Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis

Abstract

Axis formation occurs in plants, as in animals, during early embryogenesis. However, the underlying mechanism is not known. Here we show that the first manifestation of the apical–basal axis in plants, the asymmetric division of the zygote, produces a basal cell that transports and an apical cell that responds to the signalling molecule auxin. This apical–basal auxin activity gradient triggers the specification of apical embryo structures and is actively maintained by a novel component of auxin efflux, PIN7, which is located apically in the basal cell. Later, the developmentally regulated reversal of PIN7 and onset of PIN1 polar localization reorganize the auxin gradient for specification of the basal root pole. An analysis of pin quadruple mutants identifies PIN-dependent transport as an essential part of the mechanism for embryo axis formation. Our results indicate how the establishment of cell polarity, polar auxin efflux and local auxin response result in apical–basal axis formation of the embryo, and thus determine the axiality of the adult plant.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Auxin and auxin response in embryogenesis.
Figure 2: DR5 auxin response in in vitro cultured ovules and mutants.
Figure 3: PIN expression and protein localization in embryogenesis.
Figure 4: Abnormal embryogenesis in auxin transport and response mutants.
Figure 5: A model for a role of auxin in embryo patterning.

References

  1. 1

    St Johnston, D. & Nüsslein-Volhard, C. The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201–219 (1992)

    CAS  Article  Google Scholar 

  2. 2

    Lyczak, R., Gomes, J. & Bowerman, B. Heads or tails: cell polarity and axis formation in the early Caenorhabditis elegans embryo. Dev. Cell 3, 157–166 (2002)

    CAS  Article  Google Scholar 

  3. 3

    Jürgens, G. Apical–basal pattern formation in Arabidopsis embryogenesis. EMBO J. 20, 3609–3616 (2001)

    Article  Google Scholar 

  4. 4

    Mayer, U., Torres Ruiz, R. A., Berleth, T., Miséra, S. & Jürgens, G. Mutations affecting body organization in the Arabidopsis embryo. Nature 353, 402–407 (1991)

    ADS  Article  Google Scholar 

  5. 5

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

    CAS  PubMed  Google Scholar 

  6. 6

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

    CAS  Article  Google Scholar 

  7. 7

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

    CAS  Article  Google Scholar 

  8. 8

    Steinmann, T. et al. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF-GEF. Science 286, 316–318 (1999)

    CAS  Article  Google Scholar 

  9. 9

    Geldner, N. et al. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219–230 (2003)

    CAS  Article  Google Scholar 

  10. 10

    Liu, C., Xu, Z. & Chua, N. Auxin polar transport is essential for the establishment of bilateral symmetry during early plant embryogenesis. Plant Cell 5, 621–630 (1993)

    CAS  Article  Google Scholar 

  11. 11

    Hadfi, K., Speth, V. & Neuhaus, G. Auxin-induced developmental patterns in Brassica juncea embryos. Development 125, 879–887 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 12

    Sabatini, S. et al. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463–472 (1999)

    CAS  Article  Google Scholar 

  13. 13

    Friml, J. et al. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108, 661–673 (2000)

    Article  Google Scholar 

  14. 14

    Fischer-Iglesias, C., Sundberg, B., Neuhaus, G. & Jones, A. Auxin distribution and transport during embryonic pattern formation in wheat. Plant J. 26, 115–129 (2001)

    CAS  Article  Google Scholar 

  15. 15

    Ribnicky, D., Cohen, J., Hu, W. & Cooke, T. An auxin surge following fertilization in carrots: a mechanism for regulating plant totipotency. Planta 214, 505–509 (2002)

    CAS  Article  Google Scholar 

  16. 16

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

    CAS  Article  Google Scholar 

  17. 17

    Rubery, P. & Sheldrake, A. Carrier-mediated auxin transport. Planta 118, 101–121 (1974)

    CAS  Article  Google Scholar 

  18. 18

    Raven, J. Transport of indolacetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytol. 74, 163–172 (1975)

    CAS  Article  Google Scholar 

  19. 19

    Friml, J. & Palme, K. Polar auxin transport—old questions and new concepts? Plant Mol. Biol. 49, 273–284 (2002)

    CAS  Article  Google Scholar 

  20. 20

    Okada, K., Ueda, J., Komaki, M., Bell, C. & Shimura, Y. Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3, 677–684 (1991)

    CAS  Article  Google Scholar 

  21. 21

    Rashotte, A., Brady, S., Reed, R., Ante, S. & Muday, G. Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiol. 122, 481–490 (2000)

    CAS  Article  Google Scholar 

  22. 22

    Friml, J., Wisniewska, J., Benková, E., Mendgen, K. & Palme, K. Lateral relocation of auxin efflux regulator AtPIN3 mediates tropism in Arabidopsis. Nature 415, 806–809 (2002)

    ADS  Article  Google Scholar 

  23. 23

    Ottenschläger, I. et al. Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc. Natl Acad. Sci. USA 100, 2987–2991 (2003)

    ADS  Article  Google Scholar 

  24. 24

    Yamaizumi, M., Mekada, E., Uchida, T. & Okada, Y. One molecule of Diphteria Toxin fragment A introduced into a cell can kill the cell. Cell 15, 245–250 (1978)

    CAS  Article  Google Scholar 

  25. 25

    Haseloff, J. GFP variants for multispectral imaging of living cells. Methods Cell Biol. 58, 139–151 (1999)

    CAS  Article  Google Scholar 

  26. 26

    Weijers, D., Geldner, N., Offringa, R. & Jürgens, G. Early paternal gene activity in Arabidopsis. Nature 414, 709–710 (2001)

    ADS  CAS  Article  Google Scholar 

  27. 27

    Weijers, D. Hormonal Regulation of Pattern Formation in the Arabidopsis Embryo. Thesis, Univ. Leiden (2002)

    Google Scholar 

  28. 28

    Caruso, J., Pence, V. & Leverone, L. in Plant Hormones: Physiology, Biochemistry and Molecular Biology (ed. Davies, P.) 43–447 (Kluwer Academic, The Netherlands, 1995)

    Google Scholar 

  29. 29

    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)

    CAS  Article  Google Scholar 

  30. 30

    Sundaresan, V. et al. Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev. 14, 1797–1810 (1995)

    Article  Google Scholar 

  31. 31

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

    Google Scholar 

  32. 32

    Steeves, T. & Sussex, I. Patterns in Plant Development (Cambridge Univ. Press, Cambridge, 1989)

    Google Scholar 

  33. 33

    Teleman, A., Strigini, M. & Cohen, S. Shaping morphogen gradients. Cell 105, 559–562 (2001)

    CAS  Article  Google Scholar 

  34. 34

    Tabata, T. Genetics of morphogen gradients. Nature Rev. Genet. 2, 620–630 (2001)

    ADS  CAS  Article  Google Scholar 

  35. 35

    Ulmasov, T., Murfett, J., Hagen, G. & Guilfoyle, T. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9, 1963–1971 (1997)

    CAS  Article  Google Scholar 

  36. 36

    Braselton, J., Wilkinson, M. & Clulow, S. Feulgen staining of intact plant tissues for confocal microscopy. Biotechnol. Histochem. 71, 84–87 (1996)

    CAS  Article  Google Scholar 

  37. 37

    Friml, J., Benkova, E., Mayer, U., Palme, K. & Muster, G. Automated whole mount localisation techniques for plant seedlings. Plant J. 34, 115–124 (2003)

    CAS  Article  Google Scholar 

  38. 38

    Gälweiler, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230 (1998)

    ADS  Article  Google Scholar 

  39. 39

    Moctezuma, E. Changes in auxin patterns in developing gynophores of the peanut plant (Arachis hypogaea L.). Ann. Bot. 83, 235–242 (1999)

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank S. Hiller, M. Kientz, G. Martin and M. L. O. Mendes for technical assistance, and C. Luschnig and K. Palme for providing material. Sequence-indexed Arabidopsis insertion mutants were obtained from the Salk Institute Genomic Analysis Laboratory and Cold Spring Harbor Laboratory. We are grateful to K. Cornelis and N. Geldner for critical reading of the manuscript. This work was supported by the Volkswagen Stiftung programme (M.S., J.F.), Landesgraduiertenförderung (A.V.), and the Research Council for Earth and Lifesciences (ALW), with financial aid from the Dutch Organization of Scientific Research (NWO) (D.W.) and the Deutsche Forschungsgemeinschaft.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jiří Friml.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Friml, J., Vieten, A., Sauer, M. et al. Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature 426, 147–153 (2003). https://doi.org/10.1038/nature02085

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing