The regular arrangement of leaves around a plant's stem, called phyllotaxis, has for centuries attracted the attention of philosophers, mathematicians and natural scientists; however, to date, studies of phyllotaxis have been largely theoretical. Leaves and flowers are formed from the shoot apical meristem, triggered by the plant hormone auxin. Auxin is transported through plant tissues by specific cellular influx and efflux carrier proteins. Here we show that proteins involved in auxin transport regulate phyllotaxis. Our data indicate that auxin is transported upwards into the meristem through the epidermis and the outermost meristem cell layer. Existing leaf primordia act as sinks, redistributing auxin and creating its heterogeneous distribution in the meristem. Auxin accumulation occurs only at certain minimal distances from existing primordia, defining the position of future primordia. This model for phyllotaxis accounts for its reiterative nature, as well as its regularity and stability.
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Steeves, T. A. & Sussex, I. M. Patterns in Plant Development (Cambridge Univ. Press, Cambridge, UK, 1989)
Reinhardt, D. & Kuhlemeier, C. in Meristematic Tissues in Plant Growth and Development (eds McManus, M. T. & Veit, B. E.) 172–212 (Sheffield Academic, Sheffield, 2002)
Mitchison, G. J. Phyllotaxis and the Fibonacci series. Science 196, 270–275 (1977)
Jean, R. V. Phyllotaxis: A Systematic Study in Plant Morphogenesis (Cambridge Univ. Press, Cambridge, UK, 1994)
Snow, M. & Snow, R. A theory of regulation of phyllotaxis based on Lupinus albus. Phil. Trans. R. Soc. Lond. Ser. B 244, 483–513 (1962)
Green, P. B. Expression of form and pattern in plants - A role for biophysical fields. Semin. Cell Dev. Biol. 7, 903–911 (1996)
Schoute, J. C. Beiträge zur Blattstellungslehre. Récueil des Travaux Botaniques Néerlandais 10, 153–325 (1913)
Meinhardt, H. in Positional Controls in Plant Development (eds Barlow, P. W. & Carr, D. J.) 1–32 (Cambridge University Press, Cambridge, UK, 1984)
Liu, C.-M., Xu, Z.-H. & Chua, N.-H. Auxin polar transport is essential for the establishment of bilateral symmetry during early plant embryogenesis. Plant Cell 5, 621–630 (1993)
Hadfi, K., Speth, V. & Neuhaus, G. Auxin-induced developmental patterns in Brassica juncea embryos. Development 125, 879–887 (1998)
Hardtke, C. S. & Berleth, T. The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17, 1405–1411 (1998)
Aida, M., Vernoux, T., Furutani, M., Traas, J. & Tasaka, M. Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development 129, 3965–3974 (2002)
Jürgens, G. Apical-basal pattern formation in Arabidopsis embryogenesis. EMBO J. 20, 3609–3616 (2001)
Sabatini, S. et al. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463–472 (1999)
Friml, J. et al. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108, 661–673 (2002)
Mattsson, J., Ckurshumova, W. & Berleth, T. Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol. 131, 1327–1339 (2003)
Reinhardt, D., Mandel, T. & Kuhlemeier, C. Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12, 507–518 (2000)
Kuhlemeier, C. & Reinhardt, D. Auxin and phyllotaxis. Trends Plant Sci. 6, 187–189 (2001)
Lomax, T. L., Muday, G. K. & Rubery, P. H. in Plant Hormones: Physiology, Biochemistry and Molecular Biology (ed. Davies, P. J.) 509–530 (Kluwer Academic, Dordrecht, 1995)
Friml, J. & Palme, K. Polar auxin transport—old questions and new concepts? Plant Mol. Biol. 49, 273–284 (2002)
Friml, J., Wísniewska, J., Benková, E., Mendgen, K. & Palme, K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806–809 (2002)
Bennett, M. J. et al. Arabidopsis AUX1 gene: A permease-like regulator of root gravitropism. Science 273, 948–950 (1996)
Gälweiler, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230 (1998)
Steinmann, T. et al. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286, 316–318 (1999)
Sachs, T. The control of patterned differentiation of vascular tissues. Adv. Bot. Res. 9, 151–262 (1981)
Weigel, D., Alvarez, J., Smyth, D. R., Yanofsky, M. F. & Meyerowitz, E. M. LEAFY controls floral meristem identity in Arabidopsis. Cell 69, 843–859 (1992)
Okada, K., Ueda, J., Komaki, M. K., Bell, C. J. & Shimura, Y. Requirement of the auxin polar transport-system in early stages of Arabidopsis floral bud formation. Plant Cell 3, 677–684 (1991)
Bennett, S. R. M., Alvarez, J., Bossinger, G. & Smyth, D. R. Morphogenesis in pinoid mutants of Arabidopsis thaliana. Plant J. 8, 505–520 (1995)
Przemeck, G. K. H., Mattsson, J., Hardtke, C. S., Sung, Z. R. & Berleth, T. Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta 200, 229–237 (1996)
Christensen, S. K., Dagenais, N., Chory, J. & Weigel, D. Regulation of auxin response by the protein kinase PINOID. Cell 100, 469–478 (2000)
Benjamins, R., Quint, A., Weijers, D., Hooykaas, P. & Offringa, R. The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128, 4057–4067 (2001)
Vernoux, T., Kronenberger, J., Grandjean, O., Laufs, P. & Traas, J. PIN-FORMED1 regulates cell fate at the periphery of the shoot apical meristem. Development 127, 5157–5165 (2000)
Delbarre, A., Muller, P., Imhoff, V. & Guern, J. Comparison of mechanisms controlling uptake and accumulation of 2,4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198, 532–541 (1996)
Stieger, P. A., Reinhardt, D. & Kuhlemeier, C. The auxin influx carrier is essential for correct leaf positioning. Plant J. 32, 509–517 (2002)
Parry, G. et al. Quick on the uptake: Characterization of a family of plant auxin influx carriers. J. Plant Growth Regul. 20, 217–225 (2001)
Swarup, R. et al. Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev. 15, 2648–2653 (2001)
Danbolt, N. C. Glutamate uptake. Prog. Neurobiol. 65, 1–105 (2001)
Geldner, N., Friml, J., Stierhof, Y. D., Jürgens, G. & Palme, K. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425–428 (2001)
Geldner, N. et al. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219–230 (2003)
Lynn, K. et al. The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126, 469–481 (1999)
Aida, M., Ishida, T., Fukaki, H., Fujisawa, H. & Tasaka, M. Genes involved in organ separation in Arabidopsis: An analysis of the cup-shaped cotyledon mutant. Plant Cell 9, 841–857 (1997)
Fleming, A. J., McQueen-Mason, S., Mandel, T. & Kuhlemeier, C. Induction of leaf primordia by the cell wall protein expansin. Science 276, 1415–1418 (1997)
Schwabe, W. W. in Positional Controls in Plant Development (eds Barlow, P. W. & Carr, D. J.) 403–440 (Cambridge Univ. Press, Cambridge, UK, 1984)
We thank J. Moore, J. Stuurman and S. Zeeman for critical reading of the manuscript, and T. Vernoux for generating pin1;pid double mutants and H. Morin for supporting experiments. This work was supported by grants from the Swiss National Science Foundation and from the European Union.
The authors declare that they have no competing financial interests.
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Reinhardt, D., Pesce, ER., Stieger, P. et al. Regulation of phyllotaxis by polar auxin transport. Nature 426, 255–260 (2003). https://doi.org/10.1038/nature02081
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