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Cited by 176Plant Molecular Biology ResearchChromosomal and Genetic VariationsEpigenetics and DNA Methylation

siRNAs from miRNA sites mediate DNA methylation of target genes

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Chellappan, Padmanabhan, Xia, Jing, Zhou, Xuefeng, Gao, Shang, Zhang, Xiaoming, Coutino, Gabriela, Vazquez, Franck, Zhang, Weixiong +1 more·2010·Nucleic Acids Research
DOI 10.1093/nar/gkq590PMC PMC2978365
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Abstract

Arabidopsis microRNA (miRNA) genes (MIR) give rise to 20- to 22-nt miRNAs that are generated predominantly by the type III endoribonuclease Dicer-like 1 (DCL1) but do not require any RNA-dependent RNA Polymerases (RDRs) or RNA Polymerase IV (Pol IV). Here, we identify a novel class of non-conserved MIR genes that give rise to two small RNA species, a 20- to 22-nt species and a 23- to 27-nt species, at the same site. Genetic analysis using small RNA pathway mutants reveals that the 20- to 22-nt small RNAs are typical miRNAs generated by DCL1 and are associated with Argonaute 1 (AGO1). In contrast, the accumulation of the 23- to 27-nt small RNAs from the miRNA-generating sites is dependent on DCL3, RDR2 and Pol IV, components of the typical heterochromatic small interfering RNA (hc-siRNA) pathway. We further demonstrate that these MIR-derived siRNAs associate with AGO4 and direct DNA methylation at some of their target loci in trans. In addition, we find that at the miRNA-generating sites, some conserved canonical MIR genes also produce siRNAs, which also induce DNA methylation at some of their target sites. Our systematic examination of published small RNA deep sequencing datasets of rice and moss suggests that this type of dual functional MIRs exist broadly in plants.

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  • In Arabidopsis thaliana, microRNAs and small interfering RNAs are essential regulators of plant development, guide DNA methylation, and act as transcriptional repressors.

    “As proven in the model species Arabidopsis thaliana, microRNAs (miRNA) and small interfering RNAs (siRNA) are essential regulators of plant development, guide DNA methylation in plants (especially de novo methylation), and act as transcriptional repressors [127,128].”

    From Somaclonal Variation—Advantage or Disadvantage in Micropropagation of the Medicinal Plants (2023) · cites this paper as [128]

    The Discussion (page unavailable) reports that Arabidopsis MIR-derived siRNAs direct de novo DNA methylation and regulate gene expression at the transcriptional level. It distinguishes these from typical miRNAs, which act mainly through post-transcriptional repression. The cited passages do not establish that both RNA classes are essential regulators of plant development. (LLM, conf=0.87)

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Research works printed but not linked: 46

  1. [1]Vazquez F Legrand S Windels D The biosynthetic pathways and biological scopes of plant small RNAs Trends Plant Sci. 2010 15 337 345 20427224
  2. [2]Ghildiyal M Zamore PD Small silencing RNAs: an expanding universe Nat. Rev. Genet. 2009 10 94 108 19148191 PMC2724769
  3. [3]Mallory AC Vaucheret H Functions of microRNAs and related small RNAs in plants Nat. Genet. 2006 38 S37 S37 16736022
  4. [4]Carrington JC Ambros V Role of microRNAs in plant and animal development Science 2003 301 336 338 12869753
  5. [5]Bartel DP MicroRNAs: genomics, biogenesis, mechanism, and function Cell 2004 116 281 297 14744438
  6. [6]Hamilton A Voinnet O Chappell L Baulcombe D Two classes of short interfering RNA in RNA silencing EMBO J. 2002 21 4671 4679 12198169 PMC125409
  7. [7]Hamilton AJ Baulcombe DC A species of small antisense RNA in posttranscriptional gene silencing in plants Science 1999 286 950 952 10542148
  8. [8]Chapman EJ Carrington JC Specialization and evolution of endogenous small RNA pathways Nat. Rev. Genet. 2007 8 884 896 17943195
  9. [9]Vazquez F Blevins T Ailhas J Boller T Meins FJ Evolution of Arabidopsis MIR genes generates novel microRNA classes Nucleic Acids Res. 2008 36 6429 6438 18842626 PMC2582634
  10. [10]Bao N Lye KW Barton MK MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome Dev. Cell 2004 7 629 630 15525527
  11. [11]Khraiwesh B Arif MA Seumel GI Ossowski S Weigel D Reski R Frank W Transcriptional control of gene expression by microRNAs Cell 2010 140 111 122 20085706
  12. [12]Pikaard CS Haag JR Ream T Wierzbicki AT Roles of RNA polymerase IV in gene silencing Trends Plant Sci. 2008 13 390 397 18514566 PMC2679257
  13. [13]Matzke M Kanno T Daxinger L Huettel B Matzke AJ RNA-mediated chromatin-based silencing in plants Curr. Opin. Cell Biol. 2009 21 367 376 19243928
  14. [14]Katiyar-Agarwal S Morgan R Dahlbeck D Borsani O Villegas A Zhu JK Staskawicz BJ Jin HL A pathogen-inducible endogenous siRNA in plant immunity Proc. Natl Acad. Sci. USA 2006 103 18002 18007 17071740 PMC1693862
  15. [15]Chellappan P Jin H Discovery of plant microRNAs and short-interfering RNAs by deep parallel sequencing Methods Mol. Biol. 2009 495 121 132 19085152
  16. [16]Pall GS Servat-C C Byrne J Ritchie L Hamilton A Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by northern blot Nucleic Acids Res. 2007 35 E60 17405769 PMC1885651
  17. [17]He XJ Hsu YF Pontes O Zhu J Lu J Bressan RA Pikaard C Wang CS Zhu JK NRPD4, a protein related to the RPB4 subunit of RNA polymerase II, is a component of RNA polymerases IV and V and is required for RNA-directed DNA methylation Genes Dev. 2009 23 318 330 19204117 PMC2648547
  18. [18]Sunkar R Zhou X Zheng Y Zhang W Zhu J-K Identification of novel and candidate miRNAs in rice by high throughput sequencing BMC Plant Biol. 2008 8 25 18312648 PMC2292181
  19. [19]Hofacker IL Vienna RNA secondary structure server Nucleic Acids Res. 2003 31 3429 3431 12824340 PMC169005
  20. [20]Xu Y Zhou X Zhang W MicroRNA prediction with a novel ranking algorithm based on random walks Bioinformatics 2008 24 i50 i58 18586744 PMC2718653
  21. [21]Cho SH Addo-Quaye C Coruh C Arif MA Ma Z Frank W Axtell MJ Physcomitrella patens DCL3 is required for 22-24 nt siRNA accumulation, suppression of retrotransposon-derived transcripts, and normal development PLoS Genet. 2008 4 e1000314 19096705 PMC2600652
  22. [22]Zhang Y miRU: an automated plant miRNA target prediction server Nucleic Acids Res. 2005 33 W701 W704 15980567 PMC1160144
  23. [23]Jones-Rhoades MW Bartel DP Computational identification of plant MicroRNAs and their targets, including a stress-induced miRNA Mol. Cell 2004 14 787 799 15200956
  24. [24]Fahlgren N Carrington JC miRNA Target Prediction in Plants Methods Mol. Biol. 2010 592 51 57 19802588
  25. [25]Rajagopalan R Vaucheret H Trejo J Bartel DP A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana Gen. Dev. 2006 20 3407 3425 PMC1698448 17182867
  26. [26]Meyers BC Axtell MJ Bartel B Bartel DP Baulcombe D Bowman JL Cao X Carrington JC Chen X Green PJ Criteria for annotation of plant MicroRNAs Plant Cell 2008 20 3186 3190 19074682 PMC2630443
  27. [27]Katiyar-Agarwal S Gao S Vivian-Smith A Jin H A novel class of bacteria-induced small RNAs in Arabidopsis Gen. Dev. 2007 21 3123 3134 PMC2081978 18003861
  28. [28]Vazquez F Vaucheret H Rajagopalan R Lepers C Gasciolli V Mallory AC Hilbert JL Bartel DP Crete P Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs Mol. Cell 2004 16 69 79 15469823
  29. [29]Dong Z Han MH Fedoroff N The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1 Proc. Natl Acad. Sci. USA 2008 105 9970 9975 18632569 PMC2481344
  30. [30]Yu B Yang ZY Li JJ Minakhina S Yang MC Padgett RW Steward R Chen XM Methylation as a crucial step in plant microRNA biogenesis Science 2005 307 932 935 15705854 PMC5137370
  31. [31]Vaucheret H Plant ARGONAUTES Trends Plant Sci. 2008 13 350 358 18508405
  32. [32]Henderson IR Jacobsen SE Epigenetic inheritance in plants Nature 2007 447 418 424 17522675
  33. [33]Qi YJ He XY Wang XJ Kohany O Jurka J Hannon GJ Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation Nature 2006 443 1008 1012 16998468
  34. [34]Mi SJ Cai T Hu YG Chen Y Hodges E Ni FR Wu L Li S Zhou H Long CZ Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide Cell 2008 133 116 127 18342361 PMC2981139
  35. [35]Montgomery TA Howell MD Cuperus JT Li DW Hansen JE Alexander AL Chapman EJ Fahlgren N Allen E Carrington JC Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation Cell 2008 133 128 141 18342362
  36. [36]Werner S Wollmann H Schneeberger K Weigel D Structure determinants for accurate processing of miR172a in Arabidopsis thaliana Curr Biol. 2010 20 42 48 20015654
  37. [37]Wu L Zhou H Zhang Q Zhang J Ni F Liu C Qi Y DNA methylation mediated by a microRNA pathway Mol. Cell 2010 38 465 475 20381393
  38. [38]Cuperus JT Montgomery TA Fahlgren N Burke RT Townsend T Sullivan CM Carrington JC Identification of MIR390a precursor processing-defective mutants in Arabidopsis by direct genome sequencing Proc. Natl Acad. Sci. USA 2010 107 466 471 20018656 PMC2806713
  39. [39]Song L Axtell MJ Fedoroff NV RNA secondary structural determinants of miRNA precursor processing in Arabidopsis Curr. Biol. 2010 20 37 41 20015653
  40. [40]Mateos JL Bologna NG Chorostecki U Palatnik JF Identification of MicroRNA processing determinants by random mutagenesis of Arabidopsis MIR172a precursor Curr. Biol. 2010 20 49 54 20005105
  41. [41]Meyers BC Simon SA Zhai J MicroRNA processing: battle of the bulge Curr. Biol. 2010 20 R68 R70 20129044
  42. [42]Zheng B Wang Z Li S Yu B Liu J Chen X Intergenic transcription by RNA Polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis Genes Dev. 2009 23 2850 2860 19948763 PMC2800093
  43. [43]Lelandais-Brière C Naya L Sallet E Calenge F Frugier F Hartmann C Gouzy J Crespi M Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules Plant Cell 2009 21 2780 2796 19767456 PMC2768930
  44. [44]Kim VN Han J Siomi MC Biogenesis of small RNAs in animals Nat. Rev. Mol. Cell Biol. 2009 10 126 139 19165215
  45. [45]Malone CD Brennecke J Dus M Stark A McCombie WR Sachidanandam R Hannon GJ Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary Cell 2009 137 522 535 19395010 PMC2882632
  46. [46]Gunawardane LS Saito K Nishida KM Miyoshi K Kawamura Y Nagami T Siomi H Siomi MC A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila Science 2007 315 1587 1590 17322028

Cited by

Sorted by citations

Authors
Chellappan, P., Xia, J., Zhou, X., Gao, S., Zhang, X., Coutino, G., Vazquez, F., Zhang, W., & Jin, H.
Affiliations
University of California, Riverside (US)
Corresponding author
  • Zhang, Weixiong
  • Jin, Hailing
ORCID
Venue
Nucleic Acids Research
Publisher
Oxford University Press (OUP)
Published
2010-07-09
Volume
38
Issue
20
Pages
6883-6894
ISSN
  • 0305-1048 (ISSN-L)
  • 1362-4962
DOI
10.1093/nar/gkq590
PMC
PMC2978365
OpenAlex
W2166884499
Cited by
176
References
0
Citations by year
2026: 3 · 2025: 4 · 2024: 6 · 2023: 4 · 2022: 9 · 2021: 12 · 2020: 8 · 2019: 9 · 2018: 5 · 2017: 13 · 2016: 12 · 2015: 11 · 2014: 11 · 2013: 20 · 2012: 23
FWCI
26.56
Type
journal article
Language
en
Open access
Licence
Locations
  • Nucleic Acids Research (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • edoc (University of Basel) (acceptedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
  • reroDoc Digital Library (submittedVersion)
  • Digital Commons@Becker (Washington University School of Medicine) (submittedVersion, cc-by-nc)
  • HighWire Press Open Archive (submittedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
  • Zurich Open Repository and Archive (University of Zurich)
Funders
  • National Science Foundation (PPA-7517H, 0743797, 0642843)
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (126329)
  • National Institute of General Medical Sciences (R01GM093008)
  • National Institute of Allergy and Infectious Diseases (U54AI057160)
  • National Institute of Arthritis and Musculoskeletal and Skin Diseases (RC1AR058681)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Keywords
microRNA, siRNA, DNA methylation, Arabidopsis thaliana, DCL1, RNA polymerase IV, AGO1, small RNA biogenesis, rice, bryophytes
MeSH terms
Oryza, Genes, Plant, Arabidopsis, DNA Methylation, Arabidopsis Proteins, RNA, Small Interfering, MicroRNAs, Bryophyta, Genetic Loci, Argonaute Proteins

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