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Light-induced degradation of phyA is promoted by transfer of the photoreceptor into the nucleus

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Abstract

Higher plants possess multiple members of the phytochrome family of red, far-red light sensors to modulate plant growth and development according to competition from neighbors. The phytochrome family is composed of the light-labile phyA and several light-stable members (phyB-phyE in Arabidopsis). phyA accumulates to high levels in etiolated seedlings and is essential for young seedling establishment under a dense canopy. In photosynthetically active seedlings high levels of phyA counteract the shade avoidance response. phyA levels are maintained low in light-grown plants by a combination of light-dependent repression of PHYA transcription and light-induced proteasome-mediated degradation of the activated photoreceptor. Light-activated phyA is transported from the cytoplasm where it resides in darkness to the nucleus where it is needed for most phytochrome-induced responses. Here we show that phyA is degraded by a proteasome-dependent mechanism both in the cytoplasm and the nucleus. However, phyA degradation is significantly slower in the cytoplasm than in the nucleus. In the nucleus phyA is degraded in a proteasome-dependent mechanism even in its inactive Pr (red light absorbing) form, preventing the accumulation of high levels of nuclear phyA in darkness. Thus, light-induced degradation of phyA is in part controlled by a light-regulated import into the nucleus where the turnover is faster. Although most phyA responses require nuclear phyA it might be useful to maintain phyA in the cytoplasm in its inactive form to allow accumulation of high levels of the light sensor in etiolated seedlings.

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References

  • Ballare CL, Scopel AL, Jordan ET, Vierstra RD (1994) Signaling among neighboring plants and the development of size inequalities in plant populations. Proc Natl Acad Sci USA 91:10094–10098

    Article  CAS  PubMed  Google Scholar 

  • Canton FR, Quail PH (1999) Both phyA and phyB mediate light-imposed repression of PHYA gene expression in Arabidopsis. Plant Physiol 121:1207–1216

    Article  CAS  PubMed  Google Scholar 

  • Casal JJ, Luccioni LG, Oliverio KA, Boccalandro HE (2003) Light, phytochrome signalling and photomorphogenesis in Arabidopsis. Photochem Photobiol Sci 2:625–636

    Article  CAS  PubMed  Google Scholar 

  • Chen M (2008) Phytochrome nuclear body: an emerging model to study interphase nuclear dynamics and signaling. Curr Opin Plant Biol 11:503–508

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38:87–117

    Article  CAS  PubMed  Google Scholar 

  • Clough RC, Jordan-Beebe ET, Lohman KN, Marita JM, Walker JM, Gatz C, Vierstra RD (1999) Sequences within both the N- and C-terminal domains of phytochrome A are required for PFR ubiquitination and degradation. Plant J 17:155–167

    Article  CAS  PubMed  Google Scholar 

  • Fankhauser C, Chen M (2008) Transposing phytochrome into the nucleus. Trends Plant Sci 13:596–601

    Article  CAS  PubMed  Google Scholar 

  • Franklin KA, Quail PH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61:11–24

    Article  CAS  PubMed  Google Scholar 

  • Genoud T, Schweizer F, Tscheuschler A, Debrieux D, Casal JJ, Schafer E, Hiltbrunner A, Fankhauser C (2008) FHY1 mediates nuclear import of the light-activated phytochrome A photoreceptor. PLoS Genet 4:e1000143

    Article  PubMed  Google Scholar 

  • Hennig L, Buche C, Eichenberg K, Schafer E (1999) Dynamic properties of endogenous phytochrome A in Arabidopsis seedlings. Plant Physiol 121:571–577

    Article  CAS  PubMed  Google Scholar 

  • Hiltbrunner A, Tscheuschler A, Viczian A, Kunkel T, Kircher S, Schafer E (2006) FHY1 and FHL act together to mediate nuclear accumulation of the phytochrome A photoreceptor. Plant Cell Physiol 47:1023–1034

    Article  CAS  PubMed  Google Scholar 

  • Hiltbrunner A, Viczian A, Bury E, Tscheuschler A, Kircher S, Toth R, Honsberger A, Nagy F, Fankhauser C, Schafer E (2005) Nuclear accumulation of the phytochrome A photoreceptor requires FHY1. Curr Biol 15:2125–2130

    Article  CAS  PubMed  Google Scholar 

  • Huq E, Al-Sady B, Quail PH (2003) Nuclear translocation of the photoreceptor phytochrome B is necessary for its biological function in seedling photomorphogenesis. Plant J 35:660–664

    Article  CAS  PubMed  Google Scholar 

  • Jabben M, Shanklin J, Vierstra RD (1989) Red light-induced accumulation of ubiquitin-phytochrome conjugates in both monocots and dicots. Plant Physiol 90:380–384

    Article  CAS  PubMed  Google Scholar 

  • Kircher S, Gil P, Kozma-Bognar L, Fejes E, Speth V, Husselstein-Muller T, Bauer D, Adam E, Schafer E, Nagy F (2002) Nucleocytoplasmic partitioning of the plant photoreceptors phytochrome A, B, C, D, and E is regulated differentially by light and exhibits a diurnal rhythm. Plant Cell 14:1541–1555

    Article  CAS  PubMed  Google Scholar 

  • Lin R, Ding L, Casola C, Ripoll DR, Feschotte C, Wang H (2007) Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science 318:1302–1305

    Article  CAS  PubMed  Google Scholar 

  • Mackenzie JM Jr, Coleman RA, Briggs WR, Pratt LH (1975) Reversible redistribution of phytochrome within the cell upon conversion to its physiologically active form. Proc Natl Acad Sci USA 72:799–803

    Article  PubMed  Google Scholar 

  • Mathews S (2006) Phytochrome-mediated development in land plants: red light sensing evolves to meet the challenges of changing light environments. Mol Ecol 15:3483–3503

    Article  CAS  PubMed  Google Scholar 

  • Matsushita T, Mochizuki N, Nagatani A (2003) Dimers of the N-terminal domain of phytochrome B are functional in the nucleus. Nature 424:571–574

    Article  CAS  PubMed  Google Scholar 

  • Pfeiffer A, Kunkel T, Hiltbrunner A, Neuhaus G, Wolf I, Speth V, Adam E, Nagy F, Schafer E (2009) A cell-free system for light-dependent nuclear import of phytochrome. Plant J 57:680–689

    Article  CAS  PubMed  Google Scholar 

  • Quail PH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3:85–93

    Article  CAS  PubMed  Google Scholar 

  • Quint M, Ito H, Zhang W, Gray WM (2005) Characterization of a novel temperature-sensitive allele of the CUL1/AXR6 subunit of SCF ubiquitin-ligases. Plant J 43:371–383

    Article  CAS  PubMed  Google Scholar 

  • Robson PR, McCormac AC, Irvine AS, Smith H (1996) Genetic engineering of harvest index in tobacco through overexpression of a phytochrome gene. Nat Biotechnol 14:995–998

    Article  CAS  PubMed  Google Scholar 

  • Rockwell NC, Su YS, Lagarias JC (2006) Phytochrome structure and signaling mechanisms. Annu Rev Plant Biol 57:837–858

    Article  CAS  PubMed  Google Scholar 

  • Rosler J, Klein I, Zeidler M (2007) Arabidopsis fhl/fhy1 double mutant reveals a distinct cytoplasmic action of phytochrome A. Proc Natl Acad Sci USA 104:10737–10742

    Article  PubMed  Google Scholar 

  • Saijo Y, Zhu D, Li J, Rubio V, Zhou Z, Shen Y, Hoecker U, Wang H, Deng XW (2008) Arabidopsis COP1/SPA1 complex and FHY1/FHY3 associate with distinct phosphorylated forms of phytochrome A in balancing light signaling. Mol Cell 31:607–613

    Article  CAS  PubMed  Google Scholar 

  • Schumacher K, Vafeados D, McCarthy M, Sze H, Wilkins T, Chory J (1999) The Arabidopsis det3 mutant reveals a central role for the vacuolar H(+)-ATPase in plant growth and development. Genes Dev 13:3259–3270

    Article  CAS  PubMed  Google Scholar 

  • Seo HS, Watanabe E, Tokutomi S, Nagatani A, Chua NH (2004) Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes Dev 18:617–622

    Article  CAS  PubMed  Google Scholar 

  • Shanklin J, Jabben M, Vierstra RD (1987) Red light-induced formation of ubiquitin-phytochrome conjugates: identification of possible intermediates of phytochrome degradation. Proc Natl Acad Sci USA 84:359–363

    Article  CAS  PubMed  Google Scholar 

  • Sharrock RA, Clack T (2002) Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol 130:442–456

    Article  CAS  PubMed  Google Scholar 

  • Shinomura T, Nagatani A, Hanzawa H, Kubota M, Watanabe M, Furuya M (1996) Action spectra for phytochrome A- and B-specific photoinduction of seed germination in Arabidopsis thaliana. Proc Natl Acad Sci USA 93:8129–8133

    Article  CAS  PubMed  Google Scholar 

  • Trupkin SA, Debrieux D, Hiltbrunner A, Fankhauser C, Casal JJ (2007) The serine-rich N-terminal region of Arabidopsis phytochrome A is required for protein stability. Plant Mol Biol 63:669–678

    Article  CAS  PubMed  Google Scholar 

  • Wagner D, Fairchild CD, Kuhn RM, Quail PH (1996) Chromophore-bearing NH2-terminal domains of phytochromes A and B determine their photosensory specificity and differential light lability. Proc Natl Acad Sci USA 93:4011–4015

    Article  CAS  PubMed  Google Scholar 

  • Yanovsky MJ, Casal JJ, Whitelam GC (1995) Phytochrome A, Phytochrome B and HY4 are involved in hypocotyl growth-responses to natural radiation in Arabidopsis: weak de-etiolation of the phyA mutant under dense canopies. Plant Cell Environ 18:788–794

    Article  CAS  Google Scholar 

  • Zhang Y, Feng S, Chen F, Chen H, Wang J, McCall C, Xiong Y, Deng XW (2008) Arabidopsis DDB1-CUL4 ASSOCIATED FACTOR1 forms a nuclear E3 ubiquitin ligase with DDB1 and CUL4 that is involved in multiple plant developmental processes. Plant Cell 20:1437–1455

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Karin Schumacher and Akira Nagatani for providing antibodies against DET3 and phyA respectively, Sérerine Lorrain for critically reading the manuscript and Matthias Zeidler for his kind gift of the fhy1fhl double mutant. Microscopy was performed in the Cellular Imaging Facility platform (CIF) from the University of Lausanne and we wish to thank Arnaud Paradis for his help. Funding was provided by the University of Lausanne and a grant from the Swiss National Science Foundation to C. F. (Grant n° 3100A0-112638).

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Correspondence to Christian Fankhauser.

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Debrieux, D., Fankhauser, C. Light-induced degradation of phyA is promoted by transfer of the photoreceptor into the nucleus. Plant Mol Biol 73, 687–695 (2010). https://doi.org/10.1007/s11103-010-9649-9

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