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microRNA biogenesis, degradation and activity in plants

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Abstract

microRNAs (miRNAs) are important regulators of gene expression. After excised from primary miRNA transcript by dicer-like1 (DCL1, an RNAse III enzyme), miRNAs bind and guide their effector protein named argonaute 1 (AGO1) to silence the expression of target RNAs containing their complementary sequences in plants. miRNA levels and activities are tightly controlled to ensure their functions in various biological processes such as development, metabolism and responses to abiotic and biotic stresses. Studies have identified many factors that involve in miRNA accumulation and activities. Characterization of these factors in turn greatly improves our understanding of the processes related to miRNAs. Here, we review recent progress of mechanisms underlying miRNA expression and functions in plants.

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References

  1. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    CAS  PubMed  Google Scholar 

  2. Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    CAS  PubMed  Google Scholar 

  3. Bologna NG, Voinnet O (2014) The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu Rev Plant Biol 65:473–503

  4. Rogers K, Chen X (2013) Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25:2383–2399

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626

    CAS  PubMed Central  PubMed  Google Scholar 

  6. Park W, Li J, Song R, Messing J, Chen X (2002) Carpel factory, a dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495

    CAS  PubMed  Google Scholar 

  7. Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605–1619

    CAS  PubMed Central  PubMed  Google Scholar 

  8. Meyers BC, Souret FF, Lu C, Green PJ (2006) Sweating the small stuff: microRNA discovery in plants. Curr Opin Biotechnol 17:139–146

    CAS  PubMed  Google Scholar 

  9. Chen X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–44

    PubMed  Google Scholar 

  10. Martin RC, Liu PP, Goloviznina NA, Nonogaki H (2010) microRNA, seeds, and Darwin?: diverse function of miRNA in seed biology and plant responses to stress. J Exp Bot 61:2229–2234

    CAS  PubMed  Google Scholar 

  11. Poethig RS (2009) Small RNAs and developmental timing in plants. Curr Opin Genet Dev 19:374–378

    CAS  PubMed Central  PubMed  Google Scholar 

  12. Moreno-Risueno MA, Van Norman JM, Benfey PN (2012) Transcriptional switches direct plant organ formation and patterning. Curr Top Dev Biol 98:229–257

    PubMed  Google Scholar 

  13. Chuck G, Candela H, Hake S (2009) Big impacts by small RNAs in plant development. Curr Opin Plant Biol 12:81–86

    CAS  PubMed  Google Scholar 

  14. Seo JK, Wu J, Lii Y, Li Y, Jin H (2013) Contribution of small RNA pathway components in plant immunity. Mol Plant-Microbe Interact : MPMI 26:617–625

    CAS  PubMed Central  PubMed  Google Scholar 

  15. Sunkar R, Li YF, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203

    CAS  PubMed  Google Scholar 

  16. Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137–148

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Yu B, Yang Z, Li J, Minakhina S, Yang M, Padgett RW, Steward R, Chen X (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307:932–935

    CAS  PubMed  Google Scholar 

  18. Park MY, Wu G, Gonzalez-Sulser A, Vaucheret H, Poethig RS (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci USA 102:3691–3696

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 102:11928–11933

    CAS  PubMed Central  PubMed  Google Scholar 

  20. Mourrain P, Beclin C, Elmayan T, Feuerbach F, Godon C, Morel JB, Jouette D, Lacombe AM, Nikic S, Picault N, Remoue K, Sanial M, Vo TA, Vaucheret H (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533–542

    CAS  PubMed  Google Scholar 

  21. Wu L, Zhang Q, Zhou H, Ni F, Wu X, Qi Y (2009) Rice MicroRNA effector complexes and targets. Plant Cell 21:3421–3435

    CAS  PubMed Central  PubMed  Google Scholar 

  22. Nozawa M, Miura S, Nei M (2012) Origins and evolution of microRNA genes in plant species. Genome Biol Evol 4:230–239

    PubMed Central  PubMed  Google Scholar 

  23. Coruh C, Shahid S, Axtell MJ (2014) Seeing the forest for the trees: annotating small RNA producing genes in plants. Curr Opin Plant Biol 18C:87–95

    Google Scholar 

  24. Xie ZX, Allen E, Fahlgren N, Calamar A, Givan SA, Carrington JC (2005) Expression of Arabidopsis MIRNA genes. Plant Physiol 138:2145–2154

    CAS  PubMed Central  PubMed  Google Scholar 

  25. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36:D154–D158

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Yang GD, Yan K, Wu BJ, Wang YH, Gao YX, Zheng CC (2012) Genomewide analysis of intronic microRNAs in rice and Arabidopsis. J Genet 91:313–324

    CAS  PubMed  Google Scholar 

  27. Piriyapongsa J, Jordan IK (2008) Dual coding of siRNAs and miRNAs by plant transposable elements. RNA 14:814–821

    CAS  PubMed Central  PubMed  Google Scholar 

  28. Kim YJ, Zheng B, Yu Y, Won SY, Mo B, Chen X (2011) The role of Mediator in small and long noncoding RNA production in Arabidopsis thaliana. EMBO J 30:814–822

    CAS  PubMed Central  PubMed  Google Scholar 

  29. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799

    CAS  PubMed  Google Scholar 

  30. Zhang BH, Pan XP, Wang QL, Cobb GP, Anderson TA (2005) Identification and characterization of new plant microRNAs using EST analysis. Cell Res 15:336–360

    PubMed  Google Scholar 

  31. Hajheidari M, Farrona S, Huettel B, Koncz Z, Koncz C (2012) CDKF;1 and CDKD protein kinases regulate phosphorylation of serine residues in the C-terminal domain of Arabidopsis RNA polymerase II. Plant Cell 24:1626–1642

    CAS  PubMed Central  PubMed  Google Scholar 

  32. Yu B, Bi L, Zheng B, Ji L, Chevalier D, Agarwal M, Ramachandran V, Li W, Lagrange T, Walker JC, Chen X (2008) The FHA domain proteins DAWDLE in Arabidopsis and SNIP1 in humans act in small RNA biogenesis. Proc Natl Acad Sci USA 105:10073–10078

    CAS  PubMed Central  PubMed  Google Scholar 

  33. Megraw M, Baev V, Rusinov V, Jensen ST, Kalantidis K, Hatzigeorgiou AG (2006) MicroRNA promoter element discovery in Arabidopsis. RNA 12:1612–1619

    CAS  PubMed Central  PubMed  Google Scholar 

  34. Zhao X, Zhang H, Li L (2013) Identification and analysis of the proximal promoters of microRNA genes in Arabidopsis. Genomics 101:187–194

    CAS  PubMed  Google Scholar 

  35. Wang L, Song X, Gu L, Li X, Cao S, Chu C, Cui X, Chen X, Cao X (2013) NOT2 proteins promote polymerase II-dependent transcription and interact with multiple MicroRNA biogenesis factors in Arabidopsis. Plant Cell 25:715–727

    CAS  PubMed Central  PubMed  Google Scholar 

  36. Collart MA, Panasenko OO (2012) The Ccr4–not complex. Gene 492:42–53

    CAS  PubMed  Google Scholar 

  37. Palma K, Zhao Q, Cheng YT, Bi D, Monaghan J, Cheng W, Zhang Y, Li X (2007) Regulation of plant innate immunity by three proteins in a complex conserved across the plant and animal kingdoms. Genes Dev 21:1484–1493

    CAS  PubMed Central  PubMed  Google Scholar 

  38. Zhang S, Xie M, Ren G, Yu B (2013) CDC5, a DNA binding protein, positively regulates posttranscriptional processing and/or transcription of primary microRNA transcripts. Proc Natl Acad Sci USA 110:17588–17593

    CAS  PubMed Central  PubMed  Google Scholar 

  39. Yumul RE, Kim YJ, Liu X, Wang R, Ding J, Xiao L, Chen X (2013) POWERDRESS and diversified expression of the MIR172 gene family bolster the floral stem cell network. PLoS Genet 9:e1003218

    CAS  PubMed Central  PubMed  Google Scholar 

  40. Yant L, Mathieu J, Dinh TT, Ott F, Lanz C, Wollmann H, Chen X, Schmid M (2010) Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 22:2156–2170

    CAS  PubMed Central  PubMed  Google Scholar 

  41. Grigorova B, Mara C, Hollender C, Sijacic P, Chen X, Liu Z (2011) LEUNIG and SEUSS co-repressors regulate miR172 expression in Arabidopsis flowers. Development 138:2451–2456

    CAS  PubMed Central  PubMed  Google Scholar 

  42. Wang F, Perry SE (2013) Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol 161:1251–1264

    CAS  PubMed Central  PubMed  Google Scholar 

  43. Jeong DH, Park S, Zhai J, Gurazada SG, De Paoli E, Meyers BC, Green PJ (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23:4185–4207

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y (2007) Identification of drought-induced microRNAs in rice. Biochemical and biophysical research communications 354:585–590

    CAS  PubMed  Google Scholar 

  46. Liang G, He H, Yu D (2012) Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS ONE 7:e48951

    CAS  PubMed Central  PubMed  Google Scholar 

  47. Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) SQUAMOSA Promoter Binding Protein-Like7 Is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21:347–361

    CAS  PubMed Central  PubMed  Google Scholar 

  48. Baek D, Kim MC, Chun HJ, Kang S, Park HC, Shin G, Park J, Shen M, Hong H, Kim WY, Kim DH, Lee SY, Bressan RA, Bohnert HJ, Yun DJ (2013) Regulation of miR399f transcription by AtMYB2 affects phosphate starvation responses in Arabidopsis. Plant Physiol 161:362–373

    CAS  PubMed Central  PubMed  Google Scholar 

  49. Valoczi A, Varallyay E, Kauppinen S, Burgyan J, Havelda Z (2006) Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. Plant J 47:140–151

    CAS  PubMed  Google Scholar 

  50. Breakfield NW, Corcoran DL, Petricka JJ, Shen J, Sae-Seaw J, Rubio-Somoza I, Weigel D, Ohler U, Benfey PN (2012) High-resolution experimental and computational profiling of tissue-specific known and novel miRNAs in Arabidopsis. Genome Res 22:163–176

    CAS  PubMed Central  PubMed  Google Scholar 

  51. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vaten A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–321

    CAS  PubMed Central  PubMed  Google Scholar 

  52. Margis R, Fusaro AF, Smith NA, Curtin SJ, Watson JM, Finnegan EJ, Waterhouse PM (2006) The evolution and diversification of Dicers in plants. FEBS Lett 580:2442–2450

    CAS  PubMed  Google Scholar 

  53. Mateos JL, Bologna NG, Chorostecki U, Palatnik JF (2010) Identification of microRNA processing determinants by random mutagenesis of Arabidopsis MIR172a precursor. Curr Biol 20:49–54

    CAS  PubMed  Google Scholar 

  54. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20:3407–3425

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38:465–475

    CAS  PubMed  Google Scholar 

  56. Zhu H, Zhou Y, Castillo-Gonzalez C, Lu A, Ge C, Zhao YT, Duan L, Li Z, Axtell MJ, Wang XJ, Zhang X (2013) Bidirectional processing of pri-miRNAs with branched terminal loops by Arabidopsis Dicer-like1. Nat Struct Mol Biol 20:1106–1115

    CAS  PubMed Central  PubMed  Google Scholar 

  57. Song L, Axtell MJ, Fedoroff NV (2010) RNA secondary structural determinants of miRNA precursor processing in Arabidopsis. Curr Biol 20:37–41

    CAS  PubMed  Google Scholar 

  58. Werner S, Wollmann H, Schneeberger K, Weigel D (2010) Structure determinants for accurate processing of miR172a in Arabidopsis thaliana. Curr Biol 20:42–48

    CAS  PubMed  Google Scholar 

  59. Bologna NG, Mateos JL, Bresso EG, Palatnik JF (2009) A loop-to-base processing mechanism underlies the biogenesis of plant microRNAs miR319 and miR159. The EMBO journal 28:3646–3656

    CAS  PubMed Central  PubMed  Google Scholar 

  60. Cuperus JT, Montgomery TA, Fahlgren N, Burke RT, Townsend T, Sullivan CM, Carrington JC (2010) Identification of MIR390a precursor processing-defective mutants in Arabidopsis by direct genome sequencing. Proc Natl Acad Sci USA 107:466–471

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Grigg SP, Canales C, Hay A, Tsiantis M (2005) SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis. Nature 437:1022–1026

    CAS  PubMed  Google Scholar 

  62. Yang L, Liu ZQ, Lu F, Dong AW, Huang H (2006) SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J 47:841–850

    CAS  PubMed  Google Scholar 

  63. Lobbes D, Rallapalli G, Schmidt DD, Martin C, Clarke J (2006) SERRATE: a new player on the plant microRNA scene. EMBO Rep 7:1052–1058

    CAS  PubMed Central  PubMed  Google Scholar 

  64. Han MH, Goud S, Song L, Fedoroff N (2004) The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc Natl Acad Sci USA 101:1093–1098

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Vazquez F, Gasciolli V, Crete P, Vaucheret H (2004) The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr Biol 14:346–351

    CAS  PubMed  Google Scholar 

  66. Kurihara Y, Takashi Y, Watanabe Y (2006) The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12:206–212

    CAS  PubMed Central  PubMed  Google Scholar 

  67. Ren G, Xie M, Dou Y, Zhang S, Zhang C, Yu B (2012) Regulation of miRNA abundance by RNA binding protein TOUGH in Arabidopsis. Proc Natl Acad Sci USA 109:12817–12821

    CAS  PubMed Central  PubMed  Google Scholar 

  68. Fang Y, Spector DL (2007) Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr Biol 17:818–823

    CAS  PubMed Central  PubMed  Google Scholar 

  69. Song L, Han MH, Lesicka J, Fedoroff N (2007) Arabidopsis primary microRNA processing proteins HYL1 and DCL1 define a nuclear body distinct from the Cajal body. Proc Natl Acad Sci USA 104:5437–5442

    CAS  PubMed Central  PubMed  Google Scholar 

  70. Fujioka Y, Utsumi M, Ohba Y, Watanabe Y (2007) Location of a possible miRNA processing site in SmD3/SmB nuclear bodies in Arabidopsis. Plant Cell Physiol 48:1243–1253

    CAS  PubMed  Google Scholar 

  71. Dong Z, Han MH, Fedoroff N (2008) The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc Natl Acad Sci USA 105:9970–9975

    CAS  PubMed Central  PubMed  Google Scholar 

  72. Liu C, Axtell MJ, Fedoroff NV (2012) The helicase and RNaseIIIa domains of Arabidopsis Dicer-Like1 modulate catalytic parameters during microRNA biogenesis. Plant Physiol 159:748–758

    CAS  PubMed Central  PubMed  Google Scholar 

  73. Lu C, Fedoroff N (2000) A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12:2351–2366

    CAS  PubMed Central  PubMed  Google Scholar 

  74. Yang SW, Chen HY, Yang J, Machida S, Chua NH, Yuan YA (2010) Structure of Arabidopsis HYPONASTIC LEAVES1 and its molecular implications for miRNA processing. Structure 18:594–605

    CAS  PubMed Central  PubMed  Google Scholar 

  75. Wu F, Yu L, Cao W, Mao Y, Liu Z, He Y (2007) The N-terminal double-stranded RNA binding domains of Arabidopsis HYPONASTIC LEAVES1 are sufficient for pre-microRNA processing. Plant Cell 19:914–925

    CAS  PubMed Central  PubMed  Google Scholar 

  76. Machida S, Chen HY, Adam Yuan Y (2011) Molecular insights into miRNA processing by Arabidopsis thaliana SERRATE. Nucleic Acids Res 39:7828–7836

    CAS  PubMed Central  PubMed  Google Scholar 

  77. Iwata Y, Takahashi M, Fedoroff NV, Hamdan SM (2013) Dissecting the interactions of SERRATE with RNA and DICER-LIKE 1 in Arabidopsis microRNA precursor processing. Nucleic Acids Res 41:9129–9140

    CAS  PubMed Central  PubMed  Google Scholar 

  78. Ren G, Yu B (2012) Critical roles of RNA-binding proteins in miRNA biogenesis in Arabidopsis. RNA Biol 9:1424–1428

    CAS  PubMed  Google Scholar 

  79. Ren G, Yu B (2012) Post-transcriptional control of miRNA abundance in Arabidopsis. Plant Signal Behav 7:1443–1446

    CAS  PubMed Central  PubMed  Google Scholar 

  80. Lau PW, Guiley KZ, De N, Potter CS, Carragher B, MacRae IJ (2012) The molecular architecture of human Dicer. Nat Struct Mol Biol 19:436–440

    CAS  PubMed Central  PubMed  Google Scholar 

  81. Raczynska KD, Stepien A, Kierzkowski D, Kalak M, Bajczyk M, McNicol J, Simpson CG, Szweykowska-Kulinska Z, Brown JW, Jarmolowski A (2014) The SERRATE protein is involved in alternative splicing in Arabidopsis thaliana. Nucleic Acids Res 42:1224–1244

    CAS  PubMed Central  PubMed  Google Scholar 

  82. Laubinger S, Zeller G, Henz SR, Buechel S, Sachsenberg T, Wang JW, Ratsch G, Weigel D (2010) Global effects of the small RNA biogenesis machinery on the Arabidopsis thaliana transcriptome. Proc Natl Acad Sci USA 107:17466–17473

    CAS  PubMed Central  PubMed  Google Scholar 

  83. Lin Z, Yin K, Zhu D, Chen Z, Gu H, Qu LJ (2007) AtCDC5 regulates the G2 to M transition of the cell cycle and is critical for the function of Arabidopsis shoot apical meristem. Cell Res 17:815–828

    CAS  PubMed  Google Scholar 

  84. Zhan X, Wang B, Li H, Liu R, Kalia RK, Zhu JK, Chinnusamy V (2012) Arabidopsis proline-rich protein important for development and abiotic stress tolerance is involved in microRNA biogenesis. Proc Natl Acad Sci USA 109:18198–18203

    CAS  PubMed Central  PubMed  Google Scholar 

  85. Speth C, Willing EM, Rausch S, Schneeberger K, Laubinger S (2013) RACK1 scaffold proteins influence miRNA abundance in Arabidopsis. Plant J 76:433–445

    CAS  PubMed  Google Scholar 

  86. Wu X, Shi Y, Li J, Xu L, Fang Y, Li X, Qi Y (2013) A role for the RNA-binding protein MOS2 in microRNA maturation in Arabidopsis. Cell Res 23:645–657

    CAS  PubMed Central  PubMed  Google Scholar 

  87. Ben Chaabane S, Liu R, Chinnusamy V, Kwon Y, Park JH, Kim SY, Zhu JK, Yang SW, Lee BH (2013) STA1, an Arabidopsis pre-mRNA processing factor 6 homolog, is a new player involved in miRNA biogenesis. Nucleic Acids Res 41:1984–1997

    CAS  PubMed Central  PubMed  Google Scholar 

  88. Kim W, Benhamed M, Servet C, Latrasse D, Zhang W, Delarue M, Zhou DX (2009) Histone acetyltransferase GCN5 interferes with the miRNA pathway in Arabidopsis. Cell Res 19:899–909

    CAS  PubMed  Google Scholar 

  89. Xie Z, Kasschau KD, Carrington JC (2003) Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr Biol 13:784–789

    CAS  PubMed  Google Scholar 

  90. Pouch-Pelissier MN, Pelissier T, Elmayan T, Vaucheret H, Boko D, Jantsch MF, Deragon JM (2008) SINE RNA induces severe developmental defects in Arabidopsis thaliana and interacts with HYL1 (DRB1), a key member of the DCL1 complex. PLoS Genet 4:e1000096

    PubMed Central  PubMed  Google Scholar 

  91. Machida S, Yuan YA (2013) Crystal structure of Arabidopsis thaliana Dawdle forkhead-associated domain reveals a conserved phospho-threonine recognition cleft for dicer-like 1 binding. Mol Plant 6:1290–1300

    CAS  PubMed  Google Scholar 

  92. Engelsberger WR, Schulze WX (2012) Nitrate and ammonium lead to distinct global dynamic phosphorylation patterns when resupplied to nitrogen-starved Arabidopsis seedlings. Plant J 69:978–995

    CAS  PubMed Central  PubMed  Google Scholar 

  93. Manavella PA, Hagmann J, Ott F, Laubinger S, Franz M, Macek B, Weigel D (2012) Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1. Cell 151:859–870

    CAS  PubMed  Google Scholar 

  94. Kruszka K, Pacak A, Swida-Barteczka A, Stefaniak AK, Kaja E, Sierocka I, Karlowski W, Jarmolowski A, Szweykowska-Kulinska Z (2013) Developmentally regulated expression and complex processing of barley pri-microRNAs. BMC Genom 14:34

    CAS  Google Scholar 

  95. Szarzynska B, Sobkowiak L, Pant BD, Balazadeh S, Scheible WR, Mueller-Roeber B, Jarmolowski A, Szweykowska-Kulinska Z (2009) Gene structures and processing of Arabidopsis thaliana HYL1-dependent pri-miRNAs. Nucleic Acids Res 37:3083–3093

    CAS  PubMed Central  PubMed  Google Scholar 

  96. Yan K, Liu P, Wu CA, Yang GD, Xu R, Guo QH, Huang JG, Zheng CC (2012) Stress-induced alternative splicing provides a mechanism for the regulation of microRNA processing in Arabidopsis thaliana. Mol Cell 48:521–531

    CAS  PubMed  Google Scholar 

  97. Jia F, Rock CD (2013) MIR846 and MIR842 comprise a cistronic MIRNA pair that is regulated by abscisic acid by alternative splicing in roots of Arabidopsis. Plant Mol Biol 81:447–460

    CAS  PubMed Central  PubMed  Google Scholar 

  98. Hirsch J, Lefort V, Vankersschaver M, Boualem A, Lucas A, Thermes C, d’Aubenton-Carafa Y, Crespi M (2006) Characterization of 43 non-protein-coding mRNA genes in Arabidopsis, including the MIR162a-derived transcripts. Plant Physiol 140:1192–1204

    CAS  PubMed Central  PubMed  Google Scholar 

  99. Bielewicz D, Kalak M, Kalyna M, Windels D, Barta A, Vazquez F, Szweykowska-Kulinska Z, Jarmolowski A (2013) Introns of plant pri-miRNAs enhance miRNA biogenesis. EMBO Rep 14:622–628

    CAS  PubMed Central  PubMed  Google Scholar 

  100. Schwab R, Speth C, Laubinger S, Voinnet O (2013) Enhanced microRNA accumulation through stemloop-adjacent introns. EMBO Rep 14:615–621

    CAS  PubMed Central  PubMed  Google Scholar 

  101. Raczynska KD, Simpson CG, Ciesiolka A, Szewc L, Lewandowska D, McNicol J, Szweykowska-Kulinska Z, Brown JW, Jarmolowski A (2010) Involvement of the nuclear cap-binding protein complex in alternative splicing in Arabidopsis thaliana. Nucleic Acids Res 38:265–278

    CAS  PubMed Central  PubMed  Google Scholar 

  102. Gregory BD, O’Malley RC, Lister R, Urich MA, Tonti-Filippini J, Chen H, Millar AH, Ecker JR (2008) A link between RNA metabolism and silencing affecting Arabidopsis development. Dev Cell 14:854–866

    CAS  PubMed  Google Scholar 

  103. Laubinger S, Sachsenberg T, Zeller G, Busch W, Lohmann JU, Ratsch G, Weigel D (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 105:8795–8800

    CAS  PubMed Central  PubMed  Google Scholar 

  104. Kim S, Yang JY, Xu J, Jang IC, Prigge MJ, Chua NH (2008) Two cap-binding proteins CBP20 and CBP80 are involved in processing primary MicroRNAs. Plant Cell Physiol 49:1634–1644

    CAS  PubMed Central  PubMed  Google Scholar 

  105. Gruber JJ, Zatechka DS, Sabin LR, Yong J, Lum JJ, Kong M, Zong WX, Zhang Z, Lau CK, Rawlings J, Cherry S, Ihle JN, Dreyfuss G, Thompson CB (2009) Ars2 links the nuclear cap-binding complex to RNA interference and cell proliferation. Cell 138:328–339

    CAS  PubMed Central  PubMed  Google Scholar 

  106. Levine E, McHale P, Levine H (2007) Small regulatory RNAs may sharpen spatial expression patterns. PLoS Comput Biol 3:e233

    PubMed Central  PubMed  Google Scholar 

  107. Muraro D, Mellor N, Pound MP, Help H, Lucas M, Chopard J, Byrne HM, Godin C, Hodgman TC, King JR, Pridmore TP, Helariutta Y, Bennett MJ, Bishopp A (2014) Integration of hormonal signaling networks and mobile microRNAs is required for vascular patterning in Arabidopsis roots. Proc Natl Acad Sci USA 111:857–862

    CAS  PubMed Central  PubMed  Google Scholar 

  108. Yang ZY, Ebright YW, Yu B, Chen XM (2006) HEN1 recognizes 21-24 nt small RNA duplexes and deposits a methyl group onto the 2′ OH of the 3′ terminal nucleotide. Nucleic Acids Res 34:667–675

    CAS  PubMed Central  PubMed  Google Scholar 

  109. Boutet S, Vazquez F, Liu J, Beclin C, Fagard M, Gratias A, Morel JB, Crete P, Chen X, Vaucheret H (2003) Arabidopsis HEN1: a genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus resistance. Curr Biol 13:843–848

    CAS  PubMed  Google Scholar 

  110. Li J, Yang Z, Yu B, Liu J, Chen X (2005) Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr Biol 15:1501–1507

    CAS  PubMed  Google Scholar 

  111. Zhai J, Zhao Y, Simon SA, Huang S, Petsch K, Arikit S, Pillay M, Ji L, Xie M, Cao X, Yu B, Timmermans M, Yang B, Chen X, Meyers BC (2013) Plant microRNAs display differential 3′ truncation and tailing modifications that are ARGONAUTE1 dependent and conserved across species. Plant Cell 25:2417–2428

    CAS  PubMed Central  PubMed  Google Scholar 

  112. Huang Y, Ji L, Huang Q, Vassylyev DG, Chen X, Ma JB (2009) Structural insights into mechanisms of the small RNA methyltransferase HEN1. Nature 461:823–827

    CAS  PubMed  Google Scholar 

  113. Ren G, Chen X, Yu B (2012) Uridylation of miRNAs by hen1 suppressor1 in Arabidopsis. Curr Biol 22:695–700

    CAS  PubMed Central  PubMed  Google Scholar 

  114. Zhao Y, Yu Y, Zhai J, Ramachandran V, Dinh TT, Meyers BC, Mo B, Chen X (2012) The Arabidopsis nucleotidyl transferase HESO1 uridylates unmethylated small RNAs to trigger their degradation. Curr Biol 22:689–694

    CAS  PubMed Central  PubMed  Google Scholar 

  115. Ren G, Xie M, Zhang S, Vinovskis C, Chen X, Yu B (2014) Methylation protects microRNAs from an AGO1-associated activity that uridylates 5′ RNA fragments generated by AGO1 cleavage. Proc Natl Acad Sci USA 111:6365–6370

  116. Ibrahim F, Rymarquis LA, Kim EJ, Becker J, Balassa E, Green PJ, Cerutti H (2010) Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas. Proc Natl Acad Sci USA 107:3906–3911

    CAS  PubMed Central  PubMed  Google Scholar 

  117. Ramachandran V, Chen X (2008) Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 321:1490–1492

    CAS  PubMed Central  PubMed  Google Scholar 

  118. Yan J, Gu Y, Jia X, Kang W, Pan S, Tang X, Chen X, Tang G (2012) Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell 24:415–427

    CAS  PubMed Central  PubMed  Google Scholar 

  119. Han BW, Hung JH, Weng Z, Zamore PD, Ameres SL (2011) The 3′-to-5′ exoribonuclease Nibbler shapes the 3′ ends of microRNAs bound to Drosophila Argonaute1. Curr Biol 21:1878–1887

    CAS  PubMed Central  PubMed  Google Scholar 

  120. Liu N, Abe M, Sabin LR, Hendriks GJ, Naqvi AS, Yu Z, Cherry S, Bonini NM (2011) The exoribonuclease Nibbler controls 3′ end processing of microRNAs in Drosophila. Curr Biol 21:1888–1893

    CAS  PubMed Central  PubMed  Google Scholar 

  121. Vaucheret H (2008) Plant argonautes. Trends Plant Sci 13:350–358

    CAS  PubMed  Google Scholar 

  122. Tolia NH, Joshua-Tor L (2007) Slicer and the argonautes. Nat Chem Biol 3:36–43

    CAS  PubMed  Google Scholar 

  123. Rivas FV, Tolia NH, Song JJ, Aragon JP, Liu J, Hannon GJ, Joshua-Tor L (2005) Purified Argonaute2 and an siRNA form recombinant human RISC. Nat Struct Mol Biol 12:340–349

    CAS  PubMed  Google Scholar 

  124. Hutvagner G, Simard MJ (2008) Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 9:22–32

    CAS  PubMed  Google Scholar 

  125. Liu X, Lu T, Dou Y, Yu B, Zhang C (2014) Identification of RNA silencing components in soybean and sorghum. BMC Bioinformatics 15:4

    PubMed Central  PubMed  Google Scholar 

  126. Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C, Chen S, Hannon GJ, Qi Y (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133:116–127

    CAS  PubMed Central  PubMed  Google Scholar 

  127. Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC (2008) Specificity of argonaute7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128–141

    CAS  PubMed  Google Scholar 

  128. Mallory A, Vaucheret H (2010) Form, function, and regulation of argonaute proteins. Plant Cell 22:3879–3889

    CAS  PubMed Central  PubMed  Google Scholar 

  129. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520

    CAS  PubMed  Google Scholar 

  130. Vaucheret H, Vazquez F, Crete P, Bartel DP (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18:1187–1197

    CAS  PubMed Central  PubMed  Google Scholar 

  131. Earley K, Smith M, Weber R, Gregory B, Poethig R (2010) An endogenous F-box protein regulates argonaute1 in Arabidopsis thaliana. Silence 1:15

    CAS  PubMed Central  PubMed  Google Scholar 

  132. Derrien B, Baumberger N, Schepetilnikov M, Viotti C, De Cillia J, Ziegler-Graff V, Isono E, Schumacher K, Genschik P (2012) Degradation of the antiviral component argonaute1 by the autophagy pathway. Proc Natl Acad Sci USA 109:15942–15946

    CAS  PubMed Central  PubMed  Google Scholar 

  133. Zhu H, Hu F, Wang R, Zhou X, Sze SH, Liou LW, Barefoot A, Dickman M, Zhang X (2011) Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145:242–256

    CAS  PubMed Central  PubMed  Google Scholar 

  134. Eamens AL, Smith NA, Curtin SJ, Wang MB, Waterhouse PM (2009) The Arabidopsis thaliana double-stranded RNA binding protein DRB1 directs guide strand selection from microRNA duplexes. RNA 15:2219–2235

    CAS  PubMed Central  PubMed  Google Scholar 

  135. Smith MR, Willmann MR, Wu G, Berardini TZ, Moller B, Weijers D, Poethig RS (2009) Cyclophilin 40 is required for microRNA activity in Arabidopsis. Proc Natl Acad Sci USA 106:5424–5429

    CAS  PubMed Central  PubMed  Google Scholar 

  136. Iki T, Yoshikawa M, Meshi T, Ishikawa M (2012) Cyclophilin 40 facilitates HSP90-mediated RISC assembly in plants. EMBO J 31:267–278

    CAS  PubMed Central  PubMed  Google Scholar 

  137. Iki T, Yoshikawa M, Nishikiori M, Jaudal MC, Matsumoto-Yokoyama E, Mitsuhara I, Meshi T, Ishikawa M (2010) In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90. Mol Cell 39:282–291

    CAS  PubMed  Google Scholar 

  138. Earley KW, Poethig RS (2011) Binding of the cyclophilin 40 ortholog SQUINT to Hsp90 protein is required for SQUINT function in Arabidopsis. J Biol Chem 286:38184–38189

    CAS  PubMed Central  PubMed  Google Scholar 

  139. Kwak PB, Tomari Y (2012) The N domain of Argonaute drives duplex unwinding during RISC assembly. Nat Struct Mol Biol 19:145–151

    CAS  PubMed  Google Scholar 

  140. Mallory AC, Reinhart BJ, Jones-Rhoades MW, Tang G, Zamore PD, Barton MK, Bartel DP (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J 23:3356–3364

    CAS  PubMed Central  PubMed  Google Scholar 

  141. Liu Q, Wang F, Axtell MJ (2014) Analysis of complementarity requirements for plant MicroRNA targeting using a Nicotiana benthamiana quantitative transient assay. Plant Cell 26:741–753

    CAS  PubMed Central  PubMed  Google Scholar 

  142. Li J, Reichel M, Millar AA (2014) Determinants beyond both complementarity and cleavage govern microR159 efficacy in Arabidopsis. PLoS Genet 10:e1004232

    PubMed Central  PubMed  Google Scholar 

  143. Carbonell A, Fahlgren N, Garcia-Ruiz H, Gilbert KB, Montgomery TA, Nguyen T, Cuperus JT, Carrington JC (2012) Functional analysis of three Arabidopsis argonautes using slicer-defective mutants. Plant Cell 24:3613–3629

    CAS  PubMed Central  PubMed  Google Scholar 

  144. Llave C, Xie Z, Kasschau KD, Carrington JC (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056

    CAS  PubMed  Google Scholar 

  145. Souret FF, Kastenmayer JP, Green PJ (2004) AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol Cell 15:173–183

    CAS  PubMed  Google Scholar 

  146. Ibrahim F, Rohr J, Jeong WJ, Hesson J, Cerutti H (2006) Untemplated oligoadenylation promotes degradation of RISC-cleaved transcripts. Science 314:1893

    CAS  PubMed  Google Scholar 

  147. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037

    CAS  PubMed  Google Scholar 

  148. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527

    CAS  PubMed  Google Scholar 

  149. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190

    CAS  PubMed  Google Scholar 

  150. Li S, Liu L, Zhuang X, Yu Y, Liu X, Cui X, Ji L, Pan Z, Cao X, Mo B, Zhang F, Raikhel N, Jiang L, Chen X (2013) MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153:562–574

    CAS  PubMed Central  PubMed  Google Scholar 

  151. Lanet E, Delannoy E, Sormani R, Floris M, Brodersen P, Crete P, Voinnet O, Robaglia C (2009) Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell 21:1762–1768

    CAS  PubMed Central  PubMed  Google Scholar 

  152. Reynoso MA, Blanco FA, Bailey-Serres J, Crespi M, Zanetti ME (2012) Selective recruitment of mRNAs and miRNAs to polyribosomes in response to rhizobia infection in Medicago truncatula. Plant J 73:289–301

  153. Iwakawa HO, Tomari Y (2013) Molecular insights into microRNA-mediated translational repression in plants. Mol Cell 52:591–601

    CAS  PubMed  Google Scholar 

  154. Liu J, Valencia-Sanchez MA, Hannon GJ, Parker R (2005) MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat Cell Biol 7:719–723

    CAS  PubMed Central  PubMed  Google Scholar 

  155. Yang L, Wu G, Poethig RS (2012) Mutations in the GW-repeat protein SUO reveal a developmental function for microRNA-mediated translational repression in Arabidopsis. Proc Natl Acad Sci USA 109:315–320

    CAS  PubMed Central  PubMed  Google Scholar 

  156. Behm-Ansmant I, Rehwinkel J, Doerks T, Stark A, Bork P, Izaurralde E (2006) mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 20:1885–1898

    CAS  PubMed Central  PubMed  Google Scholar 

  157. Wu L, Fan J, Belasco JG (2006) MicroRNAs direct rapid deadenylation of mRNA. Proc Natl Acad Sci USA 103:4034–4039

    CAS  PubMed Central  PubMed  Google Scholar 

  158. Motomura K, Le QT, Kumakura N, Fukaya T, Takeda A, Watanabe Y (2012) The role of decapping proteins in the miRNA accumulation in Arabidopsis thaliana. RNA Biol 9:644–652

    CAS  PubMed  Google Scholar 

  159. Li JF, Chung HS, Niu Y, Bush J, McCormack M, Sheen J (2013) Comprehensive protein-based artificial microRNA screens for effective gene silencing in plants. Plant Cell 25:1507–1522

    CAS  PubMed Central  PubMed  Google Scholar 

  160. Grant-Downton R, Kourmpetli S, Hafidh S, Khatab H, Le Trionnaire G, Dickinson H, Twell D (2013) Artificial microRNAs reveal cell-specific differences in small RNA activity in pollen. Curr Biol 23:R599–R601

    CAS  PubMed  Google Scholar 

  161. Stoppin-Mellet V, Gaillard J, Vantard M (2006) Katanin’s severing activity favors bundling of cortical microtubules in plants. Plant J 46:1009–1017

    CAS  PubMed  Google Scholar 

  162. Brodersen P, Sakvarelidze-Achard L, Schaller H, Khafif M, Schott G, Bendahmane A, Voinnet O (2012) Isoprenoid biosynthesis is required for miRNA function and affects membrane association of argonaute 1 in Arabidopsis. Proc Natl Acad Sci USA 109:1778–1783

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by a National Science Foundation Grant MCB-1121193 (to B. Y).

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  1. Center for Plant Science Innovation and School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE, 68588–0660, USA

    Meng Xie, Shuxin Zhang & Bin Yu

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  1. Meng Xie
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  2. Shuxin Zhang
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  3. Bin Yu
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Correspondence to Bin Yu.

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M. Xie and S. Zhang contributed equally to this work.

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Xie, M., Zhang, S. & Yu, B. microRNA biogenesis, degradation and activity in plants. Cell. Mol. Life Sci. 72, 87–99 (2015). https://doi.org/10.1007/s00018-014-1728-7

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