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Abstract

Plants have an extraordinary diversity of transcription machineries, including five nuclear DNA-dependent RNA polymerases. Four of these enzymes are dedicated to the production of long noncoding RNAs (lncRNAs), which are ribonucleic acids with functions independent of their protein-coding potential. lncRNAs display a broad range of lengths and structures, but they are distinct from the small RNA guides of RNA interference (RNAi) pathways. lncRNAs frequently serve as structural, catalytic, or regulatory molecules for gene expression. They can affect all elements of genes, including promoters, untranslated regions, exons, introns, and terminators, controlling gene expression at various levels, including modifying chromatin accessibility, transcription, splicing, and translation. Certain lncRNAs protect genome integrity, while others respond to environmental cues like temperature, drought, nutrients, and pathogens. In this review, we explain the challenge of defining lncRNAs, introduce the machineries responsible for their production, and organize this knowledge by viewing the functions of lncRNAs throughout the structure of a typical plant gene.

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2021-06-17
2024-03-28
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Literature Cited

  1. 1. 
    Alleman M, Sidorenko L, McGinnis K, Seshadri V, Dorweiler JE et al. 2006. An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442:7100295–98
    [Google Scholar]
  2. 2. 
    Andersen PR, Tirian L, Vunjak M, Brennecke J. 2017. A heterochromatin-dependent transcription machinery drives piRNA expression. Nature 549:767054–59
    [Google Scholar]
  3. 3. 
    Anderson SN, Zynda GJ, Song J, Han Z, Vaughn MW et al. 2018. Subtle perturbations of the maize methylome reveal genes and transposons silenced by chromomethylase or RNA-directed DNA methylation pathways. G3 Genes Genomes Genet 8:61921–32
    [Google Scholar]
  4. 4. 
    Antosz W, Pfab A, Ehrnsberger HF, Holzinger P, Köllen K et al. 2017. The composition of the Arabidopsis RNA polymerase II transcript elongation complex reveals the interplay between elongation and mRNA processing factors. Plant Cell 29:4854–70
    [Google Scholar]
  5. 5. 
    Archacki R, Yatusevich R, Buszewicz D, Krzyczmonik K, Patryn J et al. 2017. Arabidopsis SWI/SNF chromatin remodeling complex binds both promoters and terminators to regulate gene expression. Nucleic Acids Res 45:63116–29
    [Google Scholar]
  6. 6. 
    Ariel F, Jegu T, Latrasse D, Romero-Barrios N, Christ A et al. 2014. Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop. Mol. Cell 55:3383–96
    [Google Scholar]
  7. 7. 
    Ariel F, Lucero L, Christ A, Mammarella MF, Jegu T et al. 2020. R-loop mediated trans action of the APOLO long noncoding RNA. Mol. Cell 77:51055–65
    [Google Scholar]
  8. 8. 
    Axtell MJ. 2013. Classification and comparison of small RNAs from plants. Annu. Rev. Plant Biol. 64:137–59
    [Google Scholar]
  9. 9. 
    Bardou F, Merchan F, Ariel F, Crespi M 2011. Dual RNAs in plants. Biochimie 93:111950–54
    [Google Scholar]
  10. 10. 
    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 19:157–69
    [Google Scholar]
  11. 11. 
    Bentsink L, Jowett J, Hanhart CJ, Koornneef M 2006. Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. PNAS 103:4517042–47
    [Google Scholar]
  12. 12. 
    Bhat SS, Bielewicz D, Gulanicz T, Bodi Z, Yu X et al. 2020. mRNA adenosine methylase (MTA) deposits m6A on pri-miRNAs to modulate miRNA biogenesis in Arabidopsis thaliana. PNAS 117:3521785–95
    [Google Scholar]
  13. 13. 
    Blevins T, Podicheti R, Mishra V, Marasco M, Wang J et al. 2015. Identification of Pol IV and RDR2-dependent precursors of 24 nt siRNAs guiding de novo DNA methylation in Arabidopsis. eLife 4:e09591
    [Google Scholar]
  14. 14. 
    Blevins T, Rajeswaran R, Aregger M, Borah BK, Schepetilnikov M et al. 2011. Massive production of small RNAs from a non-coding region of Cauliflower mosaic virus in plant defense and viral counter-defense. Nucleic Acids Res 39:125003–14
    [Google Scholar]
  15. 15. 
    Böhmdorfer G, Rowley MJ, Kuciński J, Zhu Y, Amies I, Wierzbicki AT. 2014. RNA-directed DNA methylation requires stepwise binding of silencing factors to long non-coding RNA. Plant J 79:2181–91
    [Google Scholar]
  16. 16. 
    Böhmdorfer G, Sethuraman S, Rowley MJ, Krzyszton M, Rothi MH et al. 2016. Long non-coding RNA produced by RNA polymerase V determines boundaries of heterochromatin. eLife 5:e19092
    [Google Scholar]
  17. 17. 
    Brosius J, Raabe CA. 2016. What is an RNA? A top layer for RNA classification. RNA Biol 13:2140–44
    [Google Scholar]
  18. 18. 
    Capovilla G, Pajoro A, Immink RGH, Schmid M. 2015. Role of alternative pre-mRNA splicing in temperature signaling. Curr. Opin. Plant Biol. 27:97–103
    [Google Scholar]
  19. 19. 
    Carrieri C, Cimatti L, Biagioli M, Beugnet A, Zucchelli S et al. 2012. Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 491:7424454–57
    [Google Scholar]
  20. 20. 
    Chan SW-L, Zilberman D, Xie Z, Johansen LK, Carrington JC, Jacobsen SE. 2004. RNA silencing genes control de novo DNA methylation. Science 303:56621336
    [Google Scholar]
  21. 21. 
    Chapon C, Cech TR, Zaug AJ. 1997. Polyadenylation of telomerase RNA in budding yeast. RNA 3:111337–51
    [Google Scholar]
  22. 22. 
    Chekanova JA. 2015. Long non-coding RNAs and their functions in plants. Curr. Opin. Plant Biol. 27:207–16
    [Google Scholar]
  23. 23. 
    Chekanova JA, Gregory BD, Reverdatto SV, Chen H, Kumar R et al. 2007. Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131:71340–53
    [Google Scholar]
  24. 24. 
    Chow HT, Chakraborty T, Mosher RA. 2020. RNA-directed DNA methylation and sexual reproduction: expanding beyond the seed. Curr. Opin. Plant Biol. 54:11–17
    [Google Scholar]
  25. 25. 
    Cloix C, Yukawa Y, Tutois S, Sugiura M, Tourmente S. 2003. In vitro analysis of the sequences required for transcription of the Arabidopsis thaliana 5S rRNA genes. Plant J 35:2251–61
    [Google Scholar]
  26. 26. 
    Cognat V, Pawlak G, Duchêne A-M, Daujat M, Gigant A et al. 2013. PlantRNA, a database for tRNAs of photosynthetic eukaryotes. Nucleic Acids Res 41:Database IssueD273–79
    [Google Scholar]
  27. 27. 
    Conn VM, Hugouvieux V, Nayak A, Conos SA, Capovilla G et al. 2017. A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation. Nat. Plants 3:17053
    [Google Scholar]
  28. 28. 
    Cramer P. 2019. Organization and regulation of gene transcription. Nature 573:777245–54
    [Google Scholar]
  29. 29. 
    Csorba T, Questa JI, Sun Q, Dean C 2014. Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. PNAS 111:4516160–65
    [Google Scholar]
  30. 30. 
    Cuerda-Gil D, Slotkin RK 2016. Non-canonical RNA-directed DNA methylation. Nat. Plants 2:16163
    [Google Scholar]
  31. 31. 
    Cyrek M, Fedak H, Ciesielski A, Guo Y, Sliwa A et al. 2016. Seed dormancy in Arabidopsis is controlled by alternative polyadenylation of DOG1. Plant Physiol 170:2947–55
    [Google Scholar]
  32. 32. 
    David L, Huber W, Granovskaia M, Toedling J, Palm CJ et al. 2006. A high-resolution map of transcription in the yeast genome. PNAS 103:145320–25
    [Google Scholar]
  33. 33. 
    De Almeida C, Scheer H, Zuber H, Gagliardi D. 2018. RNA uridylation: a key posttranscriptional modification shaping the coding and noncoding transcriptome. Wiley Interdiscip Rev RNA 9:1e1440
    [Google Scholar]
  34. 34. 
    Deforges J, Reis RS, Jacquet P, Sheppard S, Gadekar VP et al. 2019. Control of cognate sense mRNA translation by cis-natural antisense RNAs. Plant Physiol 180:1305–22
    [Google Scholar]
  35. 35. 
    Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T et al. 2012. Landscape of transcription in human cells. Nature 489:7414101–8
    [Google Scholar]
  36. 36. 
    Eddy SR. 2001. Non-coding RNA genes and the modern RNA world. Nat. Rev. Genet. 2:12919–29
    [Google Scholar]
  37. 37. 
    El-Shami M, Pontier D, Lahmy S, Braun L, Picart C et al. 2007. Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev 21:202539–44
    [Google Scholar]
  38. 38. 
    Erhard KFJ, Stonaker JL, Parkinson SE, Lim JP, Hale CJ, Hollick JB. 2009. RNA polymerase IV functions in paramutation in Zea mays. Science 323:59181201–5
    [Google Scholar]
  39. 39. 
    Fajkus P, Peska V, Zavodnik M, Fojtova M, Fulneckova J et al. 2019. Telomerase RNAs in land plants. Nucleic Acids Res 47:189842–56
    [Google Scholar]
  40. 40. 
    Fang X, Wu Z, Raitskin O, Webb K, Voigt P et al. 2020. The 3′ processing of antisense RNAs physically links to chromatin-based transcriptional control. PNAS 117:2615316–21
    [Google Scholar]
  41. 41. 
    Fedak H, Palusinska M, Krzyczmonik K, Brzezniak L, Yatusevich R et al. 2016. Control of seed dormancy in Arabidopsis by a cis-acting noncoding antisense transcript. PNAS 113:48E7846–55
    [Google Scholar]
  42. 42. 
    Ferrafiat L, Pflieger D, Singh J, Thieme M, Böhrer M et al. 2019. The NRPD1 N-terminus contains a Pol IV–specific motif that is critical for genome surveillance in Arabidopsis. Nucleic Acids Res 47:179037–52
    [Google Scholar]
  43. 43. 
    Fischl H, Howe FS, Furger A, Mellor J. 2017. Paf1 has distinct roles in transcription elongation and differential transcript fate. Mol. Cell 65:4685–698.e8
    [Google Scholar]
  44. 44. 
    Fontana F. 1781. Traité sur le vénin de la vipere sur les poisons americains sur le laurier-cerise et sur quelques autres poisons végetaux Florence: Nyon l'Ainé
  45. 45. 
    Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI et al. 2007. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39:81033–37
    [Google Scholar]
  46. 46. 
    Goldberg RB, Hoschek G, Kamalay JC, Timberlake WE. 1978. Sequence complexity of nuclear and polysomal RNA in leaves of the tobacco plant. Cell 14:1123–31
    [Google Scholar]
  47. 47. 
    Golicz AA, Singh MB, Bhalla PL. 2018. The long intergenic noncoding RNA (lincRNA) landscape of the soybean genome. Plant Physiol 176:32133–47
    [Google Scholar]
  48. 48. 
    Gowthaman U, García-Pichardo D, Jin Y, Schwarz I, Marquardt S 2020. DNA processing in the context of noncoding transcription. Trends Biochem Sci 45:121009–1021
    [Google Scholar]
  49. 49. 
    Graur D, Zheng Y, Price N, Azevedo RBR, Zufall RA, Elhaik E. 2013. On the immortality of television sets: “function” in the human genome according to the evolution-free gospel of ENCODE. Genome Biol. Evol. 5:3578–90
    [Google Scholar]
  50. 50. 
    Gutmann B, Gobert A, Giegé P. 2012. PRORP proteins support RNase P activity in both organelles and the nucleus in Arabidopsis. Genes Dev 26:101022–27
    [Google Scholar]
  51. 51. 
    Haag JR, Brower-Toland B, Krieger EK, Sidorenko L, Nicora CD et al. 2014. Functional diversification of maize RNA polymerase IV and V subtypes via alternative catalytic subunits. Cell Rep 9:1378–90
    [Google Scholar]
  52. 52. 
    Haag JR, Ream TS, Marasco M, Nicora CD, Norbeck AD et al. 2012. In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing. Mol. Cell 48:5811–18
    [Google Scholar]
  53. 53. 
    Hammond MC, Wachter A, Breaker RR. 2009. A plant 5S ribosomal RNA mimic regulates alternative splicing of transcription factor IIIA pre-mRNAs. Nat. Struct. Mol. Biol. 16:5541–49
    [Google Scholar]
  54. 54. 
    Haudry A, Platts AE, Vello E, Hoen DR, Leclercq M et al. 2013. An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nat. Genet. 45:8891–98
    [Google Scholar]
  55. 55. 
    Hawkes EJ, Hennelly SP, Novikova IV, Irwin JA, Dean C, Sanbonmatsu KY. 2016. COOLAIR antisense RNAs form evolutionarily conserved elaborate secondary structures. Cell Rep 16:123087–96
    [Google Scholar]
  56. 56. 
    Heo JB, Sung S 2011. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:601376–79
    [Google Scholar]
  57. 57. 
    Herr AJ, Jensen MB, Dalmay T, Baulcombe DC. 2005. RNA polymerase IV directs silencing of endogenous DNA. Science 308:5718118–20
    [Google Scholar]
  58. 58. 
    Hirsch CD, Springer NM. 2017. Transposable element influences on gene expression in plants. Biochim. Biophys. Acta Gene Regul. Mech. 1860:1157–65
    [Google Scholar]
  59. 59. 
    Hisanaga T, Okahashi K, Yamaoka S, Kajiwara T, Nishihama R et al. 2019. A cis-acting bidirectional transcription switch controls sexual dimorphism in the liverwort. EMBO J 38:6e100240
    [Google Scholar]
  60. 60. 
    Hong X, Scofield DG, Lynch M. 2006. Intron size, abundance, and distribution within untranslated regions of genes. Mol. Biol. Evol. 23:122392–404
    [Google Scholar]
  61. 61. 
    Jacob F, Monod J. 1961. Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 3:3318–56
    [Google Scholar]
  62. 62. 
    Johnson LM, Du J, Hale CJ, Bischof S, Feng S et al. 2014. SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 507:7490124–28
    [Google Scholar]
  63. 63. 
    Johnson LM, Law JA, Khattar A, Henderson IR, Jacobsen SE. 2008. SRA-domain proteins required for DRM2-mediated de novo DNA methylation. PLOS Genet 4:11e1000280
    [Google Scholar]
  64. 64. 
    Juntawong P, Girke T, Bazin J, Bailey-Serres J 2014. Translational dynamics revealed by genome-wide profiling of ribosome footprints in Arabidopsis. PNAS 111:1E203–12
    [Google Scholar]
  65. 65. 
    Kanno T, Huettel B, Mette MF, Aufsatz W, Jaligot E et al. 2005. Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat. Genet. 37:7761–65
    [Google Scholar]
  66. 66. 
    Kim D-H, Sung S. 2017. Vernalization-triggered intragenic chromatin loop formation by long noncoding RNAs. Dev. Cell 40:3302–12.e4
    [Google Scholar]
  67. 67. 
    Kindgren P, Ard R, Ivanov M, Marquardt S. 2018. Transcriptional read-through of the long non-coding RNA SVALKA governs plant cold acclimation. Nat. Commun. 9:14561
    [Google Scholar]
  68. 68. 
    Kindgren P, Ivanov M, Marquardt S. 2020. Native elongation transcript sequencing reveals temperature dependent dynamics of nascent RNAPII transcription in Arabidopsis. Nucleic Acids Res 48:52332–47
    [Google Scholar]
  69. 69. 
    Kiss T, Marshallsay C, Filipowicz W. 1991. Alteration of the RNA polymerase specificity of U3 snRNA genes during evolution and in vitro. Cell 65:3517–26
    [Google Scholar]
  70. 70. 
    Kowalczyk J, Palusinska M, Wroblewska-Swiniarska A, Pietras Z, Szewc L et al. 2017. Alternative polyadenylation of the sense transcript controls antisense transcription of DELAY OF GERMINATION 1 in Arabidopsis. Mol. Plant 10:101349–52
    [Google Scholar]
  71. 71. 
    Krzyszton M, Zakrzewska-Placzek M, Kwasnik A, Dojer N, Karlowski W, Kufel J. 2018. Defective XRN3-mediated transcription termination in Arabidopsis affects the expression of protein-coding genes. Plant J 93:61017–31
    [Google Scholar]
  72. 72. 
    Lahmy S, Pontier D, Bies-Etheve N, Laudié M, Feng S et al. 2016. Evidence for ARGONAUTE4-DNA interactions in RNA-directed DNA methylation in plants. Genes Dev 30:232565–70
    [Google Scholar]
  73. 73. 
    Lahmy S, Pontier D, Cavel E, Vega D, El-Shami M et al. 2009. PolV(PolIVb) function in RNA-directed DNA methylation requires the conserved active site and an additional plant-specific subunit. PNAS 106:3941–46
    [Google Scholar]
  74. 74. 
    Law JA, Ausin I, Johnson LM, Vashisht AA, Zhu J-K et al. 2010. A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr. Biol. 20:10951–56
    [Google Scholar]
  75. 75. 
    Law JA, Du J, Hale CJ, Feng S, Krajewski K et al. 2013. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498:7454385–89
    [Google Scholar]
  76. 76. 
    Law JA, Vashisht AA, Wohlschlegel JA, Jacobsen SE. 2011. SHH1, a homeodomain protein required for DNA methylation, as well as RDR2, RDM4, and chromatin remodeling factors, associate with RNA polymerase IV. PLOS Genet 7:7e1002195
    [Google Scholar]
  77. 77. 
    Lawit SJ, O'Grady K, Gurley WB, Czarnecka-Verner E 2007. Yeast two-hybrid map of Arabidopsis TFIID. Plant Mol. Biol. 64:1–273–87
    [Google Scholar]
  78. 78. 
    Lee H, Zhang Z, Krause HM. 2019. Long noncoding RNAs and repetitive elements: junk or intimate evolutionary partners?. Trends Genet 35:12892–902
    [Google Scholar]
  79. 79. 
    Leng X, Ivanov M, Kindgren P, Malik I, Thieffry A et al. 2020. Organismal benefits of transcription speed control at gene boundaries. EMBO Rep 21:4e49315
    [Google Scholar]
  80. 80. 
    Leng X, Thomas Q, Rasmussen SH, Marquardt S. 2020. A G(enomic)P(ositioning)S(ystem) for plant RNAPII transcription. Trends Plant Sci 25:8744–64
    [Google Scholar]
  81. 81. 
    Leppek K, Das R, Barna M. 2018. Functional 5′ UTR mRNA structures in eukaryotic translation regulation and how to find them. Nat. Rev. Mol. Cell Biol. 19:3158–74
    [Google Scholar]
  82. 82. 
    Li J, Liu C. 2019. Coding or noncoding, the converging concepts of RNAs. Front. Genet. 10:496
    [Google Scholar]
  83. 83. 
    Li P, Tao Z, Dean C. 2015. Phenotypic evolution through variation in splicing of the noncoding RNA COOLAIR. Genes Dev 29:7696–701
    [Google Scholar]
  84. 84. 
    Li Q, Gent JI, Zynda G, Song J, Makarevitch I et al. 2015. RNA-directed DNA methylation enforces boundaries between heterochromatin and euchromatin in the maize genome. PNAS 112:4714728–33
    [Google Scholar]
  85. 85. 
    Libri D. 2015. Endless quarrels at the end of genes. Mol. Cell 60:2192–94
    [Google Scholar]
  86. 86. 
    Lipovich L, Johnson R, Lin C-Y. 2010. MacroRNA underdogs in a microRNA world: evolutionary, regulatory, and biomedical significance of mammalian long non-protein-coding RNA. Biochim. Biophys. Acta Gene Regul. Mech. 1799:9597–615
    [Google Scholar]
  87. 87. 
    Lippman Z, Gendrel A-V, Black M, Vaughn MW, Dedhia N et al. 2004. Role of transposable elements in heterochromatin and epigenetic control. Nature 430:6998471–76
    [Google Scholar]
  88. 88. 
    Liu F, Marquardt S, Lister C, Swiezewski S, Dean C. 2010. Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327:596194–97
    [Google Scholar]
  89. 89. 
    Liu J, Jung C, Xu J, Wang H, Deng S et al. 2012. Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 24:114333–45
    [Google Scholar]
  90. 90. 
    Liu M, Ba Z, Costa-Nunes P, Wei W, Li L et al. 2017. IDN2 interacts with RPA and facilitates DNA double-strand break repair by homologous recombination in Arabidopsis. Plant Cell 29:3589–99
    [Google Scholar]
  91. 91. 
    Liu W, Duttke SH, Hetzel J, Groth M, Feng S et al. 2018. RNA-directed DNA methylation involves co-transcriptional small-RNA-guided slicing of polymerase V transcripts in Arabidopsis. Nat. Plants 4:3181–88
    [Google Scholar]
  92. 92. 
    Liu Z-W, Shao C-R, Zhang C-J, Zhou J-X, Zhang S-W et al. 2014. The SET domain proteins SUVH2 and SUVH9 are required for Pol V occupancy at RNA-directed DNA methylation loci. PLOS Genet 10:1e1003948
    [Google Scholar]
  93. 93. 
    Luo J, Hall BD. 2007. A multistep process gave rise to RNA polymerase IV of land plants. J. Mol. Evol. 64:1101–12
    [Google Scholar]
  94. 94. 
    Marasco M, Li W, Lynch M, Pikaard CS. 2017. Catalytic properties of RNA polymerases IV and V: accuracy, nucleotide incorporation and rNTP/dNTP discrimination. Nucleic Acids Res 45:1911315–26
    [Google Scholar]
  95. 95. 
    Marquardt S, Raitskin O, Wu Z, Liu F, Sun Q, Dean C. 2014. Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription. Mol. Cell 54:1156–65
    [Google Scholar]
  96. 96. 
    Marz M, Stadler PF. 2009. Comparative analysis of eukaryotic U3 snoRNA. RNA Biol 6:5503–7
    [Google Scholar]
  97. 97. 
    Matzke MA, Mosher RA. 2014. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat. Rev. Genet. 15:6394–408
    [Google Scholar]
  98. 98. 
    Mocavini I, Di Croce L. 2020. RNA closing the Polycomb circle. Nat. Genet. 52:9866–67
    [Google Scholar]
  99. 99. 
    Mohammadin S, Edger PP, Pires JC, Schranz ME. 2015. Positionally-conserved but sequence-diverged: identification of long non-coding RNAs in the Brassicaceae and Cleomaceae. BMC Plant Biol 15:1217
    [Google Scholar]
  100. 100. 
    Nielsen M, Ard R, Leng X, Ivanov M, Kindgren P et al. 2019. Transcription-driven chromatin repression of intragenic transcription start sites. PLOS Genet 15:2e1007969
    [Google Scholar]
  101. 101. 
    Onodera Y, Haag JR, Ream T, Costa Nunes P, Pontes O, Pikaard CS 2005. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation–dependent heterochromatin formation. Cell 120:5613–22
    [Google Scholar]
  102. 102. 
    Panda K, Ji L, Neumann DA, Daron J, Schmitz RJ, Slotkin RK 2016. Full-length autonomous transposable elements are preferentially targeted by expression-dependent forms of RNA-directed DNA methylation. Genome Biol 17:1170
    [Google Scholar]
  103. 103. 
    Pikaard CS. 2002. Transcription and tyranny in the nucleolus: the organization, activation, dominance and repression of ribosomal RNA genes. Arabidopsis Book 1:e0083
    [Google Scholar]
  104. 104. 
    Pontier D, Yahubyan G, Vega D, Bulski A, Saez-Vasquez J et al. 2005. Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev 19:172030–40
    [Google Scholar]
  105. 105. 
    Ponting CP, Oliver PL, Reik W. 2009. Evolution and functions of long noncoding RNAs. Cell 136:4629–41
    [Google Scholar]
  106. 106. 
    Preuss SB, Costa-Nunes P, Tucker S, Pontes O, Lawrence RJ et al. 2008. Multimegabase silencing in nucleolar dominance involves siRNA-directed DNA methylation and specific methylcytosine-binding proteins. Mol. Cell 32:5673–84
    [Google Scholar]
  107. 107. 
    Pumplin N, Sarazin A, Jullien PE, Bologna NG, Oberlin S, Voinnet O. 2016. DNA methylation influences the expression of DICER-LIKE4 isoforms, which encode proteins of alternative localization and function. Plant Cell 28:112786–804
    [Google Scholar]
  108. 108. 
    Qi Y, He X, Wang X-J, Kohany O, Jurka J, Hannon GJ. 2006. Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443:71141008–12
    [Google Scholar]
  109. 109. 
    Ream TS, Haag JR, Pontvianne F, Nicora CD, Norbeck AD et al. 2015. Subunit compositions of Arabidopsis RNA polymerases I and III reveal Pol I– and Pol III–specific forms of the AC40 subunit and alternative forms of the C53 subunit. Nucleic Acids Res 43:84163–78
    [Google Scholar]
  110. 110. 
    Ream TS, Haag JR, Wierzbicki AT, Nicora CD, Norbeck AD et al. 2009. Subunit compositions of the RNA-silencing enzymes Pol IV and Pol V reveal their origins as specialized forms of RNA polymerase II. Mol. Cell 33:2192–203
    [Google Scholar]
  111. 111. 
    Rheinberger H-J 2006. A history of protein biosynthesis and ribosome research. Protein Synthesis and Ribosome Structure: Translating the Genome KH Nierhaus, DN Wilson 1–51 Weinheim, Ger: Wiley
    [Google Scholar]
  112. 112. 
    Rigo R, Bazin J, Romero-Barrios N, Moison M, Lucero L et al. 2020. The Arabidopsis lncRNA ASCO modulates the transcriptome through interaction with splicing factors. EMBO Rep 21:5e48977
    [Google Scholar]
  113. 113. 
    Rinn JL, Chang HY. 2012. Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 81:145–66
    [Google Scholar]
  114. 114. 
    Romero-Barrios N, Legascue MF, Benhamed M, Ariel F, Crespi M 2018. Splicing regulation by long noncoding RNAs. Nucleic Acids Res 46:52169–84
    [Google Scholar]
  115. 115. 
    Rosa S, Duncan S, Dean C 2016. Mutually exclusive sense-antisense transcription at FLC facilitates environmentally induced gene repression. Nat. Commun. 7:13031
    [Google Scholar]
  116. 116. 
    Rowley MJ, Rothi MH, Böhmdorfer G, Kuciński J, Wierzbicki AT. 2017. Long-range control of gene expression via RNA-directed DNA methylation. PLOS Genet 13:5e1006749
    [Google Scholar]
  117. 117. 
    Saez-Vasquez J, Delseny M. 2019. Ribosome biogenesis in plants: from functional 45S ribosomal DNA organization to ribosome assembly factors. Plant Cell 31:91945–67
    [Google Scholar]
  118. 118. 
    Seo JS, Diloknawarit P, Park BS, Chua N-H. 2019. ELF18-INDUCED LONG NONCODING RNA 1 evicts fibrillarin from mediator subunit to enhance PATHOGENESIS-RELATED GENE 1 (PR1) expression. New Phytol 221:42067–79
    [Google Scholar]
  119. 119. 
    Seo JS, Sun H-X, Park BS, Huang C-H, Yeh S-D et al. 2017. ELF18-INDUCED LONG-NONCODING RNA associates with Mediator to enhance expression of innate immune response genes in Arabidopsis. Plant Cell 29:51024–38
    [Google Scholar]
  120. 120. 
    Shamovsky I, Nudler E. 2006. Gene control by large noncoding RNAs. Sci. STKE 2006:355pe40
    [Google Scholar]
  121. 121. 
    Shearwin KE, Callen BP, Egan JB. 2005. Transcriptional interference—a crash course. Trends Genet 21:6339–45
    [Google Scholar]
  122. 122. 
    Singh J, Mishra V, Wang F, Huang H-Y, Pikaard CS. 2019. Reaction mechanisms of Pol IV, RDR2, and DCL3 drive RNA channeling in the siRNA-directed DNA methylation pathway. Mol. Cell 75:3576–89.e5
    [Google Scholar]
  123. 123. 
    Srivastava AK, Lu Y, Zinta G, Lang Z, Zhu J-K. 2018. UTR-dependent control of gene expression in plants. Trends Plant Sci 23:3248–59
    [Google Scholar]
  124. 124. 
    Struhl K. 2007. Transcriptional noise and the fidelity of initiation by RNA polymerase II. Nat. Struct. Mol. Biol. 14:2103–5
    [Google Scholar]
  125. 125. 
    Sun Q, Csorba T, Skourti-Stathaki K, Proudfoot NJ, Dean C. 2013. R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340:6132619–21
    [Google Scholar]
  126. 126. 
    Swiezewski S, Liu F, Magusin A, Dean C. 2009. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462:7274799–802
    [Google Scholar]
  127. 127. 
    Teixeira FK, Heredia F, Sarazin A, Roudier F, Boccara M et al. 2009. A role for RNAi in the selective correction of DNA methylation defects. Science 323:59211600–4
    [Google Scholar]
  128. 128. 
    Thieffry A, Vigh ML, Bornholdt J, Ivanov M, Brodersen P, Sandelin A. 2020. Characterization of Arabidopsis thaliana promoter bidirectionality and antisense RNAs by inactivation of nuclear RNA decay pathways. Plant Cell 32:61845–67
    [Google Scholar]
  129. 129. 
    Thomas QA, Ard R, Liu J, Li B, Wang J et al. 2020. Transcript isoform sequencing reveals widespread promoter-proximal transcriptional termination in Arabidopsis. Nat Commun 11:12589
    [Google Scholar]
  130. 130. 
    Tsuzuki M, Sethuraman S, Coke AN, Rothi MH, Boyle AP, Wierzbicki AT 2020. Broad noncoding transcription suggests genome surveillance by RNA polymerase V. PNAS 117:4830799–804
    [Google Scholar]
  131. 131. 
    Tucker S, Vitins A, Pikaard CS. 2010. Nucleolar dominance and ribosomal RNA gene silencing. Curr. Opin. Cell Biol. 22:3351–56
    [Google Scholar]
  132. 132. 
    Tucker SL, Reece J, Ream TS, Pikaard CS. 2010. Evolutionary history of plant multisubunit RNA polymerases IV and V: subunit origins via genome-wide and segmental gene duplications, retrotransposition, and lineage-specific subfunctionalization. Cold Spring Harb. Symp. Quant. Biol. 75:285–97
    [Google Scholar]
  133. 133. 
    van der Horst S, Snel B, Hanson J, Smeekens S. 2019. Novel pipeline identifies new upstream ORFs and non-AUG initiating main ORFs with conserved amino acid sequences in the 5′ leader of mRNAs in Arabidopsis thaliana. RNA 25:3292–304
    [Google Scholar]
  134. 134. 
    Waibel F, Filipowicz W. 1990. U6 snRNA genes of Arabidopsis are transcribed by RNA polymerase III but contain the same two upstream promoter elements as RNA polymerase II–transcribed U-snRNA genes. Nucleic Acids Res 18:123451–58
    [Google Scholar]
  135. 135. 
    Wang H, Chung PJ, Liu J, Jang I-C, Kean MJ et al. 2014. Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis. Genome Res 24:3444–53
    [Google Scholar]
  136. 136. 
    Wang Z, Butel N, Santos-González J, Borges F, Yi J et al. 2020. Polymerase IV plays a crucial role in pollen development in Capsella. Plant Cell 32:4950–66
    [Google Scholar]
  137. 137. 
    Warner JR. 1999. The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24:11437–40
    [Google Scholar]
  138. 138. 
    Wei W, Ba Z, Gao M, Wu Y, Ma Y et al. 2012. A role for small RNAs in DNA double-strand break repair. Cell 149:1101–12
    [Google Scholar]
  139. 139. 
    Wendte JM, Haag JR, Singh J, McKinlay A, Pontes OM, Pikaard CS. 2017. Functional dissection of the Pol V largest subunit CTD in RNA-directed DNA methylation. Cell Rep 19:132796–808
    [Google Scholar]
  140. 140. 
    Wierzbicki AT, Cocklin R, Mayampurath A, Lister R, Rowley MJ et al. 2012. Spatial and functional relationships among Pol V–associated loci, Pol IV–dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes Dev 26:161825–36
    [Google Scholar]
  141. 141. 
    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 135:4635–48
    [Google Scholar]
  142. 142. 
    Wierzbicki AT, Ream TS, Haag JR, Pikaard CS. 2009. RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat. Genet. 41:5630–34
    [Google Scholar]
  143. 143. 
    Wilkinson ME, Charenton C, Nagai K. 2020. RNA splicing by the spliceosome. Annu. Rev. Biochem. 89:359–88
    [Google Scholar]
  144. 144. 
    Wu H-W, Deng S, Xu H, Mao H-Z, Liu J et al. 2018. A noncoding RNA transcribed from the AGAMOUS (AG) second intron binds to CURLY LEAF and represses AG expression in leaves. New Phytol 219:41480–91
    [Google Scholar]
  145. 145. 
    Xu W, Xu H, Li K, Fan Y, Liu Y et al. 2017. The R-loop is a common chromatin feature of the Arabidopsis genome. Nat. Plants 3:9704–14
    [Google Scholar]
  146. 146. 
    Yatusevich R, Fedak H, Ciesielski A, Krzyczmonik K, Kulik A et al. 2017. Antisense transcription represses Arabidopsis seed dormancy QTL DOG1 to regulate drought tolerance. EMBO Rep 18:122186–96
    [Google Scholar]
  147. 147. 
    Yu X, Martin PGP, Michaels SD. 2019. BORDER proteins protect expression of neighboring genes by promoting 3′ Pol II pausing in plants. Nat. Commun. 10:14359
    [Google Scholar]
  148. 148. 
    Yu Y, Jia T, Chen X. 2017. The “how” and “where” of plant microRNAs. New Phytol 216:41002–17
    [Google Scholar]
  149. 149. 
    Zanetti ME, Blanco F, Reynoso M, Crespi M. 2020. To keep or not to keep: mRNA stability and translatability in root nodule symbiosis. Curr. Opin. Plant Biol. 56:109–17
    [Google Scholar]
  150. 150. 
    Zemach A, Kim MY, Hsieh P-H, Coleman-Derr D, Eshed-Williams L et al. 2013. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153:1193–205
    [Google Scholar]
  151. 151. 
    Zhai J, Bischof S, Wang H, Feng S, Lee T-F et al. 2015. A one precursor one siRNA model for Pol IV–dependent siRNA biogenesis. Cell 163:2445–55
    [Google Scholar]
  152. 152. 
    Zhang Y-C, Liao J-Y, Li Z-Y, Yu Y, Zhang J-P et al. 2014. Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice. Genome Biol 15:12512
    [Google Scholar]
  153. 153. 
    Zhao X, Li J, Lian B, Gu H, Li Y, Qi Y. 2018. Global identification of Arabidopsis lncRNAs reveals the regulation of MAF4 by a natural antisense RNA. Nat. Commun. 9:15056
    [Google Scholar]
  154. 154. 
    Zheng Q, Rowley MJ, Böhmdorfer G, Sandhu D, Gregory BD, Wierzbicki AT. 2013. RNA polymerase V targets transcriptional silencing components to promoters of protein-coding genes. Plant J 73:2179–89
    [Google Scholar]
  155. 155. 
    Zhong X, Du J, Hale CJ, Gallego-Bartolome J, Feng S et al. 2014. Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell 157:51050–60
    [Google Scholar]
  156. 156. 
    Zhong X, Hale CJ, Law JA, Johnson LM, Feng S et al. 2012. DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nat. Struct. Mol. Biol. 19:9870–75
    [Google Scholar]
  157. 157. 
    Zhou M, Palanca AMS, Law JA. 2018. Locus-specific control of the de novo DNA methylation pathway in Arabidopsis by the CLASSY family. Nat. Genet. 50:6865–73
    [Google Scholar]
  158. 158. 
    Zhu Y, Rowley MJ, Böhmdorfer G, Wierzbicki AT. 2013. A SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing. Mol. Cell 49:2298–309
    [Google Scholar]
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