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* Residue conservation analysis
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Enzyme class:
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E.C.2.7.13.3
- Histidine kinase.
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Reaction:
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ATP + protein L-histidine = ADP + protein N-phospho-L-histidine
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ATP
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+
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protein L-histidine
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=
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ADP
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+
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protein N-phospho-L-histidine
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Molecule diagrams generated from .mol files obtained from the
KEGG ftp site
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Gene Ontology (GO) functional annotation
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Biological process
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signal transduction
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5 terms
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Biochemical function
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signal transducer activity
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2 terms
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DOI no:
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Nature
438:325-331
(2005)
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PubMed id:
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A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome.
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J.R.Wagner,
J.S.Brunzelle,
K.T.Forest,
R.D.Vierstra.
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ABSTRACT
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Phytochromes are red/far-red light photoreceptors that direct photosensory
responses across the bacterial, fungal and plant kingdoms. These include
photosynthetic potential and pigmentation in bacteria as well as chloroplast
development and photomorphogenesis in plants. Phytochromes consist of an
amino-terminal region that covalently binds a single bilin chromophore, followed
by a carboxy-terminal dimerization domain that often transmits the light signal
through a histidine kinase relay. Here we describe the three-dimensional
structure of the chromophore-binding domain of Deinococcus radiodurans
phytochrome assembled with its chromophore biliverdin in the Pr ground state.
Our model, refined to 2.5 A resolution, reaffirms Cys 24 as the chromophore
attachment site, locates key amino acids that form a solvent-shielded
bilin-binding pocket, and reveals an unusually formed deep trefoil knot that
stabilizes this region. The structure provides the first three-dimensional
glimpse into the photochromic behaviour of these photoreceptors and helps to
explain the evolution of higher plant phytochromes from prokaryotic precursors.
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Selected figure(s)
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Figure 2.
Figure 2: Structure of the deep trefoil knot. a, A
semi-continuous -sheet
'snake' is formed by the PAS (blue) and GAF (green) domains and
the polypeptide knot, with Arg 254, Ser 272 and Ser 274 stepping
across the chromophore via propionate side chains of rings B and
C. b, Conserved side chains from both the N-terminal extension
(blue) and the GAF-inserted lasso (yellow) form the small
hydrophobic core within the knot. c, Stereo depiction of the
'knot' region of the final refined model superimposed on the
experimental F[o] electron density map, contoured in green at
1.0 .
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Figure 3.
Figure 3: Structure and linkage of biliverdin within DrCBD.
a, Biliverdin, attached at C3^2 in the A ring, adopts a
5Z[syn],10Z[syn],15Z[anti] configuration. Inset, the A-ring
structure for the bilin chromophore before covalent attachment
to phytochrome differs for P B
(plants) and PCB (cyanobacteria) as compared to biliverdin
(bacteria). b, Final refined model of biliverdin is superimposed
on the 2F[o] - F[c] electron density map contoured at 1.0 .
c, The biliverdin-binding pocket, shown here in stereo, is
formed largely by invariant GAF domain residues (stick figure
colour scheme as for Fig. 1a).
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The above figures are
reprinted
by permission from Macmillan Publishers Ltd:
Nature
(2005,
438,
325-331)
copyright 2005.
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Figures were
selected
by an automated process.
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Literature references that cite this PDB file's key reference
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PubMed id
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Reference
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A.Strambi,
and
B.Durbeej
(2011).
Initial excited-state relaxation of the bilin chromophores of phytochromes: a computational study.
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Photochem Photobiol Sci, 10,
569-579.
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M.E.Auldridge,
and
K.T.Forest
(2011).
Bacterial phytochromes: More than meets the light.
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Crit Rev Biochem Mol Biol, 46,
67-88.
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M.H.Cho,
Y.Yoo,
S.H.Bhoo,
and
S.W.Lee
(2011).
Purification and Characterization of a Recombinant Bacteriophytochrome of Xanthomonas oryzae pathovar oryzae.
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Protein J, 30,
124-131.
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A.Möglich,
and
K.Moffat
(2010).
Engineered photoreceptors as novel optogenetic tools.
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Photochem Photobiol Sci, 9,
1286-1300.
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|
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A.Möglich,
X.Yang,
R.A.Ayers,
and
K.Moffat
(2010).
Structure and function of plant photoreceptors.
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Annu Rev Plant Biol, 61,
21-47.
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A.T.Ulijasz,
G.Cornilescu,
C.C.Cornilescu,
J.Zhang,
M.Rivera,
J.L.Markley,
and
R.D.Vierstra
(2010).
Structural basis for the photoconversion of a phytochrome to the activated Pfr form.
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Nature, 463,
250-254.
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PDB codes:
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H.Li,
J.Zhang,
R.D.Vierstra,
and
H.Li
(2010).
Quaternary organization of a phytochrome dimer as revealed by cryoelectron microscopy.
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Proc Natl Acad Sci U S A, 107,
10872-10877.
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J.Rodriguez-Romero,
M.Hedtke,
C.Kastner,
S.Müller,
and
R.Fischer
(2010).
Fungi, hidden in soil or up in the air: light makes a difference.
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Annu Rev Microbiol, 64,
585-610.
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J.Wang,
B.Yan,
G.Chen,
Y.Su,
and
T.Wang
(2010).
Adaptive evolution in the GAF domain of phytochromes in gymnosperms.
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Biochem Genet, 48,
236-247.
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K.C.Toh,
E.A.Stojkovic,
I.H.van Stokkum,
K.Moffat,
and
J.T.Kennis
(2010).
Proton-transfer and hydrogen-bond interactions determine fluorescence quantum yield and photochemical efficiency of bacteriophytochrome.
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Proc Natl Acad Sci U S A, 107,
9170-9175.
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M.Röben,
J.Hahn,
E.Klein,
T.Lamparter,
G.Psakis,
J.Hughes,
and
P.Schmieder
(2010).
NMR spectroscopic investigation of mobility and hydrogen bonding of the chromophore in the binding pocket of phytochrome proteins.
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Chemphyschem, 11,
1248-1257.
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N.C.Rockwell,
and
J.C.Lagarias
(2010).
A brief history of phytochromes.
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Chemphyschem, 11,
1172-1180.
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P.Piwowarski,
E.Ritter,
K.P.Hofmann,
P.Hildebrandt,
D.von Stetten,
P.Scheerer,
N.Michael,
T.Lamparter,
and
F.Bartl
(2010).
Light-induced activation of bacterial phytochrome Agp1 monitored by static and time-resolved FTIR spectroscopy.
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Chemphyschem, 11,
1207-1214.
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P.Scheerer,
N.Michael,
J.H.Park,
S.Nagano,
H.W.Choe,
K.Inomata,
B.Borucki,
N.Krauss,
and
T.Lamparter
(2010).
Light-induced conformational changes of the chromophore and the protein in phytochromes: bacterial phytochromes as model systems.
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Chemphyschem, 11,
1090-1105.
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T.Rohmer,
C.Lang,
W.Gärtner,
J.Hughes,
and
J.Matysik
(2010).
Role of the protein cavity in phytochrome chromoprotein assembly and double-bond isomerization: a comparison with model compounds.
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Photochem Photobiol, 86,
856-861.
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A.Möglich,
R.A.Ayers,
and
K.Moffat
(2009).
Structure and signaling mechanism of Per-ARNT-Sim domains.
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Structure, 17,
1282-1294.
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A.T.Ulijasz,
G.Cornilescu,
D.von Stetten,
C.Cornilescu,
F.Velazquez Escobar,
J.Zhang,
R.J.Stankey,
M.Rivera,
P.Hildebrandt,
and
R.D.Vierstra
(2009).
Cyanochromes are blue/green light photoreversible photoreceptors defined by a stable double cysteine linkage to a phycoviolobilin-type chromophore.
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J Biol Chem, 284,
29757-29772.
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B.Borucki,
and
T.Lamparter
(2009).
A polarity probe for monitoring light-induced structural changes at the entrance of the chromophore pocket in a bacterial phytochrome.
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J Biol Chem, 284,
26005-26016.
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B.Durbeej
(2009).
On the primary event of phytochrome: quantum chemical comparison of photoreactions at C(4), C(10) and C(15).
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Phys Chem Chem Phys, 11,
1354-1361.
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E.A.Kikis,
Y.Oka,
M.E.Hudson,
A.Nagatani,
and
P.H.Quail
(2009).
Residues clustered in the light-sensing knot of phytochrome B are necessary for conformer-specific binding to signaling partner PIF3.
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PLoS Genet, 5,
e1000352.
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J.Mailliet,
G.Psakis,
C.Schroeder,
S.Kaltofen,
U.Dürrwang,
J.Hughes,
and
L.O.Essen
(2009).
Dwelling in the dark: procedures for the crystallography of phytochromes and other photochromic proteins.
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Acta Crystallogr D Biol Crystallogr, 65,
1232-1235.
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M.A.Mroginski,
D.von Stetten,
F.V.Escobar,
H.M.Strauss,
S.Kaminski,
P.Scheerer,
M.Günther,
D.H.Murgida,
P.Schmieder,
C.Bongards,
W.Gärtner,
J.Mailliet,
J.Hughes,
L.O.Essen,
and
P.Hildebrandt
(2009).
Chromophore structure of cyanobacterial phytochrome Cph1 in the Pr state: reconciling structural and spectroscopic data by QM/MM calculations.
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Biophys J, 96,
4153-4163.
|
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N.C.Rockwell,
L.Shang,
S.S.Martin,
and
J.C.Lagarias
(2009).
Distinct classes of red/far-red photochemistry within the phytochrome superfamily.
|
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Proc Natl Acad Sci U S A, 106,
6123-6127.
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R.Narikawa,
N.Muraki,
T.Shiba,
M.Ikeuchi,
and
G.Kurisu
(2009).
Crystallization and preliminary X-ray studies of the chromophore-binding domain of cyanobacteriochrome AnPixJ from Anabaena sp. PCC 7120.
|
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Acta Crystallogr Sect F Struct Biol Cryst Commun, 65,
159-162.
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S.Yamada,
H.Sugimoto,
M.Kobayashi,
A.Ohno,
H.Nakamura,
and
Y.Shiro
(2009).
Structure of PAS-linked histidine kinase and the response regulator complex.
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Structure, 17,
1333-1344.
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PDB codes:
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T.Bornschlögl,
D.M.Anstrom,
E.Mey,
J.Dzubiella,
M.Rief,
and
K.T.Forest
(2009).
Tightening the knot in phytochrome by single-molecule atomic force microscopy.
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Biophys J, 96,
1508-1514.
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X.Shu,
A.Royant,
M.Z.Lin,
T.A.Aguilera,
V.Lev-Ram,
P.A.Steinbach,
and
R.Y.Tsien
(2009).
Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome.
|
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Science, 324,
804-807.
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A.T.Ulijasz,
G.Cornilescu,
D.von Stetten,
S.Kaminski,
M.A.Mroginski,
J.Zhang,
D.Bhaya,
P.Hildebrandt,
and
R.D.Vierstra
(2008).
Characterization of two thermostable cyanobacterial phytochromes reveals global movements in the chromophore-binding domain during photoconversion.
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J Biol Chem, 283,
21251-21266.
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C.Bongards,
and
W.Gärtner
(2008).
Interactions between chromophore and protein in phytochrome identified by novel oxa-, thia- and carba-chromophores.
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Photochem Photobiol, 84,
1109-1117.
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C.C.Heikaus,
J.R.Stout,
M.R.Sekharan,
C.M.Eakin,
P.Rajagopal,
P.S.Brzovic,
J.A.Beavo,
and
R.E.Klevit
(2008).
Solution structure of the cGMP binding GAF domain from phosphodiesterase 5: insights into nucleotide specificity, dimerization, and cGMP-dependent conformational change.
|
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J Biol Chem, 283,
22749-22759.
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PDB code:
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C.Schumann,
R.Gross,
M.M.Wolf,
R.Diller,
N.Michael,
and
T.Lamparter
(2008).
Subpicosecond midinfrared spectroscopy of the Pfr reaction of phytochrome Agp1 from Agrobacterium tumefaciens.
|
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Biophys J, 94,
3189-3197.
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D.L.Filiault,
C.A.Wessinger,
J.R.Dinneny,
J.Lutes,
J.O.Borevitz,
D.Weigel,
J.Chory,
and
J.N.Maloof
(2008).
Amino acid polymorphisms in Arabidopsis phytochrome B cause differential responses to light.
|
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Proc Natl Acad Sci U S A, 105,
3157-3162.
|
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E.Giraud,
and
A.Verméglio
(2008).
Bacteriophytochromes in anoxygenic photosynthetic bacteria.
|
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Photosynth Res, 97,
141-153.
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G.Bae,
and
G.Choi
(2008).
Decoding of light signals by plant phytochromes and their interacting proteins.
|
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Annu Rev Plant Biol, 59,
281-311.
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G.Cornilescu,
A.T.Ulijasz,
C.C.Cornilescu,
J.L.Markley,
and
R.D.Vierstra
(2008).
Solution structure of a cyanobacterial phytochrome GAF domain in the red-light-absorbing ground state.
|
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J Mol Biol, 383,
403-413.
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PDB codes:
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H.Scheer,
and
K.H.Zhao
(2008).
Biliprotein maturation: the chromophore attachment.
|
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Mol Microbiol, 68,
263-276.
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J.M.Lee,
H.Y.Cho,
H.J.Cho,
I.J.Ko,
S.W.Park,
H.S.Baik,
J.H.Oh,
C.Y.Eom,
Y.M.Kim,
B.S.Kang,
and
J.I.Oh
(2008).
O2- and NO-sensing mechanism through the DevSR two-component system in Mycobacterium smegmatis.
|
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J Bacteriol, 190,
6795-6804.
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PDB codes:
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J.R.Wagner,
J.Zhang,
D.von Stetten,
M.Günther,
D.H.Murgida,
M.A.Mroginski,
J.M.Walker,
K.T.Forest,
P.Hildebrandt,
and
R.D.Vierstra
(2008).
Mutational analysis of Deinococcus radiodurans bacteriophytochrome reveals key amino acids necessary for the photochromicity and proton exchange cycle of phytochromes.
|
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J Biol Chem, 283,
12212-12226.
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L.M.Podust,
A.Ioanoviciu,
and
P.R.Ortiz de Montellano
(2008).
2.3 A X-ray structure of the heme-bound GAF domain of sensory histidine kinase DosT of Mycobacterium tuberculosis.
|
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Biochemistry, 47,
12523-12531.
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PDB code:
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L.O.Essen,
J.Mailliet,
and
J.Hughes
(2008).
The structure of a complete phytochrome sensory module in the Pr ground state.
|
| |
Proc Natl Acad Sci U S A, 105,
14709-14714.
|
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PDB code:
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M.G.Müller,
I.Lindner,
I.Martin,
W.Gärtner,
and
A.R.Holzwarth
(2008).
Femtosecond kinetics of photoconversion of the higher plant photoreceptor phytochrome carrying native and modified chromophores.
|
| |
Biophys J, 94,
4370-4382.
|
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|
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|
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M.Ikeuchi,
and
T.Ishizuka
(2008).
Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria.
|
| |
Photochem Photobiol Sci, 7,
1159-1167.
|
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|
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|
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N.C.Rockwell,
S.L.Njuguna,
L.Roberts,
E.Castillo,
V.L.Parson,
S.Dwojak,
J.C.Lagarias,
and
S.C.Spiller
(2008).
A second conserved GAF domain cysteine is required for the blue/green photoreversibility of cyanobacteriochrome Tlr0924 from Thermosynechococcus elongatus.
|
| |
Biochemistry, 47,
7304-7316.
|
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N.Handa,
E.Mizohata,
S.Kishishita,
M.Toyama,
S.Morita,
T.Uchikubo-Kamo,
R.Akasaka,
K.Omori,
J.Kotera,
T.Terada,
M.Shirouzu,
and
S.Yokoyama
(2008).
Crystal structure of the GAF-B domain from human phosphodiesterase 10A complexed with its ligand, cAMP.
|
| |
J Biol Chem, 283,
19657-19664.
|
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PDB code:
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O.Anders Borg,
and
B.Durbeej
(2008).
Which factors determine the acidity of the phytochromobilin chromophore of plant phytochrome?
|
| |
Phys Chem Chem Phys, 10,
2528-2537.
|
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P.Schwinté,
H.Foerstendorf,
Z.Hussain,
W.Gärtner,
M.A.Mroginski,
P.Hildebrandt,
and
F.Siebert
(2008).
FTIR study of the photoinduced processes of plant phytochrome phyA using isotope-labeled bilins and density functional theory calculations.
|
| |
Biophys J, 95,
1256-1267.
|
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|
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R.A.Sharrock
(2008).
The phytochrome red/far-red photoreceptor superfamily.
|
| |
Genome Biol, 9,
230.
|
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|
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R.Narikawa,
T.Kohchi,
and
M.Ikeuchi
(2008).
Characterization of the photoactive GAF domain of the CikA homolog (SyCikA, Slr1969) of the cyanobacterium Synechocystis sp. PCC 6803.
|
| |
Photochem Photobiol Sci, 7,
1253-1259.
|
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|
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|
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S.Brandt,
D.von Stetten,
M.Günther,
P.Hildebrandt,
and
N.Frankenberg-Dinkel
(2008).
The Fungal Phytochrome FphA from Aspergillus nidulans.
|
| |
J Biol Chem, 283,
34605-34614.
|
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|
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|
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S.E.Martinez,
C.C.Heikaus,
R.E.Klevit,
and
J.A.Beavo
(2008).
The structure of the GAF A domain from phosphodiesterase 6C reveals determinants of cGMP binding, a conserved binding surface, and a large cGMP-dependent conformational change.
|
| |
J Biol Chem, 283,
25913-25919.
|
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PDB code:
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T.Rohmer,
C.Lang,
J.Hughes,
L.O.Essen,
W.Gärtner,
and
J.Matysik
(2008).
Light-induced chromophore activity and signal transduction in phytochromes observed by 13C and 15N magic-angle spinning NMR.
|
| |
Proc Natl Acad Sci U S A, 105,
15229-15234.
|
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|
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X.Yang,
J.Kuk,
and
K.Moffat
(2008).
Crystal structure of Pseudomonas aeruginosa bacteriophytochrome: photoconversion and signal transduction.
|
| |
Proc Natl Acad Sci U S A, 105,
14715-14720.
|
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|
PDB code:
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Y.Hirose,
T.Shimada,
R.Narikawa,
M.Katayama,
and
M.Ikeuchi
(2008).
Cyanobacteriochrome CcaS is the green light receptor that induces the expression of phycobilisome linker protein.
|
| |
Proc Natl Acad Sci U S A, 105,
9528-9533.
|
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|
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Y.Oka,
T.Matsushita,
N.Mochizuki,
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Mutant screen distinguishes between residues necessary for light-signal perception and signal transfer by phytochrome B.
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PLoS Genet, 4,
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B.L.Montgomery
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Sensing the light: photoreceptive systems and signal transduction in cyanobacteria.
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FEBS J, 274,
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C.Natori,
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Photochem Photobiol Sci, 6,
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Chemphyschem, 8,
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Biophys J, 93,
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(2007).
Discovery of a thermophilic protein complex stabilized by topologically interlinked chains.
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J Mol Biol, 368,
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PDB code:
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D.von Stetten,
S.Seibeck,
N.Michael,
P.Scheerer,
M.A.Mroginski,
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M.P.Heyn,
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and
T.Lamparter
(2007).
Highly conserved residues Asp-197 and His-250 in Agp1 phytochrome control the proton affinity of the chromophore and Pfr formation.
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J Biol Chem, 282,
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H.Szurmant,
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Sensor complexes regulating two-component signal transduction.
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Curr Opin Struct Biol, 17,
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J.Hahn,
R.Kühne,
and
P.Schmieder
(2007).
Solution-state (15)N NMR spectroscopic study of alpha-C-phycocyanin: implications for the structure of the chromophore-binding pocket of the cyanobacterial phytochrome Cph1.
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Chembiochem, 8,
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J.R.Wagner,
J.Zhang,
J.S.Brunzelle,
R.D.Vierstra,
and
K.T.Forest
(2007).
High resolution structure of Deinococcus bacteriophytochrome yields new insights into phytochrome architecture and evolution.
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J Biol Chem, 282,
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PDB codes:
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L.Vuillet,
M.Kojadinovic,
S.Zappa,
M.Jaubert,
J.M.Adriano,
J.Fardoux,
L.Hannibal,
D.Pignol,
A.Verméglio,
and
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(2007).
Evolution of a bacteriophytochrome from light to redox sensor.
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EMBO J, 26,
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M.A.Mroginski,
F.Mark,
W.Thiel,
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Quantum mechanics/molecular mechanics calculation of the Raman spectra of the phycocyanobilin chromophore in alpha-C-phycocyanin.
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Biophys J, 93,
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M.A.van der Horst,
J.Key,
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Photosensing in chemotrophic, non-phototrophic bacteria: let there be light sensing too.
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Trends Microbiol, 15,
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M.Jaubert,
J.Lavergne,
J.Fardoux,
L.Hannibal,
L.Vuillet,
J.M.Adriano,
P.Bouyer,
D.Pignol,
E.Giraud,
and
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(2007).
A singular bacteriophytochrome acquired by lateral gene transfer.
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J Biol Chem, 282,
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N.C.Rockwell,
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Flexible mapping of homology onto structure with homolmapper.
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BMC Bioinformatics, 8,
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S.A.Trupkin,
D.Debrieux,
A.Hiltbrunner,
C.Fankhauser,
and
J.J.Casal
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The serine-rich N-terminal region of Arabidopsis phytochrome A is required for protein stability.
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| |
Plant Mol Biol, 63,
669-678.
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|
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|
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S.Helaine,
D.H.Dyer,
X.Nassif,
V.Pelicic,
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3D structure/function analysis of PilX reveals how minor pilins can modulate the virulence properties of type IV pili.
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| |
Proc Natl Acad Sci U S A, 104,
15888-15893.
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PDB codes:
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S.Sharda,
R.Shah,
and
W.Gärtner
(2007).
Domain interaction in cyanobacterial phytochromes as a prerequisite for spectral integrity.
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Eur Biophys J, 36,
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T.O.Yeates,
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Knotted and topologically complex proteins as models for studying folding and stability.
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Curr Opin Chem Biol, 11,
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X.Yang,
E.A.Stojkovic,
J.Kuk,
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Crystal structure of the chromophore binding domain of an unusual bacteriophytochrome, RpBphP3, reveals residues that modulate photoconversion.
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| |
Proc Natl Acad Sci U S A, 104,
12571-12576.
|
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PDB code:
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|
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Y.L.Lai,
S.C.Yen,
S.H.Yu,
and
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pKNOT: the protein KNOT web server.
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Nucleic Acids Res, 35,
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Z.Lin,
L.C.Johnson,
H.Weissbach,
N.Brot,
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Free methionine-(R)-sulfoxide reductase from Escherichia coli reveals a new GAF domain function.
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Proc Natl Acad Sci U S A, 104,
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C.W.Hollars,
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Single-molecule dynamics of phytochrome-bound fluorophores probed by fluorescence correlation spectroscopy.
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Proc Natl Acad Sci U S A, 103,
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B.Borucki
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Proton transfer in the photoreceptors phytochrome and photoactive yellow protein.
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Photochem Photobiol Sci, 5,
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G.O.Paiva-Silva,
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E.S.Nakayasu,
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A heme-degradation pathway in a blood-sucking insect.
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Proc Natl Acad Sci U S A, 103,
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Probing protein-chromophore interactions in Cph1 phytochrome by mutagenesis.
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FEBS J, 273,
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Chromophore structure in the photocycle of the cyanobacterial phytochrome Cph1.
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Biophys J, 91,
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J.L.Mateos,
J.P.Luppi,
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V.A.Sineshchekov,
M.J.Yanovsky,
S.E.Braslavsky,
W.Gärtner,
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(2006).
Functional and biochemical analysis of the N-terminal domain of phytochrome A.
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J Biol Chem, 281,
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J.Purschwitz,
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Seeing the rainbow: light sensing in fungi.
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Curr Opin Microbiol, 9,
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M.A.Hammam,
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Assembly of synthetic locked chromophores with agrobacterium phytochromes Agp1 and Agp2.
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J Biol Chem, 281,
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M.Tarutina,
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An unorthodox bacteriophytochrome from Rhodobacter sphaeroides involved in turnover of the second messenger c-di-GMP.
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J Biol Chem, 281,
34751-34758.
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N.C.Rockwell,
Y.S.Su,
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Phytochrome structure and signaling mechanisms.
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Annu Rev Plant Biol, 57,
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P.Virnau,
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Intricate knots in proteins: Function and evolution.
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PLoS Comput Biol, 2,
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S.Mathews
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Phytochrome-mediated development in land plants: red light sensing evolves to meet the challenges of changing light environments.
|
| |
Mol Ecol, 15,
3483-3503.
|
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|
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|
The most recent references are shown first.
Citation data come partly from CiteXplore and partly
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only a partial list as not all journals are covered by
either method. However, we are continually building up the citation data
so more and more references will be included with time.
Where a reference describes a PDB structure, the PDB
codes are
shown on the right.
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