Advertisement

Bioinformatics Approaches to Studying Plant Long Noncoding RNAs (lncRNAs): Identification and Functional Interpretation of lncRNAs from RNA-Seq Data Sets

  • Hai-Xi Sun
  • Nam-Hai ChuaEmail author
Part of the Methods in Molecular Biology book series (MIMB, volume 1933)

Abstract

Long noncoding RNAs (lncRNAs) play important roles in regulating various biological processes including growth and stress responses in plants. RNA-seq data sets provide a good resource to exploring the noncoding transcriptome and studying their comprehensive interactions with the coding transcriptome. Here, we describe computational procedures for studying plant lncRNAs including long intergenic noncoding RNAs (lincRNAs) and long noncoding natural antisense transcripts (lncNATs). Bioinformatics tools for transcriptome assembly, lncRNA identification, and functional interpretations are included. Finally, we also introduce PLncDB, a user-friendly database that provides comprehensive information of plant lncRNAs for researchers to compare their own data sets to those in public database.

Key words

lincRNAs lncNATs RNA-seq cis-regulation lncRNA-miRNA interaction RNA-DNA triplex 

Notes

Acknowledgment

We thank Jun Liu and Huan Wang for developing the above bioinformatics methods for lincRNA and lncNAT analyses and Jingjing Jin for constructing PLncDB. This work was funded in part by Singapore NRF RSSS Grant NRF-RSSS-002.

References

  1. 1.
    Liu J, Jung C, Xu J, Wang H, Deng S, Bernad L, Arenas-Huertero C, Chua NH (2012) Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 24(11):4333–4345.  https://doi.org/10.1105/tpc.112.102855CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Wang H, Chung PJ, Liu J, Jang IC, Kean MJ, Xu J, Chua NH (2014) Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis. Genome Res 24(3):444–453.  https://doi.org/10.1101/gr.165555.113CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Ariel F, Jegu T, Latrasse D, Romero-Barrios N, Christ A, Benhamed M, Crespi M (2014) Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop. Mol Cell 55(3):383–396.  https://doi.org/10.1016/j.molcel.2014.06.011CrossRefGoogle Scholar
  4. 4.
    Bardou F, Ariel F, Simpson CG, Romero-Barrios N, Laporte P, Balzergue S, Brown JW, Crespi M (2014) Long noncoding RNA modulates alternative splicing regulators in Arabidopsis. Dev Cell 30(2):166–176.  https://doi.org/10.1016/j.devcel.2014.06.017CrossRefGoogle Scholar
  5. 5.
    Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462(7274):799–802.  https://doi.org/10.1038/nature08618CrossRefGoogle Scholar
  6. 6.
    Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331(6013):76–79.  https://doi.org/10.1126/science.1197349CrossRefGoogle Scholar
  7. 7.
    Kim DH, Sung S (2017) Vernalization-triggered intragenic chromatin loop formation by long noncoding RNAs. Dev Cell 40(3):302–312 e304.  https://doi.org/10.1016/j.devcel.2016.12.021CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    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):512.  https://doi.org/10.1186/s13059-014-0512-1CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Ding J, Lu Q, Ouyang Y, Mao H, Zhang P, Yao J, Xu C, Li X, Xiao J, Zhang Q (2012) A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc Natl Acad Sci U S A 109(7):2654–2659.  https://doi.org/10.1073/pnas.1121374109CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Seo JS, Sun HX, Park BS, Huang CH, Yeh SD, Jung C, Chua NH (2017) ELF18-INDUCED LONG-NONCODING RNA associates with mediator to enhance expression of innate immune response genes in Arabidopsis. Plant Cell 29(5):1024–1038.  https://doi.org/10.1105/tpc.16.00886CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Zhu QH, Stephen S, Taylor J, Helliwell CA, Wang MB (2014) Long noncoding RNAs responsive to Fusarium oxysporum infection in Arabidopsis thaliana. New Phytol 201(2):574–584.  https://doi.org/10.1111/nph.12537CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39(8):1033–1037.  https://doi.org/10.1038/ng2079CrossRefGoogle Scholar
  13. 13.
    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):848–861.  https://doi.org/10.1111/tpj.12679CrossRefGoogle Scholar
  14. 14.
    Liu F, Marquardt S, Lister C, Swiezewski S, Dean C (2010) Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327(5961):94–97.  https://doi.org/10.1126/science.1180278CrossRefGoogle Scholar
  15. 15.
    Wu HJ, Wang ZM, Wang M, Wang XJ (2013) Widespread long noncoding RNAs as endogenous target mimics for microRNAs in plants. Plant Physiol 161(4):1875–1884.  https://doi.org/10.1104/pp.113.215962CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Berardini TZ, Reiser L, Li D, Mezheritsky Y, Muller R, Strait E, Huala E (2015) The Arabidopsis information resource: making and mining the "gold standard" annotated reference plant genome. Genesis 53(8):474–485.  https://doi.org/10.1002/dvg.22877CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Cheng CY, Krishnakumar V, Chan AP, Thibaud-Nissen F, Schobel S, Town CD (2017) Araport11: a complete reannotation of the Arabidopsis thaliana reference genome. Plant J 89(4):789–804.  https://doi.org/10.1111/tpj.13415CrossRefGoogle Scholar
  18. 18.
    Jin J, Liu J, Wang H, Wong L, Chua NH (2013) PLncDB: plant long non-coding RNA database. Bioinformatics 29(8):1068–1071.  https://doi.org/10.1093/bioinformatics/btt107CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Zhao Y, Li H, Fang S, Kang Y, Wu W, Hao Y, Li Z, Bu D, Sun N, Zhang MQ, Chen R (2016) NONCODE 2016: an informative and valuable data source of long non-coding RNAs. Nucleic Acids Res 44(D1):D203–D208.  https://doi.org/10.1093/nar/gkv1252CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Szczesniak MW, Rosikiewicz W, Makalowska I (2016) CANTATAdb: a collection of plant long non-coding RNAs. Plant Cell Physiol 57(1):e8.  https://doi.org/10.1093/pcp/pcv201CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Yi X, Zhang Z, Ling Y, Xu W, Su Z (2015) PNRD: a plant non-coding RNA database. Nucleic Acids Res 43(Database issue):D982–D989.  https://doi.org/10.1093/nar/gku1162CrossRefGoogle Scholar
  22. 22.
    The RC (2017) RNAcentral: a comprehensive database of non-coding RNA sequences. Nucleic Acids Res 45(D1):D128–D134.  https://doi.org/10.1093/nar/gkw1008CrossRefGoogle Scholar
  23. 23.
    Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M, Satou M, Kim JM, Kobayashi N, Toyoda T, Shinozaki K, Seki M (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49(8):1135–1149.  https://doi.org/10.1093/pcp/pcn101CrossRefGoogle Scholar
  24. 24.
    Oh S, Park S, van Nocker S (2008) Genic and global functions for Paf1C in chromatin modification and gene expression in Arabidopsis. PLoS Genet 4(8):e1000077.  https://doi.org/10.1371/journal.pgen.1000077CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10(6):R62.  https://doi.org/10.1186/gb-2009-10-6-r62CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Charron JB, He H, Elling AA, Deng XW (2009) Dynamic landscapes of four histone modifications during deetiolation in Arabidopsis. Plant Cell 21(12):3732–3748.  https://doi.org/10.1105/tpc.109.066845CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Haudry A, Platts AE, Vello E, Hoen DR, Leclercq M, Williamson RJ, Forczek E, Joly-Lopez Z, Steffen JG, Hazzouri KM, Dewar K, Stinchcombe JR, Schoen DJ, Wang X, Schmutz J, Town CD, Edger PP, Pires JC, Schumaker KS, Jarvis DE, Mandakova T, Lysak MA, van den Bergh E, Schranz ME, Harrison PM, Moses AM, Bureau TE, Wright SI, Blanchette M (2013) An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nat Genet 45(8):891–898.  https://doi.org/10.1038/ng.2684CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Levin JZ, Yassour M, Adiconis X, Nusbaum C, Thompson DA, Friedman N, Gnirke A, Regev A (2010) Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat Methods 7(9):709–715.  https://doi.org/10.1038/nmeth.1491CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360.  https://doi.org/10.1038/nmeth.3317CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33(3):290–295.  https://doi.org/10.1038/nbt.3122CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL (2016) Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 11(9):1650–1667.  https://doi.org/10.1038/nprot.2016.095CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16(6):276–277CrossRefGoogle Scholar
  33. 33.
    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(Web Server issue):W345–W349.  https://doi.org/10.1093/nar/gkm391CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Wu HJ, Ma YK, Chen T, Wang M, Wang XJ (2012) PsRobot: a web-based plant small RNA meta-analysis toolbox. Nucleic Acids Res 40(Web Server issue):W22–W28.  https://doi.org/10.1093/nar/gks554CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Buske FA, Bauer DC, Mattick JS, Bailey TL (2012) Triplexator: detecting nucleic acid triple helices in genomic and transcriptomic data. Genome Res 22(7):1372–1381.  https://doi.org/10.1101/gr.130237.111CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079.  https://doi.org/10.1093/bioinformatics/btp352CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42(Database issue):D68–D73.  https://doi.org/10.1093/nar/gkt1181CrossRefGoogle Scholar
  38. 38.
    Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29(1):24–26.  https://doi.org/10.1038/nbt.1754CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratory of Plant Molecular BiologyRockefeller UniversityNew YorkUSA
  2. 2.TEMASEK Life Sciences LaboratoryNational University of SingaporeSingaporeSingapore

Personalised recommendations