Regulation of phyllotaxis by polar auxin transport
Abstract
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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Auxin response maxima instruct the position of leaf primordia at the shoot apex and the pattern of leaflets during complex leaf development.
“Auxin response maxima instruct, for example, the position of leaf primordia at the shoot apex (Reinhardt et al., 2003;Bayer et al., 2009) and the pattern of leaflets during complex leaf development (Barkoulas et al., 2008;Koenig et al., 2009;Ben-Gera et al., 2012).”
From <i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems (2016) · cites this paper as Reinhardt et al., 2003
Cites
Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant.
Aida, M., Ishida, T., Fukaki, H., Fujisawa, H., & Tasaka, M. (1997) · The Plant Cell · doi:10.1105/tpc.9.6.841 · Cited by 1,486 · see citing works
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Leyser, O. (2018) · Plant Physiology · doi:10.1104/pp.17.00765 · Cited by 715 · see citing works
Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity
Sauer, M., Balla, J., Luschnig, C., Wiśniewska, J., Reinöhl, V., Friml, J., & Benková, E. (2006) · Genes & Development · doi:10.1101/gad.390806 · Cited by 453 · see citing works
Self-citationInteractions among PIN-FORMED and P-Glycoprotein Auxin Transporters in <i>Arabidopsis</i>
Blakeslee, J. J., Bandyopadhyay, A., Lee, O. R., Mravec, J., Titapiwatanakun, B., Sauer, M., Makam, S. N., Cheng, Y., Bouchard, R., Adamec, J., et al. (2007) · The Plant Cell · doi:10.1105/tpc.106.040782 · Cited by 434 · see citing works
Self-citationAuxin Transporters--Why So Many?
Zazimalova, E., Murphy, A. S., Yang, H., Hoyerova, K., & Hosek, P. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a001552 · Cited by 400 · see citing works
Hormonal control of shoot branching
Ongaro, V., & Leyser, O. (2007) · Journal of Experimental Botany · doi:10.1093/jxb/erm134 · Cited by 373 · see citing works
Reddy, G. V., Heisler, M. G., Ehrhardt, D. W., & Meyerowitz, E. M. (2004) · Development · doi:10.1242/dev.01261 · Cited by 339 · see citing works
Furutani, M., Vernoux, T., Traas, J., Kato, T., Tasaka, M., & Aida, M. (2004) · Development · doi:10.1242/dev.01388 · Cited by 271 · see citing works
Self-citationWenzel, C. L., Schuetz, M., Yu, Q., & Mattsson, J. (2007) · The Plant Journal · doi:10.1111/j.1365-313x.2006.02977.x · Cited by 267 · see citing works
Keller, T., Abbott, J., Moritz, T., & Doerner, P. (2006) · The Plant Cell · doi:10.1105/tpc.105.038588 · Cited by 245 · see citing works
The Relationship between Auxin Transport and Maize Branching
Gallavotti, A., Yang, Y., Schmidt, R. J., & Jackson, D. (2008) · Plant Physiology · doi:10.1104/pp.108.121541 · Cited by 227 · see citing works
The Stem Cell Niche in Leaf Axils Is Established by Auxin and Cytokinin in <i>Arabidopsis</i>
Wang, Y., Wang, J., Shi, B., Yu, T., Qi, J., Meyerowitz, E. M., & Jiao, Y. (2014) · The Plant Cell · doi:10.1105/tpc.114.123083 · Cited by 207 · see citing works
Robischon, M., Du, J., Miura, E., & Groover, A. (2011) · Plant Physiology · doi:10.1104/pp.110.167007 · Cited by 189 · see citing works
Tissue remodelling through branching morphogenesis
Affolter, M., Zeller, R., & Caussinus, E. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2797 · Cited by 185 · see citing works
Auxin Perception--Structural Insights
Calderon-Villalobos, L. I., Tan, X., Zheng, N., & Estelle, M. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005546 · Cited by 177 · see citing works
Wang, Q., Kohlen, W., Rossmann, S., Vernoux, T., & Theres, K. (2014) · The Plant Cell · doi:10.1105/tpc.114.123059 · Cited by 172 · see citing works
“PIN1 encodes a transmembrane protein (Gälweiler et al., 1998) that is highly expressed in the L1 layer of the SAM and in the vascular system (Reinhardt et al., 2003; Bayer et al., 2009).”
BackgroundInfluentialBorghi, L., Bureau, M., & Simon, R. (2007) · The Plant Cell · doi:10.1105/tpc.106.047159 · Cited by 161 · see citing works
<i>Divide et impera</i>: boundaries shape the plant body and initiate new meristems
Wang, Q., Hasson, A., Rossmann, S., & Theres, K. (2016) · New Phytologist · doi:10.1111/nph.13641 · Cited by 106 · see citing works
Rast, M. I., & Simon, R. (2012) · The Plant Cell · doi:10.1105/tpc.112.099978 · Cited by 89 · see citing works
Gene expression patterns in seed plant shoot meristems and leaves: homoplasy or homology?
Floyd, S. K., & Bowman, J. L. (2010) · Journal of Plant Research · doi:10.1007/s10265-009-0256-2 · Cited by 82 · see citing works
Adaptive evolution of the enigmatic Takakia now facing climate change in Tibet
Hu, R., Li, X., Hu, Y., Zhang, R., Lv, Q., Zhang, M., Sheng, X., Zhao, F., Chen, Z., Ding, Y., et al. (2023) · Cell · doi:10.1016/j.cell.2023.07.003 · Cited by 55 · see citing works
- Authors
- Reinhardt, D., Pesce, E.-R., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J., & Kuhlemeier, C.
- Affiliations
- University of Bern (CH)
- University of Nottingham (GB)
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
- Corresponding author
- Kuhlemeier, Cris
- Venue
- Nature
- Published
- 2003-11
- Volume
- 426
- Issue
- 6964
- Pages
- 255-260
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1975288257
- Cited by
- 1,523
- References
- 1
- Citations by year
- 2026: 41 · 2025: 44 · 2024: 51 · 2023: 45 · 2022: 54 · 2021: 71 · 2020: 48 · 2019: 60 · 2018: 64 · 2017: 82 · 2016: 62 · 2015: 69 · 2014: 80 · 2013: 76 · 2012: 83
- FWCI
- 70.05
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- BORIS (University Library Bern) (submittedVersion)
- Funders
- European Commission
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Parasitism and Resistance
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
- Keywords
- phyllotaxis, polar auxin transport, auxin, shoot apical meristem, leaf primordia, plant development
- MeSH terms
- Biological Transport, Indoleacetic Acids, Membrane Proteins, Mutation, RNA, Messenger, Arabidopsis, Gene Expression Regulation, Plant, Plant Leaves, Meristem, Body Patterning, Membrane Transport Proteins, Arabidopsis Proteins, Flowers, Organogenesis
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