Skip to main content
Log in

MicroRNA biogenesis and function in higher plants

  • Review Article
  • Published:
Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) are endogenous, noncoding, small RNA molecules consisting of 21–24 nucleotides (nts) that regulate target genes at the posttranscriptional level in plants and animals. In plants, miRNAs negatively regulate target mRNAs containing a highly complementary sequence by either mRNA cleavage or translational repression. MiRNAs are processed from single-stranded precursors containing stem-loop structures by a Dicer-like enzyme and are loaded into silencing complexes, where they act on target mRNAs. Although plant miRNAs were first reported in Arabidopsis 10 years later than animal miRNAs, numerous miRNAs have since been identified from various land plants ranging from mosses to flowering plants, and their roles in diverse aspects of plant developmental processes have been characterized. Furthermore, most of the annotated plant miRNAs are evolutionarily conserved in various plants. In particular, recent functional studies using Arabidopsis mutants have contributed a great deal of information towards establishing a framework for understanding miRNA biogenesis and functional roles. Extensive appraisal of miRNA-directed regulation during a wide array of plant development and plant responses to environmental conditions has confirmed the versatile roles of miRNAs as a key component of plant molecular biology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131:3357–3365

    PubMed  CAS  Google Scholar 

  • Adai A, Johnson C, Mlotshwa S, Archer-Evans S, Manocha V, Vance V, Sundaresan V (2005) Computational prediction of miRNAs in Arabidopsis thaliana. Genome Res 15:78–91

    PubMed  CAS  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Sung GH, Spatafora JW, Carrington JC (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet 36:1282–1290

    PubMed  CAS  Google Scholar 

  • Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X, Dreyfuss G, Eddy SR, Griffiths-Jones S, Marshall M, Matzke M, Ruvkun G, Tuschl T (2003) A uniform system for microRNA annotation. RNA 9:277–279

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Arteaga-Vazquez M, Caballero-Perez J, Vielle-Calzada JP (2006) A family of microRNAs present in plants and animals. Plant Cell 18:3355–3369

    PubMed  CAS  Google Scholar 

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741

    PubMed  CAS  Google Scholar 

  • Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Baucher M, El Jaziri M, Vandeputte O (2007) From primary to secondary growth: origin and development of the vascular system. J Exp Bot 58:3485–3501

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bäurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664

    PubMed  Google Scholar 

  • Berardini TZ, Bollman K, Sun H, Poethig RS (2001) Regulation of vegetative phase change in Arabidopsis thaliana by cyclophilin 40. Science 291:2405–2407

    PubMed  CAS  Google Scholar 

  • Billoud B, De Paepe R, Baulcombe D, Boccara M (2005) Identification of new small non-coding RNAs from tobacco and Arabidopsis. Biochimie 87:905–910

    PubMed  CAS  Google Scholar 

  • Bollman KM, Aukerman MJ, Park MY, Hunter C, Berardini TZ, Poethig RS (2003) HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development 130:1493–1504

    Google Scholar 

  • Bonnet E, Van de Peer Y, Rouzé P (2006) The small RNA world of plants. New Phytol 171:451–468

    PubMed  CAS  Google Scholar 

  • Boutet S, Vazquez F, Liu J, Béclin C, Fagard M, Gratias A, Morel JB, Crété 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

    PubMed  CAS  Google Scholar 

  • Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20

    PubMed  CAS  Google Scholar 

  • Bowman JL, Eshed Y, Baum SF (2002) Establishment of polarity in angiosperm lateral organs. Trends Genet 18:134–141

    PubMed  CAS  Google Scholar 

  • Britten RJ, Davidson EH (1969) Gene regulation for higher cells: a theory. Science 165:349–357

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Byrne ME (2006) Shoot meristem function and leaf polarity: the role of class III HD-ZIP genes. PLOS Genet 2:e89

    PubMed  Google Scholar 

  • Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301:336–338

    PubMed  CAS  Google Scholar 

  • Cerutti L, Mian N, Bateman A (2000) Domains in gene silencing and cell differentiation proteins: the novel PAZ domain and redefinition of the PIWI domain. Trends Biochem Sci 25:481–482

    PubMed  CAS  Google Scholar 

  • Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8:884–896

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Chen X (2008) MicroRNA metabolism in plants. Curr Top Microbiol Immunol 320:117–136

    PubMed  CAS  Google Scholar 

  • Chen X, Liu J, Cheng Y, Jia D (2002) HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 129:1085–1094

    PubMed  CAS  Google Scholar 

  • Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332

    PubMed  CAS  Google Scholar 

  • Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. Plant Cell 18:412–421

    PubMed  CAS  Google Scholar 

  • Chitwood DH, Guo M, Nogueira FT, Timmermans MC (2007) Establishing leaf polarity: the role of small RNAs and positional signals in the shoot apex. Development 134:813–823

    PubMed  CAS  Google Scholar 

  • Chuck G, Cigan AM, Saeteurn K, Hake S (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39:544–549

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Clarke JH, Tack D, Findlay K, Van Montagu M, Van Lijsebettens M (1999) The SERRATE locus controls the formation of the early juvenile leaves and phase length in Arabidopsis. Plant J 20:493–501

    PubMed  CAS  Google Scholar 

  • Couzin J (2002) Breakthrough of the year: small RNAs make big splash. Science 298:2296–2297

    PubMed  CAS  Google Scholar 

  • De Smet I, Vanneste S, Inzé D, Beeckman T (2006) Lateral root initiation or the birth of a new meristem. Plant Mol Biol 60:871–887

    PubMed  CAS  Google Scholar 

  • Deak KI, Malamy J (2005) Osmotic regulation of root system architecture. Plant J 43:17–28

    PubMed  CAS  Google Scholar 

  • Dong Z, Han M, 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

    PubMed  CAS  Google Scholar 

  • Dugas DV, Bartel B (2008) Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol Biol 67:403–417

    PubMed  CAS  Google Scholar 

  • Eamens A, Wang MB, Smith NA, Waterhouse PM (2008) RNA silencing in plants: yesterday, today, and tomorrow. Plant Physiol 147:456–468

    PubMed  CAS  Google Scholar 

  • Eddy SR (2001) Non-coding RNA genes and the modern RNA world. Nat Rev Genet 2:919–929

    PubMed  CAS  Google Scholar 

  • Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13:1768–1774

    PubMed  CAS  Google Scholar 

  • Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE 2:e219

    PubMed  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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Friis EM, Pedersen KR, Crane PR (2004) Araceae from the early Cretaceous of Portugal: evidence on the emergence of monocotyledons. Proc Natl Acad Sci USA 101:16565–16570

    PubMed  CAS  Google Scholar 

  • Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Gandikota M, Birkenbihl RP, Hohmann S, Cardon GH, Saedler H, Huijser P (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

    PubMed  CAS  Google Scholar 

  • Garcia D (2008) A miRacle in plant development: role of microRNAs in cell differentiation and patterning. Semin Cell Dev Biol 19:586–595

    PubMed  CAS  Google Scholar 

  • Golden TA, Schauer SE, Land JD, Pien S, Mushegian AR, Grossniklaus U, Meinke DW, Ray A (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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–1386

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hiraguri A, Itoh R, Kondo N, Nomura Y, Aizawa D, Murai Y, Koiwa H, Seki M, Shinozaki K, Fukuhara T (2005) Specific interactions between Dicer-like proteins and HYL1/DRB-family dsRNA-binding proteins in Arabidopsis thaliana. Plant Mol Biol 57:173–188

    PubMed  CAS  Google Scholar 

  • Hunter C, Sun H, Poethig RS (2003) The Arabidopsis heterochronic gene ZIPPY is an ARGONAUTE family member. Curr Biol 13:1734–1739

    PubMed  CAS  Google Scholar 

  • Hutvagner G, Zamore PD (2002) A microRNA in a multiturnover RNAi enzyme complex. Science 297:2056–2060

    PubMed  CAS  Google Scholar 

  • Jacobsen SE, Running MP, Meyerowitz EM (1999) Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 126:5231–5243

    PubMed  CAS  Google Scholar 

  • Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229:1009–1014

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Barte B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    PubMed  CAS  Google Scholar 

  • Jung JH, Park CM (2007) MIR166/165 genes exhibit dynamic expression patterns in regulating shoot apical meristem and floral development in Arabidopsis. Planta 225:1327–1338

    PubMed  CAS  Google Scholar 

  • Jung JH, Seo YH, Seo PJ, Reyes JL, Yun J, Chua NH, Park CM (2007) The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19:2736–2748

    PubMed  CAS  Google Scholar 

  • Jung JH, Kim SG, Seo PJ, Park CM (2008) Molecular mechanisms underlying vascular development. Adv Bot Res 48:1–68

    CAS  Google Scholar 

  • Kasschau KD, Fahlgren N, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Carrington JC (2007) Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol 5:e57

    PubMed  Google Scholar 

  • Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T (2009) Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 57:313–321

    PubMed  CAS  Google Scholar 

  • Kidner CA, Martienssen RA (2004) Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428:81–84

    PubMed  CAS  Google Scholar 

  • Kidner CA, Martienssen RA (2005) The role of ARGONAUTE1 (AGO1) in meristem formation and identity. Dev Biol 280:504–517

    PubMed  CAS  Google Scholar 

  • Kidner CA, Timmermans MC (2007) Mixing and matching pathways in leaf polarity. Curr Opin Plant Biol 10:13–20

    PubMed  Google Scholar 

  • Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6:376–385

    PubMed  CAS  Google Scholar 

  • Kim J, Jung JH, Reyes JL, Kim YS, Kim SY, Chung KS, Kim JA, Lee M, Lee Y, Narry Kim V, Chua NH, Park CM (2005) microRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. Plant J 42:84–94

    PubMed  CAS  Google Scholar 

  • Krizek BA, Fletcher JC (2005) Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 6:688–698

    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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Kutter C, Schöb H, Stadler M, Meins F Jr, Si-Ammour A (2007) MicroRNA-mediated regulation of stomatal development in Arabidopsis. Plant Cell 19:2417–2429

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Laufs P, Peaucelle A, Morin H, Traas J (2004) MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 17:4311–4322

    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

    PubMed  CAS  Google Scholar 

  • Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23:4051–4060

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Lin S, Henriques R, Wu H, Niu Q, Yeh S, Chua N (2007) Strategies and mechanisms of plant virus resistance. Plant Biotechnol Rep 1:125–134

    Google Scholar 

  • Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, Hammond SM, Joshua-Tor L, Hannon GJ (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305:1437–1441

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Lu XY, Huang XL (2008) Plant miRNAs and abiotic stress responses. Biochem Biophys Res Commun 368:458–462

    PubMed  CAS  Google Scholar 

  • Lu S, Sun YH, Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stress-responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203

    PubMed  CAS  Google Scholar 

  • Maher C, Stein L, Ware D (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res 16:510–519

    PubMed  CAS  Google Scholar 

  • Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28:67–77

    PubMed  CAS  Google Scholar 

  • Mallory AC, Vaucheret H (2006) Functions of microRNAs and related small RNAs in plants. Nat Genet 38(Suppl):S31–S36

    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

    PubMed  CAS  Google Scholar 

  • McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T (2004) Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 15:185–197

    PubMed  CAS  Google Scholar 

  • Michlewski G, Guil S, Semple CA, Cáceres JF (2008) Posttranscriptional regulation of miRNAs harboring conserved terminal loops. Mol Cell 32:383–393

    PubMed  CAS  Google Scholar 

  • Miyoshi K, Tsukumo H, Nagami T, Siomi H, Siomi MC (2005) Slicer function of Drosophila argonautes and its involvement in RISC formation. Genes Dev 19:2837–2848

    PubMed  CAS  Google Scholar 

  • Mullen TE, Marzluff WF (2008) Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5′ to 3′ and 3′ to 5′. Genes Dev 22:50–65

    PubMed  CAS  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

    PubMed  CAS  Google Scholar 

  • Nogueira FT, Sarkar AK, Chitwood DH, Timmermans MC (2006) Organ polarity in plants is specified through the opposing activity of two distinct small regulatory RNAs. Cold Spring Harb Symp Quant Biol 71:157–164

    PubMed  CAS  Google Scholar 

  • Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Park JE, Park JY, Kim YS, Staswick PE, Jeon J, Yun J, Kim SY, Kim J, Lee YH, Park CM (2007) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 282:10036–10046

    PubMed  CAS  Google Scholar 

  • Parker JS, Roe SM, Barford D (2004) Crystal structure of a PIWI protein suggests mechanisms for siRNA recognition and slicer activity. EMBO J 23:4727–4737

    PubMed  CAS  Google Scholar 

  • Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS (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

    PubMed  CAS  Google Scholar 

  • Phillips JR, Dalmay T, Bartels D (2007) The role of small RNAs in abiotic stress. FEBS Lett 581:3592–3597

    PubMed  CAS  Google Scholar 

  • Poethig RS (2003) Phase change and the regulation of developmental timing in plants. Science 301:334–336

    PubMed  CAS  Google Scholar 

  • Pontes O, Pikaard CS (2008) siRNA and miRNA processing: new functions for Cajal bodies. Curr Opin Genet Dev 18:197–203

    PubMed  CAS  Google Scholar 

  • Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17:61–76

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Ramachandran V, Chen X (2008) Small RNA metabolism in Arabidopsis. Trends Plant Sci 13:368–374

    PubMed  CAS  Google Scholar 

  • Reeder J, Höchsmann M, Rehmsmeier M, Voss B, Giegerich R (2006) Beyond Mfold: recent advances in RNA bioinformatics. J Biotechnol 124:41–55

    PubMed  CAS  Google Scholar 

  • Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403:901–906

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49:592–606

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ronemus M, Vaughn MW, Martienssen RA (2006) MicroRNA-targeted and small interfering RNA-mediated mRNA degradation is regulated by argonaute, dicer, and RNA-dependent RNA polymerase in Arabidopsis. Plant Cell 18:1559–1574

    PubMed  CAS  Google Scholar 

  • Ru P, Xu L, Ma H, Huang H (2006) Plant fertility defects induced by the enhanced expression of microRNA167. Cell Res 16:457–465

    PubMed  CAS  Google Scholar 

  • Rybak A, Fuchs H, Smirnova L, Brandt C, Pohl EE, Nitsch R, Wulczyn FG (2008) A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol 10:987–993

    PubMed  CAS  Google Scholar 

  • Schauer SE, Jacobsen SE, Meinke DW, Ray A (2002) DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci 7:487–491

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Schwarz DS, Hutvagner G, Du T, Xu Z, Aronin N, Zamore PD (2003) Asymmetry in the assembly of the RNAi enzyme complex. Cell 115:199–208

    PubMed  CAS  Google Scholar 

  • Sharma VK, Carles C, Fletcher JC (2003) Maintenance of stem cell populations in plants. Proc Natl Acad Sci USA 1:11823–11829

    Google Scholar 

  • Shen B, Goodman HM (2004) Uridine addition after microRNA-directed cleavage. Science 306:997

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Sorin C, Bussell JD, Camus I, Ljung K, Kowalczyk M, Geiss G, McKhann H, Garcion C, Vaucheret H, Sandberg G, Bellini C (2005) Auxin and light control of adventitious rooting in Arabidopsis require ARGONAUTE1. Plant Cell 17:1343–1359

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019

    PubMed  CAS  Google Scholar 

  • Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from rice. Plant Cell 17:1397–1411

    PubMed  CAS  Google Scholar 

  • Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tang G, Reinhart BJ, Bartel DP, Zamore PD (2003) A biochemical framework for RNA silencing in plants. Genes Dev 17:49–63

    PubMed  CAS  Google Scholar 

  • Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20:759–771

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory AC, Hilbert JL, Bartel DP, Crété P (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16:69–79

    PubMed  CAS  Google Scholar 

  • Voinnet O (2008) Use, tolerance and avoidance of amplified RNA silencing by plants. Trends Plant Sci 13:317–328

    PubMed  CAS  Google Scholar 

  • Wang XJ, Reyes JL, Chua NH, Gaasterland T (2004) Prediction and identification of Arabidopsis thaliana microRNAs and their mRNA targets. Genome Biol 5:R65

    PubMed  Google Scholar 

  • Wang JW, Schwab R, Czech B, Mica E, Weigel D (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

    PubMed  CAS  Google Scholar 

  • Williams L, Grigg SP, Xie M, Christensen S, Fletcher JC (2005) Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132:3657–3668

    PubMed  CAS  Google Scholar 

  • Willmann MR, Poethig RS (2005) Time to grow up: the temporal role of smallRNAs in plants. Curr Opin Plant Biol 8:548–552

    PubMed  CAS  Google Scholar 

  • Willmann MR, Poethig RS (2007) Conservation and evolution of miRNA regulatory programs in plant development. Curr Opin Plant Biol 10:503–511

    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

    PubMed  CAS  Google Scholar 

  • Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133:4211–4218

    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

    PubMed  CAS  Google Scholar 

  • Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, Jacobsen SE, Carrington JC (2004) Genetic and functional diversification of small RNA pathways in plants. PloS Biol 2:E104

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Biol Chem 282:16369–16378

    PubMed  CAS  Google Scholar 

  • 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 (in press)

  • Yang JH, Han SJ, Yoon EK, Lee WS (2006a) Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Res 34:1892–1899

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Yang Z, Ebright YW, Yu B, Chen X (2006c) 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Zhang B, Pan X, Cannon CH, Cobb GP, Anderson TA (2006) Conservation and divergence of plant microRNA genes. Plant J 46:243–259

    PubMed  CAS  Google Scholar 

  • Zhang X, Henderson IR, Lu C, Green PJ, Jacobsen SE (2007) Role of RNA polymerase IV in plant small RNA metabolism. Proc Natl Acad Sci USA 104:4536–4541

    PubMed  CAS  Google Scholar 

  • Zhao L, Kim Y, Dinh TT, Chen X (2007) miR172 regulates stem cell fate and defines the inner boundary of APETALA3 and PISTILLATA expression domain in Arabidopsis floral meristems. Plant J 51:840–849

    PubMed  CAS  Google Scholar 

  • Zhou GK, Kubo M, Zhong R, Demura T, Ye ZH (2007) Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis. Plant Cell Physiol 48:391–404

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Brain Korea 21, Biogreen 21 (20080401034001), and National Research Laboratory Programs and by grants from Plant Signaling Network Research Center and Korea Science and Engineering Foundation (2007-03415).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chung-Mo Park.

Additional information

J.-H. Jung and P. J. Seo contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jung, JH., Seo, P.J. & Park, CM. MicroRNA biogenesis and function in higher plants. Plant Biotechnol Rep 3, 111–126 (2009). https://doi.org/10.1007/s11816-009-0085-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-009-0085-8

Keywords

Navigation