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Identification and Functional Prediction of Large Intergenic Noncoding RNAs (lincRNAs) in Rainbow Trout (Oncorhynchus mykiss)

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Abstract

Long noncoding RNAs (lncRNAs) have been recognized in recent years as key regulators of diverse cellular processes. Genome-wide large-scale projects have uncovered thousands of lncRNAs in many model organisms. Large intergenic noncoding RNAs (lincRNAs) are lncRNAs that are transcribed from intergenic regions of genomes. To date, no lincRNAs in non-model teleost fish have been reported. In this report, we present the first reference catalog of 9674 rainbow trout lincRNAs based on analysis of RNA-Seq data from 15 tissues. Systematic analysis revealed that lincRNAs in rainbow trout share many characteristics with those in other mammalian species. They are shorter and lower in exon number and expression level compared with protein-coding genes. They show tissue-specific expression pattern and are typically co-expressed with their neighboring genes. Co-expression network analysis suggested that many lincRNAs are associated with immune response, muscle differentiation, and neural development. The study provides an opportunity for future experimental and computational studies to uncover the functions of lincRNAs in rainbow trout.

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References

  • Amaral PP, Clark MB, Gascoigne DK, Dinger ME, Mattick JS (2011) lncRNAdb: a reference database for long noncoding RNAs. Nucleic Acids Res 39:D146–D151.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andreotti AH, Schwartzberg PL, Joseph RE, Berg LJ (2010) T-cell signaling regulated by the Tec family kinase, Itk. Cold Spring Harb Perspect Biol 2:a002287.

    Article  PubMed  PubMed Central  Google Scholar 

  • Berthelot C, Brunet F, Chalopin D, Juanchich A, Bernard M, Noel B, Bento P, Da Silva C, Labadie K, Alberti A, Aury JM, Louis A, Dehais P, Bardou P, Montfort J, Klopp C, Cabau C, Gaspin C, Thorgaard GH, Boussaha M, Quillet E, Guyomard R, Galiana D, Bobe J, Volff JN, Genet C, Wincker P, Jaillon O, Roest Crollius H, Guiguen Y (2014) The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun 5:3657.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhartiya D, Kapoor S, Jalali S, Sati S, Kaushik K, Sachidanandan C, Sivasubbu S, Scaria V (2012) Conceptual approaches for lncRNA drug discovery and future strategies. Expert Opin Drug Discovery 7:503–513.

    Article  CAS  Google Scholar 

  • Cabianca DS, Casa V, Bodega B, Xynos A, Ginelli E, Tanaka Y, Gabellini D (2012) A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy. Cell 149:819–831.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25:1915–1927.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, Kodzius R, Shimokawa K, Bajic VB, Brenner SE, Batalov S, Forrest AR, Zavolan M, Davis MJ, Wilming LG, Aidinis V, Allen JE, Ambesi-Impiombato A, Apweiler R, Aturaliya RN, Bailey TL, Bansal M, Baxter L, Beisel KW, Bersano T, Bono H, Chalk AM, Chiu KP, Choudhary V, Christoffels A, Clutterbuck DR, Crowe ML, Dalla E, Dalrymple BP, De Bono B, Della Gatta G, Di Bernardo D, Down T, Engstrom P, Fagiolini M, Faulkner G, Fletcher CF, Fukushima T, Furuno M, Futaki S, Gariboldi M, Georgii-Hemming P, Gingeras TR, Gojobori T, Green RE, Gustincich S, Harbers M, Hayashi Y, Hensch TK, Hirokawa N, Hill D, Huminiecki L, Iacono M, Ikeo K, Iwama A, Ishikawa T, Jakt M, Kanapin A, Katoh M, Kawasawa Y, Kelso J, Kitamura H, Kitano H, Kollias G, Krishnan SP, Kruger A, Kummerfeld SK, Kurochkin IV, Lareau LF, Lazarevic D, Lipovich L, Liu J, Liuni S, Mcwilliam S, Madan Babu M, Madera M, Marchionni L, Matsuda H, Matsuzawa S, Miki H, Mignone F, Miyake S, Morris K, Mottagui-Tabar S, Mulder N, Nakano N, Nakauchi H, Ng P, Nilsson R, Nishiguchi S, Nishikawa S et al (2005) The transcriptional landscape of the mammalian genome. Science 309:1559–1563.

    Article  CAS  PubMed  Google Scholar 

  • Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147:358–369.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark BS, Blackshaw S (2014) Long non-coding RNA-dependent transcriptional regulation in neuronal development and disease. Front Genet 5:164.

    Article  PubMed  PubMed Central  Google Scholar 

  • Conesa A, Gotz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:619832.

    Article  PubMed  PubMed Central  Google Scholar 

  • Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M, Davis CA, Shiekhattar R, Gingeras TR, Hubbard TJ, Notredame C, Harrow J, Guigo R (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22:1775–1789.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans R, Patzak I, Svensson L, De Filippo K, Jones K, Mcdowall A, Hogg N (2009) Integrins in immunity. J Cell Sci 122:215–225.

    Article  CAS  PubMed  Google Scholar 

  • Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A (2008) The Pfam protein families database. Nucleic Acids Res 36:D281–D288.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garber M, Grabherr MG, Guttman M, Trapnell C (2011) Computational methods for transcriptome annotation and quantification using RNA-seq. Nat Methods 8:469–477

    Article  CAS  PubMed  Google Scholar 

  • Gardner PP, Daub J, Tate JG, Nawrocki EP, Kolbe DL, Lindgreen S, Wilkinson AC, Finn RD, Griffiths-Jones S, Eddy SR, Bateman A (2009) Rfam: updates to the RNA families database. Nucleic Acids Res 37:D136–D140.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, Wang Y, Brzoska P, Kong B, Li R, West RB, Van De Vijver MJ, Sukumar S, Chang HY (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464:1071–1076.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, Cabili MN, Jaenisch R, Mikkelsen TS, Jacks T, Hacohen N, Bernstein BE, Kellis M, Regev A, Rinn JL, Lander ES (2009) Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458:223–227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, Rinn JL, Lander ES, Regev A (2010) Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 28:503–510.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, Kenzelmann-Broz D, Khalil AM, Zuk O, Amit I, Rabani M, Attardi LD, Regev A, Lander ES, Jacks T, Rinn JL (2010) A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142:409–419.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hung T, Wang Y, Lin MF, Koegel AK, Kotake Y, Grant GD, Horlings HM, Shah N, Umbricht C, Wang P, Wang Y, Kong B, Langerod A, Borresen-Dale AL, Kim SK, Van De Vijver M, Sukumar S, Whitfield ML, Kellis M, Xiong Y, Wong DJ, Chang HY (2011) Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters. Nat Genet 43:621–629.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaushik K, Leonard VE, Kv S, Lalwani MK, Jalali S, Patowary A, Joshi A, Scaria V, Sivasubbu S (2013) Dynamic expression of long non-coding RNAs (lncRNAs) in adult zebrafish. PLoS One 8:e83616.

    Article  PubMed  PubMed Central  Google Scholar 

  • Khaitovich P, Kelso J, Franz H, Visagie J, Giger T, Joerchel S, Petzold E, Green RE, Lachmann M, Paabo S (2006) Functionality of intergenic transcription: an evolutionary comparison. PLoS Genet 2:e171.

    Article  PubMed  PubMed Central  Google Scholar 

  • Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, Van Oudenaarden A, Regev A, Lander ES, Rinn JL (2009) Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 106:11667–11672.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, Wei L, Gao G (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35:W345–W349.

    Article  PubMed  PubMed Central  Google Scholar 

  • Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:559.

    Article  PubMed  PubMed Central  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao Q, Liu C, Yuan X, Kang S, Miao R, Xiao H, Zhao G, Luo H, Bu D, Zhao H, Skogerbo G, Wu Z, Zhao Y (2011) Large-scale prediction of long non-coding RNA functions in a coding-non-coding gene co-expression network. Nucleic Acids Res 39:3864–3878.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loewer S, Cabili MN, Guttman M, Loh YH, Thomas K, Park IH, Garber M, Curran M, Onder T, Agarwal S, Manos PD, Datta S, Lander ES, Schlaeger TM, Daley GQ, Rinn JL (2010) Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat Genet 42:1113–1117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo H, Sun S, Li P, Bu D, Cao H, Zhao Y (2013) Comprehensive characterization of 10,571 mouse large intergenic noncoding RNAs from whole transcriptome sequencing. PLoS One 8:e70835.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neefjes J, Jongsma ML, Paul P, Bakke O (2011) Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol 11:823–836.

    CAS  PubMed  Google Scholar 

  • Ng SY, Johnson R, Stanton LW (2012) Human long non-coding RNAs promote pluripotency and neuronal differentiation by association with chromatin modifiers and transcription factors. EMBO J 31:522–533.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okazaki Y, Furuno M, Kasukawa T, Adachi J, Bono H, Kondo S, Nikaido I, Osato N, Saito R, Suzuki H, Yamanaka I, Kiyosawa H, Yagi K, Tomaru Y, Hasegawa Y, Nogami A, Schonbach C, Gojobori T, Baldarelli R, Hill DP, Bult C, Hume DA, Quackenbush J, Schriml LM, Kanapin A, Matsuda H, Batalov S, Beisel KW, Blake JA, Bradt D, Brusic V, Chothia C, Corbani LE, Cousins S, Dalla E, Dragani TA, Fletcher CF, Forrest A, Frazer KS, Gaasterland T, Gariboldi M, Gissi C, Godzik A, Gough J, Grimmond S, Gustincich S, Hirokawa N, Jackson IJ, Jarvis ED, Kanai A, Kawaji H, Kawasawa Y, Kedzierski RM, King BL, Konagaya A, Kurochkin IV, Lee Y, Lenhard B, Lyons PA, Maglott DR, Maltais L, Marchionni L, Mckenzie L, Miki H, Nagashima T, Numata K, Okido T, Pavan WJ, Pertea G, Pesole G, Petrovsky N, Pillai R, Pontius JU, Qi D, Ramachandran S, Ravasi T, Reed JC, Reed DJ, Reid J, Ring BZ, Ringwald M, Sandelin A, Schneider C, Semple CA, Setou M, Shimada K, Sultana R, Takenaka Y, Taylor MS, Teasdale RD, Tomita M, Verardo R, Wagner L, Wahlestedt C, Wang Y, Watanabe Y, Wells C, Wilming LG, Wynshaw-Boris A, Yanagisawa M et al (2002) Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 420:563–573.

    Article  PubMed  Google Scholar 

  • Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, Guigo R, Shiekhattar R (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell 143:46–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, Nagano T, Mancini-Dinardo D, Kanduri C (2008) Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol Cell 32:232–246.

    Article  CAS  PubMed  Google Scholar 

  • Pang KC, Stephen S, Dinger ME, Engstrom PG, Lenhard B, Mattick JS (2007) RNAdb 2.0–an expanded database of mammalian non-coding RNAs. Nucleic Acids Res 35:D178–D182.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, Fan L, Sandelin A, Rinn JL, Regev A, Schier AF (2012) Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res 22:577–591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pei G, Repnik U, Griffiths G, Gutierrez MG (2014) Identification of an immune-regulated phagosomal Rab cascade in macrophages. J Cell Sci 127:2071–2082.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perkel JM (2013) Visiting “noncodarnia”. Biotechniques 54(301):303–304.

    Google Scholar 

  • Ponjavic J, Ponting CP, Lunter G (2007) Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res 17:556–565.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129:1311–1323.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez JC, Muller M (2011) pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics 12:77.

    Article  PubMed  PubMed Central  Google Scholar 

  • Salem M, Rexroad CE, Wang J, Thorgaard GH, Yao J (2010a) Characterization of the rainbow trout transcriptome using Sanger and 454-pyrosequencing approaches. BMC Genomics 11:564

    Article  PubMed  PubMed Central  Google Scholar 

  • Salem M, Xiao C, Womack J, Rexroad CE 3rd, Yao J (2010b) A microRNA repertoire for functional genome research in rainbow trout (Oncorhynchus mykiss). Mar Biotechnol (NY) 12:410–429.

    Article  CAS  Google Scholar 

  • Salem M, Paneru B, Al-Tobasei R, Abdouni F, Thorgaard GH, Rexroad CE, Yao J (2015) Transcriptome assembly, gene annotation and tissue gene expression atlas of the rainbow trout. PLoS One 10:e0121778.

    Article  PubMed  PubMed Central  Google Scholar 

  • Solda G, Makunin IV, Sezerman OU, Corradin A, Corti G, Guffanti A (2009) An Ariadne’s thread to the identification and annotation of noncoding RNAs in eukaryotes. Brief Bioinform 10:475–489.

    Article  CAS  PubMed  Google Scholar 

  • Sun L, Zhang Z, Bailey TL, Perkins AC, Tallack MR, Xu Z, Liu H (2012) Prediction of novel long non-coding RNAs based on RNA-Seq data of mouse Klf1 knockout study. BMC Bioinformatics 13:331.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun K, Zhao Y, Wang H, Sun H (2014) Sebnif: an integrated bioinformatics pipeline for the identification of novel large intergenic noncoding RNAs (lincRNAs)—application in human skeletal muscle cells. PLoS One 9:e84500.

    Article  PubMed  PubMed Central  Google Scholar 

  • Thorgaard GH, Bailey GS, Williams D, Buhler DR, Kaattari SL, Ristow SS, Hansen JD, Winton JR, Bartholomew JL, Nagler JJ, Walsh PJ, Vijayan MM, Devlin RH, Hardy RW, Overturf KE, Young WP, Robison BD, Rexroad C, Palti Y (2002) Status and opportunities for genomics research with rainbow trout. Comp Biochem Physiol B Biochem Mol Biol 133:609–646

    Article  PubMed  Google Scholar 

  • Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105–1111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, Lajoie BR, Protacio A, Flynn RA, Gupta RA, Wysocka J, Lei M, Dekker J, Helms JA, Chang HY (2011) A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472:120–124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Park HJ, Dasari S, Wang S, Kocher JP, Li W (2013a) CPAT: coding-potential assessment tool using an alignment-free logistic regression model. Nucleic Acids Res 41:e74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Tripurani SK, Wanna W, Rexroad CE 3rd, Yao J (2013b) Cloning and characterization of a novel oocyte-specific gene encoding an F-Box protein in rainbow trout (Oncorhynchus mykiss). Reprod Biol Endocrinol 11:86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weichhart T, Saemann MD (2008) The PI3K/Akt/mTOR pathway in innate immune cells: emerging therapeutic applications. Ann Rheum Dis 67(Suppl 3):iii70–4.

    Article  PubMed  Google Scholar 

  • Zhang K, Huang K, Luo Y, Li S (2014) Identification and functional analysis of long non-coding RNAs in mouse cleavage stage embryonic development based on single cell transcriptome data. BMC Genomics 15:845.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322:750–756.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Yu M, Li Z, Kong C, Bi J, Li J, Gao Z (2011) ncRAN, a newly identified long noncoding RNA, enhances human bladder tumor growth, invasion, and survival. Urology 77:510.e1–5.

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was supported by the USDA ARS Cooperative Agreement No. 58-1930-0-059. It is published with the approval of the director of the West Virginia Agricultural and Forestry Experiment Station as scientific paper No. 3268.

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Correspondence to Jianbo Yao.

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Supplemental file 1

Primers used for validation of expression of 10 selected lincRNAs. (XLSX 9 kb)

Supplemental file 2

Total transcript counts in each step of lincRNA prediction pipeline. (XLSX 10 kb)

Supplemental file 3

Catalog of 9764 transcribed lincRNAs in rainbow trout. (XLSX 2309 kb)

Supplemental file 4

Venn diagram representing rainbow trout lincRNAs across different tissues. (A) Overlapping expression profiles of lincRNAs across testis (blue-Te), oocyte (yellow-Oo), pineal (orange-Pi), brain (green-Br), and liver (pink-Li). (B) Overlapping expression profiles of lincRNAs across white muscle (blue-Wm), red muscle (yellow-Rm), skin (orange-Sk), fat (green-Fa) and head kidney (pink-Hk). (JPG 142 kb)

Supplemental file 5

Hierarchical clustering dendrogram of lincRNAs together with protein coding genes. (JPG 50 kb)

Supplemental file 6

Genes and their memberships to each module. MM stands for module membership, which is the correlation between a gene and a module. PMM is the p-value of MM. (XLSX 170 kb)

Supplemental file 7

GO analysis of modules. GO terms enriched in specific modules were tested by Fisher’s exact test. (XLSX 170 kb)

Supplemental file 8

KEGG pathway analysis and network of hub gene of blue module. (A) and (B) Hub gene network. (C) mTOR signaling pathway. (D) T cell receptor signaling pathway. (E) PI3K-AKT signaling pathway. (JPG 709 kb)

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Wang, J., Fu, L., Koganti, P.P. et al. Identification and Functional Prediction of Large Intergenic Noncoding RNAs (lincRNAs) in Rainbow Trout (Oncorhynchus mykiss). Mar Biotechnol 18, 271–282 (2016). https://doi.org/10.1007/s10126-016-9689-5

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