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Journal of Plant Research

, Volume 129, Issue 2, pp 123–135 | Cite as

From photon to signal in phytochromes: similarities and differences between prokaryotic and plant phytochromes

  • Soshichiro NaganoEmail author
JPR Symposium The Cutting Edge of Photoresponse Mechanisms: Photoreceptor and Signaling Mechanism

Abstract

Phytochromes represent a diverse family of red/far-red-light absorbing chromoproteins which are widespread across plants, cyanobacteria, non-photosynthetic bacteria, and more. Phytochromes play key roles in regulating physiological activities in response to light, a critical element in the acclimatization to the environment. The discovery of prokaryotic phytochromes facilitated structural studies which deepened our understanding on the general mechanisms of phytochrome action. An extrapolation of this information to plant phytochromes is justified for universally conserved functional aspects, but it is also true that there are many aspects which are unique to plant phytochromes. Here I summarize some structural studies carried out to date on both prokaryotic and plant phytochromes. I also attempt to identify aspects which are common or unique to plant and prokaryotic phytochromes. Phytochrome themselves, as well as the downstream signaling pathway in plants are more complex than in their prokaryotic counterparts. Thus many structural and functional aspects of plant phytochrome remain unresolved.

Keywords

Phytochrome Protein structure Signal transduction Photoconversion 

Notes

Acknowledgments

The author would like to thank Professor Jon Hughes for the critical reading of the manuscript. The author is supported by the Deutsche Forschungsgemeinschaft (Hu702/9).

References

  1. Ahmad M, Jarillo JA, Smirnova O, Cashmore AR (1998) The CRY1 blue light photoreceptor of Arabidopsis interacts with phytochrome A in vitro. Mol Cell 1:939–948CrossRefPubMedGoogle Scholar
  2. Andel F, Hasson KC, Gai F, Anfinrud PA, Mathies RA (1997) Femtosecond time-resolved spectroscopy of the primary photochemistry of phytochrome. Biospectroscopy 3(6):421–433CrossRefGoogle Scholar
  3. Anders K, von Stetten D, Mailliet J, Kiontke S, Sineshchekov VA, Hildebrandt P, Hughes J, Essen LO (2011) Spectroscopic and photochemical characterization of the red-light sensitive photosensory module of Cph2 from Synechocystis PCC 6803. Photochem Photobiol 87:160–173CrossRefPubMedGoogle Scholar
  4. Anders K, Daminelli-Widany G, Mroginski MA, von Stetten D, Essen LO (2013) Structure of the cyanobacterial phytochrome 2 photosensor implies a tryptophan switch for phytochrome signaling. J Biol Chem 288:35714–35725PubMedCentralCrossRefPubMedGoogle Scholar
  5. Ashenberg O, Keating AE, Laub MT (2013) Helix bundle loops determine whether histidine kinases autophosphorylate in cis or in trans. J Mol Biol 425:1198–1209PubMedCentralCrossRefPubMedGoogle Scholar
  6. Bae G, Choi G (2008) Decoding of light signals by plant phytochromes and their interacting proteins. Annu Rev Plant Biol 59:281–311CrossRefPubMedGoogle Scholar
  7. Baumgartner JW, Kim C, Brissette RE, Inouye M, Park C, Hazelbauer GL (1994) Transmembrane signalling by a hybrid protein: communication from the domain of chemoreceptor Trg that recognizes sugar-binding proteins to the kinase/phosphatase domain of osmosensor EnvZ. JBacteriol 176:1157–1163Google Scholar
  8. Bellini D, Papiz MZ (2012) Structure of a bacteriophytochrome and light-stimulated protomer swapping with a gene repressor. Structure 20:1436–1446CrossRefPubMedGoogle Scholar
  9. Beyer HM, Juillot S, Herbst K, Samodelov SL, Muller K, Schamel WW, Romer W, Schafer E, Nagy F, Strahle U, Weber W, Zurbriggen MD (2015) Red light-regulated reversible nuclear localization of proteins in mammalian cells and Zebrafish. ACS Synth Biol 4:951–958CrossRefPubMedGoogle Scholar
  10. Blumenstein A, Vienken K, Tasler R, Purschwitz J, Veith D, Frankenberg-Dinkel N, Fischer R (2005) The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Curr Biol 15:1833–1838CrossRefPubMedGoogle Scholar
  11. Borucki B, Lamparter T (2009) A polarity probe for monitoring light-induced structural changes at the entrance of the chromophore pocket in a bacterial phytochrome. J Biol Chem 284:26005–26016PubMedCentralCrossRefPubMedGoogle Scholar
  12. Borucki B, Otto H, Rottwinkel G, Hughes J, Heyn MP, Lamparter T (2003) Mechanism of Cph1 phytochrome assembly from stopped-flow kinetics and circular dichroism. Biochemistry 42:13684–13697CrossRefPubMedGoogle Scholar
  13. Burgie ES, Vierstra RD (2014) Phytochromes: an atomic perspective on photoactivation and signaling. Plant Cell 26:4568–4583PubMedCentralCrossRefPubMedGoogle Scholar
  14. Burgie ES, Bussell AN, Walker JM, Dubiel K, Vierstra RD (2014a) Crystal structure of the photosensing module from a red/far-red light-absorbing plant phytochrome. Proc Natl Acad Sci USA 111:10179–10184PubMedCentralCrossRefPubMedGoogle Scholar
  15. Burgie ES, Wang T, Bussell AN, Walker JM, Li H, Vierstra RD (2014b) Crystallographic and electron microscopic analyses of a bacterial phytochrome reveal local and global rearrangements during photoconversion. J Biol Chem 289:24573–24587Google Scholar
  16. Butler WL, Norris KH, Siegelman HW, Hendricks SB (1959) Detection, assay, and preliminary purification of the pigment controlling photoresponsive development of plants. Proc Natl Acad Sci USA 45:1703–1708PubMedCentralCrossRefPubMedGoogle Scholar
  17. Chen M, Tao Y, Lim J, Shaw A, Chory J (2005) Regulation of phytochrome B nuclear localization through light-dependent unmasking of nuclear-localization signals. Curr Biol 15:637–642CrossRefPubMedGoogle Scholar
  18. Clack T, Mathews S, Sharrock RA (1994) The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequences and expression of PHYD and PHYE. Plant Mol Biol 25:413–427CrossRefPubMedGoogle Scholar
  19. Davis SJ, Vener AV, Vierstra RD (1999) Bacteriophytochromes: phytochrome-like photoreceptors from nonphotosynthetic eubacteria. Science 286:2517–2520CrossRefPubMedGoogle Scholar
  20. DeLano WL (2009) PyMOL molecular viewer: updates and refinements. Abstracts of papers of the American Chemical Society, p 238Google Scholar
  21. Diensthuber RP, Bommer M, Gleichmann T, Moglich A (2013) Full-length structure of a sensor histidine kinase pinpoints coaxial coiled coils as signal transducers and modulators. Structure 21:1127–1136CrossRefPubMedGoogle Scholar
  22. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66:486–501PubMedCentralCrossRefPubMedGoogle Scholar
  23. Essen L-O, Mailliet J, Hughes J (2008) The structure of a complete phytochrome sensory module in the Pr ground state. Proc Natl Acad Sci USA 105:14709–14714PubMedCentralCrossRefPubMedGoogle Scholar
  24. Evans K, Grossmann JG, Fordham-Skelton AP, Papiz MZ (2006) Small-angle X-ray scattering reveals the solution structure of a bacteriophytochrome in the catalytically active Pr state. J Mol Biol 364:655–666CrossRefPubMedGoogle Scholar
  25. Fankhauser C, Yeh KC, Lagarias JC, Zhang H, Elich TD, Chory J (1999) PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. Science 284:1539–1541CrossRefPubMedGoogle Scholar
  26. Ferris HU, Coles M, Lupas AN, Hartmann MD (2014) Crystallographic snapshot of the Escherichia coli EnvZ histidine kinase in an active conformation. J Struct Biol 186:376–379CrossRefPubMedGoogle Scholar
  27. Fischer AJ, Rockwell NC, Jang AY, Ernst LA, Waggoner AS, Duan Y, Lei H, Lagarias JC (2005) Multiple roles of a conserved GAF domain tyrosine residue in cyanobacterial and plant phytochromes. Biochemistry 44:15203–15215PubMedCentralCrossRefPubMedGoogle Scholar
  28. Froehlich AC, Noh B, Vierstra RD, Loros J, Dunlap JC (2005) Genetic and molecular analysis of phytochromes from the filamentous fungus Neurospora crassa. Eukaryot Cell 4:2140–2152PubMedCentralCrossRefPubMedGoogle Scholar
  29. Giraud E, Fardoux J, Fourrier N, Hannibal L, Genty B, Bouyer P, Dreyfus B, Vermeglio A (2002) Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria. Nature 417:202–205CrossRefPubMedGoogle Scholar
  30. Hahn J, Strauss HM, Landgraf FT, Gimenez HF, Lochnit G, Schmieder P, Hughes J (2006) Probing protein-chromophore interactions in Cph1 phytochrome by mutagenesis. FEBS J 273:1415–1429CrossRefPubMedGoogle Scholar
  31. Hiltbrunner A, Viczian A, Bury E, Tscheuschler A, Kircher S, Toth R, Honsberger A, Nagy F, Fankhauser C, Schäfer E (2005) Nuclear accumulation of the phytochrome A photoreceptor requires FHY1. Curr Biol 15:2125–2130CrossRefPubMedGoogle Scholar
  32. Hughes J (2010) Phytochrome three-dimensional structures and functions. Biochem Soc Trans 38:710–716CrossRefPubMedGoogle Scholar
  33. Hughes J (2013) Phytochrome cytoplasmic signaling. Annu Rev Plant Biol 64:377–402CrossRefPubMedGoogle Scholar
  34. Hughes J, Lamparter T, Mittmann F, Hartmann E, Gärtner W, Wilde A, Börner T (1997) A prokaryotic phytochrome. Nature 386:663CrossRefPubMedGoogle Scholar
  35. Ikeuchi M, Ishizuka T (2008) Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria. Photochem Photobiol Sci 7:1159–1167CrossRefPubMedGoogle Scholar
  36. Inomata K, Hammam MA, Kinoshita H, Murata Y, Khawn H, Noack S, Michael N, Lamparter T (2005) Sterically locked synthetic bilin derivatives and phytochrome Agp1 from Agrobacterium tumefaciens form photoinsensitive Pr- and Pfr-like adducts. J Biol Chem 280:24491–24497CrossRefPubMedGoogle Scholar
  37. Inomata K, Noack S, Hammam MA, Khawn H, Kinoshita H, Murata Y, Michael N, Scheerer P, Krauss N, Lamparter T (2006) Assembly of synthetic locked chromophores with Agrobacterium phytochromes Agp1 and Agp2. J Biol Chem 281:28162–28173CrossRefPubMedGoogle Scholar
  38. Jiang Z, Swem LR, Rushing BG, Devanathan S, Tollin G, Bauer CE (1999) Bacterial photoreceptor with similarity to photoactive yellow protein and plant phytochromes. Science 285:406–409CrossRefPubMedGoogle Scholar
  39. Karniol B, Vierstra RD (2003) The pair of bacteriophytochromes from Agrobacterium tumefaciens are histidine kinases with opposing photobiological properties. Proc Natl Acad Sci USA 100:2807–2812PubMedCentralCrossRefPubMedGoogle Scholar
  40. Khanna R, Huq E, Kikis EA, Al Sady B, Lanzatella C, Quail PH (2004) A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix-loop-helix transcription factors. Plant Cell 16:3033–3044PubMedCentralCrossRefPubMedGoogle Scholar
  41. Kikis EA, Oka Y, Hudson ME, Nagatani A, Quail PH (2009) Residues clustered in the light-sensing knot of phytochrome B are necessary for conformer-specific binding to signaling partner PIF3. PLoS Genet 5:e1000352PubMedCentralCrossRefPubMedGoogle Scholar
  42. Klose C, Venezia F, Hussong A, Kircher S, Schäfer E, Fleck C (2015a) Systematic analysis of how phytochrome B dimerization determines its specificity. Nat Plants 1:15090CrossRefGoogle Scholar
  43. Klose C, Viczian A, Kircher S, Schafer E, Nagy F (2015b) Molecular mechanisms for mediating light-dependent nucleo/cytoplasmic partitioning of phytochrome photoreceptors. New Phytol 206:965–971PubMedCentralCrossRefPubMedGoogle Scholar
  44. Landgraf FT, Forreiter C, Hurtado PA, Lamparter T, Hughes J (2001) Recombinant holophytochrome in Escherichia coli. FEBS Lett 508:459–462CrossRefPubMedGoogle Scholar
  45. Lapko VN, Jiang XY, Smith DL, Song PS (1997) Posttranslational modification of oat phytochrome A: phosphorylation of a specific serine in a multiple serine cluster. Biochemistry 36:10595–10599CrossRefPubMedGoogle Scholar
  46. Lecoq J, Schnitzer MJ (2011) An infrared fluorescent protein for deeper imaging. Nat Biotechnol 29:715–716CrossRefPubMedGoogle Scholar
  47. Leitgeb B, Sokolova V, Schafer E, Viczian A (2012) Effects of missense mutation on structure and function of photoreceptor. Plant Signal Behav 7:589–591PubMedCentralCrossRefPubMedGoogle Scholar
  48. Levskaya A, Chevalier AA, Tabor JJ, Simpson ZB, Lavery LA, Levy M, Davidson EA, Scouras A, Ellington AD, Marcotte EM, Voigt CA (2005) Synthetic biology: engineering Escherichia coli to see light. Nature 438:441–442CrossRefPubMedGoogle Scholar
  49. Li H, Zhang J, Vierstra RD, Li H (2010) Quaternary organization of a phytochrome dimer as revealed by cryoelectron microscopy. Proc Natl Acad Sci USA 107:10872–10877PubMedCentralCrossRefPubMedGoogle Scholar
  50. Litts JC, Kelly JM, Lagarias JC (1983) Structure-function studies on phytochrome. Preliminary characterization of highly purified phytochrome from Avena sativa enriched in the 124-kilodalton species. J Biol Chem 258:11025–11031PubMedGoogle Scholar
  51. Lu XD, Zhou CM, Xu PB, Luo Q, Lian HL, Yang HQ (2015) Red-light-dependent interaction of phyB with SPA1 promotes COP1-SPA1 dissociation and photomorphogenic development in Arabidopsis. Mol Plant 8:467–478CrossRefPubMedGoogle Scholar
  52. Mailliet J, Psakis G, Feilke K, Sineshchekov V, Essen LO, Hughes J (2011) Spectroscopy and a high-resolution crystal structure of Tyr263 mutants of cyanobacterial phytochrome Cph1. J Mol Biol 413:115–127CrossRefPubMedGoogle Scholar
  53. Marina A, Waldburger CD, Hendrickson WA (2005) Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein. EMBO J 24:4247–4259PubMedCentralCrossRefPubMedGoogle Scholar
  54. Matsushita T, Mochizuki N, Nagatani A (2003) Dimers of the N-terminal domain of phytochrome B are functional in the nucleus. Nature 424:571–574CrossRefPubMedGoogle Scholar
  55. Möglich A, Ayers RA, Moffat K (2009) Design and signaling mechanism of light-regulated histidine kinases. J Mol Biol 385:1433–1444PubMedCentralCrossRefPubMedGoogle Scholar
  56. Montgomery BL, Lagarias JC (2002) Phytochrome ancestry: sensors of bilins and light. Trends Plant Sci 7:357–366CrossRefPubMedGoogle Scholar
  57. Nagatani A (2010) Phytochrome: structural basis for its functions. Curr Opin Plant Biol 13:565–570CrossRefPubMedGoogle Scholar
  58. Ni M, Tepperman JM, Quail PH (1999) Binding of phytochrome B to its nuclear signalling partner PIF3 is reversibly induced by light. Nature 400:781–784CrossRefPubMedGoogle Scholar
  59. Noack S, Michael N, Rosen R, Lamparter T (2007) Protein conformational changes of Agrobacterium phytochrome Agp1 during chromophore assembly and photoconversion. Biochemistry 46:4164–4176CrossRefPubMedGoogle Scholar
  60. Oka Y, Matsushita T, Mochizuki N, Suzuki T, Tokutomi S, Nagatani A (2004) Functional analysis of a 450-amino acid N-terminal fragment of phytochrome B in Arabidopsis. Plant Cell 16:2104–2116PubMedCentralCrossRefPubMedGoogle Scholar
  61. Oka Y, Matsushita T, Mochizuki N, Quail PH, Nagatani A (2008) Mutant screen distinguishes between residues necessary for light-signal perception and signal transfer by phytochrome B. PLoS Genet 4:e1000158PubMedCentralCrossRefPubMedGoogle Scholar
  62. Oka Y, Kong SG, Matsushita T (2011) A non-covalently attached chromophore can mediate phytochrome B signaling in Arabidopsis. Plant Cell Physiol 52:2088–2102CrossRefPubMedGoogle Scholar
  63. Pfeiffer A, Nagel MK, Popp C, Wust F, Bindics J, Viczian A, Hiltbrunner A, Nagy F, Kunkel T, Schäfer E (2012) Interaction with plant transcription factors can mediate nuclear import of phytochrome B. Proc Natl Acad Sci USA 109:5892–5897PubMedCentralCrossRefPubMedGoogle Scholar
  64. Rattanapisit K, Cho MH, Bhoo SH (2015) Lysine 206 in Arabidopsis phytochrome A is the major site for ubiquitin-dependent protein degradation. J Biochem. doi: 10.1093/jb/mvv085
  65. Rockwell NC, Shang L, Martin SS, Lagarias JC (2009) Distinct classes of red/far-red photochemistry within the phytochrome superfamily. Proc Natl Acad Sci USA 106:6123–6127PubMedCentralCrossRefPubMedGoogle Scholar
  66. Rockwell NC, Duanmu D, Martin SS, Bachy C, Price DC, Bhattacharya D, Worden AZ, Lagarias JC (2014) Eukaryotic algal phytochromes span the visible spectrum. Proc Natl Acad Sci USA 111:3871–3876PubMedCentralCrossRefPubMedGoogle Scholar
  67. Sadanandom A, Adam E, Orosa B, Viczian A, Klose C, Zhang C, Josse EM, Kozma-Bognar L, Nagy F (2015) SUMOylation of phytochrome-B negatively regulates light-induced signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA 112:11108–11113PubMedCentralCrossRefPubMedGoogle Scholar
  68. Salewski J, Escobar FV, Kaminski S, von Stetten D, Keidel A, Rippers Y, Michael N, Scheerer P, Piwowarski P, Bartl F, Frankenberg-Dinkel N, Ringsdorf S, Gartner W, Lamparter T, Mroginski MA, Hildebrandt P (2013) Structure of the biliverdin cofactor in the Pfr state of bathy and prototypical phytochromes. J Biol Chem 288:16800–16814PubMedCentralCrossRefPubMedGoogle Scholar
  69. Scheerer P, Michael N, Park JH, Nagano S, Choe HW, Inomata K, Borucki B, Krauss N, Lamparter T (2010) Light-induced conformational changes of the chromophore and the protein in phytochromes: bacterial phytochromes as model systems. Chem Phys Chem 11:1090–1105PubMedGoogle Scholar
  70. Schneider-Poetsch HA, Braun B, Marx S, Schaumburg A (1991) Phytochromes and bacterial sensor proteins are related by structural and functional homologies. Hypothesis on phytochrome- mediated signal- transduction. FEBS Lett 281:245–249CrossRefPubMedGoogle Scholar
  71. Sheerin DJ, Menon C, zur -Krockhaus S, Enderle B, Zhu L, Johnen P, Schleifenbaum F, Stierhof YD, Huq E, Hiltbrunner A (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 27:189–201PubMedCentralCrossRefPubMedGoogle Scholar
  72. Shin AY, Han YJ, Song PS, Kim JI (2014) Expression of recombinant full-length plant phytochromes assembled with phytochromobilin in Pichia pastoris. FEBS Lett 588:2964–2970Google Scholar
  73. Smith H (2000) Phytochromes and light signal perception by plants—an emerging synthesis. Nature 407:585–591CrossRefPubMedGoogle Scholar
  74. Song C, Psakis G, Lang C, Mailliet J, Gärtner W, Hughes J, Matysik J (2011) Two ground state isoforms and a chromophore D-ring photoflip triggering extensive intramolecular changes in a canonical phytochrome. Proc Natl Acad Sci USA 108:3842–3847PubMedCentralCrossRefPubMedGoogle Scholar
  75. Stojkovic EA, Toh KC, Alexandre MT, Baclayon M, Moffat K, Kennis JT (2014) FTIR spectroscopy revealing light-dependent refolding of the conserved tongue region of bacteriophytochrome. J Phys Chem Lett 5:2512–2515PubMedCentralCrossRefPubMedGoogle Scholar
  76. Strauss HM, Schmieder P, Hughes J (2005) Light-dependent dimerisation in the N-terminal sensory module of cyanobacterial phytochrome 1. FEBS Lett 579:3970–3974CrossRefPubMedGoogle Scholar
  77. Su YS, Lagarias JC (2007) Light-independent phytochrome signaling mediated by dominant GAF domain tyrosine mutants of Arabidopsis phytochromes in transgenic plants. Plant Cell 19:2124–2139PubMedCentralCrossRefPubMedGoogle Scholar
  78. Sweere U, Eichenberg K, Lohrmann J, Mira-Rodado V, Baurle I, Kudla J, Nagy F, Schafer E, Harter K (2001) Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling. Science 294:1108–1111CrossRefPubMedGoogle Scholar
  79. Szurmant H, Hoch JA (2010) Interaction fidelity in two-component signaling. Curr Opin Microbiol 13:190–197PubMedCentralCrossRefPubMedGoogle Scholar
  80. Takala H, Bjorling A, Berntsson O, Lehtivuori H, Niebling S, Hoernke M, Kosheleva I, Henning R, Menzel A, Ihalainen JA, Westenhoff S (2014) Signal amplification and transduction in phytochrome photosensors. Nature 509:245–248PubMedCentralCrossRefPubMedGoogle Scholar
  81. Takala H, Bjorling A, Linna M, Westenhoff S, Ihalainen JA (2015) Light-induced changes in the dimerization interface of bacteriophytochromes. J Biol Chem 290:16383–16392CrossRefPubMedGoogle Scholar
  82. Tasler R, Moises T, Frankenberg-Dinkel N (2005) Biochemical and spectroscopic characterization of the bacterial phytochrome of Pseudomonas aeruginosa. FEBS J 272:1927–1936CrossRefPubMedGoogle Scholar
  83. 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 MolBiol 63:669–678Google Scholar
  84. Ulijasz AT, Cornilescu G, von Stetten D, Kaminski S, Mroginski MA, Zhang J, Bhaya D, Hildebrandt P, Vierstra RD (2008) Characterization of two thermostable cyanobacterial phytochromes reveals global movements in the chromophore-binding domain during photoconversion. J Biol Chem 283:21251–21266PubMedCentralCrossRefPubMedGoogle Scholar
  85. Velazquez Escobar F, Piwowarski P, Salewski J, Michael N, Fernandez Lopez M, Rupp A, Qureshi BM, Scheerer P, Bartl F, Frankenberg-Dinkel N, Siebert F, Andrea Mroginski M, Hildebrandt P (2015a) A protonation-coupled feedback mechanism controls the signalling process in bathy phytochromes. Nat Chem 7:423–430CrossRefPubMedGoogle Scholar
  86. Velazquez Escobar F, von Stetten D, Gunther-Lutkens M, Keidel A, Michael N, Lamparter T, Essen LO, Hughes J, Gartner W, Yang Y, Heyne K, Mroginski MA, Hildebrandt P (2015b) Conformational heterogeneity of the Pfr chromophore in plant and cyanobacterial phytochromes. Front Mol Biosci 2:37PubMedCentralCrossRefPubMedGoogle Scholar
  87. von Stetten D, Gunther M, Scheerer P, Murgida DH, Mroginski MA, Krauss N, Lamparter T, Zhang J, Anstrom DM, Vierstra RD, Forest KT, Hildebrandt P (2008) Chromophore heterogeneity and photoconversion in phytochrome crystals and solution studied by resonance Raman spectroscopy. Angew Chem Int Ed Engl 47:4753–4755CrossRefGoogle Scholar
  88. Wagner D, Koloszvari M, Quail PH (1996) Two small spatially distinct regions of phytochrome B are required for efficient signaling rates. Plant Cell 8:859–871PubMedCentralCrossRefPubMedGoogle Scholar
  89. Wagner JR, Brunzelle JS, Forest KT, Vierstra RD (2005) A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome. Nature 438:325–331CrossRefPubMedGoogle Scholar
  90. Wagner JR, Zhang J, von Stetten D, Gunther M, Murgida DH, Mroginski MA, Walker JM, Forest KT, Hildebrandt P, Vierstra RD (2008) Mutational analysis of Deinococcus radiodurans bacteriophytochrome reveals key amino acids necessary for the photochromicity and proton exchange cycle of phytochromes. J Biol Chem 283:12212–12226PubMedCentralCrossRefPubMedGoogle Scholar
  91. Wang C, Sang J, Wang J, Su M, Downey JS, Wu Q, Wang S, Cai Y, Xu X, Wu J, Senadheera DB, Cvitkovitch DG, Chen L, Goodman SD, Han A (2013) Mechanistic insights revealed by the crystal structure of a histidine kinase with signal transducer and sensor domains. PLoS Biol 11:e1001493PubMedCentralCrossRefPubMedGoogle Scholar
  92. Yamada S, Sugimoto H, Kobayashi M, Ohno A, Nakamura H, Shiro Y (2009) Structure of PAS-linked histidine kinase and the response regulator complex. Structure 17:1333–1344CrossRefPubMedGoogle Scholar
  93. Yamaguchi R, Nakamura M, Mochizuki N, Kay SA, Nagatani A (1999) Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis. J Cell Biol 145:437–445PubMedCentralCrossRefPubMedGoogle Scholar
  94. Yang X, Stojković EA, Kuk J, Moffat K (2007) Crystal structure of the chromophore binding domain of an unusual bacteriophytochrome, RpBphP3, reveals residues that modulate photoconversion. Proc Natl Acad Sci USA 104:12571–12576PubMedCentralCrossRefPubMedGoogle Scholar
  95. Yang X, Kuk J, Moffat K (2008) Crystal structure of Pseudomonas aeruginosa bacteriophytochrome: photoconversion and signal transduction. Proc Natl Acad Sci USA 105:14715–14720PubMedCentralCrossRefPubMedGoogle Scholar
  96. Yang X, Kuk J, Moffat K (2009) Conformational differences between the Pfr and Pr states in Pseudomonas aeruginosa bacteriophytochrome. Proc Natl Acad Sci USA 106:15639–15644PubMedCentralCrossRefPubMedGoogle Scholar
  97. Yang X, Ren Z, Kuk J, Moffat K (2011) Temperature-scan cryocrystallography reveals reaction intermediates in bacteriophytochrome. Nature 479:428–432PubMedCentralCrossRefPubMedGoogle Scholar
  98. Yang XJ, Stojkovic EA, Ozarowski WB, Kuk J, Davydova E, Moffat K (2015) Light signaling mechanism of two tandem bacteriophytochromes. Structure 23:1179–1189CrossRefPubMedGoogle Scholar
  99. Yeh KC, Lagarias JC (1998) Eukaryotic phytochromes: light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc Natl Acad Sci USA 95:13976–13981PubMedCentralCrossRefPubMedGoogle Scholar
  100. Yeh KC, Wu SH, Murphy JT, Lagarias JC (1997) A cyanobacterial phytochrome two-component light sensory system. Science 277:1505–1508CrossRefPubMedGoogle Scholar
  101. Zhu Y, Inouye M (2003) Analysis of the role of the EnvZ linker region in signal transduction using a chimeric Tar/EnvZ receptor protein, Tez1. J Biol Chem 278:22812–22819CrossRefPubMedGoogle Scholar
  102. Zhu Y, Tepperman JM, Fairchild CD, Quail PH (2000) Phytochrome B binds with greater apparent affinity than phytochrome A to the basic helix-loop-helix factor PIF3 in a reaction requiring the PAS domain of PIF3. Proc Natl Acad Sci USA 97:13419–13424PubMedCentralCrossRefPubMedGoogle Scholar

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© The Botanical Society of Japan and Springer Japan 2016

Authors and Affiliations

  1. 1.Institute for Plant PhysiologyJustus Liebig University GiessenGiessenGermany

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