Skip to main content
SpringerLink
Log in

MicroRNAs as regulators of root development and architecture

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) are post-transcriptional regulators of growth and development in both plants and animals. In plants, roots play essential roles in their anchorage to the soil as well as in nutrient and water uptake. In this review, we present recent advances made in the identification of miRNAs involved in embryonic root development, radial patterning, vascular tissue differentiation and formation of lateral organs (i.e., lateral and adventitious roots and symbiotic nitrogen-fixing nodules in legumes). Certain mi/siRNAs target members of the Auxin Response Factors family involved in auxin homeostasis and signalling and participate in complex regulatory loops at several crucial stages of root development. Other miRNAs target and restrict the action of various transcription factors that control root-related processes in several species. Finally, because abiotic stresses, which include nutrient or water deficiencies, generally modulate root growth and branching, we summarise the action of certain miRNAs in response to these stresses that may be involved in the adaptation of the root system architecture to the soil environment.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120

    Article  PubMed  CAS  Google Scholar 

  • Arenas-Huertero C, Pérez B, Rabanal F, Blanco-Melo D, De la Rosa C, Estrada-Navarrete G, Sanchez F, Covarrubias AA, Reyes JL (2009) Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol Biol 70:385–401

    Article  PubMed  CAS  Google Scholar 

  • Arnaud C, Bonnot C, Desnos T, Nussaume L (2010) The root cap at the forefront. C R Biol 333:335–343

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Becraft PW, Bongard-Pierce DK, Sylvester AW, Poethig RS, Freeling M (1990) The LIGULELESS-1 gene acts tissue specifically in maize leaf development. Dev Biol 141:220–232

    Article  PubMed  CAS  Google Scholar 

  • Benfey PN, Scheres B (2000) Root development. Curr Biol 10:R813–R815

    Article  PubMed  CAS  Google Scholar 

  • Benková E, Hejátko J (2009) Hormone interactions at the root apical meristem. Plant Mol Biol 69:383–396

    Article  PubMed  CAS  Google Scholar 

  • Berleth T, Jürgens G (1993) The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development 118:575–587

    Google Scholar 

  • Boualem A, Laporte P, Jovanovic M, Laffont C, Plet J, Combier JP, Niebel A, Crespi M, Frugier F (2008) MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J 54:876–887

    Article  PubMed  CAS  Google Scholar 

  • Branscheid A, Sieh D, Pant BD, May P, Devers EA, Elkrog A, Schauser L, Scheible WR, Krajinski F (2010) Expression pattern suggests a role of MiR399 in the regulation of the cellular response to local Pi increase during arbuscular mycorrhizal symbiosis. Mol Plant Microbe Interact 23:915–926

    Article  PubMed  CAS  Google Scholar 

  • Brechenmacher L, Kim MY, Benitez M, Li M, Joshi T, Calla B, Lee MP, Libault M, Vodkin LO, Xu D, Lee SH, Clough SJ, Stacey G (2008) Transcription profiling of soybean nodulation by Bradyrhizobium japonicum. Mol Plant Microbe Interact 21:631–645

    Article  PubMed  CAS  Google Scholar 

  • Buhtz A, Pieritz J, Springer F, Kehr J (2010) Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10:64

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vatén 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

    Article  PubMed  CAS  Google Scholar 

  • Casimiro I, Beeckman T, Graham N, Rishikesh Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting arabidopsis lateral root development. Trends Plant Sci 8:165–171

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Xiong L (2010) The bifunctional abiotic stress signalling regulator and endogenous RNA silencing suppressor FIERY1 is required for lateral root formation. Plant Cell Environ 33:2180–2190

    Article  PubMed  CAS  Google Scholar 

  • Chiou TJ (2008) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Combier JP, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernié T, Ott T, Gamas P, Crespi M, Niebel A (2006) MtHAP2–1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 20:3084–3088

    Article  PubMed  CAS  Google Scholar 

  • Coudert Y, Périn C, Courtois B, Khong NG, Gantet P (2010) Genetic control of root development in rice, the model cereal. Trends Plant Sci 15:219–226

    Article  PubMed  CAS  Google Scholar 

  • Crespi M, Frugier F (2008) De novo organ formation from differentiated cells: root nodule organogenesis. Sci Signal 9:1(49):re11

    Google Scholar 

  • de Dorlodot S, Forster B, Pagès L, Price A, Tuberosa R, Draye X (2007) Root system architecture: opportunities and constraints for genetic improvement of crops. Trends Plant Sci 12:474–481

    Article  PubMed  CAS  Google Scholar 

  • Desnos T (2008) Root branching responses to phosphate and nitrate. Current Opin Plant Biol 11:82–87

    Article  CAS  Google Scholar 

  • Dharmasiri N, Estelle M (2004) Auxin signaling and regulated protein degradation. Trends Plant Sci 9:302–308

    Article  PubMed  CAS  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  PubMed  CAS  Google Scholar 

  • Ding Y, Oldroyd GE (2009) Positioning the nodule, the hormone dictum. Plant Signal Behav 4:89–93

    Article  PubMed  CAS  Google Scholar 

  • Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (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 

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

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Fukaki H, Okushima Y, Tasaka M (2007) Auxin-mediated lateral root formation in higher plants. Int Rev Cytol 256:111–137

    Article  PubMed  CAS  Google Scholar 

  • Gallagher KL, Paquette AJ, Nakajima K, Benfey PN (2004) Mechanisms regulating SHORT-ROOT intercellular movement. Curr Biol 14:1847–1851

    Article  PubMed  CAS  Google Scholar 

  • Gazzani S, Lawrenson T, Woodward C, Headon D, Sablowski R (2004) A link between mRNA turnover and RNA interference in Arabidopsis. Science 306:1046–1048

    Article  PubMed  CAS  Google Scholar 

  • Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci USA 105:803–808

    Article  PubMed  CAS  Google Scholar 

  • Godiard L, Niebel A, Micheli F, Gouzy J, Ott T, Gamas P (2007) Identification of new potential regulators of the Medicago truncatula-Sinorhizobium meliloti symbiosis using a large-scale suppression subtractive hybridization approach. Mol Plant Microbe Interact 20:321–332

    Article  PubMed  CAS  Google Scholar 

  • Gray WM, del Pozo JC, Walker L, Hobbie L, Risseeuw E, Banks T, Crosby L, Yang M, Ma H, Estelle M (1999) Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana. Genes Dev 13:1678–1691

    Article  PubMed  CAS  Google Scholar 

  • Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF (TIR1)-dependent degradation of AUX/IAA proteins. Nature 414:271–276

    Article  PubMed  CAS  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. Developmental Cell 14:854–866

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Grigg SP, Galinha C, Kornet N, Canales C, Scheres B, Tsiantis M (2009) Repression of apical homeobox genes is required for embryonic root development in arabidopsis. Curr Biol 19:1485–1490

    Article  PubMed  CAS  Google Scholar 

  • Grimsrud PA, den Os D, Wenger CD, Swaney DL, Schwartz D, Sussman MR, Ané JM, Coon JJ (2010) Large-scale phosphoprotein analysis in Medicago truncatula roots provides insight into in vivo kinase activity in legumes. Plant Physiol 152:19–28

    Article  PubMed  CAS  Google Scholar 

  • Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol Plant 138:226–237

    Article  PubMed  CAS  Google Scholar 

  • Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C (2009) Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21:3119–3132

    Article  PubMed  CAS  Google Scholar 

  • Gy I, Gasciolli V, Lauressergues D, Morel JB, Gombert J, Proux F, Proux C, Vaucheret H, Mallory AC (2007) Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 19:3451–3461

    Article  PubMed  CAS  Google Scholar 

  • Hamann T, Mayer U, Jürgens G (1999) The auxin-insensitive bodenlos mutation affects primary root formation andapical-basal patterning in the Arabidopsis embryo. Development 126:1387–1395

    PubMed  CAS  Google Scholar 

  • Hennig L, Taranto P, Walser M, Schönrock N, Gruissem W (2003) Arabidopsis MSI1 is required for epigenetic maintenance of reproductive development. Development 130:2555–2565

    Article  PubMed  CAS  Google Scholar 

  • Hernández G, Ramírez M, Valdés-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F, Wu HC, Lara M, Town CD, Kopka J, Udvardi MK, Vance CP (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 144:752–767

    Article  PubMed  CAS  Google Scholar 

  • Hernández G, Valdés-López O, Ramírez M, Goffard N, Weiller G, Aparicio-Fabre R, Fuentes SI, Erban A, Kopka J, Udvardi MK, Vance CP (2009) Global changes in the transcript and metabolic profiles during symbiotic nitrogen fixation in phosphorus-stressed common bean plants. Plant Physiol 151:1221–1238

    Article  PubMed  CAS  Google Scholar 

  • Hirota A, Kato T, Fukaki H, Aida M, Tasaka M (2007) The auxin-regulated AP2/EREBP gene PUCHI is required foorphogenesis in the early lateral root primordium of Arabidopsis. Plant Cell 19:2156–2168

    Article  PubMed  CAS  Google Scholar 

  • Hochholdinger F, Zimmermann R (2008) Conserved and diverse mechanisms in root development. Curr Opin Plant Biol 11:70–74

    Article  PubMed  CAS  Google Scholar 

  • Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151:2120–2132

    Article  PubMed  Google Scholar 

  • Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Joshi T, Yan Z, Libault M, Jeong DH, Park S, Green PJ, Sherrier DJ, Farmer A, May G, Meyers BC, Xu D, Stacey G (2010) Prediction of novel miRNAs and associated target genes in Glycine max. BMC Bioinformatics 11(1):S14

    Google Scholar 

  • Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004) Root-to- shoot transport of sulphate in Arabidopsis: evidence for the role of SULTR3;5 as a component of low-affinity sulphate transport system in the root vasculature. Plant Physiol 136:4198–4204

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  PubMed  CAS  Google Scholar 

  • Kutz A, Muller A, Henning P, Kaiser WM, Piotrowsky M, Weiler EW (2002) A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant J 30:95–106

    Article  PubMed  CAS  Google Scholar 

  • Laux T, Würschum T, Breuninger H (2004) Genetic regulation of embryonic pattern formation. Plant Cell 16:S190–S202

    Article  PubMed  CAS  Google Scholar 

  • Lelandais-Brière C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J, Crespi M (2009) Genome-wide small RNA analysis revealed differentially regulated miRNA isoforms in Medicago truncatula roots and nodules. Plant Cell 21:2780–2796

    Article  PubMed  Google Scholar 

  • Levesque MP, Vernoux T, Busch W, Cui H, Wang JY, Blilou, Hassan H, Nakajima K, Matsumoto N, Lohmann JU, Scheres B, Benfey PN (2006) Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol 4:e143

  • Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251

    Article  PubMed  CAS  Google Scholar 

  • Li H, Deng Y, Wu T, Subramanian S, Yu O (2010) Misexpression of miR482, miR1512, and miR1515 increases soybean nodulation. Plant Physiol 153:1759–1770

    Article  PubMed  CAS  Google Scholar 

  • Liang G, Yang F, Yu D (2010) MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J 62:1046–1057

    PubMed  CAS  Google Scholar 

  • Linkohr BI, Williamson LC, Fitter AH, Leyser HM (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29:751–760

    Article  PubMed  CAS  Google Scholar 

  • López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287

    Article  PubMed  CAS  Google Scholar 

  • Lundmark M, Kørner CJ, Nielsen TH (2010) Global analysis of microRNA in Arabidopsis in response to phosphate starvation as studied by locked nucleic acid-based microarrays. Physiol Plant 140:57–68

    Article  PubMed  CAS  Google Scholar 

  • Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44

    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 

  • Maraschin FS, Memelink J, Offringa R (2009) Auxin induced, SCFTIR1-mediated poly-ubiquitination marks AUX/IAA proteins for degradation. Plant J 59:100–109

    Article  CAS  Google Scholar 

  • Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume CrespiM, Maizel A (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22:1104–1117

    Article  PubMed  CAS  Google Scholar 

  • Martín AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de La Peña A, Leyva A, Paz-Ares J (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24:559–567

    Article  PubMed  Google Scholar 

  • Meng Y, Huang F, Shi Q, Cao J, Chen D, Zhang J, Ni J, Wu P, Chen M (2009) Genome-wide survey of rice microRNAs and microRNA-target pairs in the root of a novel auxin-resistant mutant. Planta 230:883–898

    Article  PubMed  CAS  Google Scholar 

  • Meng Y, Ma X, Chen D, Wu P, Chen M (2010) MicroRNA-mediated signaling involved in plant root development. Biochem Biophys Res Commun 393:345–349

    Article  PubMed  CAS  Google Scholar 

  • Naya L, Khan GA, Sorin C, Hartmann C, Crespi M, Lelandais-Brière C (2010) Cleavage of a non-conserved target by a specific miR156 isoform in root apexes of Medicago truncatula. Plant Signal Behav 5:328–331

    Article  PubMed  CAS  Google Scholar 

  • Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev of Plant Bio 59:519–546

    Article  CAS  Google Scholar 

  • Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58:93–113

    Article  PubMed  CAS  Google Scholar 

  • Overvoorde P, Fukaki H, Beeckman T. (2010) Auxin control of root development. Cold Spring Harb Perspect Biol 2(6):a001537

  • Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738

    Article  PubMed  CAS  Google Scholar 

  • Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14:399–408

    Article  PubMed  CAS  Google Scholar 

  • Petricka JJ, Benfey PN (2008) Root layers: complex regulation of developmental patterning. Curr Opin Genet Dev 18:354–361

    Article  PubMed  CAS  Google Scholar 

  • Prigge MJ, Wagner DR (2001) The Arabidopsis SERRATE gene encodes a zinc-finger protein required for normal shoot development. Plant Cell 13:1263–1279

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez RE, Mecchia MA, Debernardi JM, Schommer C, Weigel D, Palatnik JF (2010) Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 137:103–112

    Article  PubMed  CAS  Google Scholar 

  • Scheres B, Wolkenfelt H, Willemsen V, Terlouw M, Lawson E, Dean C, Weisbeek P (1994) Embryonic origin of the Arabidopsis primary root and root-meristem initials. Development 120:2475–2487

    CAS  Google Scholar 

  • Simon SA, Meyers BC, Sherrier DJ (2009) MicroRNAs in the rhizobia legume symbiosis. Plant Physiol 151:1002–1008

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Stone J, Liang X, Nekl E, Stiers J (2005) Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant J 41:744–754

    Article  PubMed  CAS  Google Scholar 

  • Subramanian S, Fu Y, Sunkar R, Barbazuk BW, Zhu JK, Yu O (2008) Novel and nodulation-regulated microRNAs in soybean roots. BMC Genomics 9:160

    Article  PubMed  CAS  Google Scholar 

  • Takahashi H (2010) Regulation of sulfate transport and assimilation in plants. Int Rev Cell Mol Biol 281:129–159

    Article  PubMed  CAS  Google Scholar 

  • Thole JM, Vermeer JE, Zhang Y, Gadella TW, Nielsen E (2008) Root hair defective4 encodes a phosphatidylinositol-4-phosphate phosphatase required for proper root hair development in Arabidopsis thaliana. Plant Cell 20:381–395

    Article  PubMed  CAS  Google Scholar 

  • Tian CE, Muto H, Higuchi K, Matamura T, Tatematsu K, Koshiba T, Yamamoto KT (2004) Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant J 40:333–343

    Article  PubMed  CAS  Google Scholar 

  • Ueda M, Koshino-Kimura Y, Okada K (2005) Stepwise understanding of root development. Curr Opin Plant Biol 8:71–76

    Article  PubMed  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999) Dimerization and DNA binding of auxin response factors. Plant J 19:309–319

    Article  PubMed  CAS  Google Scholar 

  • Valdés-López O, Yang SS, Aparicio-Fabre R, Graham PH, Reyes JL, Vance CP, Hernández G (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol 187:805–818

    Article  PubMed  CAS  Google Scholar 

  • Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutiérrez RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci 107:4477–4482

    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, Cai WJ, Xue HW, Chen XY (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 Y, Li P, Cao X, Wang X, Zhang A, Li X (2009) Identification and expression analysis of miRNAs from nitrogen-fixing soybean nodules. Biochem Biophys Res Commun 378:799–803

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Gao X, Li L, Shi X, Zhang J, Shi Z (2010) Overexpression of Osta-siR2141 caused abnormal polarity establishment and retarded growth in rice. J Exp Bot 61:1885–1895

    Article  PubMed  CAS  Google Scholar 

  • Williamson LC, Ribrioux SP, Fitter AH, Leyser HM (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Lee Bh, Ishitani M, Lee H, Zhang C, Zhu JK (2001) FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev 15:1971–1984

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Wang RG, Mao G, Koczan JM (2006) Identification of drought tolerance determinants by genetic analysis of root response to drought stress and abscisic Acid. Plant Physiol 142:1065–1074

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zeng CJ, Lee YR, Liu B (2009) The WD40 repeat protein NEDD1 Functions in microtubule organization during cell division in Arabidopsis thaliana. Plant Cell 21:1129–1140

    Article  PubMed  CAS  Google Scholar 

  • Zeng HQ, Zhu YY, Huang SQ, Yang ZM (2010) Analysis of phosphorus-deficient responsive miRNAs and cis-elements from soybean (Glycine max L.). J Plant Physiol 167:1289–1297

    Article  PubMed  CAS  Google Scholar 

  • Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10:29

    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

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut des Sciences du Végétal, Centre National de la Recherche Scientifique (C.N.R.S.), 91198, Gif-sur-Yvette Cedex, France

    Ghazanfar A. Khan, Marie Declerck, Céline Sorin, Caroline Hartmann, Martin Crespi & Christine Lelandais-Brière

  2. Université Paris Diderot-Paris 7, 5 rue Thomas Mann, 75205, Paris Cedex 13, France

    Céline Sorin, Caroline Hartmann & Christine Lelandais-Brière

Authors
  1. Ghazanfar A. Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie Declerck
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Céline Sorin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Caroline Hartmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Martin Crespi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Christine Lelandais-Brière
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Crespi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 112 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Khan, G.A., Declerck, M., Sorin, C. et al. MicroRNAs as regulators of root development and architecture. Plant Mol Biol 77, 47–58 (2011). https://doi.org/10.1007/s11103-011-9793-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-011-9793-x

Keywords

Search

Navigation