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Annual Review of Plant Biology

Volume 65, 2014

The Diversity, Biogenesis, and Activities of Endogenous Silencing Small RNAs in

Abstract

In eukaryotic RNA silencing, RNase-III classes of enzymes in the Dicer family process double-stranded RNA of cellular or exogenous origin into small-RNA (sRNA) molecules. sRNAs are then loaded into effector proteins known as ARGONAUTEs (AGOs), which, as part of RNA-induced silencing complexes, target complementary RNA or DNA for silencing. Plants have evolved a large variety of pathways over the Dicer–AGO consortium, which most likely underpins part of their phenotypic plasticity. Dicer-like proteins produce all known classes of plant silencing sRNAs, which are invariably stabilized via 2′-O-methylation mediated by HUA ENHANCER 1 (HEN1), potentially amplified by the action of several RNA-dependent RNA polymerases, and function through a variety of AGO proteins. Here, we review the known characteristics and biochemical properties of the core silencing factors found in the model plant . We also describe how interactions between these core factors and more specialized proteins allow the production of a plethora of silencing sRNAs involved in a large array of biological functions. We emphasize in particular the biogenesis and activities of silencing sRNAs of endogenous origin.

Keyword(s): Arabidopsis, PTGS, silencing, small RNA, TGS
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2014-04-29
2024-04-19
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Literature Cited

  1. Addo-Quaye C, Snyder JA, Park YB, Li YF, Sunkar R, Axtell MJ. 1.  2009. Sliced microRNA targets and precise loop-first processing of MIR319 hairpins revealed by analysis of the Physcomitrella patens degradome. RNA 15:2112–21 [Google Scholar]
  2. Allen E, Xie Z, Gustafson AM, Carrington JC. 2.  2005. MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–21 [Google Scholar]
  3. Axtell MJ, Jan C, Rajagopalan R, Bartel DP. 3.  2006. A two-hit trigger for siRNA biogenesis in plants. Cell 127:565–77 [Google Scholar]
  4. Bao N, Lye K-W, Barton MK. 4.  2004. MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev. Cell 7:653–62 [Google Scholar]
  5. Ben Chaabane S, Liu R, Chinnusamy V, Kwon Y, Park JH. 5.  et al. 2013. STA1, an Arabidopsis pre-mRNA processing factor 6 homolog, is a new player involved in miRNA biogenesis. Nucleic Acids Res. 41:1984–97 [Google Scholar]
  6. Bielewicz D, Kalak M, Kalyna M, Windels D, Barta A. 6.  et al. 2013. Introns of plant pri-miRNAs enhance miRNA biogenesis. EMBO Rep. 14:622–28 [Google Scholar]
  7. Bologna NG, Mateos JL, Bresso EG, Palatnik JF. 7.  2009. A loop-to-base processing mechanism underlies the biogenesis of plant microRNAs miR319 and miR159. EMBO J. 28:3646–56 [Google Scholar]
  8. Bologna NG, Schapire AL, Zhai J, Chorostecki U, Boisbouvier J. 8.  et al. 2013. Multiple RNA recognition patterns during microRNA biogenesis in plants. Genome Res. 23:1675–89 [Google Scholar]
  9. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY. 9.  et al. 2008. Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–90 [Google Scholar]
  10. Brodersen P, Sakvarelidze-Achard L, Schaller H, Khafif M, Schott G. 10.  et al. 2012. Isoprenoid biosynthesis is required for miRNA function and affects membrane association of ARGONAUTE 1 in Arabidopsis. Proc. Natl. Acad. Sci. USA 109:1778–83 [Google Scholar]
  11. Brosnan CA, Voinnet O. 11.  2011. Cell-to-cell and long-distance siRNA movement in plants: mechanisms and biological implications. Curr. Opin. Plant Biol. 14:580–87 [Google Scholar]
  12. Burdisso P, Suarez IP, Bologna NG, Palatnik JF, Bersch B, Rasia RM. 12.  2012. Second double-stranded RNA binding domain of dicer-like ribonuclease 1: structural and biochemical characterization. Biochemistry 51:10159–66 [Google Scholar]
  13. Carbonell A, Fahlgren N, Garcia-Ruiz H, Gilbert KB, Montgomery TA. 13.  et al. 2012. Functional analysis of three Arabidopsis ARGONAUTES using slicer-defective mutants. Plant Cell 24:3613–29 [Google Scholar]
  14. Carthew RW, Sontheimer EJ. 14.  2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–55 [Google Scholar]
  15. Cenik ES, Fukunaga R, Lu G, Dutcher R, Wang Y. 15.  et al. 2011. Phosphate and R2D2 restrict the substrate specificity of Dicer-2, an ATP-driven ribonuclease. Mol. Cell 42:172–84 [Google Scholar]
  16. Chellappan P, Xia J, Zhou X, Gao S, Zhang X. 16.  et al. 2010. siRNAs from miRNA sites mediate DNA methylation of target genes. Nucleic Acids Res. 38:6883–94 [Google Scholar]
  17. Chen H-M, Chen L-T, Patel K, Li Y-H, Baulcombe DC, Wu S-H. 17.  2010. 22-nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc. Natl. Acad. Sci. USA 107:15269–74 [Google Scholar]
  18. Cuperus JT, Carbonell A, Fahlgren N, Garcia-Ruiz H, Burke RT. 18.  et al. 2010. Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat. Struct. Mol. Biol. 17:997–1003 [Google Scholar]
  19. Cuperus JT, Fahlgren N, Carrington JC. 19.  2011. Evolution and functional diversification of MIRNA genes. Plant Cell 23:431–42 [Google Scholar]
  20. de Felippes FF, Ott F, Weigel D. 20.  2011. Comparative analysis of non-autonomous effects of tasiRNAs and miRNAs in Arabidopsis thaliana. Nucleic Acids Res. 39:2880–89 [Google Scholar]
  21. Derrien B, Baumberger N, Schepetilnikov M, Viotti C, De Cillia J. 21.  et al. 2012. Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proc. Natl. Acad. Sci. USA 109:15942–46 [Google Scholar]
  22. Devers EA, Branscheid A, May P, Krajinski F. 22.  2011. Stars and symbiosis: microRNA- and microRNA*-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis. Plant Physiol. 156:1990–2010 [Google Scholar]
  23. Dong Z, Han M-H, Fedoroff N. 23.  2008. The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc. Natl. Acad. Sci. USA 105:9970–75 [Google Scholar]
  24. Dunoyer P, Brosnan CA, Schott G, Wang Y, Jay F. 24.  et al. 2010. An endogenous, systemic RNAi pathway in plants. EMBO J. 29:1699–712 [Google Scholar]
  25. Dunoyer P, Himber C, Ruiz-Ferrer V, Alioua A, Voinnet O. 25.  2007. Intra- and intercellular RNA interference in Arabidopsis thaliana requires components of the microRNA and heterochromatic silencing pathways. Nat. Genet. 39:848–56 [Google Scholar]
  26. Eamens AL, Smith NA, Curtin SJ, Wang MB, Waterhouse PM. 26.  2009. The Arabidopsis thaliana double-stranded RNA binding protein DRB1 directs guide strand selection from microRNA duplexes. RNA 15:2219–35 [Google Scholar]
  27. Earley K, Smith M, Weber R, Gregory B, Poethig R. 27.  2010. An endogenous F-box protein regulates ARGONAUTE1 in Arabidopsis thaliana. Silence 1:15 [Google Scholar]
  28. El-Shami M, Pontier D, Lahmy S, Braun L, Picart C. 28.  et al. 2007. Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes Dev. 21:2539–44 [Google Scholar]
  29. Eun C, Lorkovic ZJ, Naumann U, Long Q, Havecker ER. 29.  et al. 2011. AGO6 functions in RNA-mediated transcriptional gene silencing in shoot and root meristems in Arabidopsis thaliana. PLoS ONE 6:e25730 [Google Scholar]
  30. Fang Y, Spector DL. 30.  2007. Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr. Biol. 17:818–23 [Google Scholar]
  31. Frank F, Hauver J, Sonenberg N, Nagar B. 31.  2012. Arabidopsis Argonaute MID domains use their nucleotide specificity loop to sort small RNAs. EMBO J. 31:3588–95 [Google Scholar]
  32. Fujioka Y, Utsumi M, Ohba Y, Watanabe Y. 32.  2007. Location of a possible miRNA processing site in SmD3/SmB nuclear bodies in Arabidopsis. Plant Cell Physiol. 48:1243–53 [Google Scholar]
  33. Garcia D, Garcia S, Pontier D, Marchais A, Renou JP. 33.  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 48:109–20 [Google Scholar]
  34. German MA, Pillay M, Jeong DH, Hetawal A, Luo S. 34.  et al. 2008. Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat. Biotechnol. 26:941–46 [Google Scholar]
  35. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. 35.  2008. miRBase: tools for microRNA genomics. Nucleic Acids Res. 36:D154–58 [Google Scholar]
  36. Gu S, Jin L, Huang Y, Zhang F, Kay MA. 36.  2012. Slicing-independent RISC activation requires the Argonaute PAZ domain. Curr. Biol. 22:1536–42 [Google Scholar]
  37. Havecker ER, Wallbridge LM, Hardcastle TJ, Bush MS, Kelly KA. 37.  et al. 2010. The Arabidopsis RNA-directed DNA methylation Argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22:321–34 [Google Scholar]
  38. Henderson IR, Zhang X, Lu C, Johnson L, Meyers BC. 38.  et al. 2006. Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat. Genet. 38:721–25 [Google Scholar]
  39. Hewezi T, Howe P, Maier TR, Baum TJ. 39.  2008. Arabidopsis small RNAs and their targets during cyst nematode parasitism. Mol. Plant-Microbe Interact. 21:1622–34 [Google Scholar]
  40. Hiraguri A, Itoh R, Kondo N, Nomura Y, Aizawa D. 40.  et al. 2005. Specific interactions between Dicer-like proteins and HYL1/DRB-family dsRNA-binding proteins in Arabidopsis thaliana. Plant Mol. Biol. 57:173–88 [Google Scholar]
  41. Hoffer P, Ivashuta S, Pontes O, Vitins A, Pikaard C. 41.  et al. 2011. Posttranscriptional gene silencing in nuclei. Proc. Natl. Acad. Sci. USA 108:409–14 [Google Scholar]
  42. Huang Y, Ji L, Huang Q, Vassylyev DG, Chen X, Ma JB. 42.  2009. Structural insights into mechanisms of the small RNA methyltransferase HEN1. Nature 461:823–27 [Google Scholar]
  43. Iki T, Yoshikawa M, Meshi T, Ishikawa M. 43.  2012. Cyclophilin 40 facilitates HSP90-mediated RISC assembly in plants. EMBO J. 31:267–78 [Google Scholar]
  44. Iki T, Yoshikawa M, Nishikiori M, Jaudal MC, Matsumoto-Yokoyama E. 44.  et al. 2010. In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90. Mol. Cell 39:282–91 [Google Scholar]
  45. Iwakawa HO, Tomari Y. 45.  2013. Molecular insights into microRNA-mediated translational repression in plants. Mol. Cell 52:591–601 [Google Scholar]
  46. Jauvion V, Elmayan T, Vaucheret H. 46.  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 22:2697–709 [Google Scholar]
  47. Jauvion V, Rivard M, Bouteiller N, Elmayan T, Vaucheret H. 47.  2012. RDR2 partially antagonizes the production of RDR6-dependent siRNA in sense transgene-mediated PTGS. PLoS ONE 7:e29785 [Google Scholar]
  48. Jouannet V, Moreno AB, Elmayan T, Vaucheret H, Crespi MD, Maizel A. 48.  2012. Cytoplasmic Arabidopsis AGO7 accumulates in membrane-associated siRNA bodies and is required for ta-siRNA biogenesis. EMBO J. 31:1704–13 [Google Scholar]
  49. Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR. 49.  et al. 2003. Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163:1109–22 [Google Scholar]
  50. Kasschau KD, Fahlgren N, Chapman EJ, Sullivan CM, Cumbie JS. 50.  et al. 2007. Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol. 5:e57 [Google Scholar]
  51. Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ. 51.  et al. 2003. P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev. Cell 4:205–17 [Google Scholar]
  52. Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A Jr. 52.  et al. 2006. A pathogen-inducible endogenous siRNA in plant immunity. Proc. Natl. Acad. Sci. USA 103:18002–7 [Google Scholar]
  53. Kim YJ, Zheng B, Yu Y, Won SY, Mo B, Chen X. 53.  2011. The role of Mediator in small and long noncoding RNA production in Arabidopsis thaliana. EMBO J. 30:814–22 [Google Scholar]
  54. Kumakura N, Takeda A, Fujioka Y, Motose H, Takano R, Watanabe Y. 54.  2009. SGS3 and RDR6 interact and colocalize in cytoplasmic SGS3/RDR6-bodies.. FEBS Lett. 583:1261–66 [Google Scholar]
  55. Kurihara Y, Watanabe Y. 55.  2004. Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc. Natl. Acad. Sci. USA 101:12753–58 [Google Scholar]
  56. Kwak PB, Tomari Y. 56.  2012. The N domain of Argonaute drives duplex unwinding during RISC assembly. Nat. Struct. Mol. Biol. 19:145–51 [Google Scholar]
  57. Lau PW, Guiley KZ, De N, Potter CS, Carragher B, MacRae IJ. 57.  2012. The molecular architecture of human Dicer. Nat. Struct. Mol. Biol. 19:436–40 [Google Scholar]
  58. Laubinger S, Sachsenberg T, Zeller G, Busch W, Lohmann JU. 58.  et al. 2008. Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 105:8795–800 [Google Scholar]
  59. Law JA, Ausin I, Johnson LM, Vashisht AA, Zhu JK. 59.  et al. 2010. A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr. Biol. 20:951–56 [Google Scholar]
  60. Law JA, Du J, Hale CJ, Feng S, Krajewski K. 60.  et al. 2013. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498:385–89 [Google Scholar]
  61. Law JA, Jacobsen SE. 61.  2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11:204–20 [Google Scholar]
  62. Li CF, Pontes O, El-Shami M, Henderson IR, Bernatavichute YV. 62.  et al. 2006. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126:93–106 [Google Scholar]
  63. Li J, Yang Z, Yu B, Liu J, Chen X. 63.  2005. Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr. Biol. 15:1501–7 [Google Scholar]
  64. Li S, Liu L, Zhuang X, Yu Y, Liu X. 64.  et al. 2013. MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153:562–74 [Google Scholar]
  65. Lindow M, Jacobsen A, Nygaard S, Mang Y, Krogh A. 65.  2007. Intragenomic matching reveals a huge potential for miRNA-mediated regulation in plants. PLoS Comput. Biol. 3:e238 [Google Scholar]
  66. Liu C, Axtell MJ, Fedoroff NV. 66.  2012. The helicase and RNaseIIIa domains of Arabidopsis Dicer-Like1 modulate catalytic parameters during microRNA biogenesis. Plant Physiol. 159:748–58 [Google Scholar]
  67. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM. 67.  et al. 2004. Argonaute2 is the catalytic engine of mammalian RNAi. Science 305:1437–41 [Google Scholar]
  68. Liu Q, Yao X, Pi L, Wang H, Cui X, Huang H. 68.  2009. The ARGONAUTE10 gene modulates shoot apical meristem maintenance and establishment of leaf polarity by repressing miR165/166 in Arabidopsis. Plant J. 58:27–40 [Google Scholar]
  69. Machida S, Yuan YA. 69.  2013. Crystal structure of Arabidopsis thaliana Dawdle forkhead-associated domain reveals a conserved phospho-threonine recognition cleft for Dicer-Like 1 binding. Mol. Plant 6:1290–300 [Google Scholar]
  70. Mallory AC, Hinze A, Tucker MR, Bouche N, Gasciolli V. 70.  et al. 2009. Redundant and specific roles of the ARGONAUTE proteins AGO1 and ZLL in development and small RNA-directed gene silencing. PLoS Genet. 5:e1000646 [Google Scholar]
  71. Mallory AC, Vaucheret H. 71.  2010. Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22:3879–89 [Google Scholar]
  72. Manavella PA, Hagmann J, Ott F, Laubinger S, Franz M. 72.  et al. 2012. Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1. Cell 151:859–70 [Google Scholar]
  73. Manavella PA, Koenig D, Weigel D. 73.  2012. Plant secondary siRNA production determined by microRNA-duplex structure. Proc. Natl. Acad. Sci. USA 109:2461–66 [Google Scholar]
  74. Margis R, Fusaro AF, Smith NA, Curtin SJ, Watson JM. 74.  et al. 2006. The evolution and diversification of Dicers in plants. FEBS Lett. 580:2442–50 [Google Scholar]
  75. Mari-Ordonez A, Marchais A, Etcheverry M, Martin A, Colot V, Voinnet O. 75.  2013. Reconstructing de novo silencing of an active plant retrotransposon. Nat. Genet. 45:1029–39 [Google Scholar]
  76. Mateos JL, Bologna NG, Chorostecki U, Palatnik JF. 76.  2010. Identification of microRNA processing determinants by random mutagenesis of Arabidopsis MIR172a precursor. Curr. Biol. 20:49–54 [Google Scholar]
  77. Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJ. 77.  2009. RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol. 21:367–76 [Google Scholar]
  78. Maunoury N, Vaucheret H. 78.  2011. AGO1 and AGO2 act redundantly in miR408-mediated plantacyanin regulation. PLoS ONE 6:e28729 [Google Scholar]
  79. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T. 79.  2004. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 15:185–97 [Google Scholar]
  80. Mi S, Cai T, Hu Y, Chen Y, Hodges E. 80.  et al. 2008. Sorting of small RNAs into Arabidopsis Argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133:116–27 [Google Scholar]
  81. Mlotshwa S, Schauer SE, Smith TH, Mallory AC, Herr JM Jr. 81.  et al. 2005. Ectopic DICER-LIKE1 expression in P1/HC-Pro Arabidopsis rescues phenotypic anomalies but not defects in microRNA and silencing pathways. Plant Cell 17:2873–85 [Google Scholar]
  82. Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE. 82.  et al. 2008. Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128–41 [Google Scholar]
  83. Moreno AB, Martínez de Alba AE, Bardou F, Crespi MD, Vaucheret H. 83.  et al. 2013. Cytoplasmic and nuclear quality control and turnover of single-stranded RNA modulate post-transcriptional gene silencing in plants. Nucleic Acids Res. 41:4699–708 [Google Scholar]
  84. Nagano H, Fukudome A, Hiraguri A, Moriyama H, Fukuhara T. 84.  2014. Distinct substrate specificities of Arabidopsis DCL3 and DCL4. Nucleic Acids Res 421845–56
  85. Olmedo-Monfil V, Durán-Figueroa N, Arteaga-Vázquez M, Demesa-Arévalo E, Autran D. 85.  et al. 2010. Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464:628–32 [Google Scholar]
  86. Pandey SP, Baldwin IT. 86.  2007. RNA-directed RNA polymerase 1 (RdR1) mediates the resistance of Nicotiana attenuata to herbivore attack in nature. Plant J. 50:40–53 [Google Scholar]
  87. Park MY, Wu G, Gonzalez-Sulser A, Vaucheret H, Poethig RS. 87.  2005. Nuclear processing and export of microRNAs in Arabidopsis. Proc. Natl. Acad. Sci. USA 102:3691–96 [Google Scholar]
  88. Pontes O, Li CF, Costa Nunes P, Haag J, Ream T. 88.  et al. 2006. The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126:79–92 [Google Scholar]
  89. Pontes O, Vitins A, Ream TS, Hong E, Pikaard CS, Costa-Nunes P. 89.  2013. Intersection of small RNA pathways in Arabidopsis thaliana sub-nuclear domains. PLoS ONE 8:e65652 [Google Scholar]
  90. Poulsen C, Vaucheret H, Brodersen P. 90.  2013. Lessons on RNA silencing mechanisms in plants from eukaryotic Argonaute structures. Plant Cell 25:22–37 [Google Scholar]
  91. Pumplin N, Voinnet O. 91.  2013. RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat. Rev. Microbiol. 11:745–60 [Google Scholar]
  92. Qi Y, He X, Wang XJ, Kohany O, Jurka J, Hannon GJ. 92.  2006. Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443:1008–12 [Google Scholar]
  93. Qin H, Chen F, Huan X, Machida S, Song J, Yuan YA. 93.  2010. Structure of the Arabidopsis thaliana DCL4 DUF283 domain reveals a noncanonical double-stranded RNA-binding fold for protein-protein interaction. RNA 16:474–81 [Google Scholar]
  94. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP. 94.  2006. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 20:3407–25 [Google Scholar]
  95. Ramachandran V, Chen X. 95.  2008. Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 321:1490–92 [Google Scholar]
  96. Ren G, Chen X, Yu B. 96.  2012. Uridylation of miRNAs by HEN1 SUPPRESSOR1 in Arabidopsis. Curr. Biol. 22:695–700 [Google Scholar]
  97. Ren G, Xie M, Dou Y, Zhang S, Zhang C, Yu B. 97.  2012. Regulation of miRNA abundance by RNA binding protein TOUGH in Arabidopsis. Proc. Natl. Acad. Sci. USA 109:12817–21 [Google Scholar]
  98. Rogers K, Chen X. 98.  2013. Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25:2383–99 [Google Scholar]
  99. Schwab R, Speth C, Laubinger S, Voinnet O. 99.  2013. Enhanced microRNA accumulation through stemloop-adjacent introns. EMBO Rep. 14:615–21 [Google Scholar]
  100. Smith MR, Willmann MR, Wu G, Berardini TZ, Moller B. 100.  et al. 2009. Cyclophilin 40 is required for microRNA activity in Arabidopsis. Proc. Natl. Acad. Sci. USA 106:5424–29 [Google Scholar]
  101. Song L, Axtell MJ, Fedoroff NV. 101.  2010. RNA secondary structural determinants of miRNA precursor processing in Arabidopsis. Curr. Biol. 20:37–41 [Google Scholar]
  102. Speth C, Willing EM, Rausch S, Schneeberger K, Laubinger S. 102.  2013. RACK1 scaffold proteins influence miRNA abundance in Arabidopsis. Plant J. 76:433–35 [Google Scholar]
  103. Stroud H, Greenberg MV, Feng S, Bernatavichute YV, Jacobsen SE. 103.  2013. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152:352–64 [Google Scholar]
  104. Taylor DW, Ma E, Shigematsu H, Cianfrocco MA, Noland CL. 104.  et al. 2013. Substrate-specific structural rearrangements of human Dicer. Nat. Struct. Mol. Biol. 20:662–70 [Google Scholar]
  105. Till S, Lejeune E, Thermann R, Bortfeld M, Hothorn M. 105.  et al. 2007. A conserved motif in Argonaute-interacting proteins mediates functional interactions through the Argonaute PIWI domain. Nat. Struct. Mol. Biol. 14:897–903 [Google Scholar]
  106. Tucker MR, Okada T, Hu Y, Scholefield A, Taylor JM, Koltunow AMG. 106.  2012. Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in Arabidopsis. Development 139:1399–404 [Google Scholar]
  107. Vaucheret H, Vazquez F, Crete P, Bartel DP. 107.  2004. The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev. 18:1187–97 [Google Scholar]
  108. Vazquez F, Gasciolli V, Cre P. 108.  2004. The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr. Biol. 14:346–51 [Google Scholar]
  109. Voinnet O. 109.  2008. Use, tolerance and avoidance of amplified RNA silencing by plants. Trends Plant Sci. 13:317–28 [Google Scholar]
  110. Wang F, Perry SE. 110.  2013. Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol. 161:1251–64 [Google Scholar]
  111. Wang HW, Noland C, Siridechadilok B, Taylor DW, Ma E. 111.  et al. 2009. Structural insights into RNA processing by the human RISC-loading complex. Nat. Struct. Mol. Biol. 16:1148–53 [Google Scholar]
  112. Wang L, Song X, Gu L, Li X, Cao S. 112.  et al. 2013. NOT2 proteins promote polymerase II-dependent transcription and interact with multiple microRNA biogenesis factors in Arabidopsis. Plant Cell 25:715–27 [Google Scholar]
  113. Wang W, Ye R, Xin Y, Fang X, Li C. 113.  et al. 2011. An importin beta protein negatively regulates microRNA activity in Arabidopsis. Plant Cell 23:3565–76 [Google Scholar]
  114. Wang XJ, Gaasterland T, Chua NH. 114.  2005. Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana. Genome Biol. 6:R30 [Google Scholar]
  115. Wei KF, Wu LJ, Chen J, Chen YF, Xie DX. 115.  2012. Structural evolution and functional diversification analyses of Argonaute protein. J. Cell. Biochem. 113:2576–85 [Google Scholar]
  116. Wei W, Ba Z, Gao M, Wu Y, Ma Y. 116.  et al. 2012. A role for small RNAs in DNA double-strand break repair. Cell 149:101–12 [Google Scholar]
  117. Welker NC, Maity TS, Ye X, Aruscavage PJ, Krauchuk AA. 117.  et al. 2011. Dicer's helicase domain discriminates dsRNA termini to promote an altered reaction mode. Mol. Cell 41:589–99 [Google Scholar]
  118. Werner S, Wollmann H, Schneeberger K, Weigel D. 118.  2010. Structure determinants for accurate processing of miR172a in Arabidopsis thaliana. Curr. Biol. 20:42–48 [Google Scholar]
  119. Wierzbicki AT, Cocklin R, Mayampurath A, Lister R, Rowley MJ. 119.  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. 26:1825–36 [Google Scholar]
  120. Willmann MR, Endres MW, Cook RT, Gregory BD. 120.  2011. The functions of RNA-dependent RNA polymerases in Arabidopsis. Arabidopsis Book 9:e0146 [Google Scholar]
  121. Willmann MR, Mehalick AJ, Packer RL, Jenik PD. 121.  2011. MicroRNAs regulate the timing of embryo maturation in Arabidopsis. Plant Physiol. 155:1871–84 [Google Scholar]
  122. Wu L, Mao L, Qi Y. 122.  2012. Roles of dicer-like and argonaute proteins in TAS-derived small interfering RNA-triggered DNA methylation. Plant Physiol. 160:990–99 [Google Scholar]
  123. Wu L, Zhou H, Zhang Q, Zhang J, Ni F. 123.  et al. 2010. DNA methylation mediated by a microRNA pathway. Mol. Cell 38:465–75 [Google Scholar]
  124. Wu X, Shi Y, Li J, Xu L, Fang Y. 124.  et al. 2013. A role for the RNA-binding protein MOS2 in microRNA maturation in Arabidopsis. Cell Res. 23:645–57 [Google Scholar]
  125. Xie Z, Allen E, Fahlgren N, Calamar A, Givan SA, Carrington JC. 125.  2005. Expression of Arabidopsis MIRNA genes. Plant Physiol. 138:2145–54 [Google Scholar]
  126. Xie Z, Allen E, Wilken A, Carrington JC. 126.  2005. DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 102:12984–89 [Google Scholar]
  127. Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD. 127.  et al. 2004. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2:e104 [Google Scholar]
  128. Xie Z, Kasschau KD, Carrington JC. 128.  2003. Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr. Biol. 13:784–89 [Google Scholar]
  129. Xu J, Chua NH. 129.  2011. Processing bodies and plant development. Curr. Opin. Plant Biol. 14:88–93 [Google Scholar]
  130. Yang L, Wu G, Poethig RS. 130.  2012. Mutations in the GW-repeat protein SUO reveal a developmental function for microRNA-mediated translational repression in Arabidopsis. Proc. Natl. Acad. Sci. USA 109:315–20 [Google Scholar]
  131. Ye R, Wang W, Iki T, Liu C, Wu Y. 131.  et al. 2012. Cytoplasmic assembly and selective nuclear import of Arabidopsis ARGONAUTE4/siRNA complexes. Mol. Cell 46:859–70 [Google Scholar]
  132. Yoshikawa M, Iki T, Tsutsui Y, Miyashita K, Poethig RS. 132.  et al. 2013. 3′ fragment of miR173-programmed RISC-cleaved RNA is protected from degradation in a complex with RISC and SGS3. Proc. Natl. Acad. Sci. USA 110:4117–22 [Google Scholar]
  133. Yoshikawa M, Peragine A, Park MY, Poethig RS. 133.  2005. A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev. 19:2164–75 [Google Scholar]
  134. Yu B, Bi L, Zhai J, Agarwal M, Li S. 134.  et al. 2010. siRNAs compete with miRNAs for methylation by HEN1 in Arabidopsis. Nucleic Acids Res. 38:5844–50 [Google Scholar]
  135. Yu B, Bi L, Zheng B, Ji L, Chevalier D. 135.  et al. 2008. The FHA domain proteins DAWDLE in Arabidopsis and SNIP1 in humans act in small RNA biogenesis. Proc. Natl. Acad. Sci. USA 105:10073–78 [Google Scholar]
  136. Yu B, Yang Z, Li J, Minakhina S, Yang M. 136.  et al. 2005. Methylation as a crucial step in plant microRNA biogenesis. Science 307:932–35 [Google Scholar]
  137. Yumul RE, Kim YJ, Liu X, Wang R, Ding J. 137.  et al. 2013. POWERDRESS and diversified expression of the MIR172 gene family bolster the floral stem cell network. PLoS Genet. 9:e1003218 [Google Scholar]
  138. Zemach A, Kim MY, Hsieh P-H, Coleman-Derr D, Eshed-Williams L. 138.  et al. 2013. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153:193–205 [Google Scholar]
  139. Zeng Y, Cullen BR. 139.  2004. Structural requirements for pre-microRNA binding and nuclear export by exportin 5. Nucleic Acids Res. 32:4776–85 [Google Scholar]
  140. Zhai J, Zhao Y, Simon SA, Huang S, Petsch K. 140.  et al. 2013. Plant microRNAs display differential 3′ truncation and tailing modifications that are ARGONAUTE1 dependent and conserved across species. Plant Cell 25:2417–28 [Google Scholar]
  141. Zhan X, Wang B, Li H, Liu R, Kalia RK. 141.  et al. 2012. Arabidopsis proline-rich protein important for development and abiotic stress tolerance is involved in microRNA biogenesis. Proc. Natl. Acad. Sci. USA 109:18198–203 [Google Scholar]
  142. Zhang X, Lii Y, Wu Z, Polishko A, Zhang H. 142.  et al. 2013. Mechanisms of small RNA generation from cis-NATs in response to environmental and developmental cues. Mol. Plant 6:704–15 [Google Scholar]
  143. Zhang X, Zhao H, Gao S, Wang WC, Katiyar-Agarwal S. 143.  et al. 2011. Arabidopsis Argonaute 2 regulates innate immunity via miRNA393*-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol. Cell 42:356–66 [Google Scholar]
  144. Zhang Z, Zhang X. 144.  2012. Argonautes compete for miR165/166 to regulate shoot apical meristem development. Curr. Opin. Plant Biol. 15:652–58 [Google Scholar]
  145. Zhao Y, Yu Y, Zhai J, Ramachandran V, Dinh TT. 145.  et al. 2012. The Arabidopsis nucleotidyl transferase HESO1 uridylates unmethylated small RNAs to trigger their degradation. Curr. Biol. 22:689–94 [Google Scholar]
  146. Zheng X, Zhu J, Kapoor A, Zhu JK. 146.  2007. Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J. 26:1691–701 [Google Scholar]
  147. Zhong X, Hale CJ, Law JA, Johnson LM, Feng S. 147.  et al. 2012. DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nat. Struct. Mol. Biol. 19:870–75 [Google Scholar]
  148. Zhu H, Hu F, Wang R, Zhou X, Sze SH. 148.  et al. 2011. Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145:242–56 [Google Scholar]
  149. Zhu H, Zhou Y, Castillo-Gonzalez C, Lu A, Ge C. 149.  et al. 2013. Bidirectional processing of pri-miRNAs with branched terminal loops by Arabidopsis Dicer-like1. Nat. Struct. Mol. Biol. 20:1106–15 [Google Scholar]
  150. Zong J, Yao X, Yin J, Zhang D, Ma H. 150.  2009. Evolution of the RNA-dependent RNA polymerase (RdRP) genes: duplications and possible losses before and after the divergence of major eukaryotic groups. Gene 447:29–39 [Google Scholar]
/content/journals/10.1146/annurev-arplant-050213-035728
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The Diversity, Biogenesis, and Activities of Endogenous Silencing Small RNAs in Arabidopsis
Annual Review of Plant Biology 65, 473 (2014); https://doi.org/10.1146/annurev-arplant-050213-035728
/content/journals/10.1146/annurev-arplant-050213-035728
/content/journals/10.1146/annurev-arplant-050213-035728
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