COLD REGULATED 27 and 28 are targets of CONSTITUTIVELY PHOTOMORPHOGENIC 1 and negatively affect phytochrome B signalling.


Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
11 2020
Historique:
received: 24 01 2020
revised: 31 07 2020
accepted: 10 08 2020
pubmed: 6 9 2020
medline: 11 5 2021
entrez: 5 9 2020
Statut: ppublish

Résumé

Phytochromes are red/far-red light receptors in plants involved in the regulation of growth and development. Phytochromes can sense the light environment and contribute to measuring day length; thereby, they allow plants to respond and adapt to changes in the ambient environment. Two well-characterized signalling pathways act downstream of phytochromes and link light perception to the regulation of gene expression. The CONSTITUTIVELY PHOTOMORPHOGENIC 1/SUPPRESSOR OF PHYA-105 (COP1/SPA) E3 ubiquitin ligase complex and the PHYTOCHROME INTERACTING FACTORs (PIFs) are key components of these pathways and repress light responses in the dark. In light-grown seedlings, phytochromes inhibit COP1/SPA and PIF activity and thereby promote light signalling. In a yeast-two-hybrid screen for proteins binding to light-activated phytochromes, we identified COLD-REGULATED GENE 27 (COR27). COR27 and its homologue COR28 bind to phyA and phyB, the two primary phytochromes in seed plants. COR27 and COR28 have been described previously with regard to a function in the regulation of freezing tolerance, flowering and the circadian clock. Here, we show that COR27 and COR28 repress early seedling development in blue, far-red and in particular red light. COR27 and COR28 contain a conserved Val-Pro (VP)-peptide motif, which mediates binding to the COP1/SPA complex. COR27 and COR28 are targeted for degradation by COP1/SPA and mutant versions with a VP to AA amino acid substitution in the VP-peptide motif are stabilized. Overall, our data suggest that COR27 and COR28 accumulate in light but act as negative regulators of light signalling during early seedling development, thereby preventing an exaggerated response to light.

Identifiants

pubmed: 32890447
doi: 10.1111/tpj.14979
doi:

Substances chimiques

Arabidopsis Proteins 0
COR27 protein, Arabidopsis 0
COR28 protein, Arabidopsis 0
Cell Cycle Proteins 0
Repressor Proteins 0
SPA1 protein, Arabidopsis 0
Phytochrome B 136250-22-1
AT2G32950 protein, Arabidopsis EC 2.3.2.27
Ubiquitin-Protein Ligases EC 2.3.2.27
Proteasome Endopeptidase Complex EC 3.4.25.1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1038-1053

Informations de copyright

© 2020 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

Références

Alonso, J.M., Stepanova, A.N., Leisse, T.J. et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
Al-Sady, B., Ni, W., Kircher, S., Schäfer, E. and Quail, P.H. (2006) Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol. Cell, 23, 439-446.
Baaske, J., Gonschorek, P., Engesser, R. et al. (2018) Dual-controlled optogenetic system for the rapid down-regulation of protein levels in mammalian cells. Sci. Rep. 8, 15024.
Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., Ren, J., Li, W.W. and Noble, W.S. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202-W208.
Balcerowicz, M., Fittinghoff, K., Wirthmueller, L., Maier, A., Fackendahl, P., Fiene, G., Koncz, C. and Hoecker, U. (2011) Light exposure of Arabidopsis seedlings causes rapid de-stabilization as well as selective post-translational inactivation of the repressor of photomorphogenesis SPA2. Plant J. 65, 712-723.
Balcerowicz, M., Kerner, K., Schenkel, C. and Hoecker, U. (2017) SPA proteins affect the subcellular localization of COP1 in the COP1/SPA ubiquitin ligase complex during photomorphogenesis. Plant Physiol. 174, 1314-1321.
Bauer, D., Viczián, A., Kircher, S. et al. (2004) CONSTITUTIVE PHOTOMORPHOGENESIS 1 and multiple photoreceptors control degradation of PHYTOCHROME INTERACTING FACTOR 3, a transcription factor required for light signaling in Arabidopsis. Plant Cell, 16, 1433-1445.
Beyer, H.M., Gonschorek, P., Samodelov, S.L., Meier, M., Weber, W. and Zurbriggen, M.D. (2015) AQUA cloning: a versatile and simple enzyme-free cloning approach. PLoS One, 10, e0137652.
Clontech. (2009) Yeast Protocols Handbook. Mountain View: Clontech Laboratories.
Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
Davis, A.M., Hall, A., Millar, A.J., Darrah, C. and Davis, S.J. (2009) Protocol: streamlined sub-protocols for floral-dip transformation and selection of transformants in Arabidopsis thaliana. Plant Methods, 5, 3.
Durzynska, I., Xu, X., Adelmant, G., Ficarro, S.B., Marto, J.A., Sliz, P., Uljon, S. and Blacklow, S.C. (2017) STK40 is a pseudokinase that binds the E3 ubiquitin ligase COP1. Structure, 25, 287-294.
Enderle, B., Sheerin, D.J., Paik, I., Kathare, P.K., Schwenk, P., Klose, C., Ulbrich, M.H., Huq, E. and Hiltbrunner, A. (2017) PCH1 and PCHL promote photomorphogenesis in plants by controlling phytochrome B dark reversion. Nat. Commun. 8, 2221.
Eriksson, M.E., Hanano, S., Southern, M.M., Hall, A. and Millar, A.J. (2003) Response regulator homologues have complementary, light-dependent functions in the Arabidopsis circadian clock. Planta, 218, 159-162.
Gangappa, S.N. and Botto, J.F. (2014) The BBX family of plant transcription factors. Trends Plant Sci. 19, 460-470.
Gangappa, S.N., Crocco, C.D., Johansson, H., Datta, S., Hettiarachchi, C., Holm, M. and Botto, J.F. (2013) The Arabidopsis B-BOX protein BBX25 interacts with HY5, negatively regulating BBX22 expression to suppress seedling photomorphogenesis. Plant Cell, 25, 1243-1257.
Golonka, D., Fischbach, P., Jena, S.G., Kleeberg, J.R.W., Essen, L.-O., Toettcher, J.E., Zurbriggen, M.D. and Möglich, A. (2019) Deconstructing and repurposing the light-regulated interplay between Arabidopsis phytochromes and interacting factors. Commun. Biol. 2, 448.
Hirschfeld, M., Tepperman, J.M., Clack, T., Quail, P.H. and Sharrock, R.A. (1998) Coordination of phytochrome levels in phyB mutants of Arabidopsis as revealed by apoprotein-specific monoclonal antibodies. Genetics, 149, 523-535.
Hoecker, U. (2005) Regulated proteolysis in light signaling. Curr. Opin. Plant Biol. 8, 469-476.
Hoecker, U. (2017) The activities of the E3 ubiquitin ligase COP1/SPA, a key repressor in light signaling. Curr. Opin. Plant Biol. 37, 63-69.
Holm, M., Ma, L.-G., Qu, L.-J. and Deng, X.-W. (2002) Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev. 16, 1247-1259.
Indorf, M., Cordero, J., Neuhaus, G. and Rodríguez-Franco, M. (2007) SALT TOLERANCE (STO), a stress-related protein, has a major role in light signalling. Plant J. 51, 563-574.
Jacobs, J.L. and Dinman, J.D. (2004) Systematic analysis of bicistronic reporter assay data. Nucleic Acids Res. 32, e160.
Jang, I.-C., Henriques, R., Seo, H.S., Nagatani, A. and Chua, N.-H. (2010) Arabidopsis PHYTOCHROME INTERACTING FACTOR proteins promote phytochrome B polyubiquitination by COP1 E3 ligase in the nucleus. Plant Cell, 22, 2370-2383.
Jang, I.-C., Yang, J.-Y., Seo, H.S. and Chua, N.-H. (2005) HFR1 is targeted by COP1 E3 ligase for post-translational proteolysis during phytochrome A signaling. Genes Dev. 19, 593-602.
Jang, K., Gil Lee, H., Jung, S.-J., Paek, N.-C. and Joon Seo, P. (2015) The E3 ubiquitin ligase COP1 regulates thermosensory flowering by triggering GI degradation in Arabidopsis. Sci. Rep. 5, 12071.
Kami, C., Lorrain, S., Hornitschek, P. and Fankhauser, C. (2010) Light-regulated plant growth and development. Curr. Top. Dev. Biol. 91, 29-66.
Kisselev, A.F., van der Linden, W.A. and Overkleeft, H.S. (2012) Proteasome inhibitors: an expanding army attacking a unique target. Chem. Biol. 19, 99-115.
Lau, K., Podolec, R., Chappuis, R., Ulm, R. and Hothorn, M. (2019) Plant photoreceptors and their signaling components compete for COP1 binding via VP peptide motifs. EMBO J. 38, e102140.
Lau, O.S. and Deng, X.W. (2012) The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci. 17, 584-593.
Laubinger, S., Fittinghoff, K. and Hoecker, U. (2004) The SPA quartet: a family of WD-repeat proteins with a central role in suppression of photomorphogenesis in Arabidopsis. Plant Cell, 16, 2293-2306.
Lee, N. and Choi, G. (2017) Phytochrome-interacting factor from Arabidopsis to liverwort. Curr. Opin. Plant Biol. 35, 54-60.
Legris, M., Ince, Y.Ç. and Fankhauser, C. (2019) Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nat. Commun. 10, 5219.
Li, N., Zhang, Y., He, Y., Wang, Y. and Wang, L. (2020) Pseudo response regulators regulate photoperiodic hypocotyl growth by repressing PIF4/5 transcription. Plant Physiol. 183, 686-699.
Li, X., Ma, D., Lu, S.X., Hu, X., Huang, R., Liang, T., Xu, T., Tobin, E.M. and Liu, H. (2016) Blue light- and low temperature-regulated COR27 and COR28 play roles in the Arabidopsis circadian clock. Plant Cell, 28, 2755-2769.
Lin, F., Jiang, Y., Li, J., Yan, T., Fan, L., Liang, J., Chen, Z.J., Xu, D. and Deng, X.W. (2018) B-BOX DOMAIN PROTEIN28 negatively regulates photomorphogenesis by repressing the activity of transcription factor HY5 and undergoes COP1-mediated degradation. Plant Cell, 30, 2006-2019.
Lu, X.-D., Zhou, C.-M., Xu, P.-B., Luo, Q., Lian, H.-L. and Yang, H.-Q. (2015) Red-light-dependent interaction of phyB with SPA1 promotes COP1-SPA1 dissociation and photomorphogenic development in Arabidopsis. Mol. Plant, 8, 467-478.
Martín, G., Rovira, A., Veciana, N. et al. (2018) Circadian waves of transcriptional repression shape PIF-regulated photoperiod-responsive growth in Arabidopsis. Curr. Biol. 28, 311-318.e5.
Más, P., Alabadí, D., Yanovsky, M.J., Oyama, T. and Kay, S.A. (2003) Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis. Plant Cell, 15, 223-236.
McNellis, T.W., von Arnim, A.G., Araki, T., Komeda, Y., Miséra, S. and Deng, X.W. (1994) Genetic and molecular analysis of an allelic series of cop1 mutants suggests functional roles for the multiple protein domains. Plant Cell, 6, 487-500.
Mikkelsen, M.D. and Thomashow, M.F. (2009) A role for circadian evening elements in cold-regulated gene expression in Arabidopsis. Plant J. 60, 328-339.
Müller, K., Engesser, R., Timmer, J., Nagy, F., Zurbriggen, M.D. and Weber, W. (2013) Synthesis of phycocyanobilin in mammalian cells. Chem. Commun. 49, 8970-8972.
Müller, K., Siegel, D., Rodriguez Jahnke, F., Gerrer, K., Wend, S., Decker, E.L., Reski, R., Weber, W. and Zurbriggen, M.D. (2014) A red light-controlled synthetic gene expression switch for plant systems. Mol. Biosyst. 10, 1679-1688.
Nakamichi, N., Kita, M., Ito, S., Yamashino, T. and Mizuno, T. (2005) PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol. 46, 686-698.
Ordoñez-Herrera, N., Fackendahl, P., Yu, X., Schaefer, S., Koncz, C. and Hoecker, U. (2015) A cop1 spa mutant deficient in COP1 and SPA proteins reveals partial co-action of COP1 and SPA during Arabidopsis post-embryonic development and photomorphogenesis. Mol. Plant, 8, 479-481.
Osterlund, M.T., Hardtke, C.S., Wei, N. and Deng, X.W. (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature, 405, 462-466.
Pacín, M., Legris, M. and Casal, J.J. (2013) COP1 re-accumulates in the nucleus under shade. Plant J. 75, 631-641.
Pacín, M., Legris, M. and Casal, J.J. (2014) Rapid decline in nuclear COSTITUTIVE PHOTOMORPHOGENESIS1 abundance anticipates the stabilization of Its target ELONGATED HYPOCOTYL5 in the light. Plant Physiol. 164, 1134-1138.
Paik, I. and Huq, E. (2019) Plant photoreceptors: multi-functional sensory proteins and their signaling networks. Semin. Cell Dev. Biol. 92, 114-121.
Park, E., Park, J., Kim, J., Nagatani, A., Lagarias, J.C. and Choi, G. (2012) Phytochrome B inhibits binding of PHYTOCHROME INTERACTING FACTORs to their target promoters. Plant J. 72, 537-546.
Park, Y.-J., Lee, H.-J., Ha, J.-H., Kim, J.Y. and Park, C.-M. (2017) COP1 conveys warm temperature information to hypocotyl thermomorphogenesis. New Phytol. 215, 269-280.
Pham, V.N., Xu, X. and Huq, E. (2018) Molecular bases for the constitutive photomorphogenic phenotypes in Arabidopsis. Development, 145, dev169870.
Podolec, R. and Ulm, R. (2018) Photoreceptor-mediated regulation of the COP1/SPA E3 ubiquitin ligase. Curr. Opin. Plant Biol. 45, 18-25.
Ponnu, J., Riedel, T., Penner, E., Schrader, A. and Hoecker, U. (2019) Cryptochrome 2 competes with COP1 substrates to repress COP1 ubiquitin ligase activity during Arabidopsis photomorphogenesis. Proc. Natl Acad. Sci. USA, 116, 27133-27141.
Reed, J.W., Nagatani, A., Elich, T.D., Fagan, M. and Chory, J. (1994) Phytochrome A and phytochrome B have overlapping but distinct functions in Arabidopsis development. Plant Physiol. 104, 1139-1149.
Reed, J.W., Nagpal, P., Poole, D.S., Furuya, M. and Chory, J. (1993) 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.
Saijo, Y., Zhu, D., Li, J., Rubio, V., Zhou, Z., Shen, Y., Hoecker, U., Wang, H. and Deng, X.W. (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.
Schneider, C.A., Rasband, W.S. and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods, 9, 671-675.
Seo, H.S., Watanabe, E., Tokutomi, S., Nagatani, A. and Chua, N.-H. (2004) Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes Dev. 18, 617-622.
Seo, H.S., Yang, J.-Y., Ishikawa, M., Bolle, C., Ballesteros, M.L. and Chua, N.-H. (2003) LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature, 423, 995-999.
Sheerin, D.J., Menon, C., Oven-Krockhaus, S. et al. (2015) Light-activated phytochrome A and B interact with members of the SPA family to promote photomorphogenesis in Arabidopsis by reorganizing the COP1/SPA complex. Plant Cell, 27, 189-201.
Shen, H., Moon, J. and Huq, E. (2005) PIF1 is regulated by light-mediated degradation through the ubiquitin-26S proteasome pathway to optimize photomorphogenesis of seedlings in Arabidopsis. Plant J. 44, 1023-1035.
Shen, H., Zhu, L., Castillon, A., Majee, M., Downie, B. and Huq, E. (2008) Light-induced phosphorylation and degradation of the negative regulator PHYTOCHROME-INTERACTING FACTOR1 from Arabidopsis depend upon its direct physical interactions with photoactivated phytochromes. Plant Cell, 20, 1586-1602.
Sievers, F., Wilm, A., Dineen, D. et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539.
Uljon, S., Xu, X., Durzynska, I., Stein, S., Adelmant, G., Marto, J., Pear, W. and Blacklow, S. (2016) Structural basis for substrate selectivity of the E3 Ligase COP1. Structure, 24, 687-696.
Viczián, A., Ádám, É., Wolf, I., Bindics, J., Kircher, S., Heijde, M., Ulm, R., Schäfer, E. and Nagy, F. (2012) A short amino-terminal part of Arabidopsis phytochrome A induces constitutive photomorphogenic response. Mol. Plant, 5, 629-641.
von Arnim, A.G. and Deng, X.-W. (1994) Light inactivation of Arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell, 79, 1035-1045.
Wang, P., Cui, X., Zhao, C. et al. (2017) COR27 and COR28 encode nighttime repressors integrating Arabidopsis circadian clock and cold response: COR27 and COR28 integrate clock and cold signaling. J. Integr. Plant Biol. 59, 78-85.
Waterhouse, A.M., Procter, J.B., Martin, D.M.A., Clamp, M. and Barton, G.J. (2009) Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics, 25, 1189-1191.
Xu, D. (2019) COP1 and BBXs-HY5-mediated light signal transduction in plants. New Phytol. https://doi.org/10.1111/nph.16296.
Yamamoto, Y., Sato, E., Shimizu, T. et al. (2003) Comparative genetic studies on the APRR5 and APRR7 genes belonging to the APRR1/TOC1 quintet implicated in circadian rhythm, control of flowering time, and early photomorphogenesis. Plant Cell Physiol. 44, 1119-1130.
Yang, H.Q., Tang, R.H. and Cashmore, A.R. (2001) The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1. Plant Cell, 13, 2573-2587.
Yu, J.-W.-W., Rubio, V., Lee, N.-Y.-Y. et al. (2008) COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol. Cell, 32, 617-630.
Zhu, L. and Huq, E. (2019) Characterization of light-regulated protein-protein interactions by in vivo coimmunoprecipitation (Co-IP) assays in plants. Methods Mol. Biol. 2026, 29-39.

Auteurs

Nikolai Kahle (N)

Institute of Biology II, Faculty of Biology, University of Freiburg, Freiburg, 79104, Germany.

David J Sheerin (DJ)

Institute of Biology II, Faculty of Biology, University of Freiburg, Freiburg, 79104, Germany.

Patrick Fischbach (P)

Institute of Synthetic Biology and CEPLAS, Heinrich Heine University Düsseldorf, Düsseldorf, 40225, Germany.

Leonie-Alexa Koch (LA)

Institute of Synthetic Biology and CEPLAS, Heinrich Heine University Düsseldorf, Düsseldorf, 40225, Germany.

Philipp Schwenk (P)

Institute of Biology II, Faculty of Biology, University of Freiburg, Freiburg, 79104, Germany.
Spemann Graduate School of Biology and Medicine (SGBM), University of Freiburg, Freiburg, 79104, Germany.

Dorothee Lambert (D)

Institute of Biology II, Faculty of Biology, University of Freiburg, Freiburg, 79104, Germany.

Ryan Rodriguez (R)

Institute of Biology II, Faculty of Biology, University of Freiburg, Freiburg, 79104, Germany.

Konstantin Kerner (K)

Institute for Plant Sciences, University of Cologne, Cologne, 50674, Germany.

Ute Hoecker (U)

Institute for Plant Sciences, University of Cologne, Cologne, 50674, Germany.

Matias D Zurbriggen (MD)

Institute of Synthetic Biology and CEPLAS, Heinrich Heine University Düsseldorf, Düsseldorf, 40225, Germany.

Andreas Hiltbrunner (A)

Institute of Biology II, Faculty of Biology, University of Freiburg, Freiburg, 79104, Germany.
Signalling Research Centres BIOSS and CIBSS, University of Freiburg, Freiburg, 79104, Germany.

Articles similaires

Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
T-Lymphocytes, Regulatory Lung Neoplasms Proto-Oncogene Proteins p21(ras) Animals Humans

Pathogenic mitochondrial DNA mutations inhibit melanoma metastasis.

Spencer D Shelton, Sara House, Luiza Martins Nascentes Melo et al.
1.00
DNA, Mitochondrial Humans Melanoma Mutation Neoplasm Metastasis

Prevalence and implications of fragile X premutation screening in Thailand.

Areerat Hnoonual, Sunita Kaewfai, Chanin Limwongse et al.
1.00
Humans Fragile X Mental Retardation Protein Thailand Male Female

Classifications MeSH