Abstract
Arabidopsis seedlings display contrasting developmental patterns depending on the ambient light. Seedlings grown in the light develop photomorphogenically, characterized by short hypocotyls and expanded green cotyledons. In contrast, seedlings grown in darkness become etiolated, with elongated hypocotyls and closed cotyledons on an apical hook. Light signals, perceived by multiple photoreceptors and transduced to downstream regulators, dictate the extent of photomorphogenic development in a quantitative manner. Two key downstream components, COP1 and HY5, act antagonistically in regulating seedling development1. HY5 is a bZIP transcription factor that binds directly to the promoters of light-inducible genes, promoting their expression and photomorphogenic development2,3. COP1 is a RING-finger protein with WD-40 repeats whose nuclear abundance is negatively regulated by light4,5. COP1 interacts directly with HY5 in the nucleus to regulate its activity negatively1. Here we show that the abundance of HY5 is directly correlated with the extent of photomorphogenic development, and that the COP1–HY5 interaction may specifically target HY5 for proteasome-mediated degradation in the nucleus.
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References
Ang, L. H. et al. Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol. Cell 1, 213–222 (1998).
Oyama, T. et al. The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev. 11, 2983–2995 (1997).
Chattopadhyay, S. et al. Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10, 673–683 (1998).
Deng, X. W. et al. COP1, an Arabidopsis regulatory gene, encodes a protein with both a Zinc-binding motif and a Gβ homologous domain. Cell 71, 791–801 (1992).
von Arnim, A. G. & Deng, X. W. Light inactivation of Arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell 79, 1035–1045 (1994).
Naidoo, N., Song, W., Hunter-Ensor, M. & Sehgal, A. A role for the proteasome in the light response of the timeless clock protein. Science 285, 1737–1741 (1999).
Kwok, S. F. et al. Characterization of two subunits of Arabidopsis 19S proteasome regulatory complex and its possible interaction with the COP9 complex. J. Mol. Biol. 285, 85–95 (1999).
Deng, X. W. et al. cop1: a regulatory locus involved in light-controlled development and gene expression in Arabidopsis. Genes Dev. 5, 1172–1182 (1992).
Kwok, S. F. et al. A complement of ten essential and pleiotropic Arabidopsis COP/DET/FUS genes is necessary for repression of photomorphogenis in darkness. Plant Physiol. 110, 731–742 (1996).
Karniol, B. et al. The Arabidopsis homologue of an eIF3 complex subunit associates with the COP9 complex. FEBS Lett. 439, 173–179 (1998).
Staub, J. M. et al. Evidence for FUS6 as a component of the nuclear-localized COP9 complex in Arabidopsis. Plant Cell 8, 2047–2056 (1996).
Wei, N. et al. Arabidopsis COP9 is a component of a novel signaling complex mediating light control of development. Cell 78, 117–124 (1994).
Serino, G. et al. Arabidopsis cop8 and fus4 mutations define the same locus that encodes subunit 4 of the COP9 signalosome. Plant Cell 11, 1967–1980 (1999).
von Arnim, A. G. Genetic and developmental control of nuclear accumulation of COP1, a repressor of photomorphogenesis in Arabidopsis. Plant Physiol. 114, 779–788 (1997).
Osterlund, M. T. et al. The role of COP1 in repression of Arabidopsis photomorphogenic development. Trends Cell Biol. 9, 113–118 (1999).
Osterlund, M. T. & Deng, X. W. Multiple photoreceptors mediate the light-induced reduction of GUS-COP1 from Arabidopsis hypocotyl nuclei. Plant J. 16, 201–208 (1998).
Reed, J. W. et al. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5, 147–157 (1993).
Whitelam, G. C. et al. Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell 5, 757–768 (1993).
Ahmad, M. & Cashmore, A. R. HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366, 162–166 (1993).
Lin, C. et al. Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. Proc. Natl Acad. Sci. USA 95, 2686–2690 (1998).
Tori, K. U. et al. Functional dissection of Arabidopsis COP1 reveals specific roles of its three structural modules in light control of seedling development. EMBO J. 17, 5577–5587 (1998).
McNellis, T. W. et al. Expression of an N terminal fragment of COP1 confers dominant-negative suppression of seedling photomorphogenic development in transgenic Arabidopsis. Plant Cell 8, 1491–1503 (1996).
Joazeiro, C. A. P. et al. The tyrosine kinase negative regulator c-Cbl as a RING-type E2-dependent ubiquitin-protein ligase. Science 8, 309–312 (1999).
Lorick, K. L. et al. RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc. Natl Acad. Sci. USA 96, 11364–11369 (1999).
Wei, N. & Deng, X. W. Making sense of the COP9 signalosome. Trends Genet. 15, 98–103 (1999).
Reed, J. W. et al. Phytochrome A and phytochrome B have overlapping but distinct function in Arabidopsis development. Plant Physiol. 104, 1139–1149 (1991).
Ahmad, M. et al. Cryptochrome blue-light photoreceptors of Arabidopsis implicated in phototropism. Nature 16, 720–723 (1994).
Wagner, D. et al. Overexpression of phytochrome B induces a short hypocotyl phenotype in transgenic Arabidopsis. Plant Cell, 3, 1275–1288 (1992).
Boylan, M. T. & Quail, P. H. Phytochrome A overexpression inhibits hypocotyl elongation in transgenic Arabidopsis. Proc. Natl Acad. Sci. USA 88, 10806–10810 (1991).
Koegl, M. et al. A novel ubiquitination factor, E4 is involved in multiubiquitin chain assembly. Cell 96, 635–644 (1999).
Acknowledgements
We thank R. Fry and H. Wang for reading and commenting on this manuscript, and A. Cashmore, C. Lin, P. Quail and G. Whitelam for providing Arabidopsis photoreceptor mutant strains. Our work was supported by grants from NIH (to X.W.D.), USDA (to N.W.) and the Human Frontiers Science Program Organization. X.W.D. is an NSF Presidential Faculty Fellow, M.T.O. is an NIH and Dept of Education predoctoral trainee and C.S.H. is a Human Frontier Science Program Organization postdoctoral fellow.
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Osterlund, M., Hardtke, C., Wei, N. et al. Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405, 462–466 (2000). https://doi.org/10.1038/35013076
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DOI: https://doi.org/10.1038/35013076
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