Real-time dynamics of peptide ligand-dependent receptor complex formation in planta

Science Signaling

Volumn 8, Issue 388, 2015, Pages

  Somssich, Marc ^a   Ma, Qijun ^a   Weidtkamp Peters, Stefanie ^a   Stahl, Yvonne ^a   Felekyan, Suren ^a   Bleckmann, Andrea ^a,b   Seidel, Claus A M ^a   Simon, Rüdiger ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; FLAGELLIN 22; LIPOPROTEIN RECEPTOR; PEPTIDE; PHOSPHOTRANSFERASE; PROTEIN SERINE THREONINE KINASE; RECEPTOR LIKE KINASE; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ARABIDOPSIS PROTEIN; CLV3 PROTEIN, ARABIDOPSIS; LIGAND; PHOTOPROTEIN;

ANISOTROPY; ARTICLE; CELL MEMBRANE; COMPLEX FORMATION; DIMERIZATION; FLUORESCENCE IMAGING; FLUORESCENCE SPECTROSCOPY; LIGAND BINDING; MEASUREMENT; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MULTIPARAMETER FLUORESCENCE IMAGING SPECTROSCOPY; NONHUMAN; PLANT CELL; PLANT DEVELOPMENT; PLANT GROWTH; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SIGNAL TRANSDUCTION; STEADY STATE; STEADY STATE ANISOTROPY; AMINO ACID SEQUENCE; CONFOCAL MICROSCOPY; FLUORESCENCE POLARIZATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; HOMEOSTASIS; METABOLISM; MOLECULAR GENETICS; TOBACCO; TRANSGENIC PLANT;

BACTERIA (MICROORGANISMS); CARNATION LATENT VIRUS;

AMINO ACID SEQUENCE; ARABIDOPSIS PROTEINS; FLAGELLIN; FLUORESCENCE POLARIZATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HOMEOSTASIS; LIGANDS; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; PEPTIDES; PLANTS, GENETICALLY MODIFIED; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TOBACCO;

EID: 84938821922     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aab0598     Document Type: Article

References (43)

1. K. Ohyama, H. Shinohara, M. Ogawa-Ohnishi, Y. Matsubayashi, A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat. Chem. Biol. 5, 578-580 (2009).
2. S. E. Clark, R. W. Williams, E. M. Meyerowitz, The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89, 575-585 (1997).
3. S. E. Clark, M. P. Running, E. M. Meyerowitz, CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121, 2057-2067 (1995).
4. J. M. Kayes, S. E. Clark, CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125, 3843-3851 (1998).
5. R. Müller, A. Bleckmann, R. Simon, The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20, 934-946 (2008).
6. J. C. Fletcher, U. Brand, M. P. Running, R. Simon, E. M. Meyerowitz, Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283, 1911-1914 (1999).
7. U. Brand, J. C. Fletcher, M. Hobe, E. M. Meyerowitz, R. Simon, Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289, 617-619 (2000).
8. K. F. X. Mayer, H. Schoof, A. Haecker, M. Lenhard, G. Jürgens, T. Laux, Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805-815 (1998).
9. M. Ogawa, H. Shinohara, Y. Sakagami, Y. Matsubayashi, Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294(2008).
10. A. Bleckmann, S. Weidtkamp-Peters, C. A. Seidel, R. Simon, Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol. 152, 166-176 (2010).
11. Y. F. Guo, L. Q. Han, M. Hymes, R. Denver, S. E. Clark, CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J. 63, 889-900 (2010).
12. H. Shinohara, Y. Matsubayashi, Reevaluation of the CLV3-receptor interaction in the shoot apical meristem: Dissection of the CLV3 signaling pathway from a direct ligand-binding point of view. Plant J. 82, 328-336 (2015).
13. Z. L. Nimchuk, P. T. Tarr, E. M. Meyerowitz, An evolutionarily conserved pseudokinase mediates stem cell production in plants. Plant Cell 23, 851-854 (2011).
14. D. Chinchilla, C. Zipfel, S. Robatzek, B. Kemmerling, T. Nürnberger, J. D. Jones, G. Felix, T. Boller, A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497-500 (2007).
15. G. Felix, J. D. Duran, S. Volko, T. Boller, Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265-276 (1999).
16. J. Li, J. Q. Wen, K. A. Lease, J. T. Doke, F. E. Tax, J. C. Walker, BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213-222 (2002).
17. L. Gómez-Gómez, T. Boller, FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5, 1003-1011 (2000).
18. W. X. Sun, Y. R. Cao, K. J. Labby, P. Bittel, T. Boller, A. F. Bent, Probing the Arabidopsis flagellin receptor: FLS2-FLS2 association and the contributions of specific domains to signaling function. Plant Cell 24, 1096-1113 (2012).
19. G. S. Ali, K. V. S. K. Prasad, I. Day, A. S. N. Reddy, Ligand-dependent reduction in the membrane mobility of FLAGELLIN SENSITIVE2, an Arabidopsis receptor-like kinase. Plant Cell Physiol. 48, 1601-1611 (2007).
20. S. Weidtkamp-Peters, S. Felekyan, A. Bleckmann, R. Simon, W. Becker, R. Kühnemuth, C. A. Seidel, Multiparameter fluorescence image spectroscopy to study molecular interactions. Photochem. Photobiol. Sci. 8, 470-480 (2009).
21. Y. Stahl, S. Grabowski, A. Bleckmann, R. Kühnemuth, S. Weidtkamp-Peters, K. G. Pinto, G. K. Kirschner, J. B. Schmid, R. H. Wink, A. Hülsewede, S. Felekyan, C. A. M. Seidel, R. Simon, Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 23, 362-371 (2013).
22. T. W. J. Gadella, T. M. Jovin, R. M. Clegg, Fluorescence lifetime imaging microscopy (FLIM): Spatial resolution of microstructures on the nanosecond time scale. Biophys. Chem. 48, 221-239 (1993).
23. F. Perrin, La fluorescence des solutions. Ann. Phys. 12, 169-275 (1929).
24. I. Gautier, M. Tramier, C. Durieux, J. Coppey, R. B. Pansu, J. C. Nicolas, K. Kemnitz, M. Coppey-Moisan, Homo-FRET microscopy in living cells to measure monomer-dimer transition of GFP-tagged proteins. Biophys. J. 80, 3000-3008 (2001).
25. V. Ntoukakis, B. Schwessinger, C. Segonzac, C. Zipfel, Cautionary notes on the use of C-terminal BAK1 fusion proteins for functional studies. Plant Cell 23, 3871-3878 (2011).
26. T. S. Karpova, C. T. Baumann, L. He, X. Wu, A. Grammer, P. Lipsky, G. L. Hager, J. G. McNally, Fluorescence resonance energy transfer from cyan to yellow fluorescent protein detected by acceptor photobleaching using confocal microscopy and a single laser. J. Microsc. 209, 56-70 (2003).
27. B. Schulze, T. Mentzel, A. K. Jehle, K. Mueller, S. Beeler, T. Boller, G. Felix, D. Chinchilla, Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J. Biol. Chem. 285, 9444-9451 (2010).
28. S. Robatzek, D. Chinchilla, T. Boller, Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20, 537-542 (2006).
29. L. P. Yu, A. K. Miller, S. E. Clark, POLTERGEIST encodes a protein phosphatase 2C that regulates CLAVATA pathways controlling stem cell identity at Arabidopsis shoot and flower meristems. Curr. Biol. 13, 179-188 (2003).
30. J. M. Stone, A. E. Trotochaud, J. C. Walker, S. E. Clark, Control of meristem development by CLAVATA1 receptor kinase and kinase-associated protein phosphatase interactions. Plant Physiol. 117, 1217-1225 (1998).
31. K. Simons, D. Toomre, Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39 (2000).
32. L. A. Gish, J. M. Gagne, L. Q. Han, B. J. DeYoung, S. E. Clark, WUSCHEL-responsive At5g65480 interacts with CLAVATA components in vitro and in transient expression. PLOS One 8, e66345 (2013).
33. N. Kozer, D. Barua, S. Orchard, E. C. Nice, A. W. Burgess, W. S. Hlavacek, A. H. A. Clayton, Exploring higher-order EGFR oligomerisation and phosphorylation-A combined experimental and theoretical approach. Mol. Biosyst. 9, 1849-1863 (2013).
34. M. Amaddii, M. Meister, A. Banning, A. Tomasovic, J. Mooz, K. Rajalingam, R. Tikkanen, Flotillin-1/Reggie-2 protein plays dual role in activation of receptor-tyrosine kinase/ mitogen-activated protein kinase signaling. J. Biol. Chem. 287, 7265-7278 (2012).
35. Y.P.Qi,K.Tsuda,L.V.Nguyen,X.Wang,J.S.Lin,A.S.Murphy,J.Glazebrook, H. Thordal-Christensen, F. Katagiri, Physical association of Arabidopsis hypersensitive induced reaction proteins (HIRs) with the immune receptor RPS2. J. Biol. Chem. 286, 31297-31307 (2011).
36. S. Betsuyaku, F. Takahashi, A. Kinoshita, H. Miwa, K. Shinozaki, H. Fukuda, S. Sawa, Mitogen-activated protein kinase regulated by the CLAVATA receptors contributes to shoot apical meristem homeostasis. Plant Cell Physiol. 52, 14-29 (2011).
37. L. Ma, Y. Z. Huang, G. M. Pitcher, J. G. Valtschanoff, Y. H. Ma, L. Y. Feng, B. Lu, W. C. Xiong, M. W. Salter, R. J. Weinberg, L. Mei, Ligand-dependent recruitment of the ErbB4 signaling complex into neuronal lipid rafts. J. Neurosci. 23, 3164-3175 (2003).
38. C. Albrecht, F. Boutrot, C. Segonzac, B. Schwessinger, S. Gimenez-Ibanez, D. Chinchilla, J. P. Rathjen, S. C. de Vries, C. Zipfel, Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proc. Natl. Acad. Sci. U.S.A. 109, 303-308 (2012).
39. C. A. Bücherl, G. W. van Esse, A. Kruis, J. Luchtenberg, A. H. Westphal, J. Aker, A. van Hoek, C. Albrecht, J. W. Borst, S. C. de Vries, Visualization of BRI1 and BAK1(SERK3) membrane receptor heterooligomers during brassinosteroid signaling. Plant Physiol. 162, 1911-1925 (2013).
40. V. Kudryavtsev, S. Felekyan, A. K. Wo?niak, M. König, C. Sandhagen, R. Kühnemuth, C. A. Seidel, F. Oesterhelt, Monitoring dynamic systems with multiparameter fluorescence imaging. Anal. Bioanal. Chem. 387, 71-82 (2007).
41. W. Becker, Advanced time-correlated single photon counting techniques, in Springer Series in Chemical Physics (Springer, Berlin, 2005).
42. J. Schaffer, A. Volkmer, C. Eggeling, V. Subramaniam, G. Striker, C. A. M. Seidel, Identification of single molecules in aqueous solution by time-resolved fluorescence anisotropy. J. Phys. Chem. A 103, 331-336 (1999).
43. M. Maus, M. Cotlet, J. Hofkens, T. Gensch, F. C. De Schryver, J. Schaffer, C. A. M. Seidel, An experimental comparison of the maximum likelihood estimation and nonlinear leastsquares fluorescence lifetime analysis of single molecules. Anal. Chem. 73, 2078-2086 (2001).