source of small functional RNA. J Mol Biol Mol Imaging 1(2):8

  • Sobala A, Hutvagner G (2011) Transfer RNA-derived fragments: origins, processing, and functions. Wiley Interdiscip Rev RNA 2:853–862

    Article  CAS  PubMed  Google Scholar 

  • Sobala A, Hutvagner G (2013) Small RNAs derived from the 5′ end of tRNA can inhibit protein translation in human cells. RNA Biol 10:553–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Springate JRC, Bromage NR, Elliott JAK, Hudson DL (1984) The timing of ovulation and stripping and their effects on the rates of fertilization and survival to eying, hatch and swim-up in the rainbow-trout (Salmo-Gairdneri R). Aquaculture 43:313–322

    Article  Google Scholar 

  • Sripada L, Tomar D, Prajapati P, Singh R, Singh AK, Singh R (2012) Systematic analysis of small RNAs associated with human mitochondria by deep sequencing: detailed analysis of mitochondrial associated miRNA. PLoS One 7:e44873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suen DF, Norris KL, Youle RJ (2008) Mitochondrial dynamics and apoptosis. Genes Dev 22:1577–1590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and cufflinks. Nat Protoc 7:562–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weber GM, Hostuttler MA (2012) Factors affecting the first cleavage interval and effects of parental generation on tetraploid production in rainbow trout (Oncorhynchus mykiss). Aquaculture 344:231–238

    Article  Google Scholar 

  • Xu P, Guo M, Hay BA (2004) MicroRNAs and the regulation of cell death. Trends Genet 20:617–624

    Article  CAS  PubMed  Google Scholar 

  • Zardoya R, Garridopertierra A, Bautista JM (1995) The complete nucleotide sequence of the mitochondrial DNA genome of the rainbow trout, Oncorhynchus mykiss. J Mol Evol 41:942–951

    CAS  PubMed  Google Scholar 

  • Zhao H, Bojanowski K, Ingber DE, Panigrahy D, Pepper MS, Montesano R, Shing Y (1999) New role for tRNA and its fragment purified from human urinary bladder carcinoma conditioned medium: inhibition of endothelial cell growth. J Cell Biochem 76:109–117

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Guangtu Gao, Mark Hostuttler, and Jill Birkett for technical assistance. This study was supported by the USDA-ARS Cooperative Agreement no. 58-1930-0-059. Mention of trade names is solely for the purpose of providing accurate information and should not imply product endorsement by the United States Department of Agriculture. USDA is an equal opportunity provider and employer.

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Authors and Affiliations

  1. National Center for Cool and Cold Water Aquaculture, Kearneysville, WV, 25430, USA

    Hao Ma & Gregory M. Weber

  2. Division of Animal and Nutritional Sciences, West Virginia University, Morgantown, WV, 26506, USA

    Hao Ma & Jianbo Yao

  3. School of Forest Resources and Environmental Science, Michigan Technological University, Houghton, MI, 49931, USA

    Hairong Wei

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  1. Hao Ma
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  2. Gregory M. Weber
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  3. Hairong Wei
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Correspondence to Hao Ma.

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Electronic Supplementary Material

Table S1

MitosRNAs identified from the D1PO, D7PO, and D14PO samples. (DOCX 25 kb)

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Ma, H., Weber, G.M., Wei, H. et al. Identification of Mitochondrial Genome-Encoded Small RNAs Related to Egg Deterioration Caused by Postovulatory Aging in Rainbow Trout. Mar Biotechnol 18, 584–597 (2016). https://doi.org/10.1007/s10126-016-9719-3

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  • DOI: https://doi.org/10.1007/s10126-016-9719-3

Keywords

  • MitosRNA
  • Egg quality
  • Postovulation
  • Rainbow trout

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