Plant Molecular Biology

, Volume 60, Issue 6, pp 915–928 | Cite as

Morphogenesis and Patterning at the Organ Boundaries in the Higher Plant Shoot Apex

  • Mitsuhiro Aida
  • Masao Tasaka


Formation of lateral organ primordia from the shoot apical meristem creates boundaries that separate the primordium from surrounding tissue. Morphological and gene expression studies indicate the presence of a distinct set of cells that define the boundaries in the plant shoot apex. Cells at the boundary usually display reduced growth activity that results in separation of adjacent organs or tissues and this morphological boundary coincides with the border of different cell identities. Such morphogenetic and patterning events and their spatial coordination are controlled by a number of boundary-specific regulatory genes. The boundary may also act as a reference point for the generation of new meristems such as axillary meristems. Many of the genes involved in meristem initiation are expressed in the boundary. This review summarizes the cellular characters of the shoot organ boundary and the roles of regulatory genes that control different aspects of this unique region in plant development.


boundary morphogenesis organ growth patterning shoot apical meristem 


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  1. Aida, M., Ishida, T., Fukaki, H., Fujisawa, H., Tasaka, M. 1997Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutantPlant Cell9841857PubMedCrossRefGoogle Scholar
  2. Aida, M., Ishida, T., Tasaka, M. 1999Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genesDevelopment12615631570PubMedGoogle Scholar
  3. Aida, M., Vernoux, T., Furutani, M., Traas, J., Tasaka, M. 2002Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryoDevelopment12939653974PubMedGoogle Scholar
  4. Benjamins, R., Quint, A., Weijers, D., Hooykaas, P., Offringa, R. 2001The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transportDevelopment12840574067PubMedGoogle Scholar
  5. Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jürgens, G., Friml, J. 2003Local, efflux-dependent auxin gradients as a common module for plant organ formationCell115591602PubMedCrossRefGoogle Scholar
  6. Bowman, J.L., Sakai, H., Jack, T., Weigel, D., Mayer, U., Meyerowitz, E.M. 1992SUPERMAN, a regulator of floral homeotic genes in ArabidopsisDevelopment114599615PubMedGoogle Scholar
  7. Breuil-Broyer, S., Morel, P., Almeida-Engler, J., Coustham, V., Negrutiu, I., Trehin, C. 2004High-resolution boundary analysis during Arabidopsis thaliana flower developmentPlant J.38182192PubMedCrossRefGoogle Scholar
  8. Brewer, P.B., Howles, P.A., Dorian, K., Griffith, M.E., Ishida, T., Kaplan-Levy, R.N., Kilinc, A., Smyth, D.R. 2004PETAL LOSS, a trihelix transcription factor gene, regulates perianth architecture in the Arabidopsis flowerDevelopment13140354045PubMedCrossRefGoogle Scholar
  9. Byrne, M.E., Barley, R., Curtis, M., Arroyo, J.M., Dunham, M., Hudson, A., Martienssen, R.A. 2000Asymmetric leaves1 mediates leaf patterning and stem cell function in ArabidopsisNature408967971PubMedCrossRefGoogle Scholar
  10. Byrne, M.E., Simorowski, J., Martienssen, R.A. 2002ASYMMETRIC LEAVES1 reveals knox gene redundancy in ArabidopsisDevelopment12919571965PubMedGoogle Scholar
  11. Christensen, S.K., Dagenais, N., Chory, J., Weigel, D. 2000Regulation of auxin response by the protein kinase PINOIDCell100469478PubMedCrossRefGoogle Scholar
  12. Chuck, G., Muszynski, M., Kellogg, E., Hake, S., Schmidt, R.J. 2002The control of spikelet meristem identity by the branched silkless1 gene in maizeScience29812381241PubMedCrossRefGoogle Scholar
  13. Dahmann, C., Basler, K. 1999Compartment boundaries: at the edge of developmentTrends Genet.15320326PubMedCrossRefGoogle Scholar
  14. Dumais, J., Kwiatkowska, D. 2002Analysis of surface growth in shoot apicesPlant J.31229241PubMedCrossRefGoogle Scholar
  15. Durfee, T., Roe, J.L., Sessions, R.A., Inouye, C., Serikawa, K., Feldmann, K.A., Weigel, D., Zambryski, P.C. 2003The F-box-containing protein UFO and AGAMOUS participate in antagonistic pathways governing early petal development in ArabidopsisProc. Natl. Acad. Sci. USA10085718576PubMedCrossRefGoogle Scholar
  16. Deveaux, Y., Peaucelle, A., Roberts, G.R., Coen, E., Simon, R., Mizukami, Y., Traas, J., Murray, J.A.H., Doonan, J.H., Laufs, P. 2003The ethanol switch: a tool for tissue-specific gene induction during plant developmentPlant J.36918930PubMedCrossRefGoogle Scholar
  17. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R., Jürgens, G. 2003Efflux-dependent auxin gradients establish the apical-basal axis of ArabidopsisNature426147153PubMedCrossRefGoogle Scholar
  18. Friml, J., Yang, X., Michniewicz, M., Weijers, D., Quint, A., Tietz, O., Benjamins, R., Ouwerkerk, P.B., Ljung, K., Sandberg, G., Hooykaas, P.J., Palme, K., Offringa, R. 2004A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin effluxScience306862865PubMedCrossRefGoogle Scholar
  19. Furutani, M., Vernoux, T., Traas, J., Kato, T., Tasaka, M., Aida, M. 2004PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesisDevelopment13150215030PubMedCrossRefGoogle Scholar
  20. Gaudin, V., Lunness, P.A., Fobert, P.R., Towers, M., Riou-Khamlichi, C., Murray, J.A., Coen, E., Doonan, J.H. 2000The expression of D-cyclin genes defines distinct developmental zones in snapdragon apical meristems and is locally regulated by the Cycloidea genePlant Physiol.12211371148PubMedCrossRefGoogle Scholar
  21. Gisel, A., Barella, S., Hempel, F.D., Zambryski, P.C. 1999Temporal and spatial regulation of symplastic trafficking during development in Arabidopsis thaliana apicesDevelopment12618791889PubMedGoogle Scholar
  22. Goto, K., Meyerowitz, E.M. 1994Function and regulation of the Arabidopsis floral homeotic gene PISTILLATAGenes Dev.815481560PubMedGoogle Scholar
  23. Grandjean, O., Vernoux, T., Laufs, P., Belcram, K., Mizukami, Y., Traas, J. 2004In vivo analysis of cell division, cell growth, and differentiation at the shoot apical meristem in ArabidopsisPlant Cell167487PubMedCrossRefGoogle Scholar
  24. Greb, T., Clarenz, O., Schäfer, E., Müller, D., Herrero, R., Schmitz, G., Theres, K. 2003Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formationGenes Dev.1711751187PubMedCrossRefGoogle Scholar
  25. Green, P.B., Lang, J.M. 1981Toward a biophysical theory of organogenesis: birefringence observations on regenerating leaves in the succulent, Graptopetalum paraguayense EWalther. Planta151413426CrossRefGoogle Scholar
  26. Gälweiler, L., Guan, C., Müller, A., Wisman, E., Mendgen, K., Yephremov, A., Palme, K. 1998Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissueScience28222262230PubMedCrossRefGoogle Scholar
  27. Hibara, K., Takada, S., Tasaka, M. 2003CUC1 gene activates the expression of SAM-related genes to induce adventitious shoot formationPlant J.36687696PubMedCrossRefGoogle Scholar
  28. Hiratsu, K., Ohta, M., Matsui, K., Ohme-Takagi, M. 2002The SUPERMAN protein is an active repressor whose carboxy-terminal repression domain is required for the development of normal flowersFEBS Lett.514351354PubMedCrossRefGoogle Scholar
  29. Hussey, G. 1971Cell division and expansion and resultant tissue tensions in the shoot apex during the formation of a leaf primordium in the tomatoJ. Exp. Bot.22702714Google Scholar
  30. Ingram, G.C., Doyle, S., Carpenter, R., Schultz, E.A., Simon, R., Coen, E.S. 1997Dual role for fimbriata in regulating floral homeotic genes and cell division in AntirrhinumEMBO J.1665216534PubMedCrossRefGoogle Scholar
  31. Ishida, T., Aida, M., Takada, S., Tasaka, M. 2000Involvement of CUP-SHAPED COTYLEDON genes in gynoecium and ovule development in Arabidopsis thalianaPlant Cell Physiol.416067PubMedGoogle Scholar
  32. Ito, T., Sakai, H., Meyerowitz, E.M. 2003Whorl-specific expression of the SUPERMAN gene of Arabidopsis is mediated by cis elements in the transcribed regionCurr. Biol.1315241530PubMedCrossRefGoogle Scholar
  33. Iwakawa, H., Ueno, Y., Semiarti, E., Onouchi, H., Kojima, S., Tsukaya, H., Hasebe, M., Soma, T., Ikezaki, M., Machida, C., Machida, Y. 2002The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipperPlant Cell Physiol.43467478PubMedCrossRefGoogle Scholar
  34. Jackson, D. 2002Double labeling of KNOTTED1 mRNA and protein reveals multiple potential sites of protein trafficking in the shoot apexPlant Physiol.12914231429PubMedCrossRefGoogle Scholar
  35. Jesuthasan, S., Green, P.B. 1989On the mechanism of decussate phyllotaxis: biophysical studies on the tunica layer of Vinca majorAm. J. Bot.7611521166CrossRefGoogle Scholar
  36. Kim, J.Y., Yuan, Z., Jackson, D. 2003Developmental regulation and significance of KNOX protein trafficking in ArabidopsisDevelopment13043514362PubMedCrossRefGoogle Scholar
  37. Komatsu, K., Maekawa, M., Ujiie, S., Satake, Y., Furutani, I., Okamoto, H., Shimamoto, K., Kyozuka, J. 2003aLAX and SPA: major regulators of shoot branching in riceProc. Natl. Acad. Sci. USA1001176511770CrossRefGoogle Scholar
  38. Komatsu, M., Chujo, A., Nagato, Y., Shimamoto, K., Kyozuka, J. 2003bFRIZZY PANICLE is required to prevent the formation of axillary meristems and to establish floral meristem identity in rice spikeletsDevelopment13038413850CrossRefGoogle Scholar
  39. Kwiatkowska, D. 2004aStructural integration at the shoot apical meristem: models, measurements, and experimentsAm. J. Bot.9112771293Google Scholar
  40. Kwiatkowska, D. 2004bSurface growth at the reproductive shoot apex of Arabidopsis thaliana pin-formed 1 and wild-typeJ. Exp. Bot.5510211032CrossRefGoogle Scholar
  41. Kwiatkowska, D., Dumais, J. 2003Growth and morphogenesis at the vegetative shoot apex of Anagallis arvensis LJ.␣Exp. Bot.5415851595PubMedCrossRefGoogle Scholar
  42. Laufs, P., Coen, E., Kronenberger, J., Traas, J., Doonan, J. 2003Separable roles of UFO during floral development revealed by conditional restoration of gene functionDevelopment130785796PubMedCrossRefGoogle Scholar
  43. Laufs, P., Peaucelle, A., Morin, H., Traas, J. 2004MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristemsDevelopment13143114322PubMedCrossRefGoogle Scholar
  44. Lee, I., Wolfe, D.S., Nilsson, O., Weigel, D. 1997A LEAFY co-regulator encoded by UNUSUAL FLORAL ORGANSCurr. Biol.795104PubMedCrossRefGoogle Scholar
  45. Lenhard, M., Laux, T. 2003Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1Development13031633173PubMedCrossRefGoogle Scholar
  46. Levin, J.Z., Fletcher, J.C., Chen, X., Meyerowitz, E.M. 1998A genetic screen for modifiers of UFO meristem activity identifies three novel FUSED FLORAL ORGANS genes required for early flower development in ArabidopsisGenetics149579595PubMedGoogle Scholar
  47. Levin, J.Z., Meyerowitz, E.M. 1995UFO: an Arabidopsis gene involved in both floral meristem and floral organ developmentPlant Cell7529548PubMedCrossRefGoogle Scholar
  48. Li, X., Qian, Q., Fu, Z., Wang, Y., Xiong, G., Zeng, D., Wang, X., Liu, X., Teng, S., Hiroshi, F., Yuan, M., Luo, D., Han, B., Li, J. 2003Control of tillering in riceNature422618621PubMedCrossRefGoogle Scholar
  49. Lincoln, C., Long, J., Yamaguchi, J., Serikawa, K., Hake, S. 1994A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plantsPlant Cell618591876PubMedCrossRefGoogle Scholar
  50. Lloyd, C., Chan, J. 2004Microtubules and the shape of plants to comeNat. Rev. Mol. Cell. Biol.51322PubMedCrossRefGoogle Scholar
  51. Long, J.A., Barton, M.K. 1998The development of apical embryonic pattern in ArabidopsisDevelopment12530273035PubMedGoogle Scholar
  52. Long, J.A., Moan, E.I., Medford, J.I., Barton, M.K. 1996A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of ArabidopsisNature3796669PubMedCrossRefGoogle Scholar
  53. Lucas, W.J., Bouché-Pillon, S., Jackson, D.P., Nguyen, L., Baker, L., Ding, B., Hake, S. 1995Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmataScience27019801983PubMedGoogle Scholar
  54. Lyndon, R.F. 1998The Shoot Apical MeristemCambridge University PressCambridgeGoogle Scholar
  55. Mallory, A.C., Dugas, D.V., Bartel, D.P., Bartel, B. 2004MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organsCurr. Biol.1410351046PubMedCrossRefGoogle Scholar
  56. Nakajima, K., Sena, G., Nawy, T., Benfey, P.N. 2001Intercellular movement of the putative transcription factor SHR in root patterningNature413307311PubMedCrossRefGoogle Scholar
  57. Perbal, M.C., Haughn, G., Saedler, H., Schwarz-Sommer, Z. 1996Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell traffickingDevelopment12234333441PubMedGoogle Scholar
  58. Reddy, G.V., Heisler, M.G., Ehrhardt, D.W., Meyerowitz, E.M. 2004Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thalianaDevelopment13142254237PubMedCrossRefGoogle Scholar
  59. Reinhardt, D., Pesce, E.R., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J., Kuhlemeier, C. 2003Regulation of phyllotaxis by polar auxin transportNature42625560PubMedCrossRefGoogle Scholar
  60. Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B., Bartel, D.P. 2002Prediction of plant microRNA targetsCell110513520PubMedCrossRefGoogle Scholar
  61. Rinne, P.L.H., Schoot, C. 1998Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic eventsDevelopment12514771485PubMedGoogle Scholar
  62. Rojo, E., Sharma, V.K., Kovaleva, V., Raikhel, N.V., Fletcher, J.C. 2002CLV3 is localized to the extracellular space, where iIt activates the Arabidopsis CLAVATA stem cell signaling pathwayPlant Cell14969977PubMedCrossRefGoogle Scholar
  63. Sakai, H., Krizek, B.A., Jacobsen, S.E., Meyerowitz, E.M. 2000Regulation of SUP expression identifies multiple regulators involved in Arabidopsis floral meristem developmentPlant Cell1216071618PubMedCrossRefGoogle Scholar
  64. Sakai, H., Medrano, L.J., Meyerowitz, E.M. 1995Role of SUPERMAN in maintaining Arabidopsis floral whorl boundariesNature378199203PubMedCrossRefGoogle Scholar
  65. Samach, A., Klenz, J.E., Kohalmi, S.E., Risseeuw, E., Haughn, G.W., Crosby, W.L. 1999The UNUSUAL FLORAL ORGANS gene of Arabidopsis thaliana is an F-box protein required for normal patterning and growth in the floral meristemPlant J.20433445PubMedCrossRefGoogle Scholar
  66. Schultz, E., Carpenter, R., Doyle, S., Coen, E. 2001The gene fimbriata interacts non-cell autonomously with floral regulatory genesPlant J.25499507PubMedCrossRefGoogle Scholar
  67. Sessions, A., Yanofsky, M.F., Weigel, D. 2000Cell–cell signaling and movement by the floral transcription factors LEAFY and APETALA1Science289779782PubMedCrossRefGoogle Scholar
  68. Shuai, B., Reynaga-Peña, C.G., Springer, P.S. 2002The LATERAL ORGAN BOUNDARIES gene defines a novel, plant-specific gene familyPlant Physiol129747761PubMedCrossRefGoogle Scholar
  69. Simon, R., Carpenter, R., Doyle, S., Coen, E. 1994Fimbriata controls flower development by mediating between meristem and organ identity genesCell7899107PubMedCrossRefGoogle Scholar
  70. Souer, E., Houwelingen, A., Bliek, M., Kloos, D., Mol, J., Koes, R. 1998Co-suppression of nam and homologous genes leads to a reduction in axillary meristem formation and increased leaf and stem size in petunia: a possible role for NAC domain genes in plant developmentFlowering Newslett.263646Google Scholar
  71. Souer, E., Houwelingen, A., Kloos, D., Mol, J., Koes, R. 1996The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundariesCell85159170PubMedCrossRefGoogle Scholar
  72. Takada, S., Hibara, K., Ishida, T., Tasaka, M. 2001The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formationDevelopment12811271135PubMedGoogle Scholar
  73. Taoka, K., Yanagimoto, Y., Daimon, Y., Hibara, K., Aida, M., Tasaka, M. 2004The NAC domain mediates functional specificity of CUP-SHAPED COTYLEDON proteinsPlant J40462473PubMedCrossRefGoogle Scholar
  74. Vernoux, T., Kronenberger, J., Grandjean, O., Laufs, P., Traas, J. 2000PIN-FORMED1 regulates cell fate at the periphery of the shoot apical meristemDevelopment12751575165PubMedGoogle Scholar
  75. Vincent, C.A., Carpenter, R., Coen, E.S. 1995Cell lineage patterns and homeotic gene activity during Antirrhinum flower developmentCurr. Biol.514491458PubMedCrossRefGoogle Scholar
  76. Vroemen, C.W., Mordhorst, A.P., Albrecht, C., Kwaaitaal, M.A., Vries, S.C. 2003The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in ArabidopsisPlant Cell1515631577PubMedCrossRefGoogle Scholar
  77. Wada, T., Kurata, T., Tominaga, R., Koshino-Kimura, Y., Tachibana, T., Goto, K., Marks, M.D., Shimura, Y., Okada, K. 2002Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiationDevelopment12954095419PubMedCrossRefGoogle Scholar
  78. Wang, X., Feng, S., Nakayama, N., Crosby, W.L., Irish, V., Deng, X.W., Wei, N. 2003The COP9 signalosome interacts with SCFUFO and participates in Arabidopsis flower developmentPlant Cell1510711082PubMedCrossRefGoogle Scholar
  79. Weigel, D., Meyerowitz, E.M. 1994The ABCs of floral homeotic genesCell78203209PubMedCrossRefGoogle Scholar
  80. Weir, I., Lu, J., Cook, H., Causier, B., Schwarz-Sommer, Z., Davies, B. 2004CUPULIFORMIS establishes lateral organ boundaries in AntirrhinumDevelopment131915922PubMedCrossRefGoogle Scholar
  81. Wilkinson, M., Andrade Silva, E., Zachgo, S., Saedler, H., Schwarz-Sommer, Z. 2000CHORIPETALA and DESPENTEADO: general regulators during plant development and potential floral targets of FIMBRIATA-mediated degradationDevelopment12737253734PubMedGoogle Scholar
  82. Wilkinson, M., Haughn, G. 1995UNUSUAL FLORAL ORGANS controls meristem identity and organ primordia fate in ArabidopsisPlant Cell714851499PubMedCrossRefGoogle Scholar
  83. Wu, X., Dinneny, J.R., Crawford, K.M., Rhee, Y., Citovsky, V., Zambryski, P.C., Weigel, D. 2003Modes of intercellular transcription factor movement in the Arabidopsis apexDevelopment13037353745PubMedCrossRefGoogle Scholar
  84. Zambryski, P. 2004Cell-to-cell transport of proteins and fluorescent tracers via plasmodesmata during plant developmentJ. Cell Biol.164165168PubMedCrossRefGoogle Scholar
  85. Zhao, D., Yu, Q., Chen, M., Ma, H. 2001The ASK1 gene regulates B function gene expression in cooperation with UFO and LEAFY in ArabidopsisDevelopment12827352746PubMedGoogle Scholar
  86. Zhao, Y., Medrano, L., Ohashi, K., Fletcher, J.C., Yu, H., Sakai, H., Meyerowitz, E.M. 2004HANABA TARANU is a GATA transcription factor that regulates shoot apical meristem and flower development in ArabidopsisPlant Cell1625862600PubMedCrossRefGoogle Scholar
  87. Zondlo, S.C., Irish, V.F. 1999CYP78A5 encodes a cytochrome P450 that marks the shoot apical meristem boundary in ArabidopsisPlant J.19259268PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  1. 1.Graduate School of Biological SciencesNara Institute of Science and TechnologyNaraJapan

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