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Coordinated regulation of Arabidopsis thaliana development by light and gibberellins

Nature volume 451, pages 475–479 (2008)Cite this article

Abstract

Light and gibberellins (GAs) mediate many essential and partially overlapping plant developmental processes. DELLA proteins are GA-signalling repressors that block GA-induced development1. GA induces degradation of DELLA proteins via the ubiquitin/proteasome pathway2, but light promotes accumulation of DELLA proteins by reducing GA levels3. It was proposed that DELLA proteins restrain plant growth largely through their effect on gene expression4,5. However, the precise mechanism of their function in coordinating GA signalling and gene expression remains unknown. Here we characterize a nuclear protein interaction cascade mediating transduction of GA signals to the activity regulation of a light-responsive transcription factor. In the absence of GA, nuclear-localized DELLA proteins accumulate to higher levels, interact with phytochrome-interacting factor 3 (PIF3, a bHLH-type transcription factor) and prevent PIF3 from binding to its target gene promoters and regulating gene expression, and therefore abrogate PIF3-mediated light control of hypocotyl elongation. In the presence of GA, GID1 proteins (GA receptors) elevate their direct interaction with DELLA proteins in the nucleus, trigger DELLA protein’s ubiquitination and proteasome-mediated degradation, and thus release PIF3 from the negative effect of DELLA proteins.

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Figure 1: Effect of GA 3 , MG132 and PAC on DELLA protein abundance.
Figure 2: DELLA proteins and PIF3 have opposite roles in regulating Arabidopsis hypocotyl elongation.
Figure 3: DELLA proteins bind PIF3 and inhibit PIF3 activity towards its target genes.
Figure 4: GA-dependent interaction between GID1s and DELLA proteins.

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Acknowledgements

We thank J. Lee, K. He and I. Lee for providing unpublished results of their ChIP-microarray studies; J. A. Sullivan for MYC- and HA-tag vectors; F. Nagy for the YFP-tag vector; X. P. Wang for the Flag-tag vector; P.H. Quail for the pPIF3-RSETb plasmid; G. Choi for pif3-1 and 35S-PIF3–His–MYC seeds; T. P. Sun for rga-24 and rgl2-13 seeds; N. P. Harberd for gai-t6 seeds; S. P. Dinesh-Kumar for tobacco seeds; and F. Parcy for providing the BiFC vector system. This work was supported by a grant from the National Institutes of Health to X.W.D., by a grant from the Ministry of Science and Technology of China to National Institute of Biological Sciences at Beijing, by a 985 program fund from Peking University and the Ministry of Education of China to the Peking-Yale Joint Center laboratory, and by a grant from Program for New Century Excellent Talents in Peking University to L.-M.F. C.M. is a recipient of a postdoctoral fellowship from the Spanish Ministerio de Educacion y Ciencia. J.M.I.-P. is a recipient of a predoctoral fellowship from the Spanish Ministerio de Educacion y Ciencia. E.S. and S.K. were supported by grants from the Deutsche Forschungsgesellschaft.

Author Contributions X.W.D. conceived the project, and S.F. and X.W.D. together designed the experiments. L.-M.F. designed some of the experiments. S.F. and G.G. performed chromatin immunoprecipitation. C.M. and G.G. analysed the gid1 mutants and performed RT–PCR. Y.W. made the anti-RGA antibody. Y.W., L.C., F.W. and L.Y. performed the yeast two-hybrid analyses. J.Z. and F.W. performed in vitro pull-down assays. C.M. and J.M.I.-P. performed the BiFC experiments. S.K. and E.S. performed phyB and PIF3 subcellular localization studies. X.F. provided the rga-24 gai-t6 double and della pentuple mutants. S.F. performed all other experiments. S.F. and X.W.D. wrote the manuscript.

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Author notes

  1. Suhua Feng

    Present address: Present address: Howard Hughes Medical Institute, University of California at Los Angeles, Los Angeles, California 90095-1606, USA.,

  2. Cristina Martinez, Giuliana Gusmaroli, Yu Wang and Junli Zhou: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520-8104, USA,

    Suhua Feng, Cristina Martinez, Giuliana Gusmaroli & Xing Wang Deng

  2. National Institute of Biological Sciences, Zhongguancun Life Science Park, Beijing 102206, China ,

    Suhua Feng, Junli Zhou, Feng Wang, Liying Chen, Lu Yu & Xing Wang Deng

  3. Peking–Yale Joint Center for Plant Molecular Genetics and Agrobiotechnology, and National Laboratory for Protein Engineering and Plant Genetic Engineering, College of Life Sciences, Peking University, Beijing 100871, China

    Yu Wang, Liu-Min Fan & Xing Wang Deng

  4. Departamento Genética Molecular de Plantas, Centro Nacional de Biotecnología-CSIC, Campus Universidad Autónoma de Madrid, 28049 Madrid, Spain

    Juan M. Iglesias-Pedraz

  5. Institut für Biologie II/Botanik, Albert Ludwigs Universität, Freiburg D-79104, Germany

    Stefan Kircher & Eberhard Schäfer

  6. Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100080, China

    Xiangdong Fu

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Corresponding author

Correspondence to Xing Wang Deng.

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This file contains Supplementary Notes, Supplementary Figures 1-7 with Legends and Supplementary Tables 1-2. (PDF 2930 kb)

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Feng, S., Martinez, C., Gusmaroli, G. et al. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451, 475–479 (2008). https://doi.org/10.1038/nature06448

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