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Cellular and Molecular Life Sciences

, Volume 68, Issue 17, pp 2885–2906 | Cite as

Organogenesis from stem cells in planta: multiple feedback loops integrating molecular and mechanical signals

  • Fabrice Besnard
  • Teva Vernoux
  • Olivier HamantEmail author
Review

Abstract

In multicellular organisms, the coordination of cell behaviors largely relies on biochemical and biophysical signals. Understanding how such signals control development is often challenging, because their distribution relies on the activity of individual cells and, in a feedback loop, on tissue behavior and geometry. This review focuses on one of the best-studied structures in biology, the shoot apical meristem (SAM). This tissue is responsible for the production of all the aerial parts of a plant. In the SAM, a population of stem cells continuously produces new cells that are incorporated in lateral organs, such as leaves, branches, and flowers. Organogenesis from stem cells involves a tight regulation of cell identity and patterning as well as large-scale morphogenetic events. The gene regulatory network controlling these processes is highly coordinated in space by various signals, such as plant hormones, peptides, intracellular mobile factors, and mechanical stresses. Many crosstalks and feedback loops interconnecting these pathways have emerged in the past 10 years. The plant hormone auxin and mechanical forces have received more attention recently and their role is more particularly detailed here. An integrated view of these signaling networks is also presented in order to help understanding how robust shape and patterning can emerge from these networks.

Keywords

Developmental biology Signaling networks Cell–cell communication Systems biology Biomechanics Plant development Meristem Morphogens Hormonal crosstalk Auxin Cytokinin 

References

  1. 1.
    Aggarwal P, Yadav RK, Reddy GV (2010) Identification of novel markers for stem-cell niche of Arabidopsis shoot apex. Gene Expr Patterns 10:259–264PubMedGoogle Scholar
  2. 2.
    Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857PubMedGoogle Scholar
  3. 3.
    Aida M, Ishida T, Tasaka M (1999) Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126:1563–1570PubMedGoogle Scholar
  4. 4.
    Aida M, Vernoux T, Furutani M, Traas J, Tasaka M (2002) Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development 129:3965–3974PubMedGoogle Scholar
  5. 5.
    Alabadi D, Blazquez MA, Carbonell J, Ferrandiz C, Perez-Amador MA (2009) Instructive roles for hormones in plant development. Int J Dev Biol 53:1597–1608PubMedGoogle Scholar
  6. 6.
    Andersen SU, Buechel S, Zhao Z, Ljung K, Novak O et al (2008) Requirement of B2-type cyclin-dependent kinases for meristem integrity in Arabidopsis thaliana. Plant Cell 20:88–100PubMedGoogle Scholar
  7. 7.
    Bainbridge K, Guyomarc’h S, Bayer E, Swarup R, Bennett M et al (2008) Auxin influx carriers stabilize phyllotactic patterning. Genes Dev 22:810–823PubMedGoogle Scholar
  8. 8.
    Barton MK (2010) Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol 341:95–113PubMedGoogle Scholar
  9. 9.
    Bayer EM, Smith RS, Mandel T, Nakayama N, Sauer M et al (2009) Integration of transport-based models for phyllotaxis and midvein formation. Genes Dev 23:373–384PubMedGoogle Scholar
  10. 10.
    Benjamins R, Ampudia CS, Hooykaas PJ, Offringa R (2003) PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol 132:1623–1630PubMedGoogle Scholar
  11. 11.
    Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D et al (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602PubMedGoogle Scholar
  12. 12.
    Bennett MJ, Marchant A, Green HG, May ST, Ward SP et al (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948–950PubMedGoogle Scholar
  13. 13.
    Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I et al (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44PubMedGoogle Scholar
  14. 14.
    Bolduc N, Hake S (2009) The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 21:1647–1658PubMedGoogle Scholar
  15. 15.
    Borghi L, Bureau M, Simon R (2007) Arabidopsis jagged lateral organs is expressed in boundaries and coordinates KNOX and PIN activity. Plant Cell 19:1795–1808PubMedGoogle Scholar
  16. 16.
    Borghi L, Gutzat R, Futterer J, Laizet Y, Hennig L et al (2010) Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22:1792–1811PubMedGoogle Scholar
  17. 17.
    Boudaoud A (2010) An introduction to the mechanics of morphogenesis for plant biologists. Trends Plant Sci 15:353–360PubMedGoogle Scholar
  18. 18.
    Bowman JL, Eshed Y, Baum SF (2002) Establishment of polarity in angiosperm lateral organs. Trends Genet 18:134–141PubMedGoogle Scholar
  19. 19.
    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 289:617–619PubMedGoogle Scholar
  20. 20.
    Breuil-Broyer S, Morel P, de Almeida-Engler J, Coustham V, Negrutiu I et al (2004) High-resolution boundary analysis during Arabidopsis thaliana flower development. Plant J 38:182–192PubMedGoogle Scholar
  21. 21.
    Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M et al (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408:967–971PubMedGoogle Scholar
  22. 22.
    Cantrill LC, Overall RL, Goodwin PB (2005) Changes in macromolecular movement accompany organogenesis in thin cell layers of Torenia fournieri. Planta 222:933–946PubMedGoogle Scholar
  23. 23.
    Carabelli M, Possenti M, Sessa G, Ciolfi A, Sassi M et al (2007) Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity. Genes Dev 21:1863–1868PubMedGoogle Scholar
  24. 24.
    Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S et al (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–321PubMedGoogle Scholar
  25. 25.
    Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43:265–285PubMedGoogle Scholar
  26. 26.
    Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20:1790–1799PubMedGoogle Scholar
  27. 27.
    Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19:2430–2439PubMedGoogle Scholar
  28. 28.
    Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC et al (2009) Pattern formation via small RNA mobility. Genes Dev 23:549–554PubMedGoogle Scholar
  29. 29.
    Cho HT, Cosgrove DJ (2002) Regulation of root hair initiation and expansin gene expression in Arabidopsis Plant Cell 14:3237–3253 PubMedGoogle Scholar
  30. 30.
    Chow B, McCourt P (2006) Plant hormone receptors: perception is everything. Genes Dev 20:1998–2008PubMedGoogle Scholar
  31. 31.
    Christensen SK, Dagenais N, Chory J, Weigel D (2000) Regulation of auxin response by the protein kinase PINOID. Cell 100:469–478PubMedGoogle Scholar
  32. 32.
    Coen E, Rolland-Lagan AG, Matthews M, Bangham JA, Prusinkiewicz P (2004) The genetics of geometry. Proc Natl Acad Sci USA 101:4728–4735PubMedGoogle Scholar
  33. 33.
    Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861PubMedGoogle Scholar
  34. 34.
    de Reuille PB, Bohn-Courseau I, Ljung K, Morin H, Carraro N et al (2006) Computer simulations reveal properties of the cell–cell signaling network at the shoot apex in Arabidopsis Proc Natl Acad Sci USA 103:1627–1632 PubMedGoogle Scholar
  35. 35.
    Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R et al (2007) Cytokinins determine Arabidopsisroot-meristem size by controlling cell differentiation. Curr Biol 17:678–682PubMedGoogle Scholar
  36. 36.
    Dhonukshe P, Tanaka H, Goh T, Ebine K, Mahonen AP et al (2008) Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456:962–966PubMedGoogle Scholar
  37. 37.
    Dodsworth S (2009) A diverse and intricate signalling network regulates stem cell fate in the shoot apical meristem. Dev Biol 336:1–9PubMedGoogle Scholar
  38. 38.
    Dumais J, Kwiatkowska D (2002) Analysis of surface growth in shoot apices. Plant J 31:229–241PubMedGoogle Scholar
  39. 39.
    Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T (1996) The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsisshoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10:967–979PubMedGoogle Scholar
  40. 40.
    Engstrom EM, Andersen CM, Gumulak-Smith J, Hu J, Orlova E et al (2010) Arabidopsishomologs of the petunia HAIRY MERISTEM gene are required for maintenance of shoot and root indeterminacy. Plant Physiol 155(2):735–750PubMedGoogle Scholar
  41. 41.
    Fernandez R, Das P, Mirabet V, Moscardi E, Traas J et al (2010) Imaging plant growth in 4D: robust tissue reconstruction and lineaging at cell resolution. Nat Methods 7:547–553PubMedGoogle Scholar
  42. 42.
    Fleming AJ, McQueenMason S, Mandel T, Kuhlemeier C (1997) Induction of leaf primordia by the cell wall protein expansion. Science 276:1415–1418Google Scholar
  43. 43.
    Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914PubMedGoogle Scholar
  44. 44.
    Frigerio M, Alabadi D, Perez-Gomez J, Garcia-Carcel L, Phillips AL et al (2006) Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol 142:553–563PubMedGoogle Scholar
  45. 45.
    Friml J (2010) Subcellular trafficking of PIN auxin efflux carriers in auxin transport. Eur J Cell Biol 89:231–235PubMedGoogle Scholar
  46. 46.
    Friml J, Yang X, Michniewicz M, Weijers D, Quint A et al (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306:862–865PubMedGoogle Scholar
  47. 47.
    Gaamouche T, Manes CL, Kwiatkowska D, Berckmans B, Koumproglou R et al (2010) Cyclin-dependent kinase activity maintains the shoot apical meristem cells in an undifferentiated state. Plant J 64:26–37PubMedGoogle Scholar
  48. 48.
    Galinha C, Bilsborough G, Tsiantis M (2009) Hormonal input in plant meristems: a balancing act. Semin Cell Dev Biol 20:1149–1156PubMedGoogle Scholar
  49. 49.
    Gallagher KL, Benfey PN (2005) Not just another hole in the wall: understanding intercellular protein trafficking. Genes Dev 19:189–195PubMedGoogle Scholar
  50. 50.
    Gallois JL, Woodward C, Reddy GV, Sablowski R (2002) Combined SHOOT MERISTEMLESS and WUSCHEL trigger ectopic organogenesis in Arabidopsis. Development 129:3207–3217PubMedGoogle Scholar
  51. 51.
    Gisel A, Hempel FD, Barella S, Zambryski P (2002) Leaf-to-shoot apex movement of symplastic tracer is restricted coincident with flowering in Arabidopsis. Proc Natl Acad Sci USA 99:1713–1717PubMedGoogle Scholar
  52. 52.
    Giulini A, Wang J, Jackson D (2004) Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1. Nature 430:1031–1034PubMedGoogle Scholar
  53. 53.
    Goldshmidt A, Alvarez JP, Bowman JL, Eshed Y (2008) Signals derived from YABBY gene activities in organ primordia regulate growth and partitioning of Arabidopsis shoot apical meristems. Plant Cell 20:1217–1230PubMedGoogle Scholar
  54. 54.
    Goldsmith MH, Goldsmith TH, Martin MH (1981) Mathematical analysis of the chemosmotic polar diffusion of auxin through plant tissues. Proc Natl Acad Sci USA 78:976–980PubMedGoogle Scholar
  55. 55.
    Golz JF (2006) Signalling between the shoot apical meristem and developing lateral organs. Plant Mol Biol 60:889–903PubMedGoogle Scholar
  56. 56.
    Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA et al (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194PubMedGoogle Scholar
  57. 57.
    Gordon SP, Chickarmane VS, Ohno C, Meyerowitz EM (2009) Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc Natl Acad Sci USA 106:16529–16534PubMedGoogle Scholar
  58. 58.
    Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P et al (2007) Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development 134:3539–3548PubMedGoogle Scholar
  59. 59.
    Grandjean O, Vernoux T, Laufs P, Belcram K, Mizukami Y et al (2004) In vivo analysis of cell division, cell growth, and differentiation at the shoot apical meristem in Arabidopsis. Plant Cell 16:74–87PubMedGoogle Scholar
  60. 60.
    Green PB (1980) Organogenesis: a biophysical view. Ann Rev Plant Phys Plant Mol Biol 31:51–82Google Scholar
  61. 61.
    Green PB, Steele CS, Rennisch SC (1996) Phyllotactic patterns: a biophysical mechanism for their origin. Ann Bot 77:515–527Google Scholar
  62. 62.
    Greenboim-Wainberg Y, Maymon I, Borochov R, Alvarez J, Olszewski N et al (2005) Cross talk between gibberellin and cytokinin: the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling. Plant Cell 17:92–102PubMedGoogle Scholar
  63. 63.
    Grieneisen VA, Scheres B (2009) Back to the future: evolution of computational models in plant morphogenesis. Curr Opin Plant Biol 12:606–614PubMedGoogle Scholar
  64. 64.
    Grunewald W, Friml J (2010) The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J 29:2700–2714PubMedGoogle Scholar
  65. 65.
    Gutierrez R, Lindeboom JJ, Paredez AR, Emons AM, Ehrhardt DW (2009) Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol 11:797–806PubMedGoogle Scholar
  66. 66.
    Ha CM, Jun JH, Fletcher JC (2010) Shoot apical meristem form and function. Curr Top Dev Biol 91:103–140PubMedGoogle Scholar
  67. 67.
    Hamant O, Heisler MG, Jonsson H, Krupinski P, Uyttewaal M et al (2008) Developmental patterning by mechanical signals in Arabidopsis. Science 322:1650–1655PubMedGoogle Scholar
  68. 68.
    Hamant O, Nogue F, Belles-Boix E, Jublot D, Grandjean O et al (2002) The KNAT2 homeodomain protein interacts with ethylene and cytokinin signaling. Plant Physiol 130:657–665PubMedGoogle Scholar
  69. 69.
    Hamant O, Traas J (2010) The mechanics behind plant development. New Phytol 185:369–385PubMedGoogle Scholar
  70. 70.
    Hamant O, Traas J, Boudaoud A (2010) Regulation of shape and patterning in plant development. Curr Opin Genet Dev 20:454–459PubMedGoogle Scholar
  71. 71.
    Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411PubMedGoogle Scholar
  72. 72.
    Hay A, Kaur H, Phillips A, Hedden P, Hake S et al (2002) The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr Biol 12:1557–1565PubMedGoogle Scholar
  73. 73.
    Heisler MG, Hamant O, Krupinski P, Uyttewaal M, Ohno C et al (2010) Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol 8:e1000516PubMedGoogle Scholar
  74. 74.
    Heisler MG, Ohno C, Das P, Sieber P, Reddy GV et al (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15:1899–1911PubMedGoogle Scholar
  75. 75.
    Hibara K, Karim MR, Takada S, Taoka K, Furutani M et al (2006) Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell 18:2946–2957PubMedGoogle Scholar
  76. 76.
    Hohm T, Zitzler E, Simon R (2010) A dynamic model for stem cell homeostasis and patterning in Arabidopsis meristems. PLoS One 5:e9189PubMedGoogle Scholar
  77. 77.
    Huang F, Zago MK, Abas L, van Marion A, Galvan-Ampudia CS et al (2010) Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22:1129–1142PubMedGoogle Scholar
  78. 78.
    Husbands AY, Chitwood DH, Plavskin Y, Timmermans MC (2009) Signals and prepatterns: new insights into organ polarity in plants. Genes Dev 23:1986–1997PubMedGoogle Scholar
  79. 79.
    Ikeda M, Mitsuda N, Ohme-Takagi M (2009) Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. Plant Cell 21:3493–3505PubMedGoogle Scholar
  80. 80.
    Jackson D, Hake S (1999) Control of phyllotaxy in maize by the abphyl1 gene. Development 126:315–323PubMedGoogle Scholar
  81. 81.
    Jacqmard A, Gadisseur I, Bernier G (2003) Cell division and morphological changes in the shoot apex of Arabidopsis thaliana during floral transition. Ann Bot 91:571–576PubMedGoogle Scholar
  82. 82.
    Jaeger J, Irons D, Monk N (2008) Regulative feedback in pattern formation: towards a general relativistic theory of positional information. Development 135:3175–3183PubMedGoogle Scholar
  83. 83.
    Jasinski S, Piazza P, Craft J, Hay A, Woolley L et al (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15:1560–1565PubMedGoogle Scholar
  84. 84.
    Jones AM, Herman EM (1993) KDEL-containing auxin-binding protein is secreted to the plasma membrane and cell wall. Plant Physiol 101:595–606PubMedGoogle Scholar
  85. 85.
    Jonsson H, Heisler M, Reddy GV, Agrawal V, Gor V et al (2005) Modeling the organization of the WUSCHEL expression domain in the shoot apical meristem. Bioinformatics 21(Suppl 1):i232–i240PubMedGoogle Scholar
  86. 86.
    Jonsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E (2006) An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci USA 103:1633–1638PubMedGoogle Scholar
  87. 87.
    Karsenti E (2008) Self-organization in cell biology: a brief history. Nat Rev Mol Cell Biol 9:255–262PubMedGoogle Scholar
  88. 88.
    Kim I, Cho E, Crawford K, Hempel FD, Zambryski PC (2005) Cell-to-cell movement of GFP during embryogenesis and early seedling development in Arabidopsis. Proc Natl Acad Sci USA 102:2227–2231PubMedGoogle Scholar
  89. 89.
    Kim I, Zambryski PC (2005) Cell-to-cell communication via plasmodesmata during Arabidopsis embryogenesis. Curr Opin Plant Biol 8:593–599PubMedGoogle Scholar
  90. 90.
    Kim JY, Yuan Z, Cilia M, Khalfan-Jagani Z, Jackson D (2002) Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis. Proc Natl Acad Sci USA 99:4103–4108PubMedGoogle Scholar
  91. 91.
    Kim JY, Yuan Z, Jackson D (2003) Developmental regulation and significance of KNOX protein trafficking in Arabidopsis. Development 130:4351–4362PubMedGoogle Scholar
  92. 92.
    Kondo S, Miura T (2010) Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329:1616–1620PubMedGoogle Scholar
  93. 93.
    Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T et al (2006) A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313:845–848PubMedGoogle Scholar
  94. 94.
    Kuhlemeier C (2007) Phyllotaxis. Trends Plant Sci 12:143–150PubMedGoogle Scholar
  95. 95.
    Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M et al (2007) Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445:652–655PubMedGoogle Scholar
  96. 96.
    Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T et al (2009) Functional analyses of lonely guy cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21:3152–3169PubMedGoogle Scholar
  97. 97.
    Kutschera U, Niklas KJ (2007) The epidermal-growth-control theory of stem elongation: an old and a new perspective. J Plant Physiol 164:1395–1409PubMedGoogle Scholar
  98. 98.
    Laufs P, Grandjean O, Jonak C, Kieu K, Traas J (1998) Cellular parameters of the shoot apical meristem in Arabidopsis. Plant Cell 10:1375–1390PubMedGoogle Scholar
  99. 99.
    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 131:4311–4322PubMedGoogle Scholar
  100. 100.
    Laux T, Mayer KF, Berger J, Jurgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96PubMedGoogle Scholar
  101. 101.
    Leblanc N, David K, Grosclaude J, Pradier JM, Barbier-Brygoo H et al (1999) A novel immunological approach establishes that the auxin-binding protein, Nt-abp1, is an element involved in auxin signaling at the plasma membrane. J Biol Chem 274:28314–28320PubMedGoogle Scholar
  102. 102.
    Lee BH, Johnston R, Yang Y, Gallavotti A, Kojima M et al (2009) Studies of aberrant phyllotaxy1 mutants of maize indicate complex interactions between auxin and cytokinin signaling in the shoot apical meristem. Plant Physiol 150:205–216PubMedGoogle Scholar
  103. 103.
    Leibfried A, To JP, Busch W, Stehling S, Kehle A et al (2005) WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438:1172–1175PubMedGoogle Scholar
  104. 104.
    Lenhard M, Jurgens G, Laux T (2002) The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulation. Development 129:3195–3206PubMedGoogle Scholar
  105. 105.
    Lewis J (2008) From signals to patterns: space, time, and mathematics in developmental biology. Science 322:399–403PubMedGoogle Scholar
  106. 106.
    Leyser O (2006) Dynamic integration of auxin transport and signalling. Curr Biol 16:R424–R433PubMedGoogle Scholar
  107. 107.
    Li Y, Jones L, McQueen-Mason S (2003) Expansins and cell growth. Curr Opin Plant Biol 6:603–610PubMedGoogle Scholar
  108. 108.
    Liu QX, Yao LPi, H Wang, X Cui et al. 2008 The ARGONAUTE10 gene modulates shoot apical meristem maintenance and leaf polarity establishment by repressing miR165/166 in Arabidopsis. Plant JGoogle Scholar
  109. 109.
    Loiseau JE (1959) Observation et experimentation sur la phyllotaxie et le fonctionnememnt du sommet vegetatif chez quelques balsaminacees. Ann Sci Nat Bot Ser 11:1–214Google Scholar
  110. 110.
    Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69PubMedGoogle Scholar
  111. 111.
    Lyndon RF (1998) The shoot apical meristem. Cambridge, UKGoogle Scholar
  112. 112.
    Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M et al (1999) The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126:469–481PubMedGoogle Scholar
  113. 113.
    Marchant A, Kargul J, May ST, Muller P, Delbarre A et al (1999) AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J 18:2066–2073PubMedGoogle Scholar
  114. 114.
    Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G et al (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815PubMedGoogle Scholar
  115. 115.
    McQueen-Mason S, Cosgrove DJ (1994) Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci USA 91:6574–6578PubMedGoogle Scholar
  116. 116.
    Medford JI (1992) Vegetative apical meristems. Plant Cell 4:1029–1039PubMedGoogle Scholar
  117. 117.
    Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A et al (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130:1044–1056PubMedGoogle Scholar
  118. 118.
    Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947PubMedGoogle Scholar
  119. 119.
    Morris CE, Homann U (2001) Cell surface area regulation and membrane tension. J Membr Biol 179:79–102PubMedGoogle Scholar
  120. 120.
    Moussian B, Schoof H, Haecker A, Jurgens G, Laux T (1998) Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J 17:1799–1809PubMedGoogle Scholar
  121. 121.
    Nawy T, Bayer M, Mravec J, Friml J, Birnbaum KD et al (2010) The GATA factor HANABA TARANU is required to position the proembryo boundary in the early Arabidopsis embryo. Dev Cell 19:103–113PubMedGoogle Scholar
  122. 122.
    Newman KL, Fernandez AG, Barton MK (2002) Regulation of axis determinacy by the Arabidopsis PINHEAD gene. Plant Cell 14:3029–3042PubMedGoogle Scholar
  123. 123.
    Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:677–684PubMedGoogle Scholar
  124. 124.
    Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof YD et al (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–1256PubMedGoogle Scholar
  125. 125.
    Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495PubMedGoogle Scholar
  126. 126.
    Peaucelle A, Louvet R, Johansen JN, Hofte H, Laufs P et al (2008) Arabidopsis phyllotaxis is controlled by the methyl-esterification status of cell-wall pectins. Curr Biol 18:1943–1948PubMedGoogle Scholar
  127. 127.
    Petrasek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M et al (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–918PubMedGoogle Scholar
  128. 128.
    Pilkington M (1929) The regeneration of the stem apex. New Phytol 28:37–53Google Scholar
  129. 129.
    Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN et al (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17:61–76PubMedGoogle Scholar
  130. 130.
    Przemeck GK, Mattsson J, Hardtke CS, Sung ZR, Berleth T (1996) Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta 200:229–237PubMedGoogle Scholar
  131. 131.
    Pulido A, Laufs P (2010) Co-ordination of developmental processes by small RNAs during leaf development. J Exp Bot 61:1277–1291PubMedGoogle Scholar
  132. 132.
    Rast MI, Simon R (2008) The meristem-to-organ boundary: more than an extremity of anything. Curr Opin Genet Dev 18:287–294PubMedGoogle Scholar
  133. 133.
    Reddy GV, Heisler MG, Ehrhardt DW, Meyerowitz EM (2004) Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. Development 131:4225–4237PubMedGoogle Scholar
  134. 134.
    Reinhardt D, Frenz M, Mandel T, Kuhlemeier C (2003) Microsurgical and laser ablation analysis of interactions between the zones and layers of the tomato shoot apical meristem. Development 130:4073–4083PubMedGoogle Scholar
  135. 135.
    Reinhardt D, Frenz M, Mandel T, Kuhlemeier C (2005) Microsurgical and laser ablation analysis of leaf positioning and dorsoventral patterning in tomato. Development 132:15–26PubMedGoogle Scholar
  136. 136.
    Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518PubMedGoogle Scholar
  137. 137.
    Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K et al (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260PubMedGoogle Scholar
  138. 138.
    Reinhardt D, Wittwer F, Mandel T, Kuhlemeier C (1998) Localized upregulation of a new expansin gene predicts the site of leaf formation in the tomato meristem. Plant Cell 10:1427–1437PubMedGoogle Scholar
  139. 139.
    Rieu I, Laux T (2009) Signaling pathways maintaining stem cells at the plant shoot apex. Semin Cell Dev Biol 20:1083–1088PubMedGoogle Scholar
  140. 140.
    Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T et al (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143:111–121PubMedGoogle Scholar
  141. 141.
    Rupp HM, Frank M, Werner T, Strnad M, Schmulling T (1999) Increased steady state mRNA levels of the STM and KNAT1 homeobox genes in cytokinin overproducing Arabidopsis thaliana indicate a role for cytokinins in the shoot apical meristem. Plant J 18:557–563PubMedGoogle Scholar
  142. 142.
    Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T et al (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472PubMedGoogle Scholar
  143. 143.
    Sachs T (1969) Polarity and the induction of organized vascular tissues. Ann Bot 33:263–275Google Scholar
  144. 144.
    Sakamoto T, Kamiya N, Ueguchi-Tanaka M, Iwahori S, Matsuoka M (2001) KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev 15:581–590PubMedGoogle Scholar
  145. 145.
    Sauer M, Balla J, Luschnig C, Wisniewska J, Reinohl V et al (2006) Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 20:2902–2911PubMedGoogle Scholar
  146. 146.
    Savaldi-Goldstein S, Chory J (2008) Growth coordination and the shoot epidermis. Curr Opin Plant Biol 11:42–48PubMedGoogle Scholar
  147. 147.
    Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027PubMedGoogle Scholar
  148. 148.
    Schoof H, Lenhard M, Haecker A, Mayer KF, Jurgens G et al (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644PubMedGoogle Scholar
  149. 149.
    Schuetz M, Berleth T, Mattsson J (2008) Multiple MONOPTEROS-dependent pathways are involved in leaf initiation. Plant Physiol 148:870–880PubMedGoogle Scholar
  150. 150.
    Sessions A, Yanofsky MF, Weigel D (2000) Cell–cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289:779–782PubMedGoogle Scholar
  151. 151.
    Shani E, Yanai O, Ori N (2006) The role of hormones in shoot apical meristem function. Curr Opin Plant Biol 9:484–489PubMedGoogle Scholar
  152. 152.
    Sijacic P, Liu Z (2010) Novel insights from live-imaging in shoot meristem development. J Integr Plant Biol 52:393–399PubMedGoogle Scholar
  153. 153.
    Silverstone AL, Tseng TS, Swain SM, Dill A, Jeong SY et al (2007) Functional analysis of SPINDLY in gibberellin signaling in Arabidopsis. Plant Physiol 143:987–1000PubMedGoogle Scholar
  154. 154.
    Smith RS (2008) The role of auxin transport in plant patterning mechanisms. PLoS Biol 6:e323PubMedGoogle Scholar
  155. 155.
    Smith RS, Guyomarc’h S, Mandel T, Reinhardt D, Kuhlemeier C et al (2006) A plausible model of phyllotaxis. Proc Natl Acad Sci USA 103:1301–1306PubMedGoogle Scholar
  156. 156.
    Snow M, Snow R (1931) Experiments on Phyllotaxis. I. The effect of isolating a primordium. Phil Trans 221:1–40Google Scholar
  157. 157.
    Snow M, Snow R (1933) Experiments on Phyllotaxis. II. The effect of displacing a primordium. Phil Trans 1933:545–566Google Scholar
  158. 158.
    Stadler R, Lauterbach C, Sauer N (2005) Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol 139:701–712PubMedGoogle Scholar
  159. 159.
    Stahl Y, Simon R (2010) Plant primary meristems: shared functions and regulatory mechanisms. Curr Opin Plant Biol 13:53–58PubMedGoogle Scholar
  160. 160.
    Steeves TA, Sussex IA (1989) Patterns in plant development, 2nd edn. Cambridge, UKGoogle Scholar
  161. 161.
    Steffens B, Feckler C, Palme K, Christian M, Bottger M et al (2001) The auxin signal for protoplast swelling is perceived by extracellular ABP1. Plant J 27:591–599PubMedGoogle Scholar
  162. 162.
    Stoma S, Lucas M, Chopard J, Schaedel M, Traas J et al (2008) Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development. PLoS Comput Biol 4:e1000207PubMedGoogle Scholar
  163. 163.
    Stuurman J, Jaggi F, Kuhlemeier C (2002) Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes Dev 16:2213–2218PubMedGoogle Scholar
  164. 164.
    Sussex IM (1951) Experiments on the cause of dorsiventrality in leaves. 167: 651–652Google Scholar
  165. 165.
    Sussex IM (1964) The permanence of meristems: developmental organizers or reactors to exogenous stimuli? Brookhaven Symp Biol 16:1–12Google Scholar
  166. 166.
    Szymkowiak EJ, Sussex IM (1996) What chimeras can tell us about plant development. Annu Rev Plant Physiol Plant Mol Biol 47:351–376PubMedGoogle Scholar
  167. 167.
    Terasaka K, Blakeslee JJ, Titapiwatanakun B, Peer WA, Bandyopadhyay A et al (2005) PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell 17:2922–2939PubMedGoogle Scholar
  168. 168.
    Traas J, Doonan JH (2001) Cellular basis of shoot apical meristem development. Int Rev Cytol 208:161–206PubMedGoogle Scholar
  169. 169.
    Traas J, Hamant O (2009) From genes to shape: understanding the control of morphogenesis at the shoot meristem in higher plants using systems biology. C R Biol 332:974–985PubMedGoogle Scholar
  170. 170.
    Tromas A, Braun N, Muller P, Khodus T, Paponov IA et al (2009) The AUXIN BINDING PROTEIN 1 is required for differential auxin responses mediating root growth. PLoS One 4:e6648PubMedGoogle Scholar
  171. 171.
    Tucker MR, Hinze A, Tucker EJ, Takada S, Jurgens G et al (2008) Vascular signalling mediated by ZWILLE potentiates WUSCHEL function during shoot meristem stem cell development in the Arabidopsis embryo. Development 135:2839–2843PubMedGoogle Scholar
  172. 172.
    Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868PubMedGoogle Scholar
  173. 173.
    Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200PubMedGoogle Scholar
  174. 174.
    Veit B (2009) Hormone-mediated regulation of the shoot apical meristem. Plant Mol Biol 69:397–408PubMedGoogle Scholar
  175. 175.
    Vidal M (2009) A unifying view of 21st century systems biology. FEBS Lett 583:3891–3894PubMedGoogle Scholar
  176. 176.
    Vidaurre DP, Ploense S, Krogan NT, Berleth T (2007) AMP1 and MP antagonistically regulate embryo and meristem development in Arabidopsis. Development 134:2561–2567PubMedGoogle Scholar
  177. 177.
    Wabnik K, Kleine-Vehn J, Balla J, Sauer M, Naramoto S et al (2010) Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Mol Syst Biol 6:447PubMedGoogle Scholar
  178. 178.
    Wardlaw CW (1949) Experiments on organogenesis in ferns. Growth 13(Suppl.):93–131Google Scholar
  179. 179.
    Wardlaw CW (1950) Experimental and analytical studies of pteridophytes. XVI. The induction of leaves and buds in Dryopteris artistata Druce. Ann Bot 14:435–455Google Scholar
  180. 180.
    Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859PubMedGoogle Scholar
  181. 181.
    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 132:3657–3668PubMedGoogle Scholar
  182. 182.
    Williams MH, Green PB (1988) Sequential scanning electron-microscopy of a growing-plant meristem. Protoplasma 147:77–79Google Scholar
  183. 183.
    Wisniewska J, Xu J, Seifertova D, Brewer PB, Ruzicka K et al (2006) Polar PIN localization directs auxin flow in plants. Science 312:883PubMedGoogle Scholar
  184. 184.
    Wu X, Dinneny JR, Crawford KM, Rhee Y, Citovsky V et al (2003) Modes of intercellular transcription factor movement in the Arabidopsis apex. Development 130:3735–3745PubMedGoogle Scholar
  185. 185.
    Wyrzykowska J, Pien S, Shen WH, Fleming AJ (2002) Manipulation of leaf shape by modulation of cell division. Development 129:957–964PubMedGoogle Scholar
  186. 186.
    Xu T, Wen M, Nagawa S, Fu Y, Chen JG et al (2010) Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143:99–110PubMedGoogle Scholar
  187. 187.
    Yadav RK, Girke T, Pasala S, Xie M, Reddy GV (2009) Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc Natl Acad Sci USA 106:4941–4946PubMedGoogle Scholar
  188. 188.
    Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R et al (2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol 15:1566–1571PubMedGoogle Scholar
  189. 189.
    Zhao Y (2008) The role of local biosynthesis of auxin and cytokinin in plant development. Curr Opin Plant Biol 11:16–22PubMedGoogle Scholar
  190. 190.
    Zhao Y, Medrano L, Ohashi K, Fletcher JC, Yu H et al (2004) HANABA TARANU is a GATA transcription factor that regulates shoot apical meristem and flower development in Arabidopsis. Plant Cell 16:2586–2600PubMedGoogle Scholar
  191. 191.
    Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A et al (2010) Hormonal control of the shoot stem-cell niche. Nature 465:1089–1092PubMedGoogle Scholar

Copyright information

© Springer Basel AG 2011

Authors and Affiliations

  • Fabrice Besnard
    • 1
  • Teva Vernoux
    • 1
  • Olivier Hamant
    • 1
    • 2
    Email author
  1. 1.Laboratoire de Reproduction et Développement des Plantes, INRA, CNRS, ENSUniversité de LyonLyon Cedex 07France
  2. 2.Laboratoire Joliot Curie, Laboratoire de Physique, CNRS, ENS Lyon, UCB Lyon 1Université de LyonLyon Cedex 07France

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