Molecular Biology Reports

, Volume 45, Issue 6, pp 1597–1609 | Cite as

Expression analysis of lncRNA AK370814 involved in the barley vitamin B6 salvage pathway under salinity

  • Elif KarlikEmail author
  • Nermin Gozukirmizi
Original Article


Long non-coding RNAs (lncRNAs), which are longer than > 200 nt, perform various functions in a variety of important biological processes. The aim of this study is the investigation of relative expression levels of AK372815 putative pyridoxal reductase (PLR) gene and sense lncRNA AK370814 on four barley genotypes (Hasat, Beysehir 99, Konevi 98 and Tarm 92) in response to 150 mM salinity application during 3 days post-germination. Seeds were placed randomly in petri dishes containing (a) only H2O (control), (b) 150 mM NaCl, for 72 h. RNA isolation was carried out using TriPure® reagent from 150 mM salt-treated root and shoot samples. Relative expression levels of AK372815 PLR and sense lncRNA AK370814 were determined by qPCR. Results demonstrated that salinity affected the expression levels of both AK372815 PLR gene and sense lncRNA AK370814 during germination. Although expression levels of AK372815 PLR tended to be down-regulated under salinity, expression levels of sense lncRNA AK370814 were up-regulated. Another goal of this study is improvement of alternative approach to NGS technologies for determination of relative expression levels of sense lncRNAs under particular circumstances. This is the first report that demonstrates a relationship between lncRNA and vitamin B6 salvage pathway.


Long non-coding RNAs Vitamin B6 Vitamin B6 salvage pathway Salinity Barley 



This work was supported by Scientific Research Projects Coordination Unit of Istanbul University. Project Number: FDK-2016-23086. Also, the authors thank Dr. Stuart James Lucas for his kind revision and Dr. Cem Horozoglu (Gelisim University) for helpful suggestions.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human and animal participants

This article does not contain any studies conducted on human or animal subjects.


  1. 1.
    Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, Xue C, Marinov GK, Khatun J, Williams BA, Zaleski C, Rozowsky J, Roder M, Kokocinski F, Abdelhamid RF, Alioto T, Antoshechkin I, Baer MT, Bar NS, Batut P, Bell K, Bell I, Chakrabortty S, Chen X, Chrast J, Curado J, Derrien T, Drenkow J, Dumais E, Dumais J, Duttagupta R, Falconnet E, Fastuca M, Fejes-Toth K, Ferreira P, Foissac S, Fullwood MJ, Gao H, Gonzalez D, Gordon A, Gunawardena H, Howald C, Jha S, Johnson R, Kapranov P, King B, Kingswood C, Luo OJ, Park E, Persaud K, Preall JB, Ribeca P, Risk B, Robyr D, Sammeth M, Schaffer L, See LH, Shahab A, Skancke J, Suzuki AM, Takahashi H, Tilgner H, Trout D, Walters N, Wang H, Wrobel J, Yu Y, Ruan X, Hayashizaki Y, Harrow J, Gerstein M, Hubbard T, Reymond A, Antonarakis SE, Hannon G, Giddings MC, Ruan Y, Wold B, Carninci P, Guigo R, Gingeras TR (2012) Landscape of transcription in human cells. Nature 489:101–108PubMedCentralPubMedGoogle Scholar
  2. 2.
    Hangauer MJ, Vaughn IW, McManus MT (2013) Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs. PLoS Genet 9(6):1–13Google Scholar
  3. 3.
    Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, Kokocinski F, Aken BL, Barrell D, Zadissa A, Searle S, Barnes I, Bignell A, Boychenko V, Hunt T, Kay M, Mukherjee G, Rajan J, Despacio-Reyes G, Saunders G, Steward C, Harte R, Lin M, Howald C, Tanzer A, Derrien T, Chrast J, Walters N, Balasubramanian S, Pei B, Tress M, Rodriguez JM, Ezkurdia I, Van Baren J, Brent M, Haussler D, Kellis M, Valencia A, Reymond A, Gerstein M, Guigó R, Hubbard TJ (2012) GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res 22:1760–1774PubMedCentralPubMedGoogle Scholar
  4. 4.
    Chekanova JA (2015) Long non-coding RNAs and their functions in plants. Curr Opin Plant Biol 27:207–216PubMedGoogle Scholar
  5. 5.
    Ma L, Bajic VB, Zhang Z (2013) On the classification of long noncoding RNAs. RNA Biol 10:925–933PubMedGoogle Scholar
  6. 6.
    Devaux Y, Zangrando J, Schroen B, Creemers EE, Pedrazzini T, Chang CP, Dorn GWII, Thum T, Heymans S, Cardiolinc N (2015) Long noncoding RNAs in cardiac development and ageing. Nat Rev Cardiol 12:415–425PubMedGoogle Scholar
  7. 7.
    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 28:511–515PubMedCentralPubMedGoogle Scholar
  8. 8.
    Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, Rinn JL, Lander E, Regev S (2010) A Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 28:503–510PubMedCentralPubMedGoogle Scholar
  9. 9.
    Kiełbasa SM, Wan R, Sato K, Horton P, Frith MC (2011) Adaptive seeds tame genomic sequence comparison. Genome Res 21:487–493PubMedCentralPubMedGoogle Scholar
  10. 10.
    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:R36PubMedCentralPubMedGoogle Scholar
  11. 11.
    Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21PubMedCentralPubMedGoogle Scholar
  12. 12.
    Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Sci 331:76–79Google Scholar
  13. 13.
    Campalans A, Kondorosi A, Crespi M (2004) Enod40, a short open reading frame–containing mRNA, induces cytoplasmic localization of a nuclear RNA binding protein in Medicago truncatula. Plant Cell 16:1047–1059PubMedCentralPubMedGoogle Scholar
  14. 14.
    Wang Y, Fan X, Lin F, He G, Terzaghi W, Zhu D, Deng XW (2014) Arabidopsis noncoding RNA mediates control of photomorphogenesis by red light. PNAS USA 111:10359–10364PubMedGoogle Scholar
  15. 15.
    Liu D, Mewalal R, Hu R, Tuskan GA, Yang X (2017) New technologies accelerate the exploration of non-coding RNAs in horticultural plants. Hortic Res 4:17031PubMedCentralPubMedGoogle Scholar
  16. 16.
    Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nat 462(7274):799–802Google Scholar
  17. 17.
    Csorba T, Questa JI, Sun Q, Dean C (2014) Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. PNAS USA 111:16160–16165PubMedGoogle Scholar
  18. 18.
    Cho J, Paszkowski J (2017) Regulation of rice root development by a retrotransposon acting as a microRNA sponge. Elife 6:e30038PubMedCentralPubMedGoogle Scholar
  19. 19.
    Rabinowitz JC, Snell EE (1941) Distribution of pyridoxal, pyridoxamine and pyridoxine in some natural products. J Biol Chem 176:1157–1167Google Scholar
  20. 20.
    Fitzpatrick TB, Amrhein N, Kappes B, Macheroux P, Tews I, Raschle T (2007) Two independent routes of de novo vitamin B6 biosynthesis: not that different after all. Biochem J 407:1–13Google Scholar
  21. 21.
    John RA (1995) Pyridoxal phosphate dependent enzymes. Bio-chim Biophys Acta 1248:81–96Google Scholar
  22. 22.
    Drewke C, Leistner E (2001) Biosynthesis of vitamin B6 and structurally related derivatives. In: Litwack G, Begley T (eds) Vitamins and hormones, vol 61: advances in research and applications, Academic Press, San Diego, pp 121–125Google Scholar
  23. 23.
    Cellini B, Montioli R, Oppici E, Astegno A, Voltattorni CB (2014) The chaperone role of the pyridoxal 5′-phosphate and its implications for rare diseases involving B6-dependent enzymes. Clin Biochem 47:158–165Google Scholar
  24. 24.
    Ehrenshaft M, Bilski P, Li MY, Chignell CF, Daub ME (1999) A highly conserved sequence is a novel gene involved in de novo vitamin B6 biosynthesis. Proc Natl Acad Sci USA 96:9374–9378Google Scholar
  25. 25.
    Mittenhuber G (2001) Phylogenetic analyses and comparative genomics of vitamin B6 (pyridoxine) and pyridoxal phosphate biosynthesis pathways. J Mol Microbiol Biotechnol 3:1–20Google Scholar
  26. 26.
    Tambasco-Studart M, Titiz O, Raschle T, Forster G, Amrhein N, Fitzpatrick TB (2005) Vitamin B6 biosynthesis in higher plants. Proc Natl Acad Sci USA 102:13687–13692Google Scholar
  27. 27.
    Ruiz A, García-Villoria J, Ormazabal A, Zschocke J, Fiol M, Navarro-Sastre A, Artuch R, Vilaseca MA, Ribes A (2008) A new fatal case of pyridox(am)ine 59-phosphate oxidase (PNPO) deficiency. Mol Genet Metab 93:216–218Google Scholar
  28. 28.
    Shi H, Xiong L, Stevenson B, Lu T, Zhu JK (2002) The Arabidopsis salt overly sensitive 4 mutants uncover a critical role for vitamin B6 in plant salt tolerance. Plant Cell 14:575–588PubMedCentralPubMedGoogle Scholar
  29. 29.
    Shi H, Zhu JK (2002) SOS4, a pyridoxal kinase gene, is required for root hair development in Arabidopsis. Plant Physiol 129:585–593PubMedCentralPubMedGoogle Scholar
  30. 30.
    González E, Danehower D, Daub ME (2007) Vitamer levels, stress response, enzyme activity, and gene regulation of Arabidopsis lines mutant in the pyridoxine/pyridoxamine 59-phosphate oxidase (PDX3) and the pyridoxal kinase (SOS4) genes involved in the vitamin B6 salvage pathway. Plant Physiol 145:985–996PubMedCentralPubMedGoogle Scholar
  31. 31.
    Sang Y, Barbosa JM, Wu H, Locy RD, Singh NK (2007) Identification of a pyridoxine (pyridoxamine) 59-phosphate oxidase from Arabidopsis thaliana. FEBS Lett 581:344–348PubMedGoogle Scholar
  32. 32.
    Sang Y, Locy RD, Goertzen LR, Rashotte AM, Si Y, Kang K, Singh NK (2011) Expression, in vivo localization and phylogenetic analysis of a pyridoxine 59-phosphate oxidase in Arabidopsis thaliana. Plant Physiol Biochem 49:88–95PubMedGoogle Scholar
  33. 33.
    Denslow SA, Walls AA, Daub ME (2005) Regulation of biosynthetic genes and antioxidant properties of vitamin B6 vitamers during plant defense responses. Physiol Mol Plant Pathol 66:244–255Google Scholar
  34. 34.
    Denslow SA, Reuschhoff EE, Daub ME (2007) Regulation of the Arabidopsis thaliana vitamin B6 biosynthesis genes by abiotic stress. Plant Physiol Biochem 45:152–161PubMedGoogle Scholar
  35. 35.
    Havaux M, Eymery F, Porfirova S, Rey P, Dormann P (2005) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17:3451–3469PubMedCentralPubMedGoogle Scholar
  36. 36.
    Bilski P, Li MY, Ehrenshaft M, Daub ME, Chignell CF (2000) Vitamin B6 (pyridoxine) and its derivatives are efficient singlet oxygen quenchers and potential fungal antioxidants. Photochem Photobiol 71:129–134Google Scholar
  37. 37.
    Chen H, Xiong L (2005) Pyridoxine is required for post-embryonic root development and tolerance to osmotic and oxidative stress. Plant J 44:396–408PubMedGoogle Scholar
  38. 38.
    Titiz O, Tambasco-Studart M, Warzych E, Apel K, Amrhein N, Laloi C, Fitzpatrick TB (2006) PDX1 is essential for vitamin B6 biosynthesis, development and stress tolerance in Arabidopsis. Plant J 48:933–946Google Scholar
  39. 39.
    Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71Google Scholar
  40. 40.
    Serrano R, Gaxiola R (1994) Microbial models and salt stress tolerance in plants. Crit Rev Plant Sci 13:121–138Google Scholar
  41. 41.
    Hasegawa PM, Bressan RA, Pardo JM (2000) The dawn of plant salt tolerance genetics. Trends Plant Sci 5:317–319PubMedGoogle Scholar
  42. 42.
    Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410PubMedCentralPubMedGoogle Scholar
  43. 43.
    Hameed A, Bibi N, Akhter J, Iqbal N (2011) Differential changes in antioxidants, proteases, and lipid peroxidation in flag leaves of wheat genotypes under different levels of water deficit conditions. Plant Physiol Biochem 49:178–185PubMedGoogle Scholar
  44. 44.
    Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797PubMedCentralPubMedGoogle Scholar
  45. 45.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874PubMedCentralPubMedGoogle Scholar
  46. 46.
    Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376PubMedGoogle Scholar
  47. 47.
    Tombuloglu H, Kekec G, Sakcali MS, Unver T (2013) Transcriptome-wide identification of R2R3-MYB transcription factors in barley with their boron responsive expression analysis. Mol Genet Genom 288:141–155Google Scholar
  48. 48.
    Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408Google Scholar
  49. 49.
    Matsumoto T, Tanaka T, Sakai H, Amano N, Kanamori H, Kurita K, Kikuta A, Kamiya K, Yamamoto M, Ikawa H, Fujii N, Hori K, Itoh T, Sato K (2011) Comprehensive sequence analysis of 24,783 barley full-length cDNAs derived from 12 clone libraries. Plant Physiol 156:20–28PubMedCentralPubMedGoogle Scholar
  50. 50.
    Karlik E, Gozukirmizi N (2018) Evaluation of barley LncRNA expression analysis in salinity stress. Russ J Genet 54(2):198–204Google Scholar
  51. 51.
    Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, Watt AT, Freier SM, Bennett CF, Sharma A, Bubulya PA, Blencowe BJ, Prasanth SG, Prasanth KV (2010) The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 39:925–938PubMedCentralPubMedGoogle Scholar
  52. 52.
    Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science 329:689–693PubMedCentralPubMedGoogle Scholar
  53. 53.
    Carrieri C, Cimatti L, Biagioli M, Beugnet A, Zucchelli S, Fedele S, Pesce E, Ferrer I, Collavin L, Santoro C, Forrest AR, Carninci P, Biffo S, Stupka E, Gustincich S (2012) Long noncoding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 491:454–457PubMedGoogle Scholar
  54. 54.
    Rinn JL, Chang HY (2012) Genome regulation by long noncoding RNAs. Annu Rev Biochem 81:145–166Google Scholar
  55. 55.
    Huang S, Zeng H, Zhang J, Wei S, Huang L (2011) Characterization of enzymes involved in the interconversions of different forms of vitamin B (6) in tobacco leaves. Plant Physiol Biochem 49:1299–1305PubMedGoogle Scholar
  56. 56.
    Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedGoogle Scholar
  57. 57.
    Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139PubMedGoogle Scholar
  58. 58.
    Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417PubMedGoogle Scholar
  59. 59.
    Osmani AH, May GS, Osmani SA (1999) The extremely conserved pyroA gene of Aspergillus nidulans is required for pyridoxine synthesis and is required indirectly for resistance to photosensitizers. J Biol Chem 274:23565–23569PubMedGoogle Scholar
  60. 60.
    Mooney S, Leuendorf JE, Hendrickson C, Hellmann H (2009) Vitamin B6: a long known compound of surprising complexity. Molecule 14:329–351Google Scholar
  61. 61.
    Zimmermann S, Ehrhardt T, Plesch G, Müller-Röber B (1999) Ion channels in plant signalling. Cell Mol Life Sci 55:183–203Google Scholar
  62. 62.
    Schroeder JI, Hedrich R (1989) Involvement of ion channels and active transport in osmoregulation and signalling of higher plant cells. Trends Biochem Sci 14:187–192Google Scholar
  63. 63.
    Blatt MR, Thiel G (1993) Hormonal control of ion channel gating. Annu Rev Plant Physiol Plant Mol Biol 44:543–567Google Scholar
  64. 64.
    Nürnberger T, Wirtz W, Nennstiel D, Hahlbrock K, Jabs T, Zimmermann S, Scheel D (1997) Signal perception and intracellular signal transduction in plant pathogen defence. J Recept Signal Transduct Res 17:127–136Google Scholar
  65. 65.
    Ralevic V, Burnstock G (1998) Receptors for purines and pyrimidines. Pharmacol Rev 50:413–492PubMedCentralPubMedGoogle Scholar
  66. 66.
    Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472Google Scholar
  67. 67.
    Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171Google Scholar
  68. 68.
    Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743Google Scholar
  69. 69.
    Goff LA, Rinn JL (2015) Linking RNA biology to lncRNAs. Genome Res 25:1456–1465PubMedCentralPubMedGoogle Scholar
  70. 70.
    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, Guigó R (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22:1775–1789PubMedCentralPubMedGoogle Scholar
  71. 71.
    Song D, Yang Y, Yu B, Zheng B, Deng Z, Lu BL, Chen X, Jiang T (2009) Computational prediction of novel non-coding RNAs in Arabidopsis thaliana. BMC Bioinform 10(Suppl 1):S36Google Scholar
  72. 72.
    Di C, Yuan J, Wu Y, Li J, Lin H, Hu L, Zhang T, Qi Y, Gerstein MB, Guo Y, Lu ZJ (2014) Characterization of stress-responsive lncRNAs in Arabidopsis thaliana by integrating expression, epigenetic and structural features. Plant J 80(5):848–861PubMedGoogle Scholar
  73. 73.
    Lu T, Zhu C, Lu G, Guo Y, Zhou Y, Zhang Z, Zhao Y, Li W, Lu Y, Tang W, Feng Q, Han B (2012) Strand-specific RNA-seq reveals widespread occurrence of novel cis natural antisense transcripts in rice. BMC Genom 13:721Google Scholar
  74. 74.
    Zhang YC, Liao JY, Li ZY, Yu Y, Zhang JP, Li QF, Qu LH, Shu WS, Chen YQ (2014) Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice. Genome Biol 15(12):512PubMedCentralPubMedGoogle Scholar
  75. 75.
    Boerner S, McGinnis KM (2012) Computational identification and functional predictions of long noncoding RNA in Zea mays. PLoS ONE 7(8):e43047PubMedCentralPubMedGoogle Scholar
  76. 76.
    Li L, Eichten SR, Shimizu R, Petsch K, Yeh CT, Wu W, Chettoor AM, Givan SA, Cole RA, Fowler JE, Evans MM, Scanlon MJ, Yu J, Schnable PS, Timmermans MC, Springer NM, Muehlbauer GJ (2014) Genome-wide discovery and characterization of maize long non-coding RNAs. Genome Biol 15(2):R40PubMedCentralPubMedGoogle Scholar
  77. 77.
    Xin M, Wang Y, Yao Y, Song N, Hu Z, Qin D, Xie C, Peng H, Ni Z, Sun Q (2011) Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing. BMC Plant Biol 11:61PubMedCentralPubMedGoogle Scholar
  78. 78.
    Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, Radchuk V, Dockter C, Hedley PE, Russell J, Bayer M, Ramsay L, Liu H, Haberer G, Zhang XQ, Zhang Q, Barrero RA, Li L, Taudien S, Groth M, Felder M, Hastie A, Šimková H, Staňková H, Vrána J, Chan S, Muñoz-Amatriaín M, Ounit R, Wanamaker S, Bolser D, Colmsee C, Schmutzer T, Aliyeva-Schnorr L, Grasso S, Tanskanen J, Chailyan A, Sampath D, Heavens D, Clissold L, Cao S, Chapman B, Dai F, Han Y, Li H, Li X, Lin C, McCooke JK, Tan C, Wang P, Wang S, Yin S, Zhou G, Poland JA, Bellgard MI, Borisjuk L, Houben A, Doležel J, Ayling S, Lonardi S, Kersey P, Langridge P, Muehlbauer GJ, Clark MD, Caccamo M, Schulman AH, Mayer KFX, Platzer M, Close TJ, Scholz U, Hansson M, Zhang G, Braumann I, Spannagl M, Li C, Waugh R, Stein N (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544:427–433Google Scholar
  79. 79.
    Rueschhoff EE, Gillikin JW, Sederoff HW, Daub ME (2013) The SOS4 pyridoxal kinase is required for maintenance of vitamin B6-mediated processes in chloroplasts. Plant Physiol Biochem 63:281–291Google Scholar
  80. 80.
    Fort A, Hashimoto K, Yamada D, Salimullah M, Keya CA, Saxena A, Bonetti A, Voineagu I, Bertin N, Kratz A, Noro Y, Wong CH, de Hoon M, Andersson R, Sandelin A, Suzuki H, Wei CL, Koseki H, Consortium FANTOM, Hasegawa Y, Forrest AR, Carninci P (2014) Deep transcriptome profiling of mammalian stem cells supports a regulatory role for retrotransposons in pluripotency maintenance. Nat Genet 46:558–566PubMedGoogle Scholar
  81. 81.
    Yamada A, Yu P, Lin W, Okugawa Y, Boland CR, Goel A (2018) A RNA-Sequencing approach for the identification of novel long non-coding RNA biomarkers in colorectal cancer. Sci Rep 8(1):575PubMedCentralPubMedGoogle Scholar
  82. 82.
    Sheik Mohamed J, Gaughwin PM, Lim B, Robson P, Lipovich L (2010) Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells. RNA 16:324–337PubMedCentralPubMedGoogle Scholar
  83. 83.
    Guil S, Soler M, Portela A, Carrère J, Fonalleras E, Gómez A, Villanueva A, Esteller M (2012) Intronic RNAs mediate EZH2 regulation of epigenetic targets. Nat Struct Mol Biol 19:664–670PubMedGoogle Scholar
  84. 84.
    Qiu JJ, Wang Y, Ding JX, Jin HY, Yang G, Hua KQ (2015) The long non-coding RNA HOTAIR promotes the proliferation of serous ovarian cancer cells through the regulation of cell cycle arrest and apoptosis. Exp Cell Res 333(2):238–248PubMedGoogle Scholar
  85. 85.
    Kampa D, Cheng J, Kapranov P, Yamanaka M, Brubaker S, Cawley S, Drenkow J, Piccolboni A, Bekiranov S, Helt G, Tammana H, Gingeras TR (2004) Novel RNAs identified from an in-depth analysis of the transcriptome of human chromosomes 21 and 22. Genome Res 14:331–342PubMedCentralPubMedGoogle Scholar
  86. 86.
    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, Nori F, Ohara O, Okazaki Y, Orlando V, Pang KC, Pavan WJ, Pavesi G, Pesole G, Petrovsky N, Piazza S, Reed J, Reid JF, Ring BZ, Ringwald M, Rost B, Ruan Y, Salzberg SL, Sandelin A, Schneider C, Schönbach C, Sekiguchi K, Semple CA, Seno S, Sessa L, Sheng Y, Shibata Y, Shimada H, Shimada K, Silva D, Sinclair B, Sperling S, Stupka E, Sugiura K, Sultana R, Takenaka Y, Taki K, Tammoja K, Tan SL, Tang S, Taylor MS, Tegner J, Teichmann SA, Ueda HR, van Nimwegen E, Verardo R, Wei CL, Yagi K, Yamanishi H, Zabarovsky E, Zhu S, Zimmer A, Hide W, Bult C, Grimmond SM, Teasdale RD, Liu ET, Brusic V, Quackenbush J, Wahlestedt C, Mattick JS, Hume DA, Kai C, Sasaki D, Tomaru Y, Fukuda S, Kanamori-Katayama M, Suzuki M, Aoki J, Arakawa T, Iida J, Imamura K, Itoh M, Kato T, Kawaji H, Kawagashira N, Kawashima T, Kojima M, Kondo S, Konno H, Nakano K, Ninomiya N, Nishio T, Okada M, Plessy C, Shibata K, Shiraki T, Suzuki S, Tagami M, Waki K, Watahiki A, Okamura-Oho Y, Suzuki H, Kawai J, Hayashizaki Y, FANTOM Consortium, RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group) (2005) The transcriptional landscape of the mammalian genome. Science 309:1559–1563PubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of BiotechnologyIstanbul UniversityVeznecilerTurkey
  2. 2.Department of Molecular Biology and GeneticsIstanbul UniversityVeznecilerTurkey
  3. 3.Department of Molecular Biology and Geneticsİstinye UniversityZeytinburnuTurkey

Personalised recommendations