Skip to main content
SpringerLink
Log in

Epigenetic regulation by long noncoding RNAs in plants

  • Review
  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Many eukaryotes, including plants, produce a large number of long noncoding RNAs (lncRNAs). Growing number of lncRNAs are being reported to have regulatory roles in various developmental processes. Emerging mechanisms underlying the function of lncRNAs indicate that lncRNAs are versatile regulatory molecules. They function as potent cis- and trans-regulators of gene expression, including the formation of modular scaffolds that recruit chromatin-modifying complexes to target chromatin. LncRNAs have also been reported in plants. Here, we describe our current understanding on potential roles of lncRNA in plants.

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

Similar content being viewed by others

Abbreviations

ncRNA:

Noncoding RNA

lncRNA:

Long noncoding RNA

miRNA:

Micro RNA

siRNA:

Small interfering RNA

piRNA:

Piwi-interacting RNA

RNA-seq:

RNA sequencing

lincRNA:

Long intergenic ncRNA

PHD:

Plant homeodomain

PRC2:

Polycomb repressive complex 2

References

  • Alvarez-Venegas R, Avramova Z (2001) Two Arabidopsis homologs of the animal trithorax genes: a new structural domain is a signature feature of the trithorax gene family. Gene 271:215–221

    Google Scholar 

  • Aubert D, Chen L, Moon YH, Martin D, Castle LA, Yang CH, Sung ZR (2001) EMF1, a novel protein involved in the control of shoot architecture and flowering in Arabidopsis. Plant Cell 13:1865–1875

    PubMed  CAS  Google Scholar 

  • Barlow DP, Stoger R, Herrmann BG, Saito K, Schweifer N (1991) The mouse insulin-like growth factor type-2 receptor is imprinted and closely linked to the Tme locus. Nature 349:84–87

    Article  PubMed  CAS  Google Scholar 

  • Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164–167

    Article  PubMed  CAS  Google Scholar 

  • Ben Amor B, Wirth S, Merchan F, Laporte P, d'Aubenton-Carafa Y et al (2009) Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res 19:57–69

    Article  PubMed  CAS  Google Scholar 

  • Bernstein E, Allis CD (2005) RNA meets chromatin. Genes Dev 19:1635–1655

    Article  PubMed  CAS  Google Scholar 

  • Berr A, Xu L, Gao J, Cognat V, Steinmetz A, Dong A, Shen WH (2009) SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering. Plant Physiol 151: 1476–1485

    Google Scholar 

  • Bezhani S, Winter C, Hershman S, Wagner JD, Kennedy JF, Kwon CS, Pfluger J, Su Y, Wagner D (2007) Unique, shared, and redundant roles for the Arabidopsis SWI/SNF chromatin remodeling ATPases BRAHMA and SPLAYED. Plant Cell 19:403–416

    Article  PubMed  CAS  Google Scholar 

  • Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR et al (2007) Identification and analysis of functional elements in 1 % of the human genome by the ENCODE pilot project. Nature 447:799–816

    Article  PubMed  CAS  Google Scholar 

  • Bratzel F, Lopez-Torrejon G, Koch M, Del Pozo JC, Calonje M (2010) Keeping cell identity in Arabidopsis requires PRC1 RING-finger homologs that catalyze H2A monoubiquitination. Curr Biol 20:1853–1859

    Article  PubMed  CAS  Google Scholar 

  • Brown CJ, Ballabio A, Rupert JL, Lafreniere RG, Grompe M, Tonlorenzi R, Willard HF (1991) A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 349:38–44

    Article  PubMed  CAS  Google Scholar 

  • Cao R, Tsukada Y, Zhang Y (2005) Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell 20:845–854

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Chaumeil J, Le Baccon P, Wutz A, Heard E (2006) A novel role for Xist RNA in the formation of a repressive nuclear compartment into which genes are recruited when silenced. Genes Dev 20:2223–2237

    Article  PubMed  CAS  Google Scholar 

  • Chitwood DH, Timmermans MC (2010) Small RNAs are on the move. Nature 467:415–419

    Article  PubMed  CAS  Google Scholar 

  • De Lucia F, Dean C (2010) Long non-coding RNAs and chromatin regulation. Curr Opin Plant Biol 14:168–173

    Google Scholar 

  • De Lucia F, Crevillen P, Jones AM, Greb T, Dean C (2008) A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci U S A 105:16831–16836

    Article  PubMed  Google Scholar 

  • De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, Tusi BK, Muller H, Ragoussis J, Wei CL, Natoli G (2010) A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol 8:e1000384

    Article  PubMed  Google Scholar 

  • Feng J, Bi C, Clark BS, Mady R, Shah P, Kohtz JD (2006) The Evf-2 noncoding RNA is transcribed from the Dlx-5/6 ultraconserved region and functions as a Dlx-2 transcriptional coactivator. Genes Dev 20:1470–1484

    Article  PubMed  CAS  Google Scholar 

  • 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 39:1033–1037

    Article  PubMed  CAS  Google Scholar 

  • Fujita T, Kouchi H, Ichikawa T, Syono K (1993) Isolation and characterization of a cDNA that encodes a novel proteinase inhibitor I from a tobacco genetic tumor. Plant Cell Physiol 34:137–142

    PubMed  CAS  Google Scholar 

  • Ghildiyal M, Zamore PD (2009) Small silencing RNAs: an expanding universe. Nat Rev Genet 10:94–108

    Article  PubMed  CAS  Google Scholar 

  • Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, Yang X, Amit I, Meissner A, Regev A, Rinn JL, Root DE, Lander ES (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477:295–300

    Article  PubMed  CAS  Google Scholar 

  • Helliwell CA, Robertson M, Finnegan EJ, Buzas DM, Dennis ES (2011) Vernalization-repression of Arabidopsis FLC requires promoter sequences but not antisense transcripts. PLoS One 6:e21513

    Article  PubMed  CAS  Google Scholar 

  • Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:76–79

    Article  PubMed  CAS  Google Scholar 

  • Kaneko S, Li G, Son J, Xu CF, Margueron R, Neubert TA, Reinberg D (2010) Phosphorylation of the PRC2 component Ezh2 is cell cycle-regulated and up-regulates its binding to ncRNA. Genes Dev 24:2615–2620

    Article  PubMed  CAS  Google Scholar 

  • Karreth FA, Tay Y, Perna D, Ala U, Tan SM et al (2011) In vivo identification of tumor- suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma. Cell 147:382–395

    Article  PubMed  CAS  Google Scholar 

  • Kim DH, Doyle MR, Sung S, Amasino RM (2009) Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol 25:277–299

    Article  PubMed  CAS  Google Scholar 

  • Kim DH, Sung S (2012) Environmentally coordinated epigenetic silencing of FLC by protein and long noncoding RNA components. Curr Opin Plant Biol 15:51–56

    Article  PubMed  CAS  Google Scholar 

  • Kim DH, Sung S (2013) Coordination of the vernalization response through a VIN3 and FLC gene family regulatory network in Arabidopsis. Plant Cell 25:454–469

    Article  PubMed  CAS  Google Scholar 

  • Kim SY, He Y, Jacob Y, Noh YS, Michaels S, Amasino R (2005) Establishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Plant Cell 17:3301–3310

    Article  PubMed  CAS  Google Scholar 

  • Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM et al (2010) Widespread transcription at neuronal activity-regulated enhancers. Nature 465:182–187

    Article  PubMed  CAS  Google Scholar 

  • Ko JH, Mitina I, Tamada Y, Hyun Y, Choi Y, Amasino RM, Noh B, Noh YS (2010) Growth habit determination by the balance of histone methylation activities in Arabidopsis. EMBO J 29:3208–3215

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921

    Article  PubMed  CAS  Google Scholar 

  • Li L, Wang X, Stolc V, Li X, Zhang D, Su N, Tongprasit W, Li S, Cheng Z, Wang J, Deng XW (2006) Genome-wide transcription analyses in rice using tiling microarrays. Nat Genet 38:124–129

    Article  PubMed  CAS  Google Scholar 

  • Liu C, Muchhal US, Raghothama KG (1997) Differential expression of TPS11, a phosphate starvation-induced gene in tomato. Plant Mol Biol 33:867–874

    Article  PubMed  CAS  Google Scholar 

  • 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 24:4333–4345

    Article  PubMed  CAS  Google Scholar 

  • Mylne JS, Barrett L, Tessadori F, Mesnage S, Johnson L, 607 Bernatavichute YV, Jacobsen SE, Fransz P, Dean C 608 (2006) LHP1, the Arabidopsis homologue of 609 HETEROCHROMATIN PROTEIN1, is required for epige- 610 netic silencing of FLC. Proc Natl Acad Sci U S A 103:5012– 611 5017

    Google Scholar 

  • Matsui A, Ishida J, Morosawa T, Okamoto M, Kim JM et al (2010) Arabidopsis tiling array analysis to identify the stress-responsive genes. Methods Mol Biol 639:141–155

    Article  PubMed  CAS  Google Scholar 

  • Mercer TR, Gerhardt DJ, Dinger ME, Crawford J, Trapnell C, Jeddeloh JA, Mattick JS, Rinn JL (2011) Targeted RNA sequencing reveals the deep complexity of the human transcriptome. Nat Biotechnol 30:99–104

    Article  PubMed  Google Scholar 

  • Nagano T, Mitchell JA, Sanz LA, Pauler FM, Ferguson-Smith AC, Feil R, Fraser P (2008) The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science 322:1717–1720

    Article  PubMed  CAS  Google Scholar 

  • Ng DW, Wang T, Chandrasekharan MB, Aramayo R, Kertbundit S, Hall TC (2007) Plant SET domain-containing proteins: structure, function and regulation. Biochim Biophys Acta 1769:316–329

    Article  PubMed  CAS  Google Scholar 

  • Okazaki Y, Furuno M, Kasukawa T, Adachi J, Bono H 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 

  • Paul J, Duerksen JD (1975) Chromatin-associated RNA content of heterochromatin and euchromatin. Mol Cell Biochem 9:9–16

    Google Scholar 

  • Pien S, Fleury D, Mylne JS, Crevillen P, Inze D, Avramova Z, Dean C, Grossniklaus U (2008) ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20:580–588

    Article  PubMed  CAS  Google Scholar 

  • Rehrauer H, Aquino C, Gruissem W, Henz SR, Hilson P et al (2010) AGRONOMICS1: a new resource for Arabidopsis transcriptome profiling. Plant Physiol 152:487–499

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Rohrig H, Schmidt J, Miklashevichs E, Schell J, John M (2002) Soybean ENOD40 encodes two peptides that bind to sucrose synthase. Proc Natl Acad Sci U S A 99:1915–1920

    Article  PubMed  CAS  Google Scholar 

  • Saleh A, Alvarez-Venegas R, Avramova Z (2008a) Dynamic and stable histone H3 methylation patterns at the Arabidopsis FLC and AP1 loci. Gene 423:43–47

    Article  PubMed  CAS  Google Scholar 

  • Saleh A, Alvarez-Venegas R, Yilmaz M, Le O, Hou G, Sadder M, Al-Abdallat A, Xia Y, Lu G, Ladunga I, Avramova Z (2008b) The highly similar Arabidopsis homologs of trithorax ATX1 and ATX2 encode proteins with divergent biochemical functions. Plant Cell 20:568–579

    Article  PubMed  CAS  Google Scholar 

  • Scheuermann JC, de Ayala Alonso AG, Oktaba K, Ly-Hartig N, McGinty RK, Fraterman S, Wilm M, Muir TW, Muller J (2010) Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB. Nature 465:243–247

    Article  PubMed  CAS  Google Scholar 

  • Sun Q, Csorba T, Skourti-Stathaki K, Proudfoot NJ, Dean C (2013) R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340:619–621

    Article  PubMed  CAS  Google Scholar 

  • Sung S, Amasino RM (2004a) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164

    Article  PubMed  CAS  Google Scholar 

  • Sung S, Amasino RM (2004b) Vernalization and epigenetics: how plants remember winter. Curr Opin Plant Biol 7:4–10

    Article  PubMed  CAS  Google Scholar 

  • Sung S, He Y, Eshoo TW, Tamada Y, Johnson L, Nakahigashi K, Goto K, Jacobsen SE, Amasino RM (2006) Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat Genet 38:706–710

    Article  PubMed  CAS  Google Scholar 

  • Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462:799–802

    Article  PubMed  CAS  Google Scholar 

  • Tamada Y, Yun JY, Woo SC, Amasino RM (2009) ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C. Plant Cell 21:3257–3269

    Article  PubMed  CAS  Google Scholar 

  • Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q (2010) The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 39:925–938

    Google Scholar 

  • 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 329:689–693

    Article  PubMed  CAS  Google Scholar 

  • Turck F, Roudier F, Farrona S, Martin-Magniette ML, Guillaume E, Buisine N, Gagnot S, Martienssen RA, Coupland G, Colot V (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3:e86

    Article  PubMed  Google Scholar 

  • Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R et al (2011) A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472:120–124

    Article  PubMed  CAS  Google Scholar 

  • Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, Goodhead I, Penkett CJ, Rogers J, Bahler J (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453:1239–1243

    Article  PubMed  CAS  Google Scholar 

  • Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, Helliwell CA (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc Natl Acad Sci U S A 103:14631–14636

    Article  PubMed  Google Scholar 

  • Xu L, Shen WH (2008) Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Curr Biol 18:1966–1971

    Article  PubMed  CAS  Google Scholar 

  • Yap KL, Li S, Munoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ, Zhou MM (2010) Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell 38:662–674

    Article  PubMed  CAS  Google Scholar 

  • Yun JY, Tamada Y, Kang YE, Amasino RM (2012) Arabidopsis trithorax-related3/SET domain GROUP2 is required for the winter-annual habit of Arabidopsis thaliana. Plant Cell Physiol 53:834–846

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Germann S, Blus BJ, Khorasanizadeh S, Gaudin V, Jacobsen SE (2007) The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat Struct Mol Biol 14:869–871

    Article  PubMed  CAS  Google Scholar 

  • 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:R62

    Article  PubMed  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  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

J.B. Heo is supported by a grant from the Next-Generation BioGreen 21 Program (SSAC, grant no.: PJ00951601) and by the National Research Foundation of Korea (NRF-MEST no. 2011–0013137). S. Sung is supported by the University of Texas at Austin, National Science Foundation (IOS-0950785) and National Institute of Health (R01GM100108).

Author information

Authors and Affiliations

  1. Department of Molecular Biotechnology, Dong-A University, Busan, 604-714, South Korea

    Jae Bok Heo

  2. Department of Biotechnology, Dong-A University, Busan, 604-714, South Korea

    Yong-Suk Lee

  3. Department of Molecular Biosciences and Institute for Cellular and Molecular Biology, University of Texas, Austin, TX, 78712, USA

    Sibum Sung

Authors
  1. Jae Bok Heo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yong-Suk Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sibum Sung
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sibum Sung.

Additional information

Responsible editors: Brian P. Chadwick, Kristin C. Scott, and Beth A. Sullivan

Jae Bok Heo and Yong-Suk Lee contributed equally to the work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heo, J.B., Lee, YS. & Sung, S. Epigenetic regulation by long noncoding RNAs in plants. Chromosome Res 21, 685–693 (2013). https://doi.org/10.1007/s10577-013-9392-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-013-9392-6

Keywords

Search

Navigation