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Functions of long intergenic non-coding (linc) RNAs in plants

  • JPR Symposium
  • Expanding plant non-coding RNA world
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Abstract

Whole transcriptome analyses in many organisms have revealed that most transcribed RNAs do not encode proteins. These non-coding RNAs likely contribute to the regulation of gene expression during the development of multicellular organisms. In eukaryotes, the roles of small RNAs, one class of non-coding RNAs, in transcriptional and post-transcriptional regulation have been well characterized. However, the functions of a second class of non-coding RNAs, long intergenic noncoding (linc) RNAs, are relatively unknown, especially in plants. Recent advances in RNA-seq and tiling microarray technologies have revealed the presence of many lincRNAs across plant species. This review focuses on the functions of lincRNAs that have been recently reported in plants. One of the most well characterized functions of lincRNAs is to epigenetically regulate gene expression by recruiting proteins for chromosome modification to specific loci. Second, lincRNAs are known to inhibit the physical interaction between microRNAs (miRNAs) and their target mRNAs thus controling protein levels of the target mRNAs. Lastly, lincRNAs control alternative splicing by binding and sequestering the proteins required for alternative splicing.

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References

  • Aichinger E, Villar CB, Di Mambro R, Sabatini S, Kohler C (2011) The CHD3 chromatin remodeler PICKLE and polycomb group proteins antagonistically regulate meristem activity in the Arabidopsis root. Plant Cell 23:1047–1060

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aloia L, Di Stefano B, Di Croce L (2013) Polycomb complexes in stem cells and embryonic development. Development 140:2525–2534

    Article  PubMed  CAS  Google Scholar 

  • 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 30:166–176

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith DW, Benfey PN (2003) A gene expression map of the Arabidopsis root. Science 302:1956–1960

    Article  PubMed  CAS  Google Scholar 

  • Birnbaum K, Jung JW, Wang JY, Lambert GM, Hirst JA, Galbraith DW, Benfey PN (2005) Cell type-specific expression profiling in plants via cell sorting of protoplasts from fluorescent reporter lines. Nat Methods 2:615–619

    Article  PubMed  CAS  Google Scholar 

  • Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318:801–806

    Article  PubMed  CAS  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  PubMed  PubMed Central  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  PubMed Central  CAS  Google Scholar 

  • Chen J, Quan M, Zhang D (2015) Genome-wide identification of novel long non-coding RNAs in Populus tomentosa tension wood, opposite wood and normal wood xylem by RNA-sEq. Planta 241:125–143

    Article  PubMed  CAS  Google Scholar 

  • Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. Plant Cell 18:412–421

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chu C, Qu K, Zhong FL, Artandi SE, Chang HY (2011) Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol Cell 44:667–678

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Consortium EP (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489:57–74

    Article  CAS  Google Scholar 

  • Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F et al (2012) Landscape of transcription in human cells. Nature 489:101–108

    Article  PubMed  PubMed Central  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 

  • Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L et al (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477:295–300

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hekimoglu B, Ringrose L (2009) Non-coding RNAs in polycomb/trithorax regulation. RNA Biol 6:129–137

    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 

  • Iyer-Pascuzzi AS, Benfey PN (2010) Fluorescence-activated cell sorting in plant developmental biology. Methods Mol Biol 655:313–319

    Article  PubMed  CAS  Google Scholar 

  • Jouannet V, Crespi M (2011) Long Nonprotein-Coding RNAs in Plants. Prog Mol Subcell Biol 51:179–200

    Article  PubMed  CAS  Google Scholar 

  • Li L, Liu B, Wapinski OL, Tsai MC, Qu K, Zhang J, Carlson JC, Lin M, Fang F, Gupta RA et al (2013) Targeted disruption of Hotair leads to homeotic transformation and gene derepression. Cell Rep 5:3–12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li L, Eichten SR, Shimizu R, Petsch K, Yeh CT, Wu W, Chettoor AM, Givan SA, Cole RA, Fowler JE et al (2014) Genome-wide discovery and characterization of maize long non-coding RNAs. Genome Biol 15:R40

    Article  PubMed  PubMed Central  Google Scholar 

  • Li S, Yamada M, Han X, Ohler U, Benfey PN (2016) High-Resolution Expression Map of the Arabidopsis Root Reveals Alternative Splicing and lincRNA Regulation. Dev Cell 39:508–522

    Article  PubMed  PubMed Central  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  PubMed Central  CAS  Google Scholar 

  • MacIntosh GC, Wilkerson C, Green PJ (2001) Identification and analysis of Arabidopsis expressed sequence tags characteristic of non-coding RNAs. Plant Physiol 127:765–776

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marker C, Zemann A, Terhorst T, Kiefmann M, Kastenmayer JP, Green P, Bachellerie JP, Brosius J, Huttenhofer A (2002) Experimental RNomics: identification of 140 candidates for small non-messenger RNAs in the plant Arabidopsis thaliana. Curr Biol 12:2002–2013

    Article  PubMed  CAS  Google Scholar 

  • Martin AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de La Pena A, Leyva A, Paz-Ares J (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24:559–567

    Article  PubMed  CAS  Google Scholar 

  • Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M et al (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49:1135–1149

    Article  PubMed  CAS  Google Scholar 

  • Okamoto M, Tatematsu K, Matsui A, Morosawa T, Ishida J, Tanaka M, Endo TA, Mochizuki Y, Toyoda T, Kamiya Y et al (2010) Genome-wide analysis of endogenous abscisic acid-mediated transcription in dry and imbibed seeds of Arabidopsis using tiling arrays. Plant J 62:39–51

    Article  PubMed  CAS  Google Scholar 

  • Petricka JJ, Schauer MA, Megraw M, Breakfield NW, Thompson JW, Georgiev S, Soderblom EJ, Ohler U, Moseley MA, Grossniklaus U et al (2012) The protein expression landscape of the Arabidopsis root. Proc Natl Acad Sci USA 109:6811–6818

    Article  PubMed  Google Scholar 

  • Ponting CP, Oliver PL, Reik W (2009) Evolution and functions of long noncoding RNAs. Cell 136:629–641

    Article  PubMed  CAS  Google Scholar 

  • Qi X, Xie S, Liu Y, Yi F, Yu J (2013) Genome-wide annotation of genes and noncoding RNAs of foxtail millet in response to simulated drought stress by deep sequencing. Plant Mol Biol 83:459–473

    Article  PubMed  CAS  Google Scholar 

  • Reddy AS, Shad Ali G (2011) Plant serine/arginine-rich proteins: roles in precursor messenger RNA splicing, plant development, and stress responses. Wiley Interdiscip Rev RNA 2:875–889

    Article  PubMed  CAS  Google Scholar 

  • Rymarquis LA, Kastenmayer JP, Huttenhofer AG, Green PJ (2008) Diamonds in the rough: mRNA-like non-coding RNAs. Trends Plant Sci 13:329–334

    Article  PubMed  CAS  Google Scholar 

  • Schindler S, Szafranski K, Hiller M, Ali GS, Palusa SG, Backofen R, Platzer M, Reddy AS (2008) Alternative splicing at NAGNAG acceptors in Arabidopsis thaliana SR and SR-related protein-coding genes. BMC Genomics 9:159

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shuai P, Liang D, Tang S, Zhang Z, Ye CY, Su Y, Xia X, Yin W (2014) Genome-wide identification and functional prediction of novel and drought-responsive lincRNAs in Populus trichocarpa. J Exp Bot 65:4975–4983

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):S36

    Article  CAS  Google Scholar 

  • Wang L, Zhao S, Gu C, Zhou Y, Zhou H, Ma J, Cheng J, Han Y (2013) Deep RNA-Seq uncovers the peach transcriptome landscape. Plant Mol Biol 83:365–377

    Article  PubMed  CAS  Google Scholar 

  • 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. Proc Natl Acad Sci USA 111:10359–10364

    Article  PubMed  CAS  Google Scholar 

  • Wu HJ, Wang ZM, Wang M, Wang XJ (2013) Widespread long noncoding RNAs as endogenous target mimics for microRNAs in plants. Plant Physiol 161:1875–1884

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 11:61

    Article  PubMed  PubMed Central  CAS  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 

  • 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 15:512

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

I thank Erin Sparks, Jazz Dickinson, Eric Rogers and Kevin Lehner for comments on the manuscript.

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Correspondence to Masashi Yamada.

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Yamada, M. Functions of long intergenic non-coding (linc) RNAs in plants. J Plant Res 130, 67–73 (2017). https://doi.org/10.1007/s10265-016-0894-0

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  • DOI: https://doi.org/10.1007/s10265-016-0894-0

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