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Root Apical Meristem Pattern: Hormone Circuitry and Transcriptional Networks

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Book cover Progress in Botany 72

Part of the book series: Progress in Botany ((BOTANY,volume 72))

Abstract

In higher plants, growth and development relies on the spatiotemporal regulation of gene expression, which is under the control of both endogenous signals and external stimuli. In this chapter, recent advances in defining signaling machinery and genetic frameworks that underlie RAM patterning and maintenance are reviewed, with a focus on the interplay between different hormone classes. The evidence for an epigenetic control of the root developmental program is also briefly considered. Conceivably, many other aspects are still to be elucidated. Future challenges deal with, on the one hand, understanding how signaling and genetic programs are modulated to achieve adaptative traits under environmental pressure and, on the other, how cell fate is reprogrammed in vivo and in vitro. We conclude that knowledge from the plant model, Arabidopsis thaliana, could enhance our understanding of more complex species encountered in crop systems and could provide relevant perspectives for both crop improvement and plant biotechnology.

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References

  • Achard P, Vriezen WH, Van Der Straeten D, Harberd NP (2003) Ethylene regulates Arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15:2816–2825

    PubMed  CAS  Google Scholar 

  • Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S, Coppens F, Beemster GT, Genschik P (2009) Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr Biol 19:1188–1193

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Altamura MM, Biondi S, Colombo L, Guzzo F (2007) Elementi di biologia dello sviluppo delle piante. EdiSES Publishers, Napoli, Italy

    Google Scholar 

  • Armstrong JE, Heimsch C (1976) Ontogenetic reorganization of the root meristem in the Compositae. Am J Bot 63:212–219

    Google Scholar 

  • Audus LJ (1960) Magnetotropism: a new plant growth response. Nature 185:132–134

    Google Scholar 

  • Azuara V, Perry P, Sauer S, Spivakov M, Jørgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, Fisher AG (2006) Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8:532–538

    PubMed  CAS  Google Scholar 

  • Barlow PW (1974) Regeneration of the cap of primary roots of Zea mays. New Phytol 73:937–954

    CAS  Google Scholar 

  • Barlow PW (1978) The concept of the stem-cell in the context of plant growth and development. In: Lord BI, Potter CS, Cole RJ (eds) Stem-cells and tissue homeostasis. Cambridge University Press, Cambridge, pp 87–113

    Google Scholar 

  • Barlow PW (1997) Stem-cells and founder zones in plants, particularly their roots. In: Potten CS (ed) Stem-cells. Academic, London, pp 29–57

    Google Scholar 

  • Behrens HM, Weisenseel MH, Sievers A (1982) Rapid changes in the pattern of electric current around the root tip of Lepidium Sativum L. following gravistimulation. Plant Physiol 70:1079–1083

    PubMed  CAS  Google Scholar 

  • Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Ann Rev Plant Biol 59:443–465

    CAS  Google Scholar 

  • Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–596

    PubMed  Google Scholar 

  • Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem-cells. Cell 125:315–326

    PubMed  CAS  Google Scholar 

  • Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM, Galbraith DW, Benfey PN (2003) A gene expression map of the Arabidopsis root. Science 302:1956–1960

    PubMed  CAS  Google Scholar 

  • Bitonti MB, Mazzuca S, Ting T, Innocenti AM (2006) Magnetic field affects meristem activity and cell differentiation in Zea mays roots. Plant Biosyst 140:87–93

    Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    PubMed  CAS  Google Scholar 

  • Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros L, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, Bell GW, Otte AP, Vidal M, Gifford DK, Young RA, Jaenisch R (2006) Polycomb complexes repress developmental regulators in murine embryonic stem-cells. Nature 441:349–353

    PubMed  CAS  Google Scholar 

  • Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318:801–806

    PubMed  CAS  Google Scholar 

  • Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem-cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–619

    PubMed  CAS  Google Scholar 

  • Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T (2008) Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell 14:867–876

    PubMed  CAS  Google Scholar 

  • Brocard-Gifford I, Linch TJ, Garcia ME, Malhotra B, Finkelstein RR (2004) The Arabidopsis thaliana ABSCISIC-ACID-INSENSITIVE8 encodes a novel protein mediating abscisic acid and sugar response essential for growth. Plant Cell 16:406–421

    PubMed  CAS  Google Scholar 

  • Chae HS, Kieber J (2005) Eto Brute? The role of ACS turnover in regulating ethylene biosynthesis. Trends Plant Sci 10:291–296

    PubMed  CAS  Google Scholar 

  • Chiappetta A, Petrarulo M, Fambrini M, Pugliesi C, Dewitte W, Van Onckelen H, Innocenti AM, Bitonti MB (2006) Zeatin accumulation and misexpression of a class I knox gene are intimately linked in the epiphyllous response of the interspecific hybrid EMB-2 (Helianthus annuus H. tuberosus). Planta 223:917–931

    PubMed  CAS  Google Scholar 

  • Chiappetta A, Fambrini M, Petrarulo M, Rapparini F, Michelotti V, Bruno L, Greco M, Baraldi R, Salvini M, Pugliesi C, Bitonti MB (2009) Ectopic expression of LEAFY COTYLEDON1-LIKE gene and localized auxin accumulation mark embryogenic competence in epiphyllous plants of Helianthus annuus x H. tuberosus. Ann Bot 103:735–747

    PubMed  CAS  Google Scholar 

  • Clowes FLA (1954) The promeristem and the minimal constructional centre in grass root apices. New Phytol 53:108–116

    Google Scholar 

  • Clowes FLA (1956) Nucleic acids in root apical meristems of Zea. New Phytol 55:29–34

    CAS  Google Scholar 

  • Clowes FLA (1959) Reorganization of root apices after irradiation. Ann Bot 23:205–210

    CAS  Google Scholar 

  • Clowes FLA (1961) Effect of β-radiation on meristems. Exp Cell Res 25:529–534

    PubMed  CAS  Google Scholar 

  • Clowes FLA (1975) The quiescent centre. In: Torrey JG, Clarkson DT (eds) The development and function of roots. Academie, London, pp 3–19

    Google Scholar 

  • Clowes FLA (1976) Estimation of growth fractions in meristems of Zea mays L. Ann Bot 40:933–938

    Google Scholar 

  • Clowes FLA (1981) The difference between open and closed meristems. Ann Bot 48:761–767

    Google Scholar 

  • Clowes FAL (2000) Pattern in root meristem development in angiosperms. New Phytol 146:83–94

    Google Scholar 

  • Clowes FAL, Stewart HE (1967) Recovery from dormancy in roots. New Phytol 66:115–123

    Google Scholar 

  • Costa S, Shaw P (2006) Chromatin organization and cell fate switch respond to positional information in Arabidopsis. Nature 439:493–496

    PubMed  CAS  Google Scholar 

  • Cui H, Benfey PN (2009) Interplay between SCARECROW, GA and LIKE HETEROCHROMATIN PROTEIN 1 in ground tissue patterning in the Arabidopsis root. Plant J 58:1016–1027

    PubMed  CAS  Google Scholar 

  • Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425

    PubMed  CAS  Google Scholar 

  • Davies PJ (1995) Plant hormones physiology biochemistry and molecular biology. Kluwer, Dordrecht

    Google Scholar 

  • De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D, Van Noorden G, Naudts M, Van Isterdael G, De Clercq R (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322:594–597

    PubMed  Google Scholar 

  • De Tullio MC, Jiang K, Feldman LJ (2009) Redox regulation of root apical meristem organization: connecting root development to its environment. Plant Physiol Biochem. doi:10.1016/j.plaphy.2009.11.005

    PubMed  Google Scholar 

  • Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17:678–682

    PubMed  CAS  Google Scholar 

  • Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008) A genetic framework for the control of cell division and differentiation in the root meristems. Science 322:1380–1384

    PubMed  CAS  Google Scholar 

  • Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86:423–433

    PubMed  Google Scholar 

  • Dinneny JR, Benfey PN (2008) Plant stem-cell niches: standing the test of time. Cell 132:553–557

    PubMed  CAS  Google Scholar 

  • Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84

    PubMed  CAS  Google Scholar 

  • Doncheva S, Amenós M, Poschenrieder C, Barceló J (2005) Root cell patterning: a primary target for aluminium toxicity in maize. J Exp Bot 56:1213–1220

    PubMed  CAS  Google Scholar 

  • Eckardt NA (2010) Redox regulation of auxin signalling and plant development. Plant Cell 22:295. doi:10.1105/tpc.110.220212

    PubMed  CAS  Google Scholar 

  • Feldman LJ, Torrey GJ (1975) The quiescent center and primary vascular tissue patter formation in cultured roots Zea. Can J Bot 53:2796–2803

    Google Scholar 

  • Fiers M, Golemiec E, van der Schors R, van der Geest L, Li KW, Stiekema WJ, Liu CM (2006) The CLAVATA3/ESR motif of CLAVATA3 is functionally independent from the nonconserved flanking sequences. Plant Physiol 141:1284–1292

    PubMed  CAS  Google Scholar 

  • Francis D (2007) The plant cell cycle – 15 years on. New Phytol 174:261–278

    PubMed  CAS  Google Scholar 

  • Francis D, Halford NG (2006) Nutrient sensing in plant meristems. Plant Mol Biol 60:981–993

    PubMed  CAS  Google Scholar 

  • Friml J (2003) Auxin transport shaping the plant. Curr Opin Plant Biol 6:7–12

    PubMed  CAS  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153

    PubMed  CAS  Google Scholar 

  • Fu XD, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743

    PubMed  CAS  Google Scholar 

  • Fukaki H, Tasaka M (2009) Hormone interaction during lateral root formation. Plant Mol Biol 69:437–449

    PubMed  CAS  Google Scholar 

  • Fusconi A, Gnavi E, Trotta A, Berta G (1999) Apical meristems of tomato roots and their modifications induced by arbuscolar mychorrhizal and soliborne pathogenic fungi. New Phytol 142:505–516

    Google Scholar 

  • Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulatorsof Arabidopsis root development. Nature 449:1053–1057

    PubMed  CAS  Google Scholar 

  • Gallois JL, Nora FR, Mizukami Y, Sablowski R (2004) WUSCHEL induces shoot stem-cell activity and developmental plasticity in the root meristem. Genes Dev 18:375–380

    PubMed  CAS  Google Scholar 

  • Goodman AM, Ennos AR (1996) A comparative study of the response of the roots and shoots of sunflower and maize to mechanical stimulation. J Exp Bot 47:1499–1507

    CAS  Google Scholar 

  • Greenboim-Wainberg Y, Maymon I, Borochov R, Alvarez J, Olszewski N, Ori N, Eshed Y, Weiss D (2005) Cross talk between gibberellin and cytokinin: the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signalling. Plant Cell 17:92–102

    PubMed  CAS  Google Scholar 

  • Grieneisen VA, Xu J, Maree AF, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449:1008–1013

    PubMed  CAS  Google Scholar 

  • Guttenberg HV (1968) Der prïmare Bau der Angiospermenwurzel. Handbuch der Pflanzenanatomie. Band 8, Teil 5. Gebrüder Borntraeger, Berlin, Germany

    Google Scholar 

  • Haecker A, Grob-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann A, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131:657–668

    PubMed  CAS  Google Scholar 

  • Hall Q, Cannon MC (2002) The cell wall hydroxyproline-rich glycoprotein RSH is essential for normal embryo development in Arabidopsis. Plant Cell 14:1161–1172

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hamann T, Benkova E, Bäurle I, Kientz M, Jürgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–1615

    PubMed  CAS  Google Scholar 

  • Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411

    PubMed  CAS  Google Scholar 

  • Heimsch C, Seago JL Jr (2008) Organization of the root apical meristem in angiosperms. Am J Bot 95:1–21

    PubMed  Google Scholar 

  • Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15:1899–1911

    PubMed  CAS  Google Scholar 

  • Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567

    PubMed  CAS  Google Scholar 

  • Hellmann H, Hobbie L, Chapman A, Dharmasiri S, Dharmasiri N, Del Pozo C, Reinhardt D, Estelle M (2003) Arabidopsis AXR6 encodes CUL1 implicating SCF E3 ligases in auxin regulation of embryogenesis. EMBO J 22:3314–3325

    PubMed  CAS  Google Scholar 

  • Hobbie L, McGovern M, Hurwitz LR, Pierro A, Liu NY, Bandyopadhyay A, Estelle M (2000) The axr6 mutants of Arabidopsis thaliana define a gene involved in auxin responses and early development. Development 127:23–32

    PubMed  CAS  Google Scholar 

  • Hobe M, Muller R, Grunewald M, Brand U, Simon R (2003) Loss of CLE40, a protein functionally equivalent to the stem-cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev Genes Evol 213:371–381

    PubMed  CAS  Google Scholar 

  • Hsieh TF, Hakim O, Ohad N, Fischer RL (2003) From flour to flower: how Polycomb group proteins influence multiple aspects of plant development. Trends Plant Sci 8:439–445

    PubMed  CAS  Google Scholar 

  • Huck-Hui N, Bird A (1999) DNA methylation and chromatin modification. Curr Opin Genet Dev 9:158–163

    Google Scholar 

  • Ikeda Y, Men S, Fischer U, Stepanova AN, Alonso JM, Ljung K, Grebe M (2009) Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nat Cell Biol 11:731–738

    PubMed  CAS  Google Scholar 

  • Innocenti AM, Bitonti MB, Arrigoni O, Liso R (1990) The size of quiescent centre in roots of Allium cepa L. grown with ascorbic acid. New Phytol 114:507–509

    Google Scholar 

  • Ishida T, Fujiwara S, Miura K, Stacey N, Yoshimura M, Schneider K, Adachi S, Minamisawa K, Umeda M, Sugimoto K (2009) Sumo E3 ligase HIGH PLOIDY2 regulates endocycle onset and meristems maintenance in Arabidopsis. Plant Cell 2:2284–2297

    Google Scholar 

  • Jackson D (2005) Transcription factor movement through plasmodesmata. In: Oparka K (ed), Plasmodesmata. Ann Plant Rev 18. Blackwell, Dundee, pp 113–130

    Google Scholar 

  • Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556–560

    Google Scholar 

  • Jiang K, Feldman LJ (2005) Regulation of root apical meristem development. Annu Rev Cell Dev Biol 21:485–509

    Google Scholar 

  • Jiang K, Zhu T, Diao Z, Huang H, Feldman LJ (2010) The maize root stem cell niche: a partnership between two sister cell populations. Planta 231:411–424

    PubMed  CAS  Google Scholar 

  • Katz A, Oliva M, Mosquna A, Hakim O, Ohad N (2004) FIE and CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. Plant J 37:707–719

    PubMed  CAS  Google Scholar 

  • Kaya H, Shibahara KI, Taoka KI, Iwabuchi M, Stillman B, Araki T (2001) FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104:131–142

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kidner CA, Martienssen R (2005) The developmental role of microRNA in plants. Curr Opin Plant Biol 8:38–44

    PubMed  CAS  Google Scholar 

  • Kiefer JC (2009) Primer and interviews: gene regulation in Arabidopsis thaliana. Dev Dyn 238:2249–2458

    Google Scholar 

  • Kornet N, Scheres B (2009) Stem-cell factors in plants: chromatin connections. Cold Spring Harb Symp Quant Biol 73:235–242

    Google Scholar 

  • Kropf DL, Bisgrove SR, Hable WE (1999) Establishing a growth axis in fucoid algae. Trends Plant Sci 4:490–494

    PubMed  Google Scholar 

  • Kwon CS, Chen C, Wagner D (2005) WUSCHEL is a primary target for transcriptional regulation by SPLAYED in dynamic control of stem-cell fate in Arabidopsis. Genes Dev 19:992–1003

    PubMed  CAS  Google Scholar 

  • Larkins BA, Dilkes BP, Dante RA, Coelho CM, Woo Y, Liu Y (2001) Investigating the hows and whys of DNA endoreduplication. J Exp Bot 52:183–192

    PubMed  CAS  Google Scholar 

  • Lau S, Jürgens G, De Smet I (2008) The evolving complexity of the auxin pathway. Plant Cell 20:1738–1746

    PubMed  CAS  Google Scholar 

  • Lauber MH, Waizenegger I, Steinmann T, Schwarz H, Mayer U, Hwang I, Lukowitz W, Jürgens G (1997) The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J Cell Biol 139:1485–1493

    PubMed  CAS  Google Scholar 

  • Law JA, Jacobsen SE (2009) Dynamic DNA methylation. Science 323:1568–1569

    PubMed  CAS  Google Scholar 

  • Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220

    PubMed  CAS  Google Scholar 

  • Lee JY, Cui W (2009) Non-cell autonomous RNA trafficking and long-distance signaling. J Plant Biol 52:10–18

    CAS  Google Scholar 

  • Levesque MP, Vernoux T, Busch W, Cui H, Wang JY, Blilou I, Hassan H, Nakajima K, Matsumoto N, Lohmann JU (2006) Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. Plant Biol 4:739–752

    CAS  Google Scholar 

  • Li L, Xie T (2005) Stem-cell niche: structure and function. Annu Rev Cell Dev Biol 21:605–631

    PubMed  CAS  Google Scholar 

  • Li H, Cheng Y, Murphy A, Hagen G, Wilfoyle TJ (2009) Constitutive repression and activation of auxin signaling in Arabidopsis. Plant Physiol 149:1277–1288

    PubMed  CAS  Google Scholar 

  • Liso R, Innocenti AM, Bitonti MB, Arrigoni O (1988) Ascorbic acid-induced progression of quiescent centre cells from G1 to S phase. New Phytol 110:469–471

    CAS  Google Scholar 

  • Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Normanly J, Sandberg G (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17:1090–1104

    PubMed  CAS  Google Scholar 

  • Long JA, Ohno C, Smith ZR, Meyerowitz EM (2006) TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312:1520–1523

    PubMed  CAS  Google Scholar 

  • Lucas WJ, Lee JY (2004) Plasmodesmata as a supracellular control network in plants. Nat Rev Mol Cell Biol 5:712–726

    PubMed  CAS  Google Scholar 

  • Macaluso M, Montanari M, Giordano A (2006) A: Rb family proteins as modulators of gene expression and new aspects regarding the interaction with chromatin remodeling enzymes. Oncogene 25:5263–5267

    PubMed  CAS  Google Scholar 

  • Mayer U, Büttner G, Jürgens G (1993) Apical–basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 117:149–162

    Google Scholar 

  • Mayer KFX, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T (1998) Role of WUSCHEL in regulating stem-cell fate in the Arabidopsis shoot meristem. Cell 95:805–815

    PubMed  CAS  Google Scholar 

  • McCulloch EA, Till JE (2005) Perspectives on the properties of stem-cells. Nat Med 11:1026–1028

    PubMed  CAS  Google Scholar 

  • McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15:1120–1130

    PubMed  CAS  Google Scholar 

  • Meyerowitz EM (2002) Plants compared to animals: the broadest comparative study of development. Science 295:1482–1485

    PubMed  CAS  Google Scholar 

  • Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553–560

    PubMed  CAS  Google Scholar 

  • Morrison SJ, Spradling AC (2008) Stem-cells and niches: mechanisms that promote stem-cell maintenance throughout life. Cell 132:598–611

    PubMed  CAS  Google Scholar 

  • Moubayidin L, Di Mambro R, Sabatini S (2009) Cytokinin-auxin crosstalk. Trends Plant Sci 14:557–562

    PubMed  CAS  Google Scholar 

  • Mouchel CF, Osmont KS, Hardtke CS (2006) BRX mediates feedback between brassinosteroid levels and auxin signaling in root growth. Nature 443:458–461

    PubMed  CAS  Google Scholar 

  • Muller B, Sheen J (2008) Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453:1094–1097

    PubMed  Google Scholar 

  • Nakajima K, Sena G, Nawy T, Benfey P (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311

    PubMed  CAS  Google Scholar 

  • Nardmann J, Reisewitz P, Werr W (2009) Discrete shoot and root stem-cell promoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Mol Biol Evol 26:1745–1755

    PubMed  CAS  Google Scholar 

  • Nawy T, Lee JY, Colinas J, Wang JY, Thongrod SC, Malamy JE, Birbaum K, Benfey PN (2005) Transcriptional profile of the Arabidopsis root quiescent center. Plant Cell 17:1908–1925

    PubMed  CAS  Google Scholar 

  • Ogas J, Kaufmann S, Henderson J, Somerville C (1999) PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci USA 96:13839–13844

    PubMed  CAS  Google Scholar 

  • Ohlstein B, Kai T, Decotto E, Spradling A (2004) The stem-cell niche: theme and variations. Curr Opin Cell Biol 16:693–699

    PubMed  CAS  Google Scholar 

  • Ortega-Martinez O, Pernas M, Carol RJ, Dolan L (2007) Ethylene modulates stem-cell division in the Arabidopsis thaliana root. Science 317:507–510

    PubMed  CAS  Google Scholar 

  • Paquette AJ, Benfey PN (2005) Maturation of the ground tissue of the root is regulated by gibberellin and SCARECROW and requires SHORT-ROOT. Plant Physiol 138:636–640

    PubMed  CAS  Google Scholar 

  • Perilli S, Moubayidin L, Sabatini S (2009) The molecular basis of cytokinin function. Curr Opin Plant Biol 13:21–26

    PubMed  Google Scholar 

  • Petersson SV, Johansson AI, Kowalczyk M, Makoveychuk A, Wang JY, Moritz T, Grebe M, Benfey PN, Sandberg G, Ljung K (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 21:1659–1668

    PubMed  CAS  Google Scholar 

  • Petrášek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688

    PubMed  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Jansen MA (2009) Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant cell Environ 32:158–169

    PubMed  Google Scholar 

  • Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18:111–119

    PubMed  CAS  Google Scholar 

  • Qu LJ, Zhu YX (2006) Transcription factor families in Arabidopsis: major progress and outstanding issues for future research. Curr Opin Plant Biol 9:544–549

    PubMed  CAS  Google Scholar 

  • Richter S, Anders N, Wolters H, Beckmann H, Thomann A, Heinrich R, Schrader J, Singh MK, Geldner N, Mayer U, Jürgens G (2010) Role of the GNOM gene in Arabidopsis apical-basal patterning – from mutant phenotype to cellular mechanism of protein action. Eur J Cell Biol 89:138–144

    PubMed  CAS  Google Scholar 

  • Riechman JL (2002) Transcriptional regulation: a genomic overview. In: Somerville CR, Meyerowitz EM (eds) The Arabidopsis book. American Society of Plant Biologists, Rockville, MD

    Google Scholar 

  • Robert HS, Friml J (2009) Auxin and other signals on the move in plants. Nat Chem Biol 5:325–332

    PubMed  CAS  Google Scholar 

  • Rodrigues A, Santiago J, Rubio S, Saez A, Osmont KS, Gadea J, Hardtke CS, Rodriguez PL (2009) The short-rooted fhenotype of the brevis radix mutant partly reflects root Abscisic Acid hypersensitivity1[C][W][OA]. Plant Physiol 149:1917–1928

    PubMed  CAS  Google Scholar 

  • Ruzicka K, Simaskova M, Duclercq J, Petrasek J, Zazimalova E, Simon S, Friml J, Van Montagu MCE, Benkova E (2009) Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc Natl Acad Sci USA 106:4284–4289

    PubMed  CAS  Google Scholar 

  • Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem-cell niche in the Arabidopsis root meristem. Genes Dev 17:354–358

    PubMed  CAS  Google Scholar 

  • Sablowski R (2007) The dynamic plant cell niches. Curr Opin Plant Biol 10:639–644

    PubMed  CAS  Google Scholar 

  • Sakakibara H (2006) CYTOKININS: activity biosynthesis, and translocation. Ann Rev Plant Biol 57:431–449

    CAS  Google Scholar 

  • Sanchez-Calderon L, Lopez-bucio J, Chacon-Lopez A, Cruz-Ramirez A, Nieto-Jacobo F, Dubrrovsky JG (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46:174–184

    PubMed  CAS  Google Scholar 

  • Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signaling in Arabidopsis thaliana shoot and root stem-cell organizers. Nature 446:811–814

    PubMed  CAS  Google Scholar 

  • Scacchi E, Osmont KS, Beuchat J, Salinas P, Navarrete-Gomez M, Trigueros M, Ferrandiz C, Hardtke CS (2009) Dynamic, auxin-responsive plasma membrane-to-nucleus movement of Arabidopsis BRX. Development 136:2059–2067

    PubMed  CAS  Google Scholar 

  • Scheres B (2001) Plant cell identity. The role of position and lineage. Plant Physiol 125:112–114

    PubMed  CAS  Google Scholar 

  • Scheres B (2007) Stem-cell niches: nursery rhymes across kingdoms. Nat Rev Mol Cell Biol 8:345–354

    PubMed  CAS  Google Scholar 

  • Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506

    PubMed  CAS  Google Scholar 

  • Schoof H, Lenhard M, Haecker A, Meyer KFX, Jürgens G, Laux T (2000) The stem-cell population of Arabidopsis shoot meristema is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644

    PubMed  CAS  Google Scholar 

  • Schwartz YB, Pirrotta V (2007) Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8:9–22

    PubMed  CAS  Google Scholar 

  • Schwartz YB, Kahn TG, Nix DA, Li XY, Bourgon R, Biggin M, Pirrotta V (2006) Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat Genet 38:700–705

    PubMed  CAS  Google Scholar 

  • Seago JL, Heimsch C (1969) Apical organization in roots of the Convolvulaceae. Am J Bot 56:131–138

    Google Scholar 

  • Sena G, Wang X, Liu HY, Hofhuis H, Birnbaum KD (2009) Organ regeneration does not require a functional stem-cell niche in plants. Nature 457:1150–1153

    PubMed  CAS  Google Scholar 

  • Sharma P, Dubey RS (2007) involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminium. Plant Cell Rep 26:2027–2038

    PubMed  CAS  Google Scholar 

  • Shishkova S, Rost TL, Dubrovsky JG (2008) Determinate root growth and meristem maintenance in Angiosperms. Ann Bot 101:319–340

    PubMed  CAS  Google Scholar 

  • Spradling A, Drummond-Barbosa D, Kai T (2001) Stem-cells find their niche. Nature 414:98–104

    PubMed  CAS  Google Scholar 

  • Stahl Y, Simon R (2009) Is the Arabidopsis root niche protected by sequestration of the CLE40 signal by its putative receptor ACR4. Plant Signal Behav 4:634–635

    PubMed  CAS  Google Scholar 

  • Stahl Y, Simon R (2010) Plant primary meristems: shared functions and regulatory mechanisms. Curr Opin Plant Biol 13:53–58

    PubMed  CAS  Google Scholar 

  • Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem-cell niche in Arabidopsis root meristems. Curr Biol 19:909–914

    PubMed  CAS  Google Scholar 

  • Stange BC, Rowland RE, Rapley BI, Podd JV (2002) ELF magnetic fields increase amino acid uptake into Vicia faba L. roots and alter ion movement across the plasma membrane. Bioelectromagnetics 23:347–354

    PubMed  CAS  Google Scholar 

  • Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Gälweiler L, Palme K, Jürgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 8:316–318

    Google Scholar 

  • Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jurgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191

    PubMed  CAS  Google Scholar 

  • Strader LC, Ritchie S, Soule JD, McGinnis KM, Steber CM (2004) Recessive-interfering mutations in the gibberellin signaling gene SLEEPY1 are rescued by overexpression of its homologue, SNEEZY. Proc Natl Acad Sci USA 101:12771–12776

    PubMed  CAS  Google Scholar 

  • Strader LC, Monroe-Augustus M, Bartel B (2008) The IBR5phosphatase promotes Arabidopsis auxin responses through a novel mechanism distinct from TIR1 mediated repressor degradation. BMC Plant Biol 8:41–56

    PubMed  Google Scholar 

  • Sung S, He Y, Eshoo TW, Tamada Y, Johnson L, Nakahigashi K, Goto K, Jacobsen SE, Amasino RM (2006) Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat Genet 38:706–710

    PubMed  CAS  Google Scholar 

  • Suzuki MM, Bird A (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9:465–476

    PubMed  CAS  Google Scholar 

  • Swain SM, Tseng TS, Thornton TM, Gopalraj M, Olszewski NE (2002) SPINDLY is a nuclearlocalized repressor of gibberellin signal transduction expressed throughout the plant. Plant Physiol 129:605–615

    PubMed  CAS  Google Scholar 

  • Swarup R, Kramer EM, Perry P, Knox K, Geyser MO, Haseloff J, Beemster GTS, Bhalerao R, Bennett MJ (2005) Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat Cell Biol 11:1057–1064

    Google Scholar 

  • Taiz L, Zeiger E (1998) Plant physiology, 2nd edn. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Taiz L, Zeiger E (2002) Fisiologia vegetale, 2nd ed, Piccin, Padova, Italy

    Google Scholar 

  • Thomann A, Lechner E, Hansen M, Dumbliauskas E, Parmentier Y, Kieber J, Scheres B, Genschik P (2009) Arabidopsis CULLIN3 genes regulate primary root growth and patterning by ethylene-dependent and – independent mechanisms. Plos Genet 5:e1000328

    PubMed  Google Scholar 

  • To JPC, Kieber JJ (2007) Cytokinin signaling: two-components and more. Trends Plant Sci 13:85–92

    Google Scholar 

  • Turck F, Roudier F, Farrona S, Martin-Magniette ML, Guillaume E, Buisine N, Gagnot S, Martienssen RA, Coupland G, Colot V (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3(6):e86

    PubMed  Google Scholar 

  • Van den Berg C, Willemsen V, Hage W, Weisbeek P, Scheres B (1995) Cell fate in the Arabidopsis root meristem determined by directional signaling. Nature 378:62–65

    PubMed  Google Scholar 

  • Van den Berg C, Willemsen V, Hage W, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390:287–289

    PubMed  Google Scholar 

  • Veit B (2006) Stem-cell signaling networks in plants. Plant Mol Biol 60:793–810

    PubMed  CAS  Google Scholar 

  • Vernon DM, Meinke DW (1994) Embryogenic transformation of the suspensor in twin, a polyembryonic mutant of Arabidopsis. Dev Biol 165:566–573

    PubMed  CAS  Google Scholar 

  • Vernoux T, Benfey PN (2005) Signal that regulate stem-cell activity during plant development. Curr Opin Genet Dev 15:388–394

    PubMed  CAS  Google Scholar 

  • Vert G, Walcher CL, Chory J, Nemhauser JL (2008) Integration of auxin and brassinosteroid pathways by Auxin Response Factor 2. Proc Natl Acad Sci USA 105:9829–9834

    PubMed  CAS  Google Scholar 

  • Vieten A, Sauer M, Brewer PB, Friml J (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci 12:160–168

    PubMed  CAS  Google Scholar 

  • Vroemen CW, Langeveld S, Mayer U, Ripper G, Jürgens G, Van Kammen A, De Vries SC (1996) Pattern formation in the Arabidopsis embryo revealed by position-specific lipid transfer protein gene expression. Plant Cell 8:783–791

    PubMed  CAS  Google Scholar 

  • Waisel Y, Eshel A, Kafkafi U (1997) Plant root: the hidden half, 2nd edn. Marcel Dekker, New York, NY, pp 483–811

    Google Scholar 

  • Waizenegger I, Lukowitz W, Assaad F, Schwarz H, Jürgens G, Mayer U (2000) The Arabidopsis KNOLLE and KEULE genes interact to promote vesicle fusion during cytokinesis. Curr Biol 10:1371–1374

    PubMed  CAS  Google Scholar 

  • Webster PL, Langenauer HD (1973) Experimental control of the activity of the quiescent centre in excised root tips of Zea mays. Planta 112:91–100

    CAS  Google Scholar 

  • Webster PL, Mc Leod RD (1996) The root apical meristems and its margins. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant root: the hidden half, 2nd edn. Marcel Dekker, New York, NY, pp 51–76

    Google Scholar 

  • Weijers D, Benkova E, Jäger KE, Schlereth A, Hamann T, Kientz M, Wilmoth JC, Reed JW, Jürgens G (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J 24:1874–1885

    PubMed  CAS  Google Scholar 

  • Welch D, Hassan H, Blilou I, Immink R, Heidstra R, Scheres B (2007) Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action. Genes Dev 21:2196–2204

    PubMed  CAS  Google Scholar 

  • Werner T, Schmülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12:527–538

    PubMed  CAS  Google Scholar 

  • Wildwater M, Campilho A, Perez-Perez JM, Heidstra R, Blilou I, Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B (2005) The RETINOBLASTOMA-RELATED gene regulates stem-cell maintenance in Arabidopsis roots. Cell 123:1337–1349

    PubMed  CAS  Google Scholar 

  • Xu J, Hofhuis H, Heidstra R, Sauer M, Friml J, Scheres B (2006) A molecular framework for plant regeneration. Science 311:385–388

    PubMed  CAS  Google Scholar 

  • Yadav RK, Girke T, Pasala S, Xie M, Reddy GV (2009) Gene expression map of the Arabidopsis shoot apical meristems stem-cell niche. Proc Natl Acad Sci USA 106:4941–4946

    PubMed  CAS  Google Scholar 

  • Yang X, Zhang F, Kudlow JE (2002) Recruitment of O-GlcNac transferase to promoters by corepressor mSin3A: coupling protein O-GlcNcylation to transcriptional repression. Cell 110:69–80

    PubMed  CAS  Google Scholar 

  • Zazímalová E, Murphy AS, Yang H, Hoyerová K, Hosek P (2010) Auxin transporters-why so many? Cold Spring Harb Perspect Biol 2(3):a001552

    PubMed  Google Scholar 

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Acknowledgments

We would like to thank Dennis Francis for fruitful discussions, helpful comments, and for critical reading of the manuscript. We also apologize to authors whose relevant work could not be cited owing to space constraints. Finally, M.B.B. is grateful to her Ph.D student Domenico Iaria for Photoshop drawings.

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Bitonti, M.B., Chiappetta, A. (2010). Root Apical Meristem Pattern: Hormone Circuitry and Transcriptional Networks. In: Lüttge, U., Beyschlag, W., Büdel, B., Francis, D. (eds) Progress in Botany 72. Progress in Botany, vol 72. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-13145-5_2

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