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Physcomitrella patens Small RNA Pathways

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Non Coding RNAs in Plants

Part of the book series: RNA Technologies ((RNATECHN))

Abstract

Small, non coding RNAs (sRNAs) are a distinct class of regulatory RNAs in plants and animals controlling a variety of biological processes. Given the great impact of sRNAs in biology, recent studies in model seed-plant species, particularly in Arabidopsis thaliana, focused on the identification, biogenesis and functional analysis of sRNAs. In seed plants, several classes of sRNAs with specific sizes and dedicated functions have evolved through a series of pathways, namely, microRNAs (miRNAs), repeat-associated small interfering RNAs (ra-siRNAs), natural antisense transcript-derived small interfering RNAs (nat-siRNAs) and trans-acting small interfering RNAs (ta-siRNAs). In the last few years, the analysis of plant sRNA pathways has been extended to the bryophyte Physcomitrella patens, a non-flowering, non-vascular ancient land plant, that diverged from the lineage of seed plants approximately 450 million years ago. Based on a number of characteristic features and its phylogenetic key position in land-plant evolution, P. patens emerged as a plant model species to address basic as well as applied topics in plant biology. The analysis of P. patens sRNA pathways has been recently advanced by the deep sequencing of sRNA libraries, the release of the P. patens genome that allowed the mapping of sRNA producing loci and first molecular analyses of P. patens mutants with targeted disruption of genes encoding essential components of endogenous sRNA pathways. Even though the major sRNA pathways are evolutionarily conserved in P. patens, there are particular differences in the functional components of sRNA pathways and the biological function of sRNAs. These include a specific amplification of initial miRNA and ta-siRNA signals by the generation of transitive siRNAs, deviating functions and specificities of DICER-LIKE proteins and an epigenetic gene silencing pathway that is triggered by miRNAs. Further, the conservation of miRNA biogenesis in P. patens was used to establish specific gene silencing by the expression of artificial miRNAs suited for functional gene analysis by reverse genetics approaches. These findings underline that P. patens serves as a valuable model system to study the evolution, diversity and function of plant sRNAs. Here, we summarise the current knowledge on different sRNA biogenesis pathways, their biological relevance and the expression of artificial miRNAs in P. patens.

Muhammad Asif Arif, Isam Fattash and Basel Khraiwesh contributed equally to this work.

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References

  • Addo-Quaye C, Eshoo TW, Bartel DP et al (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18:758–762

    Article  PubMed  CAS  Google Scholar 

  • Addo-Quaye C, Snyder JA, Park YB et al (2009) Sliced microRNA targets and precise loop-first processing of MIR319 hairpins revealed by analysis of the Physcomitrella patens degradome. RNA 15:2112–2121

    Article  PubMed  CAS  Google Scholar 

  • Adenot X, Elmayan T, Lauressergues D et al (2006) DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr Biol 16:927–932

    Article  PubMed  CAS  Google Scholar 

  • Alder MN, Dames S, Gaudet J et al (2003) Gene silencing in Caenorhabditis elegans by transitive RNA interference. RNA 9:25–32

    Article  PubMed  CAS  Google Scholar 

  • Allen E, Xie Z, Gustafson AM et al (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221

    Article  PubMed  CAS  Google Scholar 

  • Alvarez JP, Pekker I, Goldshmidt A et al (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18:1134–1151

    Article  PubMed  CAS  Google Scholar 

  • Arazi T, Talmor-Neiman M, Stav R et al (2005) Cloning and characterization of micro-RNAs from moss. Plant J 43:837–848

    Article  PubMed  CAS  Google Scholar 

  • Aufsatz W, Mette MF, van der Winden J et al (2002) RNA-directed DNA methylation in Arabidopsis. Proc Natl Acad Sci USA 99(Suppl 4):16499–16506

    Article  PubMed  CAS  Google Scholar 

  • Ausin I, Mockler TC, Chory J et al (2009) IDN1 and IDN2 are required for de novo DNA methylation in Arabidopsis thaliana. Nat Struct Mol Biol 16:1325–1327

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ (2009) The small RNAs of Physcomitrella patens: expression, function and evolution. Annu Plant Rev 36:113–142

    CAS  Google Scholar 

  • Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 17:1658–1673

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ, Jan C, Rajagopalan R et al (2006) A two-hit trigger for siRNA biogenesis in plants. Cell 127:565–577

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19:1750–1769

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bayne EH, White SA, Kagansky A et al (2010) Stc1: a critical link between RNAi and chromatin modification required for heterochromatin integrity. Cell 140:666–677

    Article  PubMed  CAS  Google Scholar 

  • Bernstein E, Caudy AA, Hammond SM et al (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–366

    Article  PubMed  CAS  Google Scholar 

  • Bezanilla M, Pan A, Quatrano RS (2003) RNA interference in the moss Physcomitrella patens. Plant Physiol 133:470–474

    Article  PubMed  CAS  Google Scholar 

  • Bezanilla M, Perroud PF, Pan A et al (2005a) An RNAi system in Physcomitrella patens with an internal marker for silencing allows for rapid identification of loss of function phenotypes. Plant Biol 7:251–257

    Article  PubMed  CAS  Google Scholar 

  • Bezanilla M, Perroud PF, Pan A et al (2005b) An RNAi system in Physcomitrella patens with an internal marker for silencing allows for rapid identification of loss of function phenotypes. Plant Biol (Stuttg) 7:251–257

    Article  CAS  Google Scholar 

  • Bohnsack MT, Czaplinski K, Gorlich D (2004) Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 10:185–191

    Article  PubMed  CAS  Google Scholar 

  • Borsani O, Zhu J, Verslues PE et al (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123:1279–1291

    Article  PubMed  CAS  Google Scholar 

  • Bouche N, Lauressergues D, Gasciolli V et al (2006) An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J 25:3347–3356

    Article  PubMed  CAS  Google Scholar 

  • Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M et al (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190

    Article  PubMed  CAS  Google Scholar 

  • Cai X, Hagedorn CH, Cullen BR (2004) Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 10:1957–1966

    Article  PubMed  CAS  Google Scholar 

  • Cao X, Jacobsen SE (2002) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci USA 99(Suppl 4):16491–16498

    Article  PubMed  CAS  Google Scholar 

  • Cao X, Aufsatz W, Zilberman D et al (2003) Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr Biol 13:2212–2217

    Article  PubMed  CAS  Google Scholar 

  • Chan SW, Zilberman D, Xie Z et al (2004) RNA silencing genes control de novo DNA methylation. Science 303:1336

    Article  PubMed  CAS  Google Scholar 

  • Chan SW, Henderson IR, Zhang X et al (2006) RNAi, DRD1, and histone methylation actively target developmentally important non-CG DNA methylation in Arabidopsis. PLoS Genet 2:e83

    Article  PubMed  CAS  Google Scholar 

  • Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025

    Article  PubMed  CAS  Google Scholar 

  • Chen HM, Chen LT, Patel K et al (2010) From the Cover: 22-nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc Natl Acad Sci USA 107:15269–15274

    Article  PubMed  CAS  Google Scholar 

  • Cho SH, Addo-Quaye C, Coruh C et al (2008) Physcomitrella patens DCL3 is required for 22–24 nt siRNA accumulation, suppression of retrotransposon-derived transcripts, and normal development. PLoS Genet 4:e1000314

    Article  PubMed  CAS  Google Scholar 

  • Dalmay T, Hamilton A, Rudd S et al (2000) An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101:543–553

    Article  PubMed  CAS  Google Scholar 

  • de la Luz Gutierrez-Nava M, Aukerman MJ, Sakai H et al (2008) Artificial trans-acting siRNAs confer consistent and effective gene silencing. Plant Physiol 147:543–551

    Article  PubMed  CAS  Google Scholar 

  • Denli AM, Tops BB, Plasterk RH et al (2004) Processing of primary microRNAs by the Microprocessor complex. Nature 432:231–235

    Article  PubMed  CAS  Google Scholar 

  • Dunoyer P, Himber C, Voinnet O (2005) DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat Genet 37:1356–1360

    Article  PubMed  CAS  Google Scholar 

  • Dunoyer P, Brosnan CA, Schott G et al (2010) An endogenous, systemic RNAi pathway in plants. EMBO J 29:1699–1712

    Article  PubMed  CAS  Google Scholar 

  • Elmayan T, Adenot X, Gissot L et al (2009) A neomorphic sgs3 allele stabilizing miRNA cleavage products reveals that SGS3 acts as a homodimer. FEBS J 276:835–844

    Article  PubMed  CAS  Google Scholar 

  • Emery JF, Floyd SK, Alvarez J et al (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13:1768–1774

    Article  PubMed  CAS  Google Scholar 

  • Fahlgren N, Montgomery TA, Howell MD et al (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16:939–944

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fattash I, Voss B, Reski R et al (2007) Evidence for the rapid expansion of microRNA-mediated regulation in early land plant evolution. BMC Plant Biol 7:13

    Article  PubMed  CAS  Google Scholar 

  • Floyd SK, Bowman JL (2004) Gene regulation: ancient microRNA target sequences in plants. Nature 428:485–486

    Article  PubMed  CAS  Google Scholar 

  • Gan J, Tropea JE, Austin BP et al (2006) Structural insight into the mechanism of double-stranded RNA processing by ribonuclease III. Cell 124:355–366

    Article  PubMed  CAS  Google Scholar 

  • Gandikota M, Birkenbihl RP, Hohmann S et al (2007) The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49:683–693

    Article  PubMed  CAS  Google Scholar 

  • Gao Z, Liu HL, Daxinger L et al (2010) An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465:106–109

    Article  PubMed  CAS  Google Scholar 

  • Garcia D, Collier SA, Byrne ME et al (2006) Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 16:933–938

    Article  PubMed  CAS  Google Scholar 

  • Gasciolli V, Mallory AC, Bartel DP et al (2005) Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr Biol 15:1494–1500

    Article  PubMed  CAS  Google Scholar 

  • Golden TA, Schauer SE, Lang JD et al (2002) SHORT INTEGUMENTS1/SUSPENSOR1/CARPEL FACTORY, a Dicer homolog, is a maternal effect gene required for embryo development in Arabidopsis. Plant Physiol 130:808–822

    Article  PubMed  Google Scholar 

  • Gregory RI, Yan KP, Amuthan G et al (2004) The Microprocessor complex mediates the genesis of microRNAs. Nature 432:235–240

    Article  PubMed  CAS  Google Scholar 

  • Griffiths-Jones S, Grocock RJ, van Dongen S et al (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34:D140–D144

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hall IM, Shankaranarayana GD, Noma K et al (2002) Establishment and maintenance of a heterochromatin domain. Science 297:2232–2237

    Article  PubMed  CAS  Google Scholar 

  • Hamilton A, Voinnet O, Chappell L et al (2002) Two classes of short interfering RNA in RNA silencing. EMBO J 21:4671–4679

    Article  PubMed  CAS  Google Scholar 

  • Hammond SM, Bernstein E, Beach D et al (2000) An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404:293–296

    Article  PubMed  CAS  Google Scholar 

  • Han J, Lee Y, Yeom KH et al (2004) The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 18:3016–3027

    Article  PubMed  CAS  Google Scholar 

  • Havecker ER, Wallbridge LM, Hardcastle TJ et al (2010) The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22:321–334

    Article  PubMed  CAS  Google Scholar 

  • Howell MD, Fahlgren N, Chapman EJ et al (2007) Genome-wide analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICER-LIKE4 pathway in Arabidopsis reveals dependency on miRNA- and tasiRNA-directed targeting. Plant Cell 19:926–942

    Article  PubMed  CAS  Google Scholar 

  • Huettel B, Kanno T, Daxinger L et al (2006) Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J 25:2828–2836

    Article  PubMed  CAS  Google Scholar 

  • Huettel B, Kanno T, Daxinger L et al (2007) RNA-directed DNA methylation mediated by DRD1 and Pol IVb: a versatile pathway for transcriptional gene silencing in plants. Biochim Biophys Acta 1769:358–374

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jeddeloh JA, Stokes TL, Richards EJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22:94–97

    Article  PubMed  CAS  Google Scholar 

  • Juarez MT, Kui JS, Thomas J et al (2004) microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84–88

    Article  PubMed  CAS  Google Scholar 

  • Kanno T, Bucher E, Daxinger L et al (2010) RNA-directed DNA methylation and plant development require an IWR1-type transcription factor. EMBO Rep 11:65–71

    Article  PubMed  CAS  Google Scholar 

  • Kasschau KD, Fahlgren N, Chapman EJ et al (2007) Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol 5:e57

    Article  PubMed  CAS  Google Scholar 

  • Kenrick P, Crane P (1997) The origin and early evolution of plants on land. Nature 389:33–39

    Article  CAS  Google Scholar 

  • Khraiwesh B, Ossowski S, Weigel D et al (2008) Specific gene silencing by artificial MicroRNAs in Physcomitrella patens: an alternative to targeted gene knockouts. Plant Physiol 148:684–693

    Article  PubMed  CAS  Google Scholar 

  • Khraiwesh B, Arif MA, Seumel GI et al (2010) Transcriptional control of gene expression by microRNAs. Cell 140:111–122

    Article  PubMed  CAS  Google Scholar 

  • Kim VN (2004) MicroRNA precursors in motion: exportin-5 mediates their nuclear export. Trends Cell Biol 14:156–159

    Article  PubMed  CAS  Google Scholar 

  • Kim J, Jung JH, Reyes JL et al (2005) microRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. Plant J 42:84–94

    Article  PubMed  CAS  Google Scholar 

  • Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101:12753–12758

    Article  PubMed  CAS  Google Scholar 

  • Lagos-Quintana M, Rauhut R, Lendeckel W et al (2001) Identification of novel genes coding for small expressed RNAs. Science 294:853–858

    Article  PubMed  CAS  Google Scholar 

  • Lanet E, Delannoy E, Sormani R et al (2009) Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell 21:1762–1768

    Article  PubMed  CAS  Google Scholar 

  • Lau NC, Lim LP, Weinstein EG et al (2001) An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294:858–862

    Article  PubMed  CAS  Google Scholar 

  • Law JA, Ausin I, Johnson LM et al (2010) A protein complex required for polymerase V transcripts and RNA-directed DNA methylation in Arabidopsis. Curr Biol 20:951–956

    Article  PubMed  CAS  Google Scholar 

  • Lee RC, Ambros V (2001) An extensive class of small RNAs in Caenorhabditis elegans. Science 294:862–864

    Article  PubMed  CAS  Google Scholar 

  • Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854

    Article  PubMed  CAS  Google Scholar 

  • Lee Y, Jeon K, Lee JT et al (2002) MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 21:4663–4670

    Article  PubMed  CAS  Google Scholar 

  • Lee Y, Kim M, Han J et al (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23:4051–4060

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Rand TA, Kalidas S et al (2003) R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 301:1921–1925

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Chen Z, Song X et al (2007a) Oryza sativa dicer-like4 reveals a key role for small interfering RNA silencing in plant development. Plant Cell 19:2705–2718

    Article  PubMed  CAS  Google Scholar 

  • Liu PP, Montgomery TA, Fahlgren N et al (2007b) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Yao X, Pi L et al (2008) The ARGONAUTE10 gene modulates shoot apical meristem maintenance and leaf polarity establishment by repressing miR165/166 in Arabidopsis. Plant J 58:27–40

    Article  PubMed  CAS  Google Scholar 

  • Lu C, Jeong DH, Kulkarni K et al (2008) Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs). Proc Natl Acad Sci USA 105:4951–4956

    Article  PubMed  CAS  Google Scholar 

  • Luo QJ, Samanta MP, Koksal F et al (2009) Evidence for antisense transcription associated with microRNA target mRNAs in Arabidopsis. PLoS Genet 5:e1000457

    Article  PubMed  CAS  Google Scholar 

  • MacRae IJ, Ma E, Zhou M et al (2008) In vitro reconstitution of the human RISC-loading complex. Proc Natl Acad Sci USA 105:512–517

    Article  PubMed  CAS  Google Scholar 

  • Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17:1360–1375

    Article  PubMed  CAS  Google Scholar 

  • Mallory AC, Hinze A, Tucker MR 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

    Article  PubMed  CAS  Google Scholar 

  • Matzke MA, Birchler JA (2005) RNAi-mediated pathways in the nucleus. Nat Rev Genet 6:24–35

    Article  PubMed  CAS  Google Scholar 

  • Matzke MA, Matzke AJ (2004) Planting the seeds of a new paradigm. PLoS Biol 2:E133

    Article  PubMed  CAS  Google Scholar 

  • Matzke M, Kanno T, Huettel B et al (2006) RNA-directed DNA methylation and Pol IVb in Arabidopsis. Cold Spring Harb Symp Quant Biol 71:449–459

    Article  PubMed  CAS  Google Scholar 

  • Melquist S, Bender J (2003) Transcription from an upstream promoter controls methylation signaling from an inverted repeat of endogenous genes in Arabidopsis. Genes Dev 17:2036–2047

    Article  PubMed  CAS  Google Scholar 

  • Mlotshwa S, Pruss GJ, Peragine A et al (2008) DICER-LIKE2 plays a primary role in transitive silencing of transgenes in Arabidopsis. PLoS ONE 3:e1755

    Article  PubMed  CAS  Google Scholar 

  • Moissiard G, Parizotto EA, Himber C et al (2007) Transitivity in Arabidopsis can be primed, requires the redundant action of the antiviral Dicer-like 4 and Dicer-like 2, and is compromised by viral-encoded suppressor proteins. RNA 13:1268–1278

    Article  PubMed  CAS  Google Scholar 

  • Montgomery TA, Howell MD, Cuperus JT et al (2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128–141

    Article  PubMed  CAS  Google Scholar 

  • Morel JB, Mourrain P, Beclin C et al (2000) DNA methylation and chromatin structure affect transcriptional and post-transcriptional transgene silencing in Arabidopsis. Curr Biol 10:1591–1594

    Article  PubMed  CAS  Google Scholar 

  • Morel JB, Godon C, Mourrain P et al (2002) Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14:629–639

    Article  PubMed  CAS  Google Scholar 

  • Morin RD, Aksay G, Dolgosheina E et al (2008) Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res 18:571–584

    Article  PubMed  CAS  Google Scholar 

  • Nagasaki H, Itoh J, Hayashi K et al (2007) The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc Natl Acad Sci USA 104:14867–14871

    Article  PubMed  CAS  Google Scholar 

  • Nishikura K (2001) A short primer on RNAi: RNA-directed RNA polymerase acts as a key catalyst. Cell 107:415–418

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama T, Fujita T, Shin IT et al (2003) Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: implication for land plant evolution. Proc Natl Acad Sci USA 100:8007–8012

    Article  PubMed  CAS  Google Scholar 

  • Niu QW, Lin SS, Reyes JL et al (2006) Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat Biotechnol 24:1420–1428

    Article  PubMed  CAS  Google Scholar 

  • Nobuta K, McCormick K, Nakano M et al (2010) Bioinformatics analysis of small RNAs in plants using next generation sequencing technologies. Methods Mol Biol 592:89–106

    Article  PubMed  CAS  Google Scholar 

  • Noma K, Sugiyama T, Cam H et al (2004) RITS acts in cis to promote RNA interference-mediated transcriptional and post-transcriptional silencing. Nat Genet 36:1174–1180

    Article  PubMed  CAS  Google Scholar 

  • Olmedo-Monfil V, Duran-Figueroa N, Arteaga-Vazquez M et al (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464:628–632

    Article  PubMed  CAS  Google Scholar 

  • Pak J, Fire A (2007) Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 315:241–244

    Article  PubMed  CAS  Google Scholar 

  • Pandey SP, Gaquerel E, Gase K et al (2008) RNA-directed RNA polymerase3 from Nicotiana attenuata is required for competitive growth in natural environments. Plant Physiol 147:1212–1224

    Article  PubMed  CAS  Google Scholar 

  • Parizotto EA, Dunoyer P, Rahm N et al (2004) In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev 18:2237–2242

    Article  PubMed  CAS  Google Scholar 

  • Park W, Li J, Song R et al (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495

    Article  PubMed  CAS  Google Scholar 

  • Park MY, Wu G, Gonzalez-Sulser A et al (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci USA 102:3691–3696

    Article  PubMed  CAS  Google Scholar 

  • Peragine A, Yoshikawa M, Wu G et al (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18:2368–2379

    Article  PubMed  CAS  Google Scholar 

  • Pontes O, Li CF, Nunes PC et al (2006) The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126:79–92

    Article  PubMed  CAS  Google Scholar 

  • Pontes O, Costa-Nunes P, Vithayathil P et al (2009) RNA polymerase V functions in Arabidopsis interphase heterochromatin organization independently of the 24-nt siRNA-directed DNA methylation pathway. Mol Plant 2:700–710

    Article  PubMed  CAS  Google Scholar 

  • Qi Y, Denli AM, Hannon GJ (2005) Biochemical specialization within Arabidopsis RNA silencing pathways. Mol Cell 19:421–428

    Article  PubMed  CAS  Google Scholar 

  • Qin H, Chen F, Huan X et al (2010) Structure of the Arabidopsis thaliana DCL4 DUF283 domain reveals a noncanonical double-stranded RNA-binding fold for protein-protein interaction. RNA 16:474–481

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Reinhart BJ, Weinstein EG, Rhoades MW et al (2002) MicroRNAs in plants. Genes Dev 16:1616–1626

    Article  PubMed  CAS  Google Scholar 

  • Rensing SA, Lang D, Zimmer AD et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69

    Article  PubMed  CAS  Google Scholar 

  • Satoh N, Itoh J, Nagato Y (2003) The SHOOTLESS2 and SHOOTLESS1 genes are involved in both initiation and maintenance of the shoot apical meristem through regulating the number of indeterminate cells. Genetics 164:335–346

    PubMed  CAS  Google Scholar 

  • Schaefer DG, Zryd JP (1997) Efficient gene targeting in the moss Physcomitrella patens. Plant J 11:1195–1206

    Article  PubMed  CAS  Google Scholar 

  • Schramke V, Allshire R (2004) Those interfering little RNAs! Silencing and eliminating chromatin. Curr Opin Genet Dev 14:174–180

    Article  PubMed  CAS  Google Scholar 

  • Schwab R, Palatnik JF, Riester M et al (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527

    Article  PubMed  CAS  Google Scholar 

  • Schwab R, Ossowski S, Riester M et al (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133

    Article  PubMed  CAS  Google Scholar 

  • Sempere LF, Cole CN, McPeek MA et al (2006) The phylogenetic distribution of metazoan microRNAs: insights into evolutionary complexity and constraint. J Exp Zool B Mol Dev Evol 306:575–588

    Article  PubMed  CAS  Google Scholar 

  • Shaked H, Avivi-Ragolsky N, Levy AA (2006) Involvement of the Arabidopsis SWI2/SNF2 chromatin remodeling gene family in DNA damage response and recombination. Genetics 173:985–994

    Article  PubMed  CAS  Google Scholar 

  • Sijen T, Steiner FA, Thijssen KL et al (2007) Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science 315:244–247

    Article  PubMed  CAS  Google Scholar 

  • Smith LM, Pontes O, Searle I et al (2007) An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 19:1507–1521

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Strepp R, Scholz S, Kruse S et al (1998) Plant nuclear gene knockout reveals a role in plastid division for the homolog of the bacterial cell division protein FtsZ, an ancestral tubulin. Proc Natl Acad Sci USA 95:4368–4373

    Article  PubMed  CAS  Google Scholar 

  • Sugiyama T, Cam H, Verdel A et al (2005) RNA-dependent RNA polymerase is an essential component of a self-enforcing loop coupling heterochromatin assembly to siRNA production. Proc Natl Acad Sci USA 102:152–157

    Article  PubMed  CAS  Google Scholar 

  • Tabara H, Yigit E, Siomi H et al (2002) The dsRNA binding protein RDE-4 interacts with RDE-1, DCR-1, and a DExH-box helicase to direct RNAi in C. elegans. Cell 109:861–871

    Article  PubMed  CAS  Google Scholar 

  • Talmor-Neiman M, Stav R, Klipcan L et al (2006) Identification of trans-acting siRNAs in moss and an RNA-dependent RNA polymerase required for their biogenesis. Plant J 48:511–521

    Article  PubMed  CAS  Google Scholar 

  • Timmermans MC, Juarez MT, Phelps-Durr TL (2004) A conserved microRNA signal specifies leaf polarity. Cold Spring Harb Symp Quant Biol 69:409–417

    Article  PubMed  CAS  Google Scholar 

  • Tomari Y, Zamore PD (2005) Perspective: machines for RNAi. Genes Dev 19:517–529

    Article  PubMed  CAS  Google Scholar 

  • Toriba T, Suzaki T, Yamaguchi T et al (2010) Distinct regulation of adaxial-abaxial polarity in anther patterning in rice. Plant Cell 22:1452–1462

    Article  PubMed  CAS  Google Scholar 

  • Vaistij FE, Jones L, Baulcombe DC (2002) Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell 14:857–867

    Article  PubMed  CAS  Google Scholar 

  • Vaucheret H (2008) Plant ARGONAUTES. Trends Plant Sci 13:350–358

    Article  PubMed  CAS  Google Scholar 

  • Vaucheret H, Vazquez F, Crete P et al (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

    Article  PubMed  CAS  Google Scholar 

  • Vaucheret H, Mallory AC, Bartel DP (2006) AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Mol Cell 22:129–136

    Article  PubMed  CAS  Google Scholar 

  • Vazquez F (2006) Arabidopsis endogenous small RNAs: highways and byways. Trends Plant Sci 11:460–468

    Article  PubMed  CAS  Google Scholar 

  • Vazquez F, Vaucheret H, Rajagopalan R et al (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16:69–79

    Article  PubMed  CAS  Google Scholar 

  • Verdel A, Jia S, Gerber S et al (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303:672–676

    Article  PubMed  CAS  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Wang LJ, Mao YB et al (2005) Control of root cap formation by MicroRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17:2204–2216

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Schwab R, Czech B et al (2008) Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20:1231–1243

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749

    Article  PubMed  CAS  Google Scholar 

  • Warthmann N, Chen H, Ossowski S et al (2008) Highly specific gene silencing by artificial miRNAs in rice. PLoS ONE 3:e1829

    Article  PubMed  CAS  Google Scholar 

  • Wierzbicki AT, Haag JR, Pikaard CS (2008) Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135:635–648

    Article  PubMed  CAS  Google Scholar 

  • Williams L, Carles CC, Osmont KS et al (2005) A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc Natl Acad Sci USA 102:9703–9708

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Xie Z, Johansen LK, Gustafson AM et al (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2:E104

    Article  PubMed  Google Scholar 

  • Xie Z, Allen E, Wilken A et al (2005) DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc Natl Acad Sci USA 102:12984–12989

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi A, Wu MF, Yang L et al (2009) The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17:268–278

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Ebright YW, Yu B et al (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

    Article  PubMed  CAS  Google Scholar 

  • Yao X, Wang H, Li H et al (2009) Two types of cis-acting elements control the abaxial epidermis-specific transcription of the MIR165a and MIR166a genes. FEBS Lett 583:3711–3717

    Article  PubMed  CAS  Google Scholar 

  • Yoshikawa M, Peragine A, Park MY et al (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19:2164–2175

    Article  PubMed  CAS  Google Scholar 

  • Yu B, Yang Z, Li J et al (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307:932–935

    Article  PubMed  CAS  Google Scholar 

  • Zeng Y, Wagner EJ, Cullen BR (2002) Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells. Mol Cell 9:1327–1333

    Article  PubMed  CAS  Google Scholar 

  • Zheng X, Zhu J, Kapoor A et al (2007) Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J 26:1691–1701

    Article  PubMed  CAS  Google Scholar 

  • Zheng Z, Xing Y, He XJ et al (2010) An SGS3-like protein functions in RNA-directed DNA methylation and transcriptional gene silencing in Arabidopsis. Plant J 62:92–99

    Article  PubMed  CAS  Google Scholar 

  • Zilberman D, Cao X, Jacobsen SE (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299:716–719

    Article  PubMed  CAS  Google Scholar 

  • Zilberman D, Cao X, Johansen LK et al (2004) Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats. Curr Biol 14:1214–1220

    Article  PubMed  CAS  Google Scholar 

  • Zong J, Yao X, Yin J et al (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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We gratefully acknowledge financial support to our work on small RNA pathways by the Landesstiftung Baden-Württemberg (P-LS-RNS/40 to W.F.), the German Federal Ministry of Education and Research (BMBF; FRISYS 0313921 to W.F.), the German Research Foundation (DFG; FR 1677/3-1 to W.F.) and the German Academic Exchange Service (DAAD; Ph.D. fellowships to M.A.A. and I.F.).

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Arif, M.A., Fattash, I., Khraiwesh, B., Frank, W. (2011). Physcomitrella patens Small RNA Pathways. In: Erdmann, V., Barciszewski, J. (eds) Non Coding RNAs in Plants. RNA Technologies. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19454-2_10

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