Interaction of COP1 and UVR8 regulates UV‐B‐induced photomorphogenesis and stress acclimation in Arabidopsis

The ultraviolet‐B (UV‐B) portion of the solar radiation functions as an environmental signal for which plants have evolved specific and sensitive UV‐B perception systems. The UV‐B‐specific UV RESPONSE LOCUS 8 (UVR8) and the multifunctional E3 ubiquitin ligase CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) are key regulators of the UV‐B response. We show here that uvr8‐null mutants are deficient in UV‐B‐induced photomorphogenesis and hypersensitive to UV‐B stress, whereas overexpression of UVR8 results in enhanced UV‐B photomorphogenesis, acclimation and tolerance to UV‐B stress. By using sun simulators, we provide evidence at the physiological level that UV‐B acclimation mediated by the UV‐B‐specific photoregulatory pathway is indeed required for survival in sunlight. At the molecular level, we demonstrate that the wild type but not the mutant UVR8 and COP1 proteins directly interact in a UV‐B‐dependent, rapid manner in planta. These data collectively suggest that UV‐B‐specific interaction of COP1 and UVR8 in the nucleus is a very early step in signalling and responsible for the plant's coordinated response to UV‐B ensuring UV‐B acclimation and protection in the natural environment.

[1]  E. Wiemer,et al.  Major vault protein, in concert with constitutively photomorphogenic 1, negatively regulates c-Jun-mediated activator protein 1 transcription in mammalian cells. , 2005, Cancer research.

[2]  Gareth I Jenkins,et al.  UV-B Signaling Pathways with Different Fluence-Rate Response Profiles Are Distinguished in Mature Arabidopsis Leaf Tissue by Requirement for UVR8, HY5, and HYH1[W][OA] , 2007, Plant Physiology.

[3]  K. Okada,et al.  The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. , 1997, Genes & development.

[4]  M. Caldwell,et al.  Chapter 4 – SOLAR UV IRRADIATION AND THE GROWTH AND DEVELOPMENT OF HIGHER PLANTS , 1971 .

[5]  S. Kircher,et al.  In planta analysis of protein–protein interactions related to light signaling by bimolecular fluorescence complementation , 2005, Protoplasma.

[6]  S. Flint,et al.  Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with other climate change factors , 2007, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[7]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[8]  Pawel Herzyk,et al.  A UV-B-specific signaling component orchestrates plant UV protection. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Meng Chen,et al.  Light signal transduction in higher plants. , 2004, Annual review of genetics.

[10]  L. Björn,et al.  Terrestrial ecosystems, increased solar ultraviolet radiation and interactions with other climatic change factors. , 2003, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[11]  Dirk Inzé,et al.  GATEWAY vectors for Agrobacterium-mediated plant transformation. , 2002, Trends in plant science.

[12]  X. Deng,et al.  Light inactivation of arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning , 1994, Cell.

[13]  Alfred Wittinghofer,et al.  The 1.7 Å crystal structure of the regulator of chromosome condensation (RCC1) reveals a seven-bladed propeller , 1998, Nature.

[14]  Y. Sang,et al.  From The Cover: A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[15]  P. Martín,et al.  A Phytotron for Plant Stress Research: How Far Can Artificial Lighting Compare to Natural Sunlight? , 1996 .

[16]  Xing Wang Deng,et al.  COP1 - from plant photomorphogenesis to mammalian tumorigenesis. , 2005, Trends in cell biology.

[17]  E. Oakeley,et al.  Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[18]  E. Spalding,et al.  Anion channels and the stimulation of anthocyanin accumulation by blue light in Arabidopsis seedlings. , 1998, Plant physiology.

[19]  D. Kliebenstein,et al.  Arabidopsis UVR8 Regulates Ultraviolet-B Signal Transduction and Tolerance and Contains Sequence Similarity to Human Regulator of Chromatin Condensation 1 , 2002, Plant Physiology.

[20]  Y. Sang,et al.  COP1-Mediated Ubiquitination of CONSTANS Is Implicated in Cryptochrome Regulation of Flowering in Arabidopsis[W] , 2008, The Plant Cell Online.

[21]  Xing Wang Deng,et al.  Targeted destabilization of HY5 during light-regulated development of Arabidopsis , 2000, Nature.

[22]  Edward J Oakeley,et al.  CONSTITUTIVELY PHOTOMORPHOGENIC1 Is Required for the UV-B Response in Arabidopsis[W] , 2006, The Plant Cell Online.

[23]  G. Jenkins,et al.  UV‐B Perception and Signal Transduction , 2007 .

[24]  Klaus Harter,et al.  Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. , 2004, The Plant journal : for cell and molecular biology.

[25]  Y. Komeda,et al.  Genetic and molecular analysis of an allelic series of cop1 mutants suggests functional roles for the multiple protein domains. , 1994, The Plant cell.

[26]  M. Schmid,et al.  Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana , 2003, Science.

[27]  C. Büche,et al.  Characterization of a Novel Non-Constitutive Photomorphogenic cop1 Allele1 , 2003, Plant Physiology.

[28]  V. Rubio,et al.  The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. , 2003, Genes & development.

[29]  Xing Wang Deng,et al.  Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. , 1998, Molecular cell.

[30]  X. Deng,et al.  Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response , 2008, The EMBO journal.

[31]  C. Fankhauser,et al.  The Degradation of HFR1, a Putative bHLH Class Transcription Factor Involved in Light Signaling, Is Regulated by Phosphorylation and Requires COP1 , 2004, Current Biology.

[32]  S. Penfield Temperature perception and signal transduction in plants. , 2008, The New phytologist.

[33]  Somasekar Seshagiri,et al.  ATM Engages Autodegradation of the E3 Ubiquitin Ligase COP1 After DNA Damage , 2006, Science.

[34]  Gareth I Jenkins,et al.  UV-B Promotes Rapid Nuclear Translocation of the Arabidopsis UV-B–Specific Signaling Component UVR8 and Activates Its Function in the Nucleus , 2007, The Plant Cell Online.

[35]  R. Pardi,et al.  COP1D, an alternatively spliced constitutive photomorphogenic-1 (COP1) product, stabilizes UV stress-induced c-Jun through inhibition of full-length COP1 , 2008, Oncogene.

[36]  T. Kerppola,et al.  Visualization of molecular interactions by fluorescence complementation , 2006, Nature Reviews Molecular Cell Biology.

[37]  C. Cloix,et al.  Interaction of the Arabidopsis UV-B-specific signaling component UVR8 with chromatin. , 2008, Molecular plant.

[38]  F. Nagy,et al.  Signalling and gene regulation in response to ultraviolet light. , 2005, Current opinion in plant biology.

[39]  M. Hetzer,et al.  The Ran GTPase as a marker of chromosome position in spindle formation and nuclear envelope assembly , 2002, Nature Cell Biology.

[40]  Promotion of photomorphogenesis by COP1 , 2004, Plant Molecular Biology.

[41]  Rongcheng Lin,et al.  Light Regulates COP1-Mediated Degradation of HFR1, a Transcription Factor Essential for Light Signaling in Arabidopsis , 2005, The Plant Cell Online.

[42]  John D. Storey,et al.  Statistical significance for genomewide studies , 2003, Proceedings of the National Academy of Sciences of the United States of America.