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.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
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)
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)
Peng, J. et al. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev. 11, 3194–3205 (1997)
Peng, J. et al. ‘Green Revolution’ genes encode mutant gibberellin response modulators. Nature 400, 256–261 (1999)
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)
Dill, A. & Sun, T.-p. Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159, 777–785 (2001)
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)
Wen, C.-K. & Chang, C. Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14, 87–100 (2002)
Silverstone, A. L. et al. Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13, 1555–1565 (2001)
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)
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)
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)
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)
Fu, X. et al. Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14, 3191–3200 (2002)
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)
Rogg, L. E. & Bärtel, B. Auxin signalling: derepression through regulated proteolysis. Dev. Cell 1, 595–604 (2001)
Davies, P. J. (ed.) Plant Hormones: Physiology, Biochemistry and Molecular Biology (Kluwer, Dordrecht, 1995)
Brian, P. W. & Hemming, H. G. Complementary action of gibberellic acid and auxins in pea internode extension. Ann. Bot. 22, 1–17 (1958)
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)
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)
Bennett, M. J. et al. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273, 948–950 (1996)
Muller, A. et al. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17, 6903–6911 (1998)
Galweiler, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230 (1998)
Geldner, N. et al. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425–428 (2001)
Baulcombe, D. RNA silencing. Curr. Biol. 12, R82–R84 (2002)
Mlotshwa, S. et al. RNA silencing and the mobile silencing signal. Plant Cell 14, S289–S301 (2002)
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)
Xu, L. et al. The SCFCOI1 ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14, 1919–1935 (2002)
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)
Fu, X. et al. Expression of Arabidopsis GAI in transgenic rice represses multiple gibberellin responses. Plant Cell 13, 1791–1802 (2001)
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).
The authors declare that they have no competing financial interests.
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
Low-Nitrogen Stress Stimulates Lateral Root Initiation and Nitrogen Assimilation in Wheat: Roles of Phytohormone Signaling
Journal of Plant Growth Regulation (2021)
OsNAC109 regulates senescence, growth and development by altering the expression of senescence- and phytohormone-associated genes in rice
Plant Molecular Biology (2021)
Journal of Forestry Research (2021)
Gibberellic acid and thidiazuron promote micropropagation of an endangered woody tree (Pterocarpus marsupium Roxb.) using in vitro seedlings
Plant Cell, Tissue and Organ Culture (PCTOC) (2021)
Plant Growth Regulation (2021)