Abstract
Phytochromes are ubiquitous photosensor proteins, which control the growth, reproduction and movement in plants, fungi and bacteria. Phytochromes switch between two photophysical states depending on the light conditions. In analogy to molecular machines, light absorption induces a series of structural changes that are transduced from the bilin chromophore, through the protein, and to the output domains. Recent progress towards understanding this structural mechanism of signal transduction has been manifold. We describe this progress with a focus on bacteriophytochromes. We describe the mechanism along three structural tiers, which are the chromophore-binding pocket, the photosensory module, and the output domains. We discuss possible interconnections between the tiers and conclude by presenting future directions and open questions. We hope that this review may serve as a compendium to guide future structural and spectroscopic studies designed to understand structural signaling in phytochromes.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
L. H. Flint and E. D. McAlister, Wave lengths of radiation in the visible spectrum inhibiting the germination of light-sensitive lettuce seed, Smithson. Misc. Collect. 1935 94 1–11
H. A. Borthwick, S. B. Hendricks, M. W. Parker, E. H. Toole and V. K. Toole, A Reversible Photoreaction Controlling Seed Germination, Proc. Natl. Acad. Sci. U. S. A. 1952 38 662–666, DOI: 10.1073/pnas.38.8.662
W. L. Butler, K. H. Norris, H. W. Siegelman and S. B. Hendricks, Detection, Assay, and Preliminary Purification of the Pigment Controlling Photoresponsive Development of Plants, Proc. Natl. Acad. Sci. U. S. A. 1959 45 1703–1708, DOI: 10.1073/pnas.45.12.1703
R. D. Vierstra and P. H. Quail, Purification and initial characterization of 124 kDalton phytochrome from Avena, Biochemistry 1983 22 2498–2505, DOI: 10.1021/bi00279a029
H. P. Hershey, R. F. Barker, K. B. Idler, J. L. Lissemore and P. H. Quail, Analysis of cloned cDNA and genomic sequences for phytochrome: complete amino acid sequences for two gene products expressed in etiolated Avena, Nucleic Acids Res. 1985 13 8543–8559, DOI: 10.1093/nar/13.23.8543
J. J. Casal, Photoreceptor signaling networks in plant responses to shade, Annu. Rev. Plant Biol. 2013 64 403–427, DOI: 10.1146/annurev-arplant-050312-120221
H. Schneider-Poetsch, Ü. Kolukisaoglu, D. H. Clapham, J. Hughes and T. Lamparter, Non-angiosperm phytochromes and the evolution of vascular plants, Physiol. Plant. 1998 102 612–622, DOI: 10.1034/j.1399-3054.1998.1020417.x
Z. Jiang, L. R. Swem, B. G. Rushing, S. Devanathan, G. Tollin and C. E. Bauer, Bacterial photoreceptor with similarity to photoactive yellow protein and plant phytochromes, Science 1999 285 406–409, DOI: 10.1126/science.285.5426.406
N. C. Rockwell and J. C. Lagarias, Phytochrome evolution in 3D: deletion, duplication, and diversification, New Phytol. 2020 225 2283–2300, DOI: 10.1111/nph.16240
J. Hughes, T. Lamparter, F. Mittmann, E. Hartmann, W. Gartner, A. Wilde and T. Borner, A prokaryotic phytochrome, Nature 1997 386 663, DOI: 10.1038/386663a0
K. C. Yeh, S. H. Wu, J. T. Murphy and J. C. Lagarias, A cyanobacterial phytochrome two-component light sensory system, Science 1997 277 1505–1508, DOI: 10.1126/science.277.5331.1505
S. J. Davis, A. V. Vener and R. D. Vierstra, Bacteriophytochromes: phytochrome-like photoreceptors from nonphotosynthetic eubacteria, Science 1999 286 2517–2520, DOI: 10.1126/science.286.5449.2517
D. M. Kehoe and A. R. Grossman, Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors, Science 1996 273 1409–1412, DOI: 10.1126/science.273.5280.1409
Y. Hirose, T. Shimada, R. Narikawa, M. Katayama and M. Ikeuchi, Cyanobacteriochrome CcaS is the green light receptor that induces the expression of phycobilisome linker protein, Proc. Natl. Acad. Sci. U. S. A. 2008 105 9528–9533, DOI: 10.1073/pnas.0801826105
A. Blumenstein, K. Vienken, R. Tasler, J. Purschwitz, D. Veith, N. Frankenberg-Dinkel and R. Fischer, The Aspergillus nidulans phytochrome FphA represses sexual development in red light, Curr. Biol. 2005 15 1833–1838, DOI: 10.1016/j.cub.2005.08.061
N. C. Rockwell, D. Duanmu, S. S. Martin, C. Bachy, D. C. Price, D. Bhattacharya, A. Z. Worden and J. C. Lagarias, Eukaryotic algal phytochromes span the visible spectrum, Proc. Natl. Acad. Sci. U. S. A. 2014 111 3871–3876, DOI: 10.1073/pnas.1401871111
P. R. Robson, A. C. McCormac, A. S. Irvine and H. Smith, Genetic engineering of harvest index in tobacco through overexpression of a phytochrome gene, Nat. Biotechnol. 1996 14 995–998, DOI: 10.1038/nbt0896-995
D. M. Shcherbakova, M. Baloban and V. V. Verkhusha, Near-infrared fluorescent proteins engineered from bacterial phytochromes, Curr. Opin. Chem. Biol. 2015 27 52–63, DOI: 10.1016/j.cbpa.2015.06.005
D. M. Shcherbakova, M. Baloban, S. Pletnev, V. N. Malashkevich, H. Xiao, Z. Dauter and V. V. Verkhusha, Molecular Basis of Spectral Diversity in Near-Infrared Phytochrome-Based Fluorescent Proteins, Chem. Biol. 2015 22 1540–1551, DOI: 10.1016/j.chembiol.2015.10.007
D. M. Shcherbakova, M. Baloban, A. V. Emelyanov, M. Brenowitz, P. Guo and V. V. Verkhusha, Bright monomeric near-infrared fluorescent proteins as tags and biosensors for multiscale imaging, Nat. Commun. 2016 7 12405, DOI: 10.1038/ncomms12405
A. Moglich and K. Moffat, Engineered photoreceptors as novel optogenetic tools, Photochem. Photobiol. Sci. 2010 9 1286–1300, DOI: 10.1039/c0pp00167h
A. A. Kaberniuk, A. A. Shemetov and V. V. Verkhusha, A bacterial phytochrome-based optogenetic system controllable with near-infrared light, Nat. Methods 2016 13 591–597, DOI: 10.1038/nmeth.3864
K. G. Chernov, T. A. Redchuk, E. S. Omelina and V. V. Verkhusha, Near-Infrared Fluorescent Proteins, Biosensors, and Optogenetic Tools Engineered from Phytochromes, Chem. Rev. 2017 117 6423–6446, DOI: 10.1021/acs.chemrev.6b00700
K. C. Yeh and J. C. Lagarias, Eukaryotic phytochromes: light-regulated serine/threonine protein kinases with histidine kinase ancestry, Proc. Natl. Acad. Sci. U. S. A. 1998 95 13976–13981, DOI: 10.1073/pnas.95.23.13976
W. Ni, S. L. Xu, E. Gonzalez-Grandio, R. J. Chalkley, A. F. R. Huhmer, A. L. Burlingame, Z. Y. Wang and P. H. Quail, PPKs mediate direct signal transfer from phytochrome photoreceptors to transcription factor PIF3, Nat. Commun. 2017 8 15236, DOI: 10.1038/ncomms15236
G. Bae and G. Choi, Decoding of light signals by plant phytochromes and their interacting proteins, Annu. Rev. Plant Biol. 2008 59 281–311, DOI: 10.1146/annurev.arplant.59.032607.092859
K. A. Franklin and P. H. Quail, Phytochrome functions in Arabidopsis development, J. Exp. Bot. 2010 61 11–24, DOI: 10.1093/jxb/erp304
J. Hughes, Phytochrome cytoplasmic signaling, Annu. Rev. Plant Biol. 2013 64 377–402, DOI: 10.1146/annurev-arplant-050312-120045
E. Giraud, J. Fardoux, N. Fourrier, L. Hannibal, B. Genty, P. Bouyer, B. Dreyfus and A. Vermeglio, Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria, Nature 2002 417 202–205, DOI: 10.1038/417202a
F. Gan, S. Zhang, N. C. Rockwell, S. S. Martin, J. C. Lagarias and D. A. Bryant, Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light, Science 2014 345 1312–1317, DOI: 10.1126/science.1256963
N. C. Woitowich, A. S. Halavaty, P. Waltz, C. Kupitz, J. Valera, G. Tracy, K. D. Gallagher, E. Claesson, T. Nakane, S. Pandey, G. Nelson, R. Tanaka, E. Nango, E. Mizohata, S. Owada, K. Tono, Y. Joti, A. C. Nugent, H. Patel, A. Mapara, J. Hopkins, P. Duong, D. Bizhga, S. E. Kovaleva, R. St Peter, C. N. Hernandez, W. B. Ozarowski, S. Roy-Chowdhuri, J. H. Yang, P. Edlund, H. Takala, J. Ihalainen, J. Brayshaw, T. Norwood, I. Poudyal, P. Fromme, J. C. H. Spence, K. Moffat, S. Westenhoff, M. Schmidt and E. A. Stojkovic, Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome, IUCrJ 2018 5 619–634, DOI: 10.1107/S2052252518010631
M. E. Auldridge and K. T. Forest, Bacterial phytochromes: more than meets the light, Crit. Rev. Biochem. Mol. Biol. 2011 46 67–88, DOI: 10.3109/10409238.2010.546389
G. Gourinchas, S. Etzl and A. Winkler, Bacteriophytochromes - from informative model systems of phytochrome function to powerful tools in cell biology, Curr. Opin. Struct. Biol. 2019 57 72–83, DOI: 10.1016/j.sbi.2019.02.005
S. H. Bhoo, S. J. Davis, J. Walker, B. Karniol and R. D. Vierstra, Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore, Nature 2001 414 776–779, DOI: 10.1038/414776a.
R. D. Vierstra and S. J. Davis, Bacteriophytochromes: new tools for understanding phytochrome signal transduction, Semin. Cell Dev. Biol. 2000 11 511–521, DOI: 10.1006/scdb.2000.0206
R. D. Vierstra and J. Zhang, Phytochrome signaling: solving the Gordian knot with microbial relatives, Trends Plant Sci. 2011 16 417–426, DOI: 10.1016/j.tplants.2011.05.011
E. S. Burgie, A. N. Bussell, J. M. Walker, K. Dubiel and R. D. Vierstra, Crystal structure of the photosensing module from a red/far-red light-absorbing plant phytochrome, Proc. Natl. Acad. Sci. U. S. A. 2014 111 10179–10184, DOI: 10.1073/pnas.1403096111
S. Nagano, K. Guan, S. M. Shenkutie, C. Feiler, M. Weiss, A. Kraskov, D. Buhrke, P. Hildebrandt and J. Hughes, Structural insights into photoactivation and signalling in plant phytochromes, Nat. Plants 2020 6 581–588, DOI: 10.1038/s41477-020-0638-y
N. C. Rockwell, L. Shang, S. S. Martin and J. C. Lagarias, Distinct classes of red/far-red photochemistry within the phytochrome superfamily, Proc. Natl. Acad. Sci. U. S. A. 2009 106 6123–6127, DOI: 10.1073/pnas.0902370106, 10.1073/pnas.0902370106
N. C. Rockwell, Y. S. Su and J. C. Lagarias, Phytochrome structure and signaling mechanisms, Annu. Rev. Plant Biol. 2006 57 837–858, DOI: 10.1146/annurev.arplant.56.032604.144208
B. L. Montgomery, Sensing the light: photoreceptive systems and signal transduction in cyanobacteria, Mol. Microbiol. 2007 64 16–27, DOI: 10.1111/j.1365-2958.2007.05622.x
M. A. van der Horst, J. Key and K. J. Hellingwerf, Photosensing in chemotrophic, non-phototrophic bacteria: let there be light sensing too, Trends Microbiol. 2007 15 554–562, DOI: 10.1016/j.tim.2007.09.009
P. Scheerer, N. Michael, J. H. Park, S. Nagano, H. W. Choe, K. Inomata, B. Borucki, N. Krauss and T. Lamparter, Light-induced conformational changes of the chromophore and the protein in phytochromes: bacterial phytochromes as model systems, ChemPhysChem 2010 11 1090–1105, DOI: 10.1002/cphc.200900913
E. S. Burgie and R. D. Vierstra, Phytochromes: an atomic perspective on photoactivation and signaling, Plant Cell 2014 26 4568–4583, DOI: 10.1105/tpc.114.131623
A. Moglich, X. Yang, R. A. Ayers and K. Moffat, Structure and function of plant photoreceptors, Annu. Rev. Plant Biol. 2010 61 21–47, DOI: 10.1146/annurev-arplant-042809-112259
N. C. Rockwell and J. C. Lagarias, A brief history of phytochromes, ChemPhysChem 2010 11 1172–1180, DOI: 10.1002/cphc.200900894
H. Wang and H. Wang, Phytochrome signaling: time to tighten up the loose ends, Mol. Plant 2015 8 540–551, DOI: 10.1016/j.molp.2014.11.021
M. Legris, Y. C. Ince and C. Fankhauser, Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants, Nat. Commun. 2019 10 5219, DOI: 10.1038/s41467-019-13045-0
J. Rodriguez-Romero, M. Hedtke, C. Kastner, S. Muller and R. Fischer, Fungi, hidden in soil or up in the air: light makes a difference, Annu. Rev. Microbiol. 2010 64 585–610, DOI: 10.1146/annurev.micro.112408.134000
B. Karniol and R. D. Vierstra, The pair of bacteriophytochromes from Agrobacterium tumefaciens are histidine kinases with opposing photobiological properties, Proc. Natl. Acad. Sci. U. S. A. 2003 100 2807–2812, DOI: 10.1073/pnas.0437914100
B. Karniol, J. R. Wagner, J. M. Walker and R. D. Vierstra, Phylogenetic analysis of the phytochrome superfamily reveals distinct microbial subfamilies of photoreceptors, Biochem. J. 2005 392 103–116, DOI: 10.1042/BJ20050826
T. Dammeyer and N. Frankenberg-Dinkel, Function and distribution of bilin biosynthesis enzymes in photosynthetic organisms, Photochem. Photobiol. Sci. 2008 7 1121–1130, DOI: 10.1039/b807209b
M. Jaubert, J. Lavergne, J. Fardoux, L. Hannibal, L. Vuillet, J. M. Adriano, P. Bouyer, D. Pignol, E. Giraud and A. Vermeglio, A singular bacteriophytochrome acquired by lateral gene transfer, J. Biol. Chem. 2007 282 7320–7328, DOI: 10.1074/jbc.M611173200
B. Frankland, Biosynthesis and dark transformations of phytochrome, 1972, vol. 1972, pp. 195–225
M. Legris, C. Klose, E. S. Burgie, C. C. Rojas, M. Neme, A. Hiltbrunner, P. A. Wigge, E. Schafer, R. D. Vierstra and J. J. Casal, Phytochrome B integrates light and temperature signals in Arabidopsis, Science 2016 354 897–900, DOI: 10.1126/science.aaf5656
M. Legris, C. Nieto, R. Sellaro, S. Prat and J. J. Casal, Perception and signalling of light and temperature cues in plants, Plant J. 2017 90 683–697, DOI: 10.1111/tpj.13467
G. Rottwinkel, I. Oberpichler and T. Lamparter, Bathy phytochromes in rhizobial soil bacteria, J. Bacteriol. 2010 192 5124–5133, DOI: 10.1128/JB.00672-10
T. Lamparter, N. Michael, F. Mittmann and B. Esteban, Phytochrome from Agrobacterium tumefaciens has unusual spectral properties and reveals an N-terminal chromophore attachment site, Proc. Natl. Acad. Sci. U. S. A. 2002 99 11628–11633, DOI: 10.1073/pnas.152263999
A. Björling, O. Berntsson, H. Takala, K. D. Gallagher, H. Patel, E. Gustavsson, R. St Peter, P. Duong, A. Nugent, F. Zhang, P. Berntsen, R. Appio, I. Rajkovic, H. Lehtivuori, M. R. Panman, M. Hoernke, S. Niebling, R. Harimoorthy, T. Lamparter, E. A. Stojkovic, J. A. Ihalainen and S. Westenhoff, Ubiquitous Structural Signaling in Bacterial Phytochromes, J. Phys. Chem. Lett. 2015 6 3379–3383, DOI: 10.1021/acs.jpclett.5b01629
A. Björling, O. Berntsson, H. Lehtivuori, H. Takala, A. J. Hughes, M. Panman, M. Hoernke, S. Niebling, L. Henry, R. Henning, I. Kosheleva, V. Chukharev, N. V. Tkachenko, A. Menzel, G. Newby, D. Khakhulin, M. Wulff, J. A. Ihalainen and S. Westenhoff, Structural photoactivation of a full-length bacterial phytochrome, Sci. Adv. 2016 2 e1600920, DOI: 10.1126/sciadv.1600920
J. Matysik, P. Hildebrandt, W. Schlamann, S. E. Braslavsky and K. Schaffner, Fourier-transform resonance Raman spectroscopy of intermediates of the phytochrome photocycle, Biochemistry 1995 34 10497–10507, DOI: 10.1021/bi00033a023
F. Andel III, K. C. Hasson, F. Gai, P. A. Anfinrud and R. A. Mathies, Femtosecond time-resolved spectroscopy of the primary photochemistry of phytochrome, Biospectroscopy 1997 3 421–433, DOI: 10.1002/(SICI)1520-6343(1997)3:63.0.CO;2-3
A. Remberg, I. Lindner, T. Lamparter, J. Hughes, C. Kneip, P. Hildebrandt, S. E. Braslavsky, W. Gartner and K. Schaffner, Raman spectroscopic and light-induced kinetic characterization of a recombinant phytochrome of the cyanobacterium Synechocystis, Biochemistry 1997 36 13389–13395, DOI: 10.1021/bi971563z
J. J. van Thor, K. L. Ronayne and M. Towrie, Formation of the early photoproduct lumi-R of cyanobacterial phytochrome cph1 observed by ultrafast mid-infrared spectroscopy, J. Am. Chem. Soc. 2007 129 126–132, DOI: 10.1021/ja0660709
J. Dasgupta, R. R. Frontiera, K. C. Taylor, J. C. Lagarias and R. A. Mathies, Ultrafast excited-state isomerization in phytochrome revealed by femtosecond stimulated Raman spectroscopy, Proc. Natl. Acad. Sci. U. S. A. 2009 106 1784–1789, DOI: 10.1073/pnas.0812056106
M. A. Mroginski, D. H. Murgida and P. Hildebrandt, The chromophore structural changes during the photocycle of phytochrome: a combined resonance Raman and quantum chemical approach, Acc. Chem. Res. 2007 40 258–266, DOI: 10.1021/ar6000523
U. Robben, I. Lindner and W. Gartner, New open-chain tetrapyrroles as chromophores in the plant photoreceptor phytochrome, J. Am. Chem. Soc. 2008 130 11303–11311, DOI: 10.1021/ja076728y
Y. Yang, M. Linke, T. von Haimberger, J. Hahn, R. Matute, L. Gonzalez, P. Schmieder and K. Heyne, Real-time tracking of phytochrome’s orientational changes during Pr photoisomerization, J. Am. Chem. Soc. 2012 134 1408–1411, DOI: 10.1021/ja209413d
T. Mathes, J. Ravensbergen, M. Kloz, T. Gleichmann, K. D. Gallagher, N. C. Woitowich, R. St Peter, S. E. Kovaleva, E. A. Stojkovic and J. T. Kennis, Femto- to Microsecond Photodynamics of an Unusual Bacteriophytochrome, J. Phys. Chem. Lett. 2015 6 239–243, DOI: 10.1021/jz502408n
D. Buhrke, U. Kuhlmann, N. Michael and P. Hildebrandt, The Photoconversion of Phytochrome Includes an Unproductive Shunt Reaction Pathway, ChemPhysChem 2018 19 566–570, DOI: 10.1002/cphc.201701311
J. J. van Thor, B. Borucki, W. Crielaard, H. Otto, T. Lamparter, J. Hughes, K. J. Hellingwerf and M. P. Heyn, Light-induced proton release and proton uptake reactions in the cyanobacterial phytochrome Cph1, Biochemistry 2001 40 11460–11471, DOI: 10.1021/bi002651d
B. Borucki, Proton transfer in the photoreceptors phytochrome and photoactive yellow protein, Photochem. Photobiol. Sci. 2006 5 553–566, DOI: 10.1039/b603846h
J. R. Wagner, J. Zhang, D. von Stetten, M. Gunther, D. H. Murgida, M. A. Mroginski, J. M. Walker, K. T. Forest, P. Hildebrandt and R. D. Vierstra, Mutational analysis of Deinococcus radiodurans bacteriophytochrome reveals key amino acids necessary for the photochromicity and proton exchange cycle of phytochromes, J. Biol. Chem. 2008 283 12212–12226, DOI: 10.1074/jbc.M709355200
F. Velazquez-Escobar, P. Piwowarski, J. Salewski, N. Michael, M. Fernandez Lopez, A. Rupp, B. M. Qureshi, P. Scheerer, F. Bartl, N. Frankenberg-Dinkel, F. Siebert, M. A. Mroginski and P. Hildebrandt, A protonation-coupled feedback mechanism controls the signalling process in bathy phytochromes, Nat. Chem. 2015 7 423–430, DOI: 10.1038/nchem.2225
B. Borucki, D. von Stetten, S. Seibeck, T. Lamparter, N. Michael, M. A. Mroginski, H. Otto, D. H. Murgida, M. P. Heyn and P. Hildebrandt, Light-induced proton release of phytochrome is coupled to the transient deprotonation of the tetrapyrrole chromophore, J. Biol. Chem. 2005 280 34358–34364, DOI: 10.1074/jbc.M505493200
C. Song, G. Psakis, C. Lang, J. Mailliet, W. Gartner, J. Hughes and J. Matysik, Two ground state isoforms and a chromophore D-ring photoflip triggering extensive intramolecular changes in a canonical phytochrome, Proc. Natl. Acad. Sci. U. S. A. 2011 108 3842–3847, DOI: 10.1073/pnas.1013377108
T. Rohmer, C. Lang, C. Bongards, K. B. Gupta, J. Neugebauer, J. Hughes, W. Gartner and J. Matysik, Phytochrome as molecular machine: revealing chromophore action during the Pfr → Pr photoconversion by magic-angle spinning NMR spectroscopy, J. Am. Chem. Soc. 2010 132 4431–4437, DOI: 10.1021/ja9108616
X. Yang, Z. Ren, J. Kuk and K. Moffat, Temperature-scan cryocrystallography reveals reaction intermediates in bacteriophytochrome, Nature 2011 479 428–432, DOI: 10.1038/nature10506
E. Consiglieri, A. Gutt, W. Gartner, L. Schubert, C. Viappiani, S. Abbruzzetti and A. Losi, Dynamics and efficiency of photoswitching in biliverdin-binding phytochromes, Photochem. Photobiol. Sci. 2019 18 2484–2496, DOI: 10.1039/c9pp00264b
A. Schmidt, L. Sauthof, M. Szczepek, M. F. Lopez, F. V. Escobar, B. M. Qureshi, N. Michael, D. Buhrke, T. Stevens, D. Kwiatkowski, D. von Stetten, M. A. Mroginski, N. Krauss, T. Lamparter, P. Hildebrandt and P. Scheerer, Structural snapshot of a bacterial phytochrome in its functional intermediate state, Nat. Commun. 2018 9 4912–4917, DOI: 10.1038/s41467-018-07392-7
S. Brandt, D. von Stetten, M. Gunther, P. Hildebrandt and N. Frankenberg-Dinkel, The fungal phytochrome FphA from Aspergillus nidulans, J. Biol. Chem. 2008 283 34605–34614, DOI: 10.1074/jbc.M805506200
M. Medzihradszky, J. Bindics, E. Adam, A. Viczian, E. Klement, S. Lorrain, P. Gyula, Z. Merai, C. Fankhauser, K. F. Medzihradszky, T. Kunkel, E. Schafer and F. Nagy, Phosphorylation of phytochrome B inhibits light-induced signaling via accelerated dark reversion in Arabidopsis, Plant Cell 2013 25 535–544, DOI: 10.1105/tpc.112.106898
K. Nito, C. C. Wong, J. R. Yates and J. Chory, Tyrosine phosphorylation regulates the activity of phytochrome photoreceptors, Cell Rep. 2013 3 1970–1979, DOI: 10.1016/j.celrep.2013.05.006
S. von Horsten, S. Strass, N. Hellwig, V. Gruth, R. Klasen, A. Mielcarek, U. Linne, N. Morgner and L. O. Essen, Mapping light-driven conformational changes within the photosensory module of plant phytochrome B, Sci. Rep. 2016 6 34366, DOI: 10.1038/srep34366
F. Velazquez-Escobar, D. Buhrke, M. Fernandez Lopez, S. M. Shenkutie, S. von Horsten, L. O. Essen, J. Hughes and P. Hildebrandt, Structural communication between the chromophore-binding pocket and the N-terminal extension in plant phytochrome phyB, FEBS Lett. 2017 591 1258–1265, DOI: 10.1002/1873-3468.12642
M. Ikeuchi and T. Ishizuka, Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria, Photochem. Photobiol. Sci. 2008 7 1159–1167, DOI: 10.1039/b802660m
B. L. Taylor and I. B. Zhulin, PAS domains: internal sensors of oxygen, redox potential, and light, Microbiol. Mol. Biol. Rev. 1999 63 479–506
J. R. Wagner, J. S. Brunzelle, K. T. Forest and R. D. Vierstra, A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome, Nature 2005 438 325–331, DOI: 10.1038/nature04118
L. O. Essen, J. Mailliet and J. Hughes, The structure of a complete phytochrome sensory module in the Pr ground state, Proc. Natl. Acad. Sci. U. S. A. 2008 105 14709–14714, DOI: 10.1073/pnas.0806477105
X. Yang, J. Kuk and K. Moffat, Crystal structure of Pseudomonas aeruginosa bacteriophytochrome: photoconversion and signal transduction, Proc. Natl. Acad. Sci. U. S. A. 2008 105 14715–14720, DOI: 10.1073/pnas.0806718105
D. Bellini and M. Z. Papiz, Structure of a bacteriophytochrome and light-stimulated protomer swapping with a gene repressor, Structure 2012 20 1436–1446, DOI: 10.1016/j.str.2012.06.002
G. Gourinchas, S. Etzl, C. Gobl, U. Vide, T. Madl and A. Winkler, Long-range allosteric signaling in red light-regulated diguanylyl cyclases, Sci. Adv. 2017 3 e1602498, DOI: 10.1126/sciadv.1602498
L. H. Otero, S. Klinke, J. Rinaldi, F. Velazquez-Escobar, M. A. Mroginski, M. Fernandez Lopez, F. Malamud, A. A. Vojnov, P. Hildebrandt, F. A. Goldbaum and H. R. Bonomi, Structure of the Full-Length Bacteriophytochrome from the Plant Pathogen Xanthomonas campestris Provides Clues to its Long-Range Signaling Mechanism, J. Mol. Biol. 2016 428 3702–3720, DOI: 10.1016/j.jmb.2016.04.012
G. Gourinchas, U. Heintz and A. Winkler, Asymmetric activation mechanism of a homodimeric red light-regulated photoreceptor, eLife 2018 7 e34815, DOI: 10.7554/eLife.34815
E. Claesson, W. Y. Wahlgren, H. Takala, S. Pandey, L. Castillon, V. Kuznetsova, L. Henry, M. Panman, M. Carrillo, J. Kubel, R. Nanekar, L. Isaksson, A. Nimmrich, A. Cellini, D. Morozov, M. Maj, M. Kurttila, R. Bosman, E. Nango, R. Tanaka, T. Tanaka, L. Fangjia, S. Iwata, S. Owada, K. Moffat, G. Groenhof, E. A. Stojkovic, J. A. Ihalainen, M. Schmidt and S. Westenhoff, The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser, eLife 2020 9 e53514, DOI: 10.7554/eLife.53514
E. S. Burgie, T. Wang, A. N. Bussell, J. M. Walker, H. Li and R. D. Vierstra, Crystallographic and electron microscopic analyses of a bacterial phytochrome reveal local and global rearrangements during photoconversion, J. Biol. Chem. 2014 289 24573–24587, DOI: 10.1074/jbc.M114.571661
X. Yang, E. A. Stojkovic, J. Kuk and K. Moffat, Crystal structure of the chromophore binding domain of an unusual bacteriophytochrome, RpBphP3, reveals residues that modulate photoconversion, Proc. Natl. Acad. Sci. U. S. A. 2007 104 12571–12576, DOI: 10.1073/pnas.0701737104
X. Yang, E. A. Stojkovic, W. B. Ozarowski, J. Kuk, E. Davydova and K. Moffat, Light Signaling Mechanism of Two Tandem Bacteriophytochromes, Structure 2015 23 1179–1189, DOI: 10.1016/j.str.2015.04.022
S. Nagano, P. Scheerer, K. Zubow, N. Michael, K. Inomata, T. Lamparter and N. Krauss, The Crystal Structures of the N-terminal Photosensory Core Module of Agrobacterium Phytochrome Agp1 as Parallel and Anti-parallel Dimers, J. Biol. Chem. 2016 291 20674–20691, DOI: 10.1074/jbc.M116.739136
H. Takala, A. Björling, O. Berntsson, H. Lehtivuori, S. Niebling, M. Hoernke, I. Kosheleva, R. Henning, A. Menzel, J. A. Ihalainen and S. Westenhoff, Signal amplification and transduction in phytochrome photosensors, Nature 2014 509 245–248, DOI: 10.1038/nature13310
J. R. Wagner, J. Zhang, J. S. Brunzelle, R. D. Vierstra and K. T. Forest, High resolution structure of Deinococcus bacteriophytochrome yields new insights into phytochrome architecture and evolution, J. Biol. Chem. 2007 282 12298–12309, DOI: 10.1074/jbc.M611824200
M. E. Auldridge, K. A. Satyshur, D. M. Anstrom and K. T. Forest, Structure-guided engineering enhances a phytochrome-based infrared fluorescent protein, J. Biol. Chem. 2012 287 7000–7009, DOI: 10.1074/jbc.M111.295121
D. Yu, W. C. Gustafson, C. Han, C. Lafaye, M. Noirclerc-Savoye, W. P. Ge, D. A. Thayer, H. Huang, T. B. Kornberg, A. Royant, L. Y. Jan, Y. N. Jan, W. A. Weiss and X. Shu, An improved monomeric infrared fluorescent protein for neuronal and tumour brain imaging, Nat. Commun. 2014 5 3626, DOI: 10.1038/ncomms4626
D. Bellini and M. Z. Papiz, Dimerization properties of the RpBphP2 chromophore-binding domain crystallized by homologue-directed mutagenesis, Acta Crystallogr., Sect. D: Biol. Crystallogr. 2012 68 1058–1066, DOI: 10.1107/S0907444912020537
S. Bhattacharya, M. E. Auldridge, H. Lehtivuori, J. A. Ihalainen and K. T. Forest, Origins of fluorescence in evolved bacteriophytochromes, J. Biol. Chem. 2014 289 32144–32152, DOI: 10.1074/jbc.M114.589739
F. Li, E. S. Burgie, T. Yu, A. Heroux, G. C. Schatz, R. D. Vierstra and A. M. Orville, X-ray radiation induces deprotonation of the bilin chromophore in crystalline D. radiodurans phytochrome, J. Am. Chem. Soc. 2015 137 2792–2795, DOI: 10.1021/ja510923m
H. Lehtivuori, S. Bhattacharya, N. M. Angenent-Mari, K. A. Satyshur and K. T. Forest, Removal of Chromophore-Proximal Polar Atoms Decreases Water Content and Increases Fluorescence in a Near Infrared Phytofluor, Front. Mol. Biosci. 2015 2 65, DOI: 10.3389/fmolb.2015.00065
M. Feliks, C. Lafaye, X. Shu, A. Royant and M. Field, Structural Determinants of Improved Fluorescence in a Family of Bacteriophytochrome-Based Infrared Fluorescent Proteins: Insights from Continuum Electrostatic Calculations and Molecular Dynamics Simulations, Biochemistry 2016 55 4263–4274, DOI: 10.1021/acs.biochem.6b00295
P. Edlund, H. Takala, E. Claesson, L. Henry, R. Dods, H. Lehtivuori, M. Panman, K. Pande, T. White, T. Nakane, O. Berntsson, E. Gustavsson, P. Bath, V. Modi, S. Roy-Chowdhury, J. Zook, P. Berntsen, S. Pandey, I. Poudyal, J. Tenboer, C. Kupitz, A. Barty, P. Fromme, J. D. Koralek, T. Tanaka, J. Spence, M. Liang, M. S. Hunter, S. Boutet, E. Nango, K. Moffat, G. Groenhof, J. Ihalainen, E. A. Stojkovic, M. Schmidt and S. Westenhoff, The room temperature crystal structure of a bacterial phytochrome determined by serial femtosecond crystallography, Sci. Rep. 2016 6 35279, DOI: 10.1038/srep35279
F. D. Fuller, S. Gul, R. Chatterjee, E. S. Burgie, I. D. Young, H. Lebrette, V. Srinivas, A. S. Brewster, T. Michels-Clark, J. A. Clinger, B. Andi, M. Ibrahim, E. Pastor, C. de Lichtenberg, R. Hussein, C. J. Pollock, M. Zhang, C. A. Stan, T. Kroll, T. Fransson, C. Weninger, M. Kubin, P. Aller, L. Lassalle, P. Brauer, M. D. Miller, M. Amin, S. Koroidov, C. G. Roessler, M. Allaire, R. G. Sierra, P. T. Docker, J. M. Glownia, S. Nelson, J. E. Koglin, D. Zhu, M. Chollet, S. Song, H. Lemke, M. Liang, D. Sokaras, R. Alonso-Mori, A. Zouni, J. Messinger, U. Bergmann, A. K. Boal, J. M. Bollinger, C. Krebs, M. Hogbom, G. N. Phillips, R. D. Vierstra, N. K. Sauter, A. M. Orville, J. Kern, V. K. Yachandra and J. Yano, Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers, Nat. Methods 2017 14 443–449, DOI: 10.1038/nmeth.4195
H. Takala, H. K. Lehtivuori, O. Berntsson, A. Hughes, R. Nanekar, S. Niebling, M. Panman, L. Henry, A. Menzel, S. Westenhoff and J. A. Ihalainen, On the (un)coupling of the chromophore, tongue interactions, and overall conformation in a bacterial phytochrome, J. Biol. Chem. 2018 293 8161–8172, DOI: 10.1074/jbc.RA118.001794
M. Baloban, D. M. Shcherbakova, S. Pletnev, V. Z. Pletnev, J. C. Lagarias and V. V. Verkhusha, Designing brighter near-infrared fluorescent proteins: insights from structural and biochemical studies, Chem. Sci. 2017 8 4546–4557, DOI: 10.1039/c7sc00855d
N. Lenngren, P. Edlund, H. Takala, B. Stucki-Buchli, J. Rumfeldt, I. Peshev, H. Hakkanen, S. Westenhoff and J. A. Ihalainen, Coordination of the biliverdin D-ring in bacteriophytochromes, Phys. Chem. Chem. Phys. 2018 20 18216–18225, DOI: 10.1039/c8cp01696h
D. Buhrke, G. Gourinchas, M. Muller, N. Michael, P. Hildebrandt and A. Winkler, Distinct chromophore-protein environments enable asymmetric activation of a bacteriophytochrome-activated diguanylate cyclase, J. Biol. Chem. 2020 295 539–551, DOI: 10.1074/jbc.RA119.011915
F. Andel, J. C. Lagarias and R. A. Mathies, Resonance raman analysis of chromophore structure in the lumi-R photoproduct of phytochrome, Biochemistry 1996 35 15997–16008, DOI: 10.1021/bi962175k
C. Kneip, P. Hildebrandt, W. Schlamann, S. E. Braslavsky, F. Mark and K. Schaffner, Protonation state and structural changes of the tetrapyrrole chromophore during the Pr → Pfr phototransformation of phytochrome: a resonance Raman spectroscopic study, Biochemistry 1999 38 15185–15192, DOI: 10.1021/bi990688w
F. Andel, J. T. Murphy, J. A. Haas, M. T. McDowell, I. van der Hoef, J. Lugtenburg, J. C. Lagarias and R. A. Mathies, Probing the photoreaction mechanism of phytochrome through analysis of resonance Raman vibrational spectra of recombinant analogues, Biochemistry 2000 39 2667–2676, DOI: 10.1021/bi991688z
W. Rudiger, F. Thummler, E. Cmiel and S. Schneider, Chromophore structure of the physiologically active form (P(fr)) of phytochrome, Proc. Natl. Acad. Sci. U. S. A. 1983 80 6244–6248, DOI: 10.1073/pnas.80.20.6244
E. S. Burgie, J. Zhang and R. D. Vierstra, Crystal Structure of Deinococcus Phytochrome in the Photoactivated State Reveals a Cascade of Structural Rearrangements during Photoconversion, Structure 2016 24 448–457, DOI: 10.1016/j.str.2016.01.001
A. J. Fischer and J. C. Lagarias, Harnessing phytochrome’s glowing potential, Proc. Natl. Acad. Sci. U. S. A. 2004 101 17334–17339, DOI: 10.1073/pnas.0407645101
J. Hahn, H. M. Strauss, F. T. Landgraf, H. F. Gimenez, G. Lochnit, P. Schmieder and J. Hughes, Probing protein-chromophore interactions in Cph1 phytochrome by mutagenesis, FEBS J. 2006 273 1415–1429, DOI: 10.1111/j.1742-4658.2006.05164.x
J. Zhang, R. J. Stankey and R. D. Vierstra, Structure-guided engineering of plant phytochrome B with altered photochemistry and light signaling, Plant Physiol. 2013 161 1445–1457, DOI: 10.1104/pp.112.208892
F. Velazquez-Escobar, C. Lang, A. Takiden, C. Schneider, J. Balke, J. Hughes, U. Alexiev, P. Hildebrandt and M. A. Mroginski, Protonation-Dependent Structural Heterogeneity in the Chromophore Binding Site of Cyanobacterial Phytochrome Cph1, J. Phys. Chem. B 2017 121 47–57, DOI: 10.1021/acs.jpcb.6b09600
J. A. Rumfeldt, H. Takala, A. Liukkonen and J. A. Ihalainen, UV-Vis Spectroscopy Reveals a Correlation Between Y263 and BV Protonation States in Bacteriophytochromes, Photochem. Photobiol. 2019 95 969–979, DOI: 10.1111/php.13095
J. Mailliet, G. Psakis, K. Feilke, V. Sineshchekov, L. O. Essen and J. Hughes, Spectroscopy and a high-resolution crystal structure of Tyr263 mutants of cyanobacterial phytochrome Cph1, J. Mol. Biol. 2011 413 115–127, DOI: 10.1016/j.jmb.2011.08.023
J. A. Ihalainen, E. Gustavsson, L. Schroeder, S. Donnini, H. Lehtivuori, L. Isaksson, C. Thoing, V. Modi, O. Berntsson, B. Stucki-Buchli, A. Liukkonen, H. Hakkanen, E. Kalenius, S. Westenhoff and T. Kottke, Chromophore-Protein Interplay during the Phytochrome Photocycle Revealed by Step-Scan FTIR Spectroscopy, J. Am. Chem. Soc. 2018 140 12396–12404, DOI: 10.1021/jacs.8b04659
K. C. Toh, E. A. Stojkovic, A. B. Rupenyan, I. H. van Stokkum, M. Salumbides, M. L. Groot, K. Moffat and J. T. Kennis, Primary reactions of bacteriophytochrome observed with ultrafast mid-infrared spectroscopy, J. Phys. Chem. A 2011 115 3778–3786, DOI: 10.1021/jp106891x
Y. Yang, K. Heyne, R. A. Mathies and J. Dasgupta, Non-Bonded Interactions Drive the Sub-Picosecond Bilin Photoisomerization in the P(fr) State of Phytochrome Cph1, ChemPhysChem 2016 17 369–374, DOI: 10.1002/cphc.201501073
H. Li, J. Zhang, R. D. Vierstra and H. Li, Quaternary organization of a phytochrome dimer as revealed by cryoelectron microscopy, Proc. Natl. Acad. Sci. U. S. A. 2010 107 10872–10877, DOI: 10.1073/pnas.1001908107
H. Takala, H. Lehtivuori, H. Hammarén, V. P. Hytönen and J. A. Ihalainen, Connection between absorption properties and conformational changes in Deinococcus radiodurans phytochrome, Biochemistry 2014 53 7076–7085, DOI: 10.1021/bi501180s
E. A. Stojkovic, K. C. Toh, M. T. Alexandre, M. Baclayon, K. Moffat and J. T. Kennis, FTIR Spectroscopy Revealing Light-Dependent Refolding of the Conserved Tongue Region of Bacteriophytochrome, J. Phys. Chem. Lett. 2014 5 2512–2515, DOI: 10.1021/jz501189t
X. Yang, J. Kuk and K. Moffat, Conformational differences between the Pfr and Pr states in Pseudomonas aeruginosa bacteriophytochrome, Proc. Natl. Acad. Sci. U. S. A. 2009 106 15639–15644, DOI: 10.1073/pnas.0902178106
K. Anders, G. Daminelli-Widany, M. A. Mroginski, D. von Stetten and L. O. Essen, Structure of the cyanobacterial phytochrome 2 photosensor implies a tryptophan switch for phytochrome signaling, J. Biol. Chem. 2013 288 35714–35725, DOI: 10.1074/jbc.M113.510461
J. C. Sanchez, M. Carrillo, S. Pandey, M. Noda, L. Aldama, D. Feliz, E. Claesson, W. Y. Wahlgren, G. Tracy, P. Duong, A. C. Nugent, A. Field, V. Srajer, C. Kupitz, S. Iwata, E. Nango, R. Tanaka, T. Tanaka, L. Fangjia, K. Tono, S. Owada, S. Westenhoff, M. Schmidt and E. A. Stojkovic, High-resolution crystal structures of a myxobacterial phytochrome at cryo and room temperatures, Struct. Dyn. 2019 6 054701, DOI: 10.1063/1.5120527
H. Takala, S. Niebling, O. Berntsson, A. Björling, H. Lehtivuori, H. Hakkanen, M. Panman, E. Gustavsson, M. Hoernke, G. Newby, F. Zontone, M. Wulff, A. Menzel, J. A. Ihalainen and S. Westenhoff, Light-induced structural changes in a monomeric bacteriophytochrome, Struct. Dyn. 2016 3 054701, DOI: 10.1063/1.4961911
T. E. Assafa, K. Anders, U. Linne, L. O. Essen and E. Bordignon, Light-Driven Domain Mechanics of a Minimal Phytochrome Photosensory Module Studied by EPR, Structure 2018 26 1534–1545
V. Anantharaman, S. Balaji and L. Aravind, The signaling helix: a common functional theme in diverse signaling proteins, Biol. Direct 2006 1 25, DOI: 10.1186/1745-6150-1-25
S. Kacprzak, I. Njimona, A. Renz, J. Feng, E. Reijerse, W. Lubitz, N. Krauss, P. Scheerer, S. Nagano, T. Lamparter and S. Weber, Intersubunit distances in full-length, dimeric, bacterial phytochrome Agp1, as measured by pulsed electron-electron double resonance (PELDOR) between different spin label positions, remain unchanged upon photoconversion, J. Biol. Chem. 2017 292 7598–7606, DOI: 10.1074/jbc.M116.761882
M. P. Bhate, K. S. Molnar, M. Goulian and W. F. DeGrado, Signal transduction in histidine kinases: insights from new structures, Structure 2015 23 981–994, DOI: 10.1016/j.str.2015.04.002
S. Nagano, From photon to signal in phytochromes: similarities and differences between prokaryotic and plant phytochromes, J. Plant Res. 2016 129 123–135, DOI: 10.1007/s10265-016-0789-0
A. Moglich, Signal transduction in photoreceptor histidine kinases, Protein Sci. 2019 28 1923–1946, DOI: 10.1002/pro.3705
L. E. Ulrich and I. B. Zhulin, The MiST2 database: a comprehensive genomics resource on microbial signal transduction, Nucleic Acids Res. 2010 38 401, DOI: 10.1093/nar/gkp940
J. S. Parkinson, Signal transduction schemes of bacteria, Cell 1993 73 857–871, DOI: 10.1016/0092-8674(93)90267-t
A. H. West and A. M. Stock, Histidine kinases and response regulator proteins in two-component signaling systems, Trends Biochem. Sci. 2001 26 369–376, DOI: 10.1016/s0968-0004(01)01852-7
P. Casino, V. Rubio and A. Marina, Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction, Cell 2009 139 325–336, DOI: 10.1016/j.cell.2009.08.032
B. Zienicke, I. Molina, R. Glenz, P. Singer, D. Ehmer, F. V. Escobar, P. Hildebrandt, R. Diller and T. Lamparter, Unusual spectral properties of bacteriophytochrome Agp2 result from a deprotonation of the chromophore in the red-absorbing form Pr, J. Biol. Chem. 2013 288 31738–31751, DOI: 10.1074/jbc.M113.479535
T. Hubschmann, H. J. Jorissen, T. Borner, W. Gartner, N. Tandeau de Marsac, Phosphorylation of proteins in the light-dependent signalling pathway of a filamentous cyanobacterium, Eur. J. Biochem. 2001 268 3383–3389, DOI: 10.1046/j.1432-1327.2001.02229.x
T. Lamparter, B. Esteban and J. Hughes, Phytochrome Cph1 from the cyanobacterium Synechocystis PCC6803. Purification, assembly, and quaternary structure, Eur. J. Biochem. 2001 268 4720–4730, DOI: 10.1046/j.1432-1327.2001.02395.x
B. Esteban, M. Carrascal, J. Abian and T. Lamparter, Light-induced conformational changes of cyanobacterial phytochrome Cph1 probed by limited proteolysis and autophosphorylation, Biochemistry 2005 44 450–461, DOI: 10.1021/bi0484365
E. Giraud, S. Zappa, L. Vuillet, J. M. Adriano, L. Hannibal, J. Fardoux, C. Berthomieu, P. Bouyer, D. Pignol and A. Vermeglio, A new type of bacteriophytochrome acts in tandem with a classical bacteriophytochrome to control the antennae synthesis in Rhodopseudomonas palustris, J. Biol. Chem. 2005 280 32389–32397, DOI: 10.1074/jbc.M506890200
K. Evans, J. G. Grossmann, A. P. Fordham-Skelton and M. Z. Papiz, Small-angle X-ray scattering reveals the solution structure of a bacteriophytochrome in the catalytically active Pr state, J. Mol. Biol. 2006 364 655–666, DOI: 10.1016/j.jmb.2006.09.045
H. Takala, A. Björling, M. Linna, S. Westenhoff and J. A. Ihalainen, Light-induced Changes in the Dimerization Interface of Bacteriophytochromes, J. Biol. Chem. 2015 290 16383–16392, DOI: 10.1074/jbc.M115.650127
S. Etzl, R. Lindner, M. D. Nelson and A. Winkler, Structure-guided design and functional characterization of an artificial red light-regulated guanylate/adenylate cyclase for optogenetic applications, J. Biol. Chem. 2018 293 9078–9089, DOI: 10.1074/jbc.RA118.003069
H. R. Bonomi, L. Toum, G. Sycz, R. Sieira, A. M. Toscani, G. E. Gudesblat, F. C. Leskow, F. A. Goldbaum, A. A. Vojnov and F. Malamud, Xanthomonas campestris attenuates virulence by sensing light through a bacteriophytochrome photoreceptor, EMBO Rep. 2016 17 1565–1577, DOI: 10.15252/embr.201541691
N. Ausmees, R. Mayer, H. Weinhouse, G. Volman, D. Amikam, M. Benziman and M. Lindberg, Genetic data indicate that proteins containing the GGDEF domain possess diguanylate cyclase activity, FEMS Microbiol. Lett. 2001 204 163–167, DOI: 10.1111/j.1574-6968.2001.tb10880.x
A. Marina, C. D. Waldburger and W. A. Hendrickson, Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein, EMBO J. 2005 24 4247–4259
S. Yamada, H. Sugimoto, M. Kobayashi, A. Ohno, H. Nakamura and Y. Shiro, Structure of PAS-linked histidine kinase and the response regulator complex, Structure 2009 17 1333–1344, DOI: 10.1016/j.str.2009.07.016
O. Berntsson, R. P. Diensthuber, M. R. Panman, A. Björling, E. Gustavsson, M. Hoernke, A. J. Hughes, L. Henry, S. Niebling, H. Takala, J. A. Ihalainen, G. Newby, S. Kerruth, J. Heberle, M. Liebi, A. Menzel, R. Henning, I. Kosheleva, A. Moglich and S. Westenhoff, Sequential conformational transitions and alpha-helical supercoiling regulate a sensor histidine kinase, Nat. Commun. 2017 8 284–285, DOI: 10.1038/s41467-017-00300-5
I. Gushchin, I. Melnikov, V. Polovinkin, A. Ishchenko, A. Yuzhakova, P. Buslaev, G. Bourenkov, S. Grudinin, E. Round, T. Balandin, V. Borshchevskiy, D. Willbold, G. Leonard, G. Buldt, A. Popov and V. Gordeliy, Mechanism of transmembrane signaling by sensor histidine kinases, Science 2017 356(6342) eaah6345, DOI: 10.1126/science.aah6345
T. Matsushita, N. Mochizuki and A. Nagatani, Dimers of the N-terminal domain of phytochrome B are functional in the nucleus, Nature 2003 424 571–574, DOI: 10.1038/nature01837
Y. Oka, T. Matsushita, N. Mochizuki, T. Suzuki, S. Tokutomi and A. Nagatani, Functional analysis of a 450-amino acid N-terminal fragment of phytochrome B in Arabidopsis, Plant Cell 2004 16 2104–2116, DOI: 10.1105/tpc.104.022350
N. De, M. V. Navarro, R. V. Raghavan and H. Sondermann, Determinants for the activation and autoinhibition of the diguanylate cyclase response regulator WspR, J. Mol. Biol. 2009 393 619–633, DOI: 10.1016/j.jmb.2009.08.030
T. Schirmer and U. Jenal, Structural and mechanistic determinants of c-di-GMP signalling, Nat. Rev. Microbiol. 2009 7 724–735, DOI: 10.1038/nrmicro2203
S. Lim, Q. Yu, S. M. Gottlieb, C. W. Chang, N. C. Rockwell, S. S. Martin, D. Madsen, J. C. Lagarias, D. S. Larsen and J. B. Ames, Correlating structural and photochemical heterogeneity in cyanobacteriochrome NpR6012g4, Proc. Natl. Acad. Sci. U. S. A. 2018 115 4387–4392, DOI: 10.1073/pnas.1720682115
E. Gustavsson, L. Isaksson, C. Persson, M. Mayzel, U. Brath, L. Vrhovac, J. A. Ihalainen, B. G. Karlsson, V. Orekhov and S. Westenhoff, Modulation of Structural Heterogeneity Controls Phytochrome Photoswitching, Biophys. J. 2020 118 415–421, DOI: 10.1016/j.bpj.2019.11.025
C. Song, T. Rohmer, M. Tiersch, J. Zaanen, J. Hughes and J. Matysik, Solid-state NMR spectroscopy to probe photoactivation in canonical phytochromes, Photochem. Photobiol. 2013 89 259–273, DOI: 10.1111/php.12029; 10.1111/php.12029
H. N. Chapman, P. Fromme, A. Barty, T. A. White, R. A. Kirian, A. Aquila, M. S. Hunter, J. Schulz, D. P. DePonte, U. Weierstall, R. B. Doak, F. R. Maia, A. V. Martin, I. Schlichting, L. Lomb, N. Coppola, R. L. Shoeman, S. W. Epp, R. Hartmann, D. Rolles, A. Rudenko, L. Foucar, N. Kimmel, G. Weidenspointner, P. Holl, M. Liang, M. Barthelmess, C. Caleman, S. Boutet, M. J. Bogan, J. Krzywinski, C. Bostedt, S. Bajt, L. Gumprecht, B. Rudek, B. Erk, C. Schmidt, A. Homke, C. Reich, D. Pietschner, L. Struder, G. Hauser, H. Gorke, J. Ullrich, S. Herrmann, G. Schaller, F. Schopper, H. Soltau, K. U. Kuhnel, M. Messerschmidt, J. D. Bozek, S. P. Hau-Riege, M. Frank, C. Y. Hampton, R. G. Sierra, D. Starodub, G. J. Williams, J. Hajdu, N. Timneanu, M. M. Seibert, J. Andreasson, A. Rocker, O. Jonsson, M. Svenda, S. Stern, K. Nass, R. Andritschke, C. D. Schroter, F. Krasniqi, M. Bott, K. E. Schmidt, X. Wang, I. Grotjohann, J. M. Holton, T. R. Barends, R. Neutze, S. Marchesini, R. Fromme, S. Schorb, D. Rupp, M. Adolph, T. Gorkhover, I. Andersson, H. Hirsemann, G. Potdevin, H. Graafsma, B. Nilsson and J. C. Spence, Femtosecond X-ray protein nanocrystallography, Nature 2011 470 73–77, DOI: 10.1038/nature09750
F. Stellato, D. Oberthur, M. Liang, R. Bean, C. Gati, O. Yefanov, A. Barty, A. Burkhardt, P. Fischer, L. Galli, R. A. Kirian, J. Meyer, S. Panneerselvam, C. H. Yoon, F. Chervinskii, E. Speller, T. A. White, C. Betzel, A. Meents and H. N. Chapman, Room-temperature macromolecular serial crystallography using synchrotron radiation, IUCrJ 2014 1 204–212, DOI: 10.1107/S2052252514010070
N. Coquelle, A. S. Brewster, U. Kapp, A. Shilova, B. Weinhausen, M. Burghammer and J. P. Colletier, Raster-scanning serial protein crystallography using micro- and nano-focused synchrotron beams, Acta Crystallogr., Sect. D: Biol. Crystallogr. 2015 71 1184–1196, DOI: 10.1107/S1399004715004514
P. Nogly, D. James, D. Wang, T. A. White, N. Zatsepin, A. Shilova, G. Nelson, H. Liu, L. Johansson, M. Heymann, K. Jaeger, M. Metz, C. Wickstrand, W. Wu, P. Bath, P. Berntsen, D. Oberthuer, V. Panneels, V. Cherezov, H. Chapman, G. Schertler, R. Neutze, J. Spence, I. Moraes, M. Burghammer, J. Standfuss and U. Weierstall, Lipidic cubic phase serial millisecond crystallography using synchrotron radiation, IUCrJ 2015 2 168–176, DOI: 10.1107/S2052252514026487
R. Neutze, R. Wouts, D. van der Spoel, E. Weckert and J. Hajdu, Potential for biomolecular imaging with femtosecond X-ray pulses, Nature 2000 406 752–757, DOI: 10.1038/35021099
J. Tenboer, S. Basu, N. Zatsepin, K. Pande, D. Milathianaki, M. Frank, M. Hunter, S. Boutet, G. J. Williams, J. E. Koglin, D. Oberthuer, M. Heymann, C. Kupitz, C. Conrad, J. Coe, S. Roy-Chowdhury, U. Weierstall, D. James, D. Wang, T. Grant, A. Barty, O. Yefanov, J. Scales, C. Gati, C. Seuring, V. Srajer, R. Henning, P. Schwander, R. Fromme, A. Ourmazd, K. Moffat, J. J. Van Thor, J. C. Spence, P. Fromme, H. N. Chapman and M. Schmidt, Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein, Science 2014 346 1242–1246, DOI: 10.1126/science.1259357
E. S. Burgie, J. A. Clinger, M. D. Miller, A. S. Brewster, P. Aller, A. Butryn, F. D. Fuller, S. Gul, I. D. Young, C. C. Pham, I. S. Kim, A. Bhowmick, L. J. O’Riordan, K. D. Sutherlin, J. V. Heinemann, A. Batyuk, R. Alonso-Mori, M. S. Hunter, J. E. Koglin, J. Yano, V. K. Yachandra, N. K. Sauter, A. E. Cohen, J. Kern, A. M. Orville, G. N. Phillips and R. D. Vierstra, Photoreversible interconversion of a phytochrome photosensory module in the crystalline state, Proc. Natl. Acad. Sci. U. S. A. 2020 117 300–307, DOI: 10.1073/pnas.1912041116
D. von Stetten, M. Gunther, P. Scheerer, D. H. Murgida, M. A. Mroginski, N. Krauss, T. Lamparter, J. Zhang, D. M. Anstrom, R. D. Vierstra, K. T. Forest and P. Hildebrandt, Chromophore heterogeneity and photoconversion in phytochrome crystals and solution studied by resonance Raman spectroscopy, Angew. Chem., Int. Ed. 2008 47 4753–4755, DOI: 10.1002/anie.200705716
P. W. Kim, N. C. Rockwell, S. S. Martin, J. C. Lagarias and D. S. Larsen, Dynamic inhomogeneity in the photodynamics of cyanobacterial phytochrome Cph1, Biochemistry 2014 53 2818–2826, DOI: 10.1021/bi500108s
F. Velazquez Escobar, D. von Stetten, M. Gunther-Lutkens, A. Keidel, N. Michael, T. Lamparter, L. O. Essen, J. Hughes, W. Gartner, Y. Yang, K. Heyne, M. A. Mroginski and P. Hildebrandt, Conformational heterogeneity of the Pfr chromophore in plant and cyanobacterial phytochromes, Front. Mol. Biosci. 2015 2 37, DOI: 10.3389/fmolb.2015.00037
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution-NonCommercial 3.0 License, which permits any non-commercial use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.
The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.
To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc/3.0/.
About this article
Cite this article
Takala, H., Edlund, P., Ihalainen, J.A. et al. Tips and turns of bacteriophytochrome photoactivation. Photochem Photobiol Sci 19, 1488–1510 (2020). https://doi.org/10.1039/d0pp00117a
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1039/d0pp00117a