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The Involvement of Long Noncoding RNAs in Response to Plant Stress

  • Akihiro MatsuiEmail author
  • Motoaki SekiEmail author
Part of the Methods in Molecular Biology book series (MIMB, volume 1933)

Abstract

Plant growth and productivity are greatly impacted by environmental stresses. Therefore, plants have evolved mechanisms which allow them to adapt to abiotic stresses through alterations in gene expression and metabolism. In recent years, studies have investigated the role of long noncoding RNA (lncRNA) in regulating gene expression in plants and characterized their involvement in various biological functions through their regulation of DNA methylation, DNA structural modifications, histone modifications, and RNA–RNA interactions. Genome-wide transcriptome analyses have identified various types of noncoding RNAs (ncRNAs) that respond to abiotic stress. These ncRNAs are in addition to the well-known housekeeping ncRNAs, such as rRNAs, tRNAs, snoRNAs, and snRNAs. In this review, recent research pertaining to the role of lncRNAs in the response of plants to abiotic stress is summarized and discussed.

Key words

Long noncoding RNA Small RNA RNA metabolism Epigenetic Abiotic stress response 

Notes

Acknowledgments

This work was supported by grants from RIKEN, Grants-in-Aid for Scientific Research provided from the Ministry of Education, Culture, Sports, Science, and Technology, (Innovative Areas 18H04791 and 18H04705), the Japan Science and Technology Agency (JST), and the Core Research for Evolutionary Science and Technology (CREST) JPMJCR13B4 to M.S.

References

  1. 1.
    Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052.  https://doi.org/10.1111/j.1365-313X.2010.04124.xCrossRefGoogle Scholar
  2. 2.
    Yamada K, Lim J, Dale JM et al (2003) Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 31:842–846.  https://doi.org/10.1126/science.1088305CrossRefGoogle Scholar
  3. 3.
    Jin J, Liu J, Wang H et al (2013) PLncDB: plant long non-coding RNA database. Bioinformatics 29:1068–1071.  https://doi.org/10.1093/bioinformatics/btt107CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Liu J, Jung C, Xu J et al (2012) Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 24:4333–4345.  https://doi.org/10.1105/tpc.112.102855CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Matsui A, Ishida J, Morosawa T 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.  https://doi.org/10.1093/pcp/pcn101CrossRefGoogle Scholar
  6. 6.
    Wang H, Chung PJ, Liu IC et al (2014) Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis. Genome Res 24:444–453CrossRefGoogle Scholar
  7. 7.
    Cech TR, Steitz J (2014) The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157:77–94.  https://doi.org/10.1016/j.cell.2014.03.008CrossRefGoogle Scholar
  8. 8.
    Berretta J, Morillon A (2009) Pervasive transcription constitutes a new level of eukaryotic genome regulation. EMBO Rep 10:973–982.  https://doi.org/10.1038/embor.2009.181CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Chen XM (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–44.  https://doi.org/10.1146/annurev.cellbio.042308.113417CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Lee Y, Kim M, Han J et al (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23:4051–4060.  https://doi.org/10.1038/sj.emboj.7600385CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Gazzani S, Lawrenson T, Woodward C et al (2004) A link between mRNA turnover and RNA interference in Arabidopsis. Science 306:1046–1048.  https://doi.org/10.1126/science.1101092CrossRefGoogle Scholar
  12. 12.
    Luo Z, Chen Z (2007) Improperly terminated, unpolyadenylated mRNA of sense transgenes is targeted by RDR6-mediated RNA silencing in Arabidopsis. Plant Cell 19:943–958.  https://doi.org/10.1105/tpc.106.045724CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Lukiw WJ, Handley P, Wong L et al (1992) BC200 RNA in normal human neocortex, non-Alzheimer dementia (NAD), and senile dementia of the Alzheimer type (AD). Neurochem Res 17:591–597CrossRefGoogle Scholar
  14. 14.
    Carninci P, Kasukawa T, Katayama S et al (2005) The transcriptional landscape of the mammalian genome. Science 309:1559–1563.  https://doi.org/10.1126/science.1112014CrossRefGoogle Scholar
  15. 15.
    Iyer MK, Niknafs YS, Malik R et al (2015) The landscape of long noncoding RNAs in the human transcriptome. Nat Genet 47:199–208.  https://doi.org/10.1038/ng.3192CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Djebali S, Davis CA, Merkel A et al (2012) Landscape of transcription in human cells. Nature 489:101–108.  https://doi.org/10.1038/nature11233CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    David L, Huber W, Granovskaia M et al (2006) A high-resolution map of transcription in the yeast genome. Proc Natl Acad Sci U S A 103:5320–5325.  https://doi.org/10.1073/pnas.0601091103CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Yang WC, Katinakis P, Hendriks P et al (1993) Characterization of GmENOD40, a gene showing novel patterns of cell-specific expression during soybean nodule development. Plant J 3:573–585CrossRefGoogle Scholar
  19. 19.
    Crespi MD, Jurkevitch E, Poiret M et al (1994) enod40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. EMBO J 13:5099–5112CrossRefGoogle Scholar
  20. 20.
    Liu C, Muchhal US, Raghothama KG (1997) Differential expression of TPS11, a phosphate starvation-induced gene in tomato. Plant Mol Biol 33:867–874CrossRefGoogle Scholar
  21. 21.
    Wasaki J, Yonetani R, Shinano T et al (2003) Expression of the OsPI1 gene, cloned from rice roots using cDNA microarray, rapidly responds to phosphorus status. New Phytol 158:239–248.  https://doi.org/10.1046/j.1469-8137.2003.00748.xCrossRefGoogle Scholar
  22. 22.
    Li L, Wang X, Stolc V et al (2006) Genome-wide transcription analyses in rice using tiling microarrays. Nat Genet 38:124–129.  https://doi.org/10.1038/ng1704CrossRefGoogle Scholar
  23. 23.
    Bhatia G, Goyal N, Sharma S et al (2017) Present Scenario of Long Non-Coding RNAs in Plants. RNA 3:16.  https://doi.org/10.3390/ncrna3020016CrossRefGoogle Scholar
  24. 24.
    Ponting CP, Oliver PL, Reik W (2009) Evolution and functions of long noncoding RNAs. Cell 136:629–641.  https://doi.org/10.1016/j.cell.2009.02.006CrossRefGoogle Scholar
  25. 25.
    Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10:155–159.  https://doi.org/10.1038/nrg2521CrossRefPubMedGoogle Scholar
  26. 26.
    Wang Y, Wang X, Deng XW et al (2014) Genomic features and regulatory roles of intermediate-sized non-coding RNAs in Arabidopsis. Mol Plant 7:514–527.  https://doi.org/10.1093/mp/sst177CrossRefGoogle Scholar
  27. 27.
    Liu T-T, Zhu D, Chen W et al (2013) A global identification and analysis of small nucleolar RNAs and possible intermediate-sized non-coding RNAs in Oryza sativa. Mol Plant 6:830–846.  https://doi.org/10.1093/mp/sss087CrossRefGoogle Scholar
  28. 28.
    Ulitsky I, Bartel DP (2013) lincRNAs, genomics, evolution, and mechanisms. Cell 154:26–46.  https://doi.org/10.1016/j.cell.2013.06.020CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Vannini A, Cramer P (2012) Conservation between the RNA polymerase I, II, and III transcription initiation machineries. Mol Cell 45:439–446.  https://doi.org/10.1016/j.molcel.2012.01.023CrossRefGoogle Scholar
  30. 30.
    Wen J, Parker BJ, Weiller GF (2007) In Silico identification and characterization of mRNA-like noncoding transcripts in Medicago truncatula. In Silico Biol 7:485–505Google Scholar
  31. 31.
    Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:76–79.  https://doi.org/10.1126/science.1197349CrossRefGoogle Scholar
  32. 32.
    Di C, Yuan J, Wu Y et al (2014) Characterization of stress-responsive lncRNAs in Arabidopsis thaliana by integrating expression, epigenetic and structural features. Plant J 80:848–861.  https://doi.org/10.1111/tpj.12679CrossRefGoogle Scholar
  33. 33.
    Ben Amor B, Wirth S, Merchan F et al (2009) Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res 19:57–69.  https://doi.org/10.1101/gr.080275.108CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Wu J, Okada T, Fukushima T et al (2012) A novel hypoxic stress-responsive long non-coding RNA transcribed by RNA polymerase III in Arabidopsis. RNA Biol 9:302–313.  https://doi.org/10.4161/rna.19101CrossRefGoogle Scholar
  35. 35.
    Li D, Huang X, Liu Z et al (2016) Effect of AtR8 lncRNA partial deletion on Arabidopsis seed germination. Mol Soil Biol 7:1–7.  https://doi.org/10.5376/msb.2016.07.0007CrossRefGoogle Scholar
  36. 36.
    Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687.  https://doi.org/10.1016/j.cell.2009.01.046CrossRefGoogle Scholar
  37. 37.
    Hirsch J, Lefort V, Vankersschaver M et al (2006) Characterization of 43 non-protein-coding mRNA genes in Arabidopsis, including the MIR162a-derived transcripts. Plant Physiol 140:1192–1204.  https://doi.org/10.1104/pp.105.073817CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065.  https://doi.org/10.1105/tpc.106.041673CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Yamasaki H, Abdel-Ghany SE, Cohu CM et al (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Biol Chem 282:16369–16378.  https://doi.org/10.1074/jbc.M700138200CrossRefGoogle Scholar
  40. 40.
    Yan K, Liu P, Wu CA et al (2012) Stress-induced alternative splicing provides a mechanism for the regulation of microRNA processing in Arabidopsis thaliana. Mol Cell 48:521–531.  https://doi.org/10.1016/j.molcel.2012.08.032CrossRefGoogle Scholar
  41. 41.
    Li W, Cui X, Meng Z et al (2012) Transcriptional regulation of Arabidopsis MIR168a and ARGONAUTE1 homeostasis in abscisic acid and abiotic stress responses. Plant Physiol 158:1279–1292.  https://doi.org/10.1104/pp.111.188789CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Liu PP, Montgomery TA, Fahlgren N et al (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146.  https://doi.org/10.1111/j.1365-313X.2007.03218.xCrossRefGoogle Scholar
  43. 43.
    Blomster T, Salojärvi J, Sipari N et al (2011) Apoplastic reactive oxygen species transiently decrease auxin signaling and cause stress-induced morphogenic response in Arabidopsis. Plant Physiol 157:1866–1883.  https://doi.org/10.1104/pp.111.181883CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Kawashima CG, Matthewman CA, Huang S et al (2011) Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J 66:863–876.  https://doi.org/10.1111/j.1365-313X.2011.04547.xCrossRefGoogle Scholar
  45. 45.
    Aung K, Lin SI, Wu CC et al (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011.  https://doi.org/10.1104/pp.106.078063CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Fuji H, Chiou TJ, Lin SI et al (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043.  https://doi.org/10.1016/j.cub.2005.10.016CrossRefGoogle Scholar
  47. 47.
    Franco-Zorrilla JM, Valli A, Todesco M et al (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037.  https://doi.org/10.1038/ng2079CrossRefGoogle Scholar
  48. 48.
    Allen E, Xie Z, Gustafson AM et al (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221.  https://doi.org/10.1016/j.cell.2005.04.004CrossRefGoogle Scholar
  49. 49.
    Ronemus M, Vaughn MW, Martienssen RA (2006) MicroRNA-targeted and small interfering RNA-mediated mRNA degradation is regulated by argonaute, dicer, and RNA-dependent RNA polymerase in Arabidopsis. Plant Cell 18:1559–1574.  https://doi.org/10.1105/tpc.106.042127CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Marin E, Jouannet V, Herz A et al (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22:1104–1117.  https://doi.org/10.1105/tpc.109.072553CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Duan L, Dietrich D, Ng CH et al (2013) Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. Plant Cell 25:324–341.  https://doi.org/10.1105/tpc.112.107227CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Geng Y, Wu R, Wee CW et al (2013) A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis. Plant Cell 25:2132–2154.  https://doi.org/10.1105/tpc.113.112896CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Matsui A, Mizunashi K, Tanaka M et al (2014) tasiRNA-ARF pathway moderates floral architecture in Arabidopsis plants subjected to drought stress. Biomed Res Int 2014:303451.  https://doi.org/10.1155/2014/303451CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58.  https://doi.org/10.1080/07352680590910410CrossRefGoogle Scholar
  55. 55.
    Li S, Liu J, Liu Z et al (2014) Heat-induced TAS1 TARGET1 mediates thermotolerance via heat stress transcription factor A1a-directed pathways in Arabidopsis. Plant Cell 26:1764–1780.  https://doi.org/10.1105/tpc.114.124883CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Zhong SH, Liu JZ, Jin H et al (2013) Warm temperatures induce transgenerational epigenetic release of RNA silencing by inhibiting siRNA biogenesis in Arabidopsis. Proc Natl Acad Sci U S A 110:9171–9176.  https://doi.org/10.1073/pnas.1219655110CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Wierzbicki AT, Haag JR, Pikaard CS (2008) Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135:635–648.  https://doi.org/10.1016/j.cell.2008.09.035CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394–408.  https://doi.org/10.1038/nrg3683CrossRefGoogle Scholar
  59. 59.
    Zheng B, Wang Z, Li S et al (2009) Intergenic transcription by RNA Polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev 23:2850–2860.  https://doi.org/10.1101/gad.1868009CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Matzke M, Kanno T, Daxinger L et al (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21:367–376.  https://doi.org/10.1016/j.ceb.2009.01.025CrossRefGoogle Scholar
  61. 61.
    Li S, Vandivier LE, Tu B et al (2015) Detection of Pol IV/RDR2-dependent transcripts at the genomic scale in Arabidopsis reveals features and regulation of siRNA biogenesis. Genome Res 25:235–245.  https://doi.org/10.1101/gr.182238.114CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress response in plant. Curr Opin Plant Biol 12:133–139.  https://doi.org/10.1016/j.pbi.2008.12.006CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Popova OV, Dinh HQ, Aufsatz W et al (2013) The RdDM pathway is required for basal heat tolerance in Arabidopsis. Mol Plant 6:396–410.  https://doi.org/10.1093/mp/sst023CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Tricker PJ, Gibbings JG, Rodríguez-López CM et al (2012) Low relative humidity triggers RNA-directed de novo DNA methylation and suppression of genes controlling stomatal development. J Exp Bot 63:3799–3814.  https://doi.org/10.1093/jxb/ers076CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Choi CS, Sano H (2007) Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Mol Genet Genomics 277:589–600.  https://doi.org/10.1007/s00438-007-0209-1CrossRefGoogle Scholar
  66. 66.
    Song Y, Ji D, Li S et al (2012) The dynamic changes of DNA methylation and histone modifications of salt responsive transcription factor genes in soybean. PLoS One 7:e41274.  https://doi.org/10.1371/journal.pone.0041274CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Borsani O, Zhu J, Verslues PE et al (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123:1279–1291.  https://doi.org/10.1016/j.cell.2005.11.035CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Zhang X, Lii Y, Wu Z et al (2013) Mechanisms of small RNA generation from cis-NATs in response to environmental and developmental cues. Mol Plant 6:704–715.  https://doi.org/10.1093/mp/sst051CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Henz SR, Cumbie JS, Kasschau KD et al (2007) Distinct expression patterns of natural antisense transcripts in Arabidopsis. Plant Physiol 144:1247–1255.  https://doi.org/10.1104/pp.107.100396CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Zhan S, Lukens L (2013) Protein-coding cis-natural antisense transcripts have high and broad expression in Arabidopsis. thaliana Plant Physiol 161:2171–2180.  https://doi.org/10.1104/pp.112.212100CrossRefGoogle Scholar
  71. 71.
    Jabnoune M, Secco D, Lecampion C et al (2013) A rice cis-natural antisense RNA acts as a translational enhancer for its cognate mRNA and contributes to phosphate homeostasis and plant fitness. Plant Cell 25:4166–4182.  https://doi.org/10.1105/tpc.113.116251CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Carrieri C, Cimatti L Biagioli M et al (2012) Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 491:454–457.  https://doi.org/10.1038/nature11508CrossRefGoogle Scholar
  73. 73.
    Takahashi H, Kozhuharova A, Sharma H et al (2018) Identification of functional features of synthetic SINEUPs, antisense lncRNAs that specifically enhance protein translation. PLoS One 13:e0183229.  https://doi.org/10.1371/journal.pone.0183229CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Jauvion V, Elmayan T, Vaucheret H (2010) The conserved RNA trafficking proteins HPR1 and TEX1 are involved in the production of endogenous and exogenous small interfering RNA in Arabidopsis. Plant Cell 22:2697–2709.  https://doi.org/10.1105/tpc.110.076638CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Mourrain P, Beclin C, Elmayan T et al (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533–542.  https://doi.org/10.1016/S0092-8674(00)80863-6CrossRefGoogle Scholar
  76. 76.
    Parent JS, Jauvion V, Bouché N et al (2015) Post-transcriptional gene silencing triggered by sense transgenes involves uncapped antisense RNA and differs from silencing intentionally triggered by antisense transgenes. Nucleic Acids Res 43:8464–8475.  https://doi.org/10.1093/nar/gkv753CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci U S A 102:11928–11933.  https://doi.org/10.1073/pnas.0505461102CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Dalmay T, Horsefield R, Braunstein TH et al (2001) SDE3 encodes an RNA helicase required for post-transcriptional gene silencing in Arabidopsis. EMBO J 20:2069–2078.  https://doi.org/10.1093/emboj/20.8.2069CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Garcia D, Garcia S, Pontier D et al (2012) Ago hook and RNA helicase motifs underpin dual roles for SDE3 in antiviral defense and silencing of nonconserved intergenic regions. Mol Cell 48:109–120.  https://doi.org/10.1016/j.molcel.2012.07.028CrossRefGoogle Scholar
  80. 80.
    Parent JS, Bouteiller N, Elmayan T et al (2015) Respective contributions of Arabidopsis DCL2 and DCL4 to RNA silencing. Plant J 81:223–232.  https://doi.org/10.1111/tpj.12720CrossRefGoogle Scholar
  81. 81.
    Belostotsky DA, Sieburth LE (2009) Kill the messenger: mRNA decay and plant development. Curr Opin Plant Biol 12:96–102.  https://doi.org/10.1016/j.pbi.2008.09.003CrossRefGoogle Scholar
  82. 82.
    Kastenmayer JP, Green PJ (2000) Novel features of the XRN-family in Arabidopsis: evidence that AtXRN4, one of several orthologs of nuclear Xrn2p/Rat1p, functions in the cytoplasm. Proc Natl Acad Sci U S A 97:13985–13990.  https://doi.org/10.1073/pnas.97.25.13985CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Chekanova JA, Gregory BD, Reverdatto SV et al (2007) Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131:1340–1353.  https://doi.org/10.1016/j.cell.2007.10.056CrossRefGoogle Scholar
  84. 84.
    Lange H, Zuber H, Sement FM et al (2014) The RNA helicases AtMTR4 and HEN2 target specific subsets of nuclear transcripts for degradation by the nuclear exosome in Arabidopsis thaliana. PLoS Genet 10:e1004564.  https://doi.org/10.1371/journal.pgen.1004564CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Yu A, Saudemont B, Bouteiller N et al (2015) Second-site mutagenesis of a hypomorphic argonaute1 allele identifies SUPERKILLER3 as an endogenous suppressor of transgene posttranscriptional gene silencing. Plant Physiol 169:1266–1274.  https://doi.org/10.1104/pp.15.00585CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Zhang X, Zhu Y, Liu X et al (2015) Plant biology. Suppression of endogenous gene silencing by bidirectional cytoplasmic RNA decay in Arabidopsis. Science 348:120–123.  https://doi.org/10.1126/science.aaa2618CrossRefGoogle Scholar
  87. 87.
    Gy I, Gasciolli V, Lauressergues D et al (2007) Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 19:3451–3461.  https://doi.org/10.1105/tpc.107.055319CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Thran M, Link K, Sonnewald U (2012) The Arabidopsis DCP2 gene is required for proper mRNA turnover and prevents transgene silencing in Arabidopsis. Plant J 72:368–377.  https://doi.org/10.1111/j.1365-313X.2012.05066.xCrossRefGoogle Scholar
  89. 89.
    Moreno AB, Martinez de Alba AE, Bardou F et al (2013) Cytoplasmic and nuclear quality control and turnover of single-stranded RNA modulate post-transcriptional gene silencing in plants. Nucleic Acids Res 41:4699–4708.  https://doi.org/10.1093/nar/gkt152CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Hematy K, Bellec Y, Podicheti R et al (2016) The Zinc-finger protein SOP1 is required for a subset of the nuclear exosome functions in Arabidopsis. PLoS Genet 12:e1005817.  https://doi.org/10.1371/journal.pgen.1005817CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Martínez de Alba AE, Moreno AB et al (2015) In plants, decapping prevents RDR6-dependent production of small interfering RNAs from endogenous mRNAs. Nucleic Acids Res 43:2902–2913.  https://doi.org/10.1093/nar/gkv119CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Branscheid A, Marchais A, Schott G et al (2015) SKI2 mediates degradation of RISC 5′-cleavage fragments and prevents secondary siRNA production from miRNA targets in Arabidopsis. Nucleic Acids Res 43:10975–10988.  https://doi.org/10.1093/nar/gkv1014CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Xu J, Chua NH (2012) Dehydration stress activates Arabidopsis MPK6 to signal DCP1 phosphorylation. EMBO J 31:1975–1984.  https://doi.org/10.1038/emboj.2012.56CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Soma F, Mogami J, Yoshida T et al (2017) ABA-unresponsive SnRK2 protein kinases regulate mRNA decay under osmotic stress in plants. Nat Plants 3:16204.  https://doi.org/10.1038/nplants.2016.204CrossRefGoogle Scholar
  95. 95.
    Estavillo GM, Crisp PA, Pornsiriwong W et al (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:3992–4012.  https://doi.org/10.1105/tpc.111.091033CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Matsui A, Iida K, Tanaka M et al (2017) Novel stress-inducible antisense RNAs of protein-coding loci are synthesized by RNA-Dependent RNA Polymerase. Plant Physiol 175:457–472.  https://doi.org/10.1104/pp.17.00787CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Liu F, Marquardt S, Lister C et al (2010) Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327:94–97.  https://doi.org/10.1126/science.1180278CrossRefGoogle Scholar
  98. 98.
    Buzas DM, Robertson M, Finnegan EJ et al (2011) Transcription-dependence of histone H3 lysine 27 trimethylation at the Arabidopsis polycomb target gene FLC. Plant J 65:872–881.  https://doi.org/10.1111/j.1365-313X.2010.04471.xCrossRefGoogle Scholar
  99. 99.
    Luo C, Sidote D, Zhang Y et al (2013) Integrative analysis of chromatin states in Arabidopsis identified potential regulatory mechanisms for natural antisense transcript production. Plant J 73:77–90.  https://doi.org/10.1111/tpj.12017CrossRefGoogle Scholar
  100. 100.
    Helliwell CA, Robertson M, Finnegan EJ et al (2011) Vernalization-repression of Arabidopsis FLC requires promoter sequences but not antisense transcripts. PLoS One 6:e21513.  https://doi.org/10.1371/journal.pone.0021513CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Csorba T, Questa JI, Sun Q et al (2014) Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. Proc Natl Acad Sci U S A 111:16160–16165.  https://doi.org/10.1073/pnas.1419030111CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Hornyik C, Terzi LC, Simpson GG (2010) The spen family protein FPA controls alternative cleavage and polyadenylation of RNA. Dev Cell 18:203–213.  https://doi.org/10.1016/j.devcel.2009.12.009CrossRefGoogle Scholar
  103. 103.
    Marquardt S, Raitskin O, Wu Z et al (2014) Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription. Mol Cell 54:156–165.  https://doi.org/10.1016/j.molcel.2014.03.026CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Liu F, Quesada V, Crevillén P et al (2007) The Arabidopsis RNA-binding protein FCA requires a lysinespecific demethylase 1 homolog to downregulate FLC. Mol Cell 28:398–407.  https://doi.org/10.1016/j.molcel.2007.10.018CrossRefGoogle Scholar
  105. 105.
    Sun Q, Csorba T, Skourti-Stathaki K et al (2011) R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340:619–621.  https://doi.org/10.1126/science.1234848CrossRefGoogle Scholar
  106. 106.
    Shin JH, Chekanova JA (2014) Arabidopsis RRP6L1 and RRP6L2 function in FLOWERING LOCUS C silencing via regulation of antisense RNA synthesis. PLoS Genet 10:e1004612.  https://doi.org/10.1371/journal.pgen.1004612CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Kim DH, Sung S (2017) Vernalization-triggered intragenic chromatin loop formation by long noncoding RNAs. Dev Cell 40:302–312.e4.  https://doi.org/10.1016/j.devcel.2016.12.021CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Gultyaev AP, Roussis A (2007) Identification of conserved secondary structures and expansion segments in enod40 RNAs reveals new enod40 homologues in plants. Nucleic Acids Res 35:3144–3152.  https://doi.org/10.1093/nar/gkm173CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    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 16:1047–1059.  https://doi.org/10.1105/tpc.019406CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Bardou F, Ariel F, Simpson CG et al (2014) Long noncoding RNA modulates alternative splicing regulators in Arabidopsis. Dev Cell 30:166–176.  https://doi.org/10.1016/j.devcel.2014.06.017CrossRefGoogle Scholar
  111. 111.
    Ariel F, Jegu T, Latrasse D et al (2014) Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop. Mol Cell 55:383–396.  https://doi.org/10.1016/j.molcel.2014.06.011CrossRefGoogle Scholar
  112. 112.
    Wang Y, Fan X, Lin F et al (2014) Arabidopsis noncoding RNA mediates control of photomorphogenesis by red light. Proc Natl Acad Sci U S A 111:10359–10364.  https://doi.org/10.1073/pnas.1409457111CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Shin H, Shin HS, Chen R et al (2006) Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant J 45:712–726.  https://doi.org/10.1111/j.1365-313X.2005.02629.xCrossRefGoogle Scholar
  114. 114.
    Lin SI, Chiang SF, Lin WY et al (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746.  https://doi.org/10.1104/pp.108.116269CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Wu HJ, Wang ZM, Wang M et al (2013) Wide-spread long non-coding RNAs (lncRNAs) as endogenous target mimics (eTMs) for microRNAs in plants. Plant Physiol 161:1875–1884.  https://doi.org/10.1104/pp.113.215962CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Kartha RV, Subramanian S (2014) Competing endogenous RNAs (ceRNAs): new entrants to the intricacies of gene regulation. Front Genet 5:8.  https://doi.org/10.3389/fgene.2014.00008CrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    Zhang Y, Zhang XO, Chen T et al (2013) Circular intronic long noncoding RNAs. Mol Cell 51:792–806.  https://doi.org/10.1016/j.molcel.2013.08.017CrossRefGoogle Scholar
  118. 118.
    Starke S, Jost I, Rossbach O et al (2015) Exon circularization requires canonical splice signals. Cell Rep 10:103–111.  https://doi.org/10.1016/j.celrep.2014.12.002CrossRefGoogle Scholar
  119. 119.
    Chen LL (2016) The biogenesis and emerging roles of circular RNAs. Nat Rev Mol Cell Biol 17:205–211.  https://doi.org/10.1038/nrm.2015.32CrossRefGoogle Scholar
  120. 120.
    Wang PL, Bao Y, Yee MC et al (2014) Circular RNA is expressed across the eukaryotic tree of life. PLoS One 9:e90859.  https://doi.org/10.1371/journal.pone.0090859CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Chu Q, Zhang X, Zhu X et al (2017) PlantcircBase: a database for plant circular RNAs. Mol Plant 10:1126–1128.  https://doi.org/10.1016/j.molp.2017.03.003CrossRefGoogle Scholar
  122. 122.
    Ye CY, Chen L, Liu C et al (2015) Widespread noncoding circular RNAs in plants. New Phytol 208:88–95.  https://doi.org/10.1111/nph.13585CrossRefGoogle Scholar
  123. 123.
    Hansen TB, Jensen TI, Clausen BH et al (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495:384–388.  https://doi.org/10.1038/nature11993CrossRefGoogle Scholar
  124. 124.
    Conn VM, Hugouvieux V, Nayak A et al (2017) A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation. Nat Plants 3:17053.  https://doi.org/10.1038/nplants.2017.53CrossRefGoogle Scholar
  125. 125.
    Lu T, Cui L, Zhou Y et al (2015) Transcriptome-wide investigation of circular RNAs in rice. RNA 21:2076–2087.  https://doi.org/10.1261/rna.052282.115CrossRefPubMedPubMedCentralGoogle Scholar
  126. 126.
    Pan T, Sun X, Liu Y et al (2018) Heat stress alters genome-wide profiles of circular RNAs in Arabidopsis. Plant Mol Biol 96:217–229.  https://doi.org/10.1007/s11103-017-0684-7CrossRefGoogle Scholar
  127. 127.
    Zuo J, Wang Q, Zhu B et al (2016) Deciphering the roles of circRNAs on chilling injury in tomato. Biochem Biophys Res Commun 479:132–138.  https://doi.org/10.1016/j.bbrc.2016.07.032CrossRefGoogle Scholar
  128. 128.
    Ding B (2009) The biology of viroid–host interactions. Annu Rev Phytopathol 47:105–131CrossRefGoogle Scholar
  129. 129.
    Wassenegger M, Heimes S, Riedel L et al (1994) RNA-directed de novo methylation of genomic sequences in plants. Cell 76:567–576.  https://doi.org/10.1016/0092-8674(94)90119-8CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Plant Genomic Network Research Team, RIKEN Center for Sustainable Resource ScienceYokohamaJapan
  2. 2.Plant Epigenome Regulation Laboratory, RIKEN Cluster for Pioneering ResearchWakoJapan
  3. 3.Kihara Institute for Biological Research, Yokohama City UniversityYokohamaJapan
  4. 4.Core Research for Evolutional Science and Technology, Japan Science and TechnologyKawaguchiJapan

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