Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Auxin promotes Arabidopsis root growth by modulating gibberellin response

Nature volume 421, pages740–743(2003)Cite this article

Abstract

The growth of plant organs is influenced by a stream of the phytohormone auxin that flows from the shoot apex to the tip of the root1. However, until now it has not been known how auxin regulates the cell proliferation and enlargement that characterizes organ growth. Here we show that auxin controls the growth of roots by modulating cellular responses to the phytohormone gibberellin (GA). GA promotes the growth of plants by opposing the effects of nuclear DELLA protein growth repressors2,3,4,5,6,7,8, one of which is Arabidopsis RGA (for repressor of gal-3)9,10. GA opposes the action of several DELLA proteins by destabilizing them, reducing both the concentration of detectable DELLA proteins and their growth-restraining effects9,10,11,12,13,14. We also show that auxin is necessary for GA-mediated control of root growth, and that attenuation of auxin transport or signalling delays the GA-induced disappearance of RGA from root cell nuclei. Our observations indicate that the shoot apex exerts long-distance control on the growth of plant organs through the effect of auxin on GA-mediated DELLA protein destabilization.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

Rent or Buy

All prices are NET prices.

Figure 1: GA regulates root elongation via DELLA proteins.
Figure 2: Shoot apex-derived auxin controls root growth.
Figure 3: NPA inhibits the effect of GA on root growth and disappearance of GFP–RGA from root cell nuclei.
Figure 4: Decrease in AtPIN1 or AXR1 function delays GA-induced disappearance of GFP–RGA.

References

  1. 1

    Lomax, T. L., Muday, G. K. & Rubery, P. H. in Plant Hormones: Physiology, Biochemistry and Molecular Biology (ed. Davies, P. J.) 509–530 (Kluwer, Dordrecht, 1995)

    Google Scholar 

  2. 2

    Richards, D. E., King, K. E., Ait-ali, T. & Harberd, N. P. How gibberellin regulates plant growth and development: A molecular genetic analysis of gibberellin signalling. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 67–88 (2001)

    CAS  Article  Google Scholar 

  3. 3

    Peng, J. et al. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev. 11, 3194–3205 (1997)

    CAS  Article  Google Scholar 

  4. 4

    Peng, J. et al. ‘Green Revolution’ genes encode mutant gibberellin response modulators. Nature 400, 256–261 (1999)

    ADS  CAS  Article  Google Scholar 

  5. 5

    King, K. E., Moritz, T. & Harberd, N. P. Gibberellins are not required for stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159, 767–776 (2001)

    CAS  PubMed  Google Scholar 

  6. 6

    Dill, A. & Sun, T.-p. Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159, 777–785 (2001)

    CAS  PubMed  Google Scholar 

  7. 7

    Lee, S. et al. Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev. 16, 646–658 (2002)

    CAS  Article  Google Scholar 

  8. 8

    Wen, C.-K. & Chang, C. Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14, 87–100 (2002)

    CAS  Article  Google Scholar 

  9. 9

    Silverstone, A. L. et al. Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13, 1555–1565 (2001)

    CAS  Article  Google Scholar 

  10. 10

    Dill, A., Jung, H.-S. & Sun, T.-p. The DELLA motif is essential for gibberellin-induced degradation of RGA. Proc. Natl Acad. Sci. USA 98, 14162–14167 (2001)

    ADS  CAS  Article  Google Scholar 

  11. 11

    Itoh, H., Ueguchi-Tanaka, M., Sato, Y., Ashikari, M. & Matsuoka, M. The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14, 1–16 (2002)

    Article  Google Scholar 

  12. 12

    Chandler, P. M., Marion-Poll, A., Ellis, M. & Gubler, F. Mutants at the Slender1 locus of barley cv Himalaya. Molecular and physiological characterization. Plant Physiol. 129, 181–190 (2002)

    CAS  Article  Google Scholar 

  13. 13

    Gubler, F., Chandler, P. M., White, R. G., Llewellyn, D. J. & Jacobsen, J. V. Gibberellin signaling in barley aleurone cells. Control of SLN1 and GAMYB expression. Plant Physiol. 129, 191–200 (2002)

    CAS  Article  Google Scholar 

  14. 14

    Fu, X. et al. Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14, 3191–3200 (2002)

    CAS  Article  Google Scholar 

  15. 15

    Gray, W. M., Kepinski, S., Rouse, D., Leyser, O. & Estelle, M. Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414, 271–276 (2001)

    ADS  CAS  Article  Google Scholar 

  16. 16

    Rogg, L. E. & Bärtel, B. Auxin signalling: derepression through regulated proteolysis. Dev. Cell 1, 595–604 (2001)

    CAS  Article  Google Scholar 

  17. 17

    Davies, P. J. (ed.) Plant Hormones: Physiology, Biochemistry and Molecular Biology (Kluwer, Dordrecht, 1995)

  18. 18

    Brian, P. W. & Hemming, H. G. Complementary action of gibberellic acid and auxins in pea internode extension. Ann. Bot. 22, 1–17 (1958)

    CAS  Article  Google Scholar 

  19. 19

    Evans, M. L., Ishikawa, H. & Estelle, M. A. Responses of Arabidopsis roots to auxin studied with high temporal resolution: comparison of wild type and auxin-response mutants. Planta 194, 215–222 (1994)

    CAS  Article  Google Scholar 

  20. 20

    Ruegger, M. et al. Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects. Plant Cell 9, 745–773 (1997)

    CAS  Article  Google Scholar 

  21. 21

    Bennett, M. J. et al. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273, 948–950 (1996)

    ADS  CAS  Article  Google Scholar 

  22. 22

    Muller, A. et al. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17, 6903–6911 (1998)

    CAS  Article  Google Scholar 

  23. 23

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

    ADS  CAS  Article  Google Scholar 

  24. 24

    Geldner, N. et al. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425–428 (2001)

    ADS  CAS  Article  Google Scholar 

  25. 25

    Baulcombe, D. RNA silencing. Curr. Biol. 12, R82–R84 (2002)

    CAS  Article  Google Scholar 

  26. 26

    Mlotshwa, S. et al. RNA silencing and the mobile silencing signal. Plant Cell 14, S289–S301 (2002)

    CAS  Article  Google Scholar 

  27. 27

    del Pozzo, J. C. et al. AXR1-ECR1-dependent conjugation of RUB1 to the Arabidopsis cullin AtCUL1 is required for auxin response. Plant Cell 14, 421–433 (2002)

    Article  Google Scholar 

  28. 28

    Xu, L. et al. The SCFCOI1 ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14, 1919–1935 (2002)

    CAS  Article  Google Scholar 

  29. 29

    Ross, J. J., O'Neill, D. P., Smith, J. J., Kerckhoffs, L. H. J. & Elliott, R. C. Evidence that auxin promotes gibberellin A1 biosynthesis in pea. Plant J. 21, 547–552 (2000)

    CAS  Article  Google Scholar 

  30. 30

    Fu, X. et al. Expression of Arabidopsis GAI in transgenic rice represses multiple gibberellin responses. Plant Cell 13, 1791–1802 (2001)

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank T.-p. Sun (Duke University) for the pRGA:GFP–RGA line, O. Leyser for axr1-12, G. Calder for assistance with confocal microscopy, and P. Achard, T. Ait-ali, E. Coen, O. Leyser, D. Richards and X. Zhang for comments on the manuscript. Funding was received from the BBSRC (Core Strategic Grant to the John Innes Centre and a response mode grant).

Author information

Affiliations

  1. John Innes Centre, Norwich Research Park, Colney Lane, NR4 7UH, Norwich, UK

    Xiangdong Fu & Nicholas P. Harberd

Authors
  1. Xiangdong Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicholas P. Harberd
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicholas P. Harberd.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Fu, X., Harberd, N. Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421, 740–743 (2003). https://doi.org/10.1038/nature01387

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

Quick links

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