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Structure and Function of Plant Photoreceptors

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DOI: 10.1146/annurev-arplant-042809-112259 · Source: PubMed

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 Structure and Function
of Plant Photoreceptors
Andreas Möglich,1,∗ Xiaojing Yang,1,∗
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

Rebecca A. Ayers,1 and Keith Moffat1,2

1
Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics,
by National Taiwan University on 06/01/10. For personal use only.

University of Chicago, Chicago, Illinois 60637; email: moeglich@uchicago.edu,

xiaojingyang@uchicago.edu, rayers@uchicago.edu
2
Consortium for Advanced Radiation Sources (CARS), University of Chicago, Chicago,
Illinois 60637; email: moffat@cars.uchicago.edu

Annu. Rev. Plant Biol. 2010. 61:21–47 Key Words

First published online as a Review in Advance on cryptochrome, light-oxygen-voltage, photochemistry, phytochrome,
January 25, 2010
rhodopsin, signal transduction
The Annual Review of Plant Biology is online at
plant.annualreviews.org Abstract
This article’s doi: Signaling photoreceptors use the information contained in the ab-
10.1146/annurev-arplant-042809-112259
sorption of a photon to modulate biological activity in plants and a
Copyright  c 2010 by Annual Reviews. wide range of organisms. The fundamental—and as yet imperfectly
All rights reserved
answered—question is, how is this achieved at the molecular level? We
1543-5008/10/0602-0021$20.00 adopt the perspective of biophysicists interested in light-dependent sig-
∗
These authors contributed equally. nal transduction in nature and the three-dimensional structures that
underpin signaling. Six classes of photoreceptors are known: light-
oxygen-voltage (LOV) sensors, xanthopsins, phytochromes, blue-light
sensors using flavin adenine dinucleotide (BLUF), cryptochromes, and
rhodopsins. All are water-soluble proteins except rhodopsins, which
are integral membrane proteins; all are based on a modular architec-
ture except cryptochromes and rhodopsins; and each displays a distinct,
light-dependent chemical process based on the photochemistry of their
nonprotein chromophore, such as isomerization about a double bond
(xanthopsins, phytochromes, and rhodopsins), formation or rupture of
a covalent bond (LOV sensors), or electron transfer (BLUF sensors and
cryptochromes).

21
 rather than the cellular or organismal level of
Contents structure. Important though they surely are,
the influence of these higher levels of structure
INTRODUCTION . . . . . . . . . . . . . . . . . . 22
on the transduction of light into physiological
LIGHT-OXYGEN-VOLTAGE
function or behavior is not yet well understood.
SENSORS . . . . . . . . . . . . . . . . . . . . . . . . 27
Light that will modify behavior is directly
LOV Photochemistry . . . . . . . . . . . . . . 27
absorbed by protein molecules known as
LOV Domain Structure . . . . . . . . . . . . 28
signaling photoreceptors or more simply
LOV Signal Transduction . . . . . . . . . . 29
as photoreceptors. Because membranes are
XANTHOPSINS . . . . . . . . . . . . . . . . . . . . . 30
effectively transparent to light, most photore-
PHYTOCHROMES . . . . . . . . . . . . . . . . . 31
ceptors are cytoplasmic and water soluble. In
Phytochrome Structure . . . . . . . . . . . . 31
other key molecules that absorb light, e.g.,
Phytochrome Photochemistry . . . . . . 32
light-harvesting complexes or photosynthetic
Phytochrome Signal Transduction . . 33
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

reaction centers, the energy derived from ab-

BLUF SENSORS . . . . . . . . . . . . . . . . . . . . 33
sorbing a photon generates an electrochemical
CRYPTOCHROMES . . . . . . . . . . . . . . . . 34
potential gradient across a membrane that
by National Taiwan University on 06/01/10. For personal use only.

Cryptochrome Structure . . . . . . . . . . . 34
can be harnessed to drive energy-requiring
Cryptochrome Photochemistry . . . . . 35
chemical processes. Thus, in contrast to most
Cryptochrome Signal
signaling photoreceptors (but in common with
Transduction . . . . . . . . . . . . . . . . . . . 36
chemoreceptors, whose small molecule ligands
RHODOPSINS . . . . . . . . . . . . . . . . . . . . . . 36
cannot traverse membranes), light-harvesting
Rhodopsin Photochemistry . . . . . . . . . 36
complexes and reaction centers are integral
Rhodopsin Structure . . . . . . . . . . . . . . . 37
membrane proteins. Signaling photoreceptors
Rhodopsin Signal Transduction . . . . . 37
and the more widely studied chemoreceptors
COMMON STRUCTURAL AND
thus have quite different cellular locations
SIGNALING PRINCIPLES. . . . . . . 37
but may retain intriguing similarities in their
PHOTORECEPTOR
signaling properties (99).
BIOTECHNOLOGY . . . . . . . . . . . . . 38
The absorption properties of photorecep-
FUTURE CHALLENGES
tors match the spectrum of light falling
AND OUTLOOK. . . . . . . . . . . . . . . . . 40
on them, typically the solar spectrum at
Earth’s surface extending from the near UV
(∼350 nm) through the blue to the red/far
red (∼750 nm), filtered by, for example, a leaf
INTRODUCTION canopy. Because the polypeptide backbone and
Light is a major developmental cue that amino acid side chains do not absorb in this
generates an initial signal upon absorption of visible range, all photoreceptors contain an or-
a photon of visible light, transmits this signal ganic, nonprotein component known as a chro-
through elaborate molecular and metabolic mophore that serves as the primary site of
pathways, and ultimately modifies the “behav- photon absorption and may be covalently or
ior” of plants: It influences critical aspects of noncovalently bound to the protein. All chro-
development, morphology, and metabolism. mophores are partly unsaturated, thus allow-
In this review, we adopt the perspective of ing electron delocalization across a conjugated
biophysicists interested in processes of light- π system. The larger the chromophore, the
dependent signal transduction in nature and greater is the possible extent of electron delo-
the three-dimensional structures that underpin calization and the longer is the wavelength at
them. We focus on the better-understood which it will absorb. Examples of plant chro-
upstream events closest to the site of photon mophores include flavin adenine dinucleotide
absorption and explore results at the molecular (FAD), which absorbs in the blue, and the

22 Möglich et al.
 linear tetrapyrrole phytochromobilin (PB), modules or domains, each of which forms a co-
which absorbs in the red to far red (Figure 1). valently connected, compactly folded portion of
The presence of chromophores enables vari- the sequence. Domains are linked together by
ous forms of UV/visible spectroscopies to be elements of secondary structure such as α he-
successfully applied. Photoreceptors are com- lices or by extended loops. One or more mod-
monly classified by the chemical nature and ules may bind the chromophore that absorbs
photochemistry of their chromophore and at light and serves as a sensor or input domain; an-
present, six distinct classes are known: light- other may promote dimerization or association
oxygen-voltage (LOV) sensors, xanthopsins, with another protein, small molecule, or mem-
phytochromes, sensors of blue-light utilizing brane; yet another may exhibit light-dependent
FAD (BLUF), cryptochromes, and rhodopsins catalytic activity or DNA binding and serve as
(Figure 1) (146). an effector or output domain, which interacts
The energy contained in a photon in the vis- with one or more components further down-
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

ible spectrum, 40–60 kcal mol−1 , is sufficiently stream in the signaling pathway. The sensor do-
large to easily drive chemical processes such main is usually (but not exclusively) located N-
as electron transfer, formation or rupture of a terminal to the effector domain. Although less
by National Taiwan University on 06/01/10. For personal use only.

covalent chemical bond, or isomerization about emphasis is typically placed on the linker seg-
a double bond, if suitably harnessed. Thus light ments and extensions at the N and C termini,
can readily influence chemistry. Each of these their structures are often also light dependent
processes is accompanied by changes in atomic and play important roles in signal transduc-
position or extent of motion, both of which can tion (99). The modular structure of representa-
change the affinity of one part of the photore- tive photoreceptors from each of the six known
ceptor for another part, or of the photoreceptor classes is illustrated in Figure 2. Some photore-
for another cellular constituent, e.g., a small ceptors such as phototropins, neochrome, and
molecule, protein, DNA, or membrane. A Rhodospirillum centenum Ppr (Figure 2) contain
change in affinity is essentially thermody- two or more chromophores, which introduces
namic in nature; thus a signal possesses both the possibility of interaction between signals.
thermodynamic and structural aspects (99). For example, signals may originate in absorp-
Each chromophore exhibits a specific pho- tion of both blue and red light, or in absorption
tochemistry and photophysics, and particular of blue light and a redox or other chemical sig-
photoreceptors thus utilize different chemical nal. A representative tertiary structure of each
processes. Photoreceptors have evolved to max- class of sensor domain is shown in Figure 3.
imize the quantum yield for generating a signal Comparative genomics suggests that the
and, correspondingly, to minimize the quantum number of different types of domains has been
yields for nonproductive, rapid, competing conserved during evolution; this number is
processes of vibrational/thermal and fluores- roughly the same in the worm, fly, plants,
cence de-excitation. In practice this means that and humans. It appears that individual do-
the initial changes in the excited state of the mains have been substantially conserved in both
chromophore must be efficient, specific, and structure and function, but their combination
very fast, e.g., intersystem crossing, electron into multidomain proteins differs in plants and
transfer, excited state proton transfer, or facile other evolutionarily distant organisms. Thus,
isomerization about one or more double bonds. human proteins contain almost twice the num-
Two features are very characteristic of both ber of multidomain combinations in a single
photoreceptors and chemoreceptors: They are polypeptide chain than do proteins from lower
modular in their architecture, and each module organisms (79). Combinatorial mixing of do-
is associated with a different aspect of receptor mains during evolution apparently has con-
function (110). A photoreceptor typically com- ferred greater phenotypic complexity in sig-
prises several discrete protein units known as naling and regulation (85). Thus, a single class

www.annualreviews.org • Structure and Function of Plant Photoreceptors 23

 a R b O– c O O–
O O–
N N O
D450 NH
pG Pr
N
S O
Cys H N +
H N H
S O Cys S H N O
hν Cys NH
T R
R O
N N O
hν hν hν
L660 NH
N
S O
O O–
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

Cys H
O O–
O–

pB Pfr
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R
N N O N +
H N
S390 O Cys S H R
NH
N NH
H S N
S O H
Cys Cys O O

R R R
d N N O N N O N N O

NH NH NH
N hν N N
H
P H H O FADH• O Pred O
O HN O H 2N OH O
O O NH2

Tyr Gln Tyr Gln Tyr Gln

e R e–, H+ R e– R
N N O hν N N O hν N N– O
FAD NH FADH• NH FADH– NH
N N N
H H O
O O

f Lys hν
D470 N+ P510
H Lys
N+
H

Figure 1
Chromophores and simplified photochemistry of the six photoreceptor classes. (a) Light-oxygen-voltage (LOV). (b) Xanthopsin.
(c) Phytochrome. (d ) Blue-light sensors using FAD (BLUF). (e) Cryptochrome. ( f ) Rhodopsin.

24 Möglich et al.
 a LOV LOV Ser/ThrK Arabidopsis thaliana phototropin 1 (PHOT1_ARATH)

PAS GAF PHY LOV LOV Ser/ThrK Adiantum capillus-veneris neochrome 1 (Q9ZWQ6_ADICA)

LOV F Kelch Arabidopsis thaliana ZEITLUPE (ADO1_ARATH)

bZ LOV Vaucheria frigida aureochrome 1 (A8QW55_9STRA)

PAS LOV Arabidopsis thaliana PAS-LOV (TLOV1_ARATH)

b PYP Halorhodospira halophila PYP (PYP_HALHA)

PYP PAS GAF PHY HisK Rhodospirillum centenum Ppr (Q9X2W8_RHOCE)

c PAS GAF PHY PAS PAS HKRD Arabidopsis thaliana phytochrome A (PHYA_ARATH)

PAS GAF PHY HisK Pseudomonas aeruginosa bacteriophytochrome (BPHY_PSEAE)

Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

PAS GAF PHY HisK RR Rhodopseudomonas palustris bacteriophytochrome 5 (Q6NB40_RHOPA)

d
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BLUF Synechococcus elongatus Tll0078 (Q8DMN3_SYNEL)

BLUF EAL Klebsiella pneumoniae BlrP1 (A6T8V8_KLEPN)

BLUF A/G-cycl. BLUF A/G-cycl. Euglena gracilis photoactivated adenyl cyclase α (PCYAA_EUGGR)

e Photly. FAD CCT Arabidopsis thaliana cryptochrome 1 (CRY1_ARATH)

Photly. FAD Arabidopsis thaliana cryptochrome 3 (CRYD_ARATH)

f Rhodopsin Acetabularia acetabulum rhodopsin (Q1AJZ3_ACEAT)

Rhodopsin Chlamydomonas reinhardtii channelrhodopsin 2 (Q8RUT8_CHLRE)

Rhodopsin HisK RR A/G-cycl. Chlamydomonas reinhardtii chlamyopsin-5 (Q6WRU3_CHLRE)

200 aa

Figure 2
Domain composition of representative photoreceptors of the six classes according to the Pfam database (41). (a) Light-oxygen-voltage
(LOV). (b) Xanthopsin. (c) Phytochrome. (d ) Blue-light sensors using FAD (BLUF). (e) Cryptochrome. ( f ) Rhodopsin. Proteins are
drawn approximately to scale and labeled with their UniProt identifiers (145). Domain abbreviations are Ser/ThrK (serine/threonine
kinase), GAF (GAF domain), PHY (phytochrome), F (F box), Kelch (Kelch repeat), bZ (basic zipper), HisK (histidine kinase), HKRD
(histidine kinase-related domain), RR (response regulator), EAL (diguanylate phosphodiesterase), A/G-cycl. (adenylate/guanylate
cyclase), Photly. (photolyase α/β domain), FAD (photolyase α domain), CCT (cryptochrome C-terminal domain).

of photosensor domain such as the LOV blue- the design of novel sensor molecules. This has
light sensors is found covalently attached to a indeed proved to be the case (81, 98, 133), as
very wide range of effector domains that dif- we discuss below.
fer markedly in their tertiary structure and bi- The modular nature of photoreceptors has
ological activity (28). Conversely, a single class enabled a “divide and conquer” experimental
of effector domains such as phosphodiesterases strategy in which individual domains within a
is found covalently attached to more than one longer, complex photoreceptor are identified,
class of sensor domains, e.g., to LOV or BLUF isolated, and characterized separately in both
domains. The effectiveness of combinatorial structural and functional aspects. The com-
mixing of domains during evolution implies pact nature of each domain implies that it folds
that it can be used as a powerful principle for more or less independently of all other domains

www.annualreviews.org • Structure and Function of Plant Photoreceptors 25

 Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org
by National Taiwan University on 06/01/10. For personal use only.

e
a

Chromophore

26
Möglich et al.
PAS

GAF

PHY

f
d
b

Chromophore

Cytoplasm
Extra-cellular
BLUF

EAL
 present in the intact, full-length photorecep- LIGHT-OXYGEN-VOLTAGE
tor and, hence, that when isolated, it is likely SENSORS
to retain critical aspects of both its structure
Light-oxygen-voltage (LOV) domains utilize
and more importantly, its function. For exam-
flavin nucleotide cofactors to detect blue light.
ple, plant phototropins contain two LOV in-
First discovered as tandem sensor domains in
put or sensor domains, a serine/threonine ki-
the plant photoreceptor phototropin (23), LOV
nase output or effector domain whose kinase
domains have since been found in several plant,
enzymatic activity is light dependent, several
fungal, and bacterial proteins (28, 89). In plants,
linkers between these domains, and small exten-
to date, three families of bona fide photorecep-
sions at the N and C termini (Figure 2a) (21,
tors utilizing LOV domains have been iden-
23, 24). Each LOV domain has been isolated
tified (Figure 2a). First, phototropins 1 and
from intact phototropin and effectively studied.
2 mediate a variety of relatively fast, light-
Nevertheless, an intact photoreceptor is more
induced responses in plants including pho-
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

than the sum of its parts. The interfaces and

totropism, chloroplast and leaf movements, and
interactions between domains are lost in sepa-
stomatal opening (21, 23). Second, proteins of
rated domains, the linkers between domains are
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the ZEITLUPE family control slower light

disrupted or absent, and the critical functional
responses such as entrainment of the circa-
property of long-range signal transmission is
dian clock and onset of flowering (32, 105).
absent. Further, photoreceptors in vivo may as-
Third, aureochromes occur in photosynthetic
sociate noncovalently with other proteins and
stramenopiles and regulate aspects of morpho-
cellular constituents, and their overall function
genesis in response to light (138). The Ara-
may be importantly influenced by these associ-
bidopsis thaliana PAS-LOV protein is a further,
ations, as for example the interaction of pho-
putative plant photoreceptor for which blue-
totropin and 14–3-3 proteins (73). Isolation ex-
light-dependent protein interactions were re-
tracts its price.
ported but neither correct flavin incorporation
The modular nature also enables results on
nor the characteristic LOV photoreaction has
photoreceptors from other organisms to be re-
yet been demonstrated (107).
lated with some confidence to those on plants,
because distant organisms share common do-
mains and identical (or closely related) chro- LOV Photochemistry
mophores and photochemistry (Figures 1 and LOV domains are distinguished from other
2). Although there is little direct information flavin-based blue-light photoreceptors such as
available today at the atomic level specifically BLUF domains by the characteristic LOV pho-
on plant photoreceptors, a review of photore- tochemistry (77, 96, 122) (Figure 1a). After
ceptors across all kingdoms does enable extrap- absorption of a photon in the blue spectral
olations toward plant photoreceptors. We or- region around 450 nm by the dark-adapted
ganize this review by class of photoreceptor D450 state, the flavin nucleotide cofactor under-
and concentrate on those of most relevance to goes efficient intersystem crossing in picosec-
plants. onds to yield a triplet L660 state (136). Within

←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−
Figure 3
Three-dimensional structures of representatives of the six photoreceptor classes. Chromophores are shown as space-filling models in
cyan, chromophore-binding domains in green, and additional protein domains in yellow and blue. Gray color denotes the second
subunit within homodimeric structures. (a) LOV: A. sativa phototropin 1 LOV2 domain (PDB entry 2V0U) (52). (b) Xanthopsin:
photoactive yellow protein from H. halophila (2PHY) (12). (c) Phytochrome: P. aeruginosa bacteriophytochrome (3C2W) (157).
(d ) BLUF: K. pneumoniae BlrP1 (3GFZ) (10). (e) Cryptochrome: cryptochrome 1 from A. thaliana (1U3D) (17). ( f ) Rhodopsin:
Halobacterium salinarum bacteriorhodopsin (1C3W) (91).

www.annualreviews.org • Structure and Function of Plant Photoreceptors 27

 microseconds a covalent, thioether bond be- flavin chromophore (3), where mutations can
tween atom C(4a) of the flavin ring and a con- strongly affect photocycle kinetics (22).
served, spatially proximal cysteine residue is
formed, the S390 state (117). This reaction prob-
ably proceeds through an intermediate radical LOV Domain Structure
pair (96, 122). The overall quantum yield for the LOV domains constitute a subclass of the Per-
photoreaction leading to formation of the S390 ARNT-Sim (PAS) family whose members serve
state is high, ∼0.3 in phototropin LOV2 do- as versatile sensor and interaction domains in
mains (71). Usually, the photoreaction is fully diverse signaling proteins (99, 139). The first
reversible and the signaling state thermally re- structure of a LOV domain and indeed of any
verts to the ground, dark state. Despite closely plant photoreceptor, that of the LOV2 do-
similar sequence and structure, individual LOV main of Adiantum capillus-veneris neochrome
domains differ markedly in the kinetics and 1 (26), displayed the canonical PAS fold. As
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

quantum yield of their photocycle (24, 69). For illustrated for the LOV2 domain of Avena
example, the time constants for dark recovery sativa phototropin 1, the PAS core domain
in phototropin LOV domains are about 10– comprises a five-stranded antiparallel β sheet,
by National Taiwan University on 06/01/10. For personal use only.

100 seconds (69), but much longer (or even whose strands are in the topological order Bβ-
irreversible) in the isolated LOV domain of Aβ-Iβ-Hβ-Gβ (that is, 2-1-5-4-3), and sev-
A. thaliana FKF1 (63) and in a LOV histidine eral α helices (Cα, Dα, Eα, Fα) are packed on
kinase from Brucella melitensis (137). However, either side of the sheet (Figures 3a and 4a).
photochemical properties of LOV domains de- A flavin nucleotide cofactor, flavin mononu-
pend on the protein context, providing a spe- cleotide (FMN) in plant LOV proteins, is
cific example of a difference in properties be- bound in a cleft formed by the central β sheet
tween isolated domains and full-length proteins and helices Eα and Fα. Residues involved in
(24). The basis for these differences may be FMN coordination and the photoreaction are
linked to protein flexibility, or to solvent ac- largely conserved and line the flavin-binding
cessibility, and the specific environment of the pocket. LOV domains frequently display

a FMN
b Thioether FMN
bond

C450
C450

Q513 Q513
N414 N414
D515 D515

A'α A'α
Jα Jα

Figure 4
Light-induced structural changes in the A. sativa phototropin 1 LOV2 domain (52). The LOV core domain is shown in white and N-
and C-terminal α-helical extensions, A’α and Jα, in green. For clarity, helix Cα is not displayed. (a) In the dark the active-site cysteine
450 adopts two conformations. Hydrogen bonds are formed between Q513 and atom O4 of the FMN ring, and from N414 to D515.
(b) Upon blue-light absorption, a thioether bond ( yellow) forms and induces a slight tilt in the FMN ring. Q513 presumably flips its side
chain to form new hydrogen bonds to the FMN ring and N414. Conformational changes could thus be propagated to the terminal
helices and could cause unfolding of the Jα helix (54). Note that alternate conformations of residues N414 and Q513 are not shown (52).

28 Möglich et al.
 structured N- and C-terminal extensions flank- other physiological phosphorylation target has
ing their core, which predominantly adopt been identified (21). Recent data indicate
an α-helical conformation and may be cru- that autophosphorylation of a particular serine
cial for signal transduction (see below and residue in the kinase activation loop is essential
Reference 99). for all phototropin-dependent responses; phos-
Crystallographic studies identify blue-light- phorylation at other sites may be required for
induced structural changes around the flavin specific phototropin-dependent responses (64).
cofactor that are similar in all LOV domains Repression of phototropin kinase activity in the
studied to date (27, 38, 52) (Figure 4a). For- dark is relieved upon blue-light absorption by
mation of the covalent thioether bond causes the LOV2 domain (97). In contrast, the photo-
a tilt of the isoalloxazine ring of the FMN by chemically identical LOV1 domain is not es-
about 6◦ and slight movements of the coor- sential for light regulation of kinase activity;
dinating residues. The side chain of a nearby, rather, it attenuates the effect of LOV2 and
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

conserved glutamine residue is proposed to ro- may contribute to dimerization (97). Structural
tate and thereby changes its hydrogen-bonding (54) and functional (53) data implicate unfold-
pattern (27, 38, 163). For the A. sativa pho- ing of the Jα helix in the light regulation of
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totropin 1 LOV2 domain, further structural phototropin kinase activity. However, it is un-
changes occur within the β sheet and the C- clear whether the Jα helix and its unfolding are
terminal Jα helix that extends from the core strictly necessary, because the LOV2 domain
(52, 54) (Figure 4b). Indeed, nuclear magnetic can exert its regulatory effect on the kinase do-
resonance (NMR) data suggest that this Jα helix main in trans and in the absence of the Jα helix
unfolds (54). Infrared spectroscopic results sug- (97). Further, recent data from infrared spec-
gest that this reaction proceeds through distinct troscopy suggest that the role of the Jα he-
intermediate structures (66) that remain to be lix differs among phototropin LOV domains;
fully characterized. in the Adiantum neochrome 1 LOV2 domain,
Light-induced structural changes are gener- this helix does not unfold upon blue-light ab-
ally small in extent and (with the clear exception sorption (78). Helical extensions similar to the
of the Jα helix) largely confined to the imme- Jα helix are also found at the N and C ter-
diate vicinity of the flavin, which may be due to mini of several phototropin LOV domains and
several reasons. Light-induced conformational may be involved in signal transduction, possibly
changes may be qualitatively affected or atten- also undergoing light-induced conformational
uated in magnitude by the crystal context or by changes (52, 103). Although the molecular de-
isolation of the photoreceptor domain, or the tails remain elusive, light-dependent interac-
changes may be largely dynamic in nature, not tions both among individual phototropin do-
associated with substantial atomic translation. mains (104) and between phototropin and other
proteins, such as 14–3-3 proteins (73) and pre-
sumably the unidentified phosphorylation tar-
LOV Signal Transduction gets of phototropins, play key roles in signaling
We provide here a brief overview of plant LOV (99).
photoreceptors with a focus on structural and
mechanistic aspects; an in-depth treatment is ZEITLUPE family. The A. thaliana
provided in recent reviews (21, 32). ZEITLUPE, FKF1, and LKP2 proteins
contain a LOV domain followed by an
Phototropins. Phototropins comprise two F-box domain and several Kelch repeats
LOV domains, LOV1 and LOV2, and a ser- (Figure 2a) (130). These proteins mediate
ine/threonine kinase domain (23) (Figure 2a). ubiquitin-dependent protein degradation in
Phototropins undergo autophosphorylation at a light-controlled manner (92), ultimately
several serine and threonine residues but no leading to photoperiodic expression (121)

www.annualreviews.org • Structure and Function of Plant Photoreceptors 29

 and/or accumulation (72) of key proteins domains (see above) form a prominent subfam-
involved in regulating the circadian clock and ily. Through application of cryocrystallogra-
flowering onset. No structural information phy, time-resolved crystallography, NMR, and
is available yet on ZEITLUPE proteins, and ultrafast spectroscopic techniques, PYP has also
their detailed mechanism of action is only provided the most detailed results on the photo-
beginning to be understood (32). However, cycle of any photosensor domain at the atomic
as for phototropins, light-regulated protein level.
interactions are crucial for signal transduc- PYP contains a 4-hydroxycinnamic acid
tion of the ZEITLUPE-family proteins chromophore, covalently attached by a
(72, 121). thioester bond to a cysteine residue and
completely buried in the interior of the protein
Aureochromes. Stramenopile aureochromes (Figures 1b and 3b). The primary photochem-
are transcription factors that comprise an N- ical event is trans to cis isomerization about
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

terminal basic-zipper DNA-binding domain the sole double bond in the tail of its chro-
and a C-terminal LOV domain (Figure 2a), mophore. Reversion to the trans state occurs
thus resembling the modular composition of purely thermally as the photocycle concludes.
by National Taiwan University on 06/01/10. For personal use only.

bacterial one-component systems (144). Blue- In the dark, ground state, the phenolate anion
light absorption increases the affinity of the at the head of the chromophore is stabilized by
basic-zipper domain for DNA (138). Although unusually short hydrogen bonds (7) to nearby
the molecular details remain to be elucidated, glutamic acid and tyrosine side chains. Thus
aureochromes regulate cell branching and dif- isomerization must occur in a molecularly
ferentiation (138). Because basic-zipper do- constrained environment, in which one end
mains act as homo- and heterodimers (41), it of the chromophore is pinned by the covalent
is likely that light-dependent protein interac- bond and the other by these hydrogen bonds.
tions and changes in quaternary structure and Complete isomerization occurs within a few
dynamics will be revealed as components of sig- nanoseconds and introduces severe strain into
nal transduction. the chromophore and the surrounding protein.
Relaxation of this strain initiates a long series of
changes in tertiary structure: rupture of these
XANTHOPSINS hydrogen bonds; ejection of the chromophore
Photoactive yellow protein (PYP) is a small, toward the solvent; partial unfolding of the
cytoplasmic photoreceptor of 126 amino acids Cα helix, which contains these glutamic
that, upon absorption of blue light, undergoes acid and tyrosine residues; and, ultimately,
a fully reversible photocycle spanning around unfolding of a pair of short, N-terminal α
1 second that contains several spectroscopically helices packed on the distal side of the β
and structurally distinct intermediates (146). sheet, which forms the structural core of all
PYP thus represents an isolated sensor domain PAS and LOV domains including PYP (99,
(Figure 2b), the paradigm of the xanthopsin 139). Time-resolved crystallographic studies
class of photoreceptors. Despite considerable identify each of the intermediates as relaxation
effort, no other protein with which PYP might occurs over the timescale from nanoseconds
interact in a noncovalent, light-dependent fash- to seconds [Ihee et al. (62) and references
ion has been identified nor has its physiologi- therein]. These intermediates differ in tertiary
cal role been identified in any organism. Thus, structure. Each therefore represents a distinct
interest in PYP is more evident among bio- structural signal, which could differ in affinity
physicists than physiologists. No homolog of for another protein to which the signal could
PYP has been identified in plants. Neverthe- be transmitted. More recent studies (H. Ihee
less, PYP serves as the structural paradigm for et al., personal communication) have extended
the PAS domain family (99), of which LOV the time resolution toward 100 picoseconds to

30 Möglich et al.
 explore isomerization itself and characterize (denoted phyA–E in A. thaliana), the C termi-
earlier stages of the photocycle. nus contains a histidine-kinase-related domain
Although ultimately unsatisfying from a (HKRD) in place of an authentic HK domain
physiological standpoint, these studies on PYP and two additional PAS domains are inserted
point the way to an understanding at the atomic between the PCM and HKRD (Figure 2c).
level of the generation of a structural signal in an When difference spectra between the Pr and
isolated photosensor domain. But small is not Pfr states are probed by UV-vis absorption,
simple; even PYP turns out to be deceptively resonance Raman, or Fourier transform
complicated when studied in detail. infrared (FTIR) spectroscopy (6, 43, 147),
they exhibit striking similarities between plant
and microbial phytochromes, which suggests
PHYTOCHROMES that they share a common photoconversion
Phytochromes are red/far-red photoreceptors mechanism. The extent to which findings on
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

and, together with cryptochromes and pho- microbial phytochromes are relevant to plant
totropins, constitute one of the three major phytochromes is not established, but a working
regulators of photomorphogenesis in plants hypothesis is that they are closely related (113).
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(20). Although the first plant phytochrome The phytochrome field has been the subject
was discovered about 50 years ago, progress in of excellent reviews (112, 113). Here, we focus
understanding these photoreceptors has been on recent advances in structural studies and cur-
greatly stimulated by the recent discovery of rent views on the molecular basis of photocon-
homologous microbial phytochrome systems, version and the signal transduction mechanism.
denoted bacteriophytochromes (30, 61, 149).
Phytochromes and bacteriophytochromes uti-
lize a linear tetrapyrrole, bilin chromophore to Phytochrome Structure
sense red/far-red light (Figure 1c). Substituents Bacteriophytochromes (BphPs) and cyanobac-
on the pyrrole rings and their mode of covalent terial phytochromes (Cphs) share a similar do-
attachment to the protein differ between main structure and high sequence homology
phytochromes and bacteriophytochromes with plant phytochromes (Phys), particularly in
(113). In both, absorption of a photon causes the N-terminal CBM that binds the bilin chro-
the red-absorbing (Pr) spectroscopic state to mophore and absorbs red light (113). The crys-
photoconvert to the far-red-absorbing (Pfr) tal structure of the CBM from Deinococcus ra-
spectroscopic state; absorption of a second diodurans bacteriophytochrome (DrBphP) was
photon causes reversion to the Pr state. In some the first for domains of any phytochrome (150).
(bacterio-)phytochromes the Pr state forms the Two recent crystal structures of Synechocystis sp.
dark, ground state and in others, the Pfr state. Cph1 and Pseudomonas aeruginosa PaBphP in
Two N-terminal domains (PAS and GAF) their dark state, Pr and Pfr respectively, advance
together form a chromophore binding module our understanding of the Pr↔Pfr photoconver-
(CBM) that displays only limited photocon- sion (37, 157). Both structures include the en-
version from the dark state. However, addition tire PCM and retain the photoconversion prop-
of the phytochrome-specific (PHY) domain erties of the corresponding full-length proteins.
yields the three-domain, PAS-GAF-PHY, The PAS, GAF, and PHY domains share a
photosensory core module (PCM) that retains common core fold defined by a central, antipar-
the full photoconversion properties of full- allel β sheet with the strands in the order of
length proteins (113). The C-terminal effector 2–1-5–4-3 and a connecting element between
domain in bacteriophytochromes is a histidine strands 2 and 3 containing an α helix. Although
kinase (HK) domain and forms part of a the overall spatial arrangement of these three
two-component signaling system (Figure 2c). domains is linear in a beads-on-a-string fashion,
In all five classes of plant phytochromes they are closely integrated via the N-terminal

www.annualreviews.org • Structure and Function of Plant Photoreceptors 31

 extension of the PAS domain, a highly unusual Phytochrome Photochemistry
knot (150), and an arm extending from the All four pyrrole nitrogens in the bilin chro-
PHY core domain (37, 157). All three domains mophore are protonated in both the Pr
converge near the chromophore binding site. and Pfr states (76, 115, 132) (Figure 1c).
In addition, the GAF and PHY domains are Femtosecond- to picosecond-absorption spec-
linked by a long, continuous helix spanning troscopy revealed the presence of two elec-
both domains that forms part of a helical bundle tronic states before fully isomerized photoprod-
(37, 150, 157). ucts are formed. These photoproducts occur in
In the crystals, PaBphP-PCM forms a head- both the Pr→Pfr and the Pfr→Pr directions
to-head, parallel dimer with an extensive helical and are denoted Lumi-R and Lumi-F, respec-
bundle at the dimer interface, but in contrast tively (29). Transient proton release and uptake
Cph1-PCM packs as an antiparallel dimer. A in the chromophore may accompany the for-
parallel dimer is also observed in other crys- mation and decay of the later (micro- to mil-
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

tal structures of bacteriophytochromes (150, liseconds) intermediates denoted Meta-R and

159) and may well prove to be more bio- Meta-F (14). However, the structural bases of
logically relevant for phytochromes in general these reaction intermediates and the identity of
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(157). transient proton donor/acceptors in the reac-

tions are not yet established (151).
It is generally accepted that the primary
photochemical event in the reversible Pr↔Pfr
photoconversion in Phys and BphPs is Z/E
R241 isomerization around the C15 = C16 double
R209
bond between rings C and D in the bilin chro-
mophore (Figures 1c and 5) (113). Indeed,
S261 crystal structures directly confirm that the
chromophores of Cph1-PCM, DrBphP-CBM,
H277
and RpBphP3-CBM adopt distinct config-
urations in the Pr and Pfr states (37, 150,
157). We have recently proposed a “flip-and-
rotate” model to summarize conformational
B S275
differences between the Pr and Pfr states in
the chromophore and its surrounding protein
matrix (158). Upon absorbing a photon, rapid
C isomerization occurs and ring D flips about
A Y163 the C15 = C16 double bond. Eventually, the
entire chromophore slightly rotates relative
to the protein matrix around an axis roughly
centered at ring A and approximately perpen-
D dicular to rings B and C. Consequently, ring
D and the propionate substituents on rings B
and C interact with different sets of protein
D194 Y190
side chains in the Pr and Pfr states (Figure 5).
In addition, a pair of aromatic side chains near
ring D undergoes concerted rotamer changes
Figure 5
coupled to flipping of ring D (157, 158).
Flip-and-rotate model for Pr↔Pfr photoconversion in bacteriophytochromes
as shown for P. aeruginosa BphP (158). Pyrrole rings of biliverdin are labeled
Whether this flip-and-rotate model applies
A–D. Residues interacting with the D ring are shown in cyan for the Pfr state to photoconversion reactions in both forward
and in gray for the Pr state. and reverse directions and how it progresses

32 Möglich et al.
 through intermediate structures are open ques- BLUF SENSORS
tions. The model requires more pronounced BLUF domains comprise a family of photo-
conformational changes around ring D (distant sensor domains that use FAD to detect blue
from the rotation axis) and the propionate side light (49). BLUF domains predominantly occur
chain of ring C, consistent with observations in in prokaryotes (41) and were first identified in
Cph1 and phyA (13, 114). However, other evi- AppA from Rhodobacter sphaeroides where they
dence suggests that structural changes are more regulate expression of photosynthesis genes
dramatic around ring A in Cph1-PCM (148). (48, 49, 93). BLUF domains occur either as iso-
Ring D remains nearly unchanged between the lated domains or covalently linked to effector
Pr and Pfr structures of the GAF domain of a domains mostly involved in cyclic nucleotide
“PAS-less” phytochrome (25, 143) (A. Ulijasz, metabolism, e.g., adenylate/guanylate cyclases
personal communication). and phosphodiesterases (41, 49) (Figure 2d ).
BLUF domains are also found in eukaryotes
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

Phytochrome Signal Transduction such as euglenozoa (65) and fungi (41, 49), but
to date no BLUF proteins have been identified
How do signals originating in the chromophore
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in plants.
and its binding pocket propagate to the spa- In contrast to the flavin-containing LOV
tially remote effector domain? Any answer must domains, upon absorption of blue light by a
be indirect, because no crystal structure is yet BLUF domain, the FAD cofactor undergoes
available for full-length phytochromes of any minimal conformational changes and the sig-
kind. In our model for dimeric, full-length naling state is rapidly formed on the sub-
PaBphP, the C-terminal helix of the PHY do- nanosecond timescale (46, 94) (Figure 1d ).
main is directly fused to the N-terminal he- Upon light absorption by the ground state P,
lix of the HK domain, thus further extending an electron is transferred from a conserved ty-
the helical bundles at the dimer interface (157). rosine residue to the flavin ring and gives rise
The relative positioning between the phospho- to a short-lived radical pair (46). The side chain
acceptor histidine and the kinase active site of a nearby, conserved glutamine residue is as-
in the HK domain supports the proposed in sumed to rotate (8), followed by back transfer
trans autophosphorylation. A similar interdo- of an electron to the tyrosine (46) to form the
main linkage and disposition of the sensor signaling state, Pred . Pred shows a slightly red-
and effector domains may be present in plant shifted absorption spectrum and differs from
phytochromes. the ground state in the hydrogen bonds that the
The extended arm of the PHY domain found flavin ring forms. In both the ground and sig-
in both the PaBphP and Cph1 structures seems naling states, FAD maintains its fully oxidized
to be conserved in all phytochromes. Its close state. Pred is formed with a quantum yield of
proximity to the chromophore makes the PHY ∼0.25–0.4 and thermally reverts to the ground
domain an effective and direct mediator of state within seconds (46). Details of the BLUF
transduction of the signal toward the HK do- photocycle are still under debate; an alterna-
main. Conformational changes in the chro- tive mechanism based on tautomerization of the
mophore binding pocket could be transmitted side chain of the conserved glutamine residue
to the HK domain either via direct, interdomain has been advanced (33).
interactions or via alterations in the stability of BLUF domains are oligomeric, are usu-
the helical bundle that comprises much of the ally dimeric, and adopt a ferredoxin-like core
dimer interface. Long interdomain helices are fold comprising a five-stranded mixed paral-
found in a wide range of signaling proteins (4), lel/antiparallel β sheet with a strand order of
where they may play important roles in signal 4-1-3-2-5 and two α helices running parallel to
transduction and in spatially aligning multiple the strands (8, 68, 74) (Figure 3d ). The FAD
domains.

www.annualreviews.org • Structure and Function of Plant Photoreceptors 33

 cofactor is embedded in a cleft between the two Cry-DASH proteins bind both double-
α helices. A C-terminal, α-helical cap of ∼40– stranded and single-stranded DNA and can
50 residues packs against the outer face of the also repair single-stranded DNA containing
β sheet in orientations that differ from domain cyclobutane-pyrimidine-dimer (CPD) lesions,
to domain (67, 74, 153). As discussed above, but their function in signal transduction, if any,
blue-light-induced rotation of the side chain of is not yet known (60, 111).
a conserved glutamine residue alters its hydro- Compared to photolyases, cryptochromes
gen bonding pattern. Movement of a conserved often possess additional terminal regions of var-
methionine residue in strand β5 out of the FAD ious lengths that may be involved in signal-
binding pocket leaves a void that is filled by ing (see below) (75). AtCry1 and AtCry2 are
the side chain of another residue (tryptophan composed of an N-terminal photolyase homol-
in AppA) (8, 68). In addition, light also induces ogy region (PHR) and a C-terminal extension
conformational changes within the β sheet and (CCT); AtCry3 contains a shorter N-terminal
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

the C-terminal cap (51, 153). extension of the PHR domain (Figure 2e).
Very recently, a groundbreaking study re- Although largely divergent in sequence, these
ported the first crystal structure of a full- N-terminal or C-terminal regions carry three
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length photoreceptor, that of Klebsiella pneumo- short sequence motifs known as the DAS mo-
niae BlrP1, which comprises BLUF and EAL tif, DQXVP, followed by acidic and serine-rich
phosphodiesterase domains (10). Briefly, within sequences.
an antiparallel dimer the BLUF domain of one The structural biology of DNA photolyases
molecule interacts with the EAL domain of and cryptochromes has been extensively dis-
the other molecule through its C-terminal cap. cussed in several reviews (36, 86, 87, 100).
Light-induced conformational changes could We focus here on the characteristics of cryp-
thus be propagated to the effector domain, lead- tochromes as photoreceptors directly rele-
ing to changes in quaternary structure and en- vant to mechanisms of light perception and
zymatic activity (10). Interestingly, changes in signaling.
quaternary structure and dynamics are common
components of signal transduction in BLUF
(160), LOV (see above), and PAS proteins Cryptochrome Structure
(99). The photosensory PHR domains in AtCry1
and AtCry3 share the same architecture with
DNA photolyases, composed of an N-terminal
CRYPTOCHROMES α/β domain and a C-terminal α-helical domain
Cryptochromes are widely distributed blue- (17, 60, 75, 111) (Figure 3e). The α/β domain
light photoreceptors mediating various adopts a dinucleotide-binding fold consisting
responses in plants and animals (1, 18, 47, 86, of a five-stranded parallel β sheet surrounded
87, 100, 118). Examples in plants are A. thaliana by five helices. The helical domain consists of
cryptochrome 1 and 2 (AtCry1 and AtCry2) 16 helices and noncovalently binds the FAD
that entrain the circadian clock and trigger chromophore in a U-shaped conformation.
developmental processes such as de-etiolation The linker region between the α/β and helical
and flower induction (84, 125, 126). Cryp- domains is extended and largely unstructured,
tochromes are flavoproteins whose photo- with conformations that vary among photolyase
sensory domains are closely related to DNA and cryptochrome structures. In the crystal
photolyases, but typically lack their DNA structure of AtCry3 (and as in photolyases),
repair activity (87). A. thaliana cryptochrome a second light-harvesting chromophore, 5,10-
3 (AtCry3) belongs to a different class of methenyltetrahydrofolate (MTHF), is located
cryptochromes found in Drosophila, Arabidopsis, at the interface between these domains
Synechocystis, and Homo (cry-DASH) (18). (111).

34 Möglich et al.
 In contrast to DNA photolyases and DASH
cryptochromes such as AtCry3, the surface
of AtCry1-PHR is predominantly negatively
charged, which accounts for its lack of
DNA binding activity (17, 100). However,
the nucleotides ATP (adenosine triphos-
phate) or AMP-PNP [adenosine 5 -(β,γ-
imido)triphosphate] bind to AtCry1-PHR in MTHF e–
close proximity to the FAD chromophore, in
a manner similar to the binding of the substrate W324

cyclobutane pyrimidine dimers to photolyase W377

e–
(17).
The putative signaling CCT domains of W400
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

cryptochromes are not yet characterized struc- FRET

e–
turally, nor is any sequence-based homol-
ogy model available. Both secondary structure
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prediction and circular dichroism (CD) and

NMR spectroscopy suggest that the isolated
FAD
AtCry1-CCT domain mostly adopts a flexi-
ble, extended structure with short stretches of AMP-PNP
helices (109). However, in the context of the
full-length protein, it adopts a more stable con-
formation through interaction with its cognate
PHR domain. Such direct interdomain con- Figure 6
tacts occur in the crystal structure of AtCry3, in Spatial configuration of key components involved in
which a 40-residue N-terminal extension con- the photoreaction of cryptochromes based on the
taining the DAS motif in an extended struc- structural superimposition of A. thaliana
cryptochromes 1 and 3 (PDB entries 1U3D, 2VTB)
ture wraps around the helical domain of PHR
(17, 111). Putative paths of electron and resonance
(111). energy transfer are marked in red dashed lines.
Residue numbering refers to cryptochrome 1.

Cryptochrome Photochemistry
Absorption of light by DNA photolyases causes In the vicinity of the FAD chromophore,
photoreduction of the oxidized ground state a chain of three tryptophan residues and
of FAD to a fully reduced, catalytic FADH− , antenna pigments such as MTHF or
the light-activated state, which further enables 8-hydroxy-5-deazariboflavin (8-HDF) are
electron transfer to DNA to split and repair conserved among DNA photolyases and
the UV lesions. In contrast, plant and ani- cryptochromes (Figure 6). This Trp triad is
mal cryptochromes exhibit more complicated required for FAD reduction in AtCry1 (161)
photochemistry. Absorption of blue light by and participates in intramolecular electron
the oxidized ground state of FAD in AtCry1 transfer to the FAD chromophore upon
and AtCry2 induces formation of a radical in- photoactivation. Light energy absorbed by
termediate state (semiquinone), FADH··, that an antenna pigment is transferred to FAD
accumulates in the activated signaling state. by fluorescence resonance energy transfer to
Absorption of green light by FADH·· causes fur- ensure efficient photoreduction. Although not
ther reduction to FADH− , which abrogates sig- observed in the structure (17), biochemical
naling. FADH− reoxidizes to the fully oxidized evidence shows that MTHF also binds to
form during dark reversion (9, 16). AtCry1, where it functions as an antenna (58).

www.annualreviews.org • Structure and Function of Plant Photoreceptors 35

 Cryptochrome Signal Transduction membrane proteins. Light detection is achieved
via a retinal chromophore that is covalently
The biochemical nature of the output signals
bound to a lysine residue as a protonated
remains elusive for plant cryptochromes. The
Schiff base. Long recognized as the photore-
cryptochrome C-terminal extensions CCT
ceptor in animal vision, related rhodopsins
probably form the effector domain as evidenced
were subsequently identified as photoreceptors
by a constitutive photomorphogenetic pheno-
in microorganisms (11, 106) and algae (44).
type resulting from overexpression of the iso-
Known plant rhodopsins belong to the micro-
lated CCT domains of either AtCry1 or AtCry2
bial (type-1) rhodopsins (55, 131), which are
(156) and an inactive cry1 allele that carries
exemplified by bacteriorhodopsin (106). Chan-
mutations in the C-terminal region (2). Sig-
nelrhodopsins mediate phototaxis in flagellate
naling is likely mediated by direct interactions
algae (55, 128), and were first identified in
between the CCT domain and downstream
Chlamydomonas reinhardtii as light-gated cation
effector proteins such as the ubiquitin ligase
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

channels (101, 129, 135) (Figure 2f ). Chlamy-

COP1 (152, 155). Proteolysis experiments on
domonas also expresses other rhodopsins for
full-length AtCry1 in the dark and after illu-
which no clear functional role has yet been
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mination suggest that the CCT domain under-

ascertained (55). The first identified chlamy-
goes a light-induced order-to-disorder transi-
opsins 1 and 2 are prevalent in the Chlamy-
tion particularly in the serine-rich region of the
domonas eyespot but their physiological role
DAS motif (109).
is unclear (45, 55, 70). In chlamyopsins 5–
Light-dependent autophosphorylation,
7, known as the enzymerhodopsins, rhodopsin
common among photoreceptors, has also
sensor domains are covalently connected to
been examined as a potential output signal in
histidine kinase, response regulator, or adeny-
AtCry1 and animal cryptochromes. AtCry1
late/guanylate cyclase effector domains (70).
binds ATP and exhibits FAD-dependent kinase
Other algal rhodopsins (142) function as light-
activity in vitro (15). The crystal structure of
driven H+ -pumps akin to bacteriorhodopsin al-
AtCry1-PHR reveals binding of the nonhy-
though their physiological role in photosyn-
drolyzable analog AMP-PNP near the FAD
thetic organisms remains mysterious (55).
chromophore. Indeed, the autokinase activity
of AtCry1 is not affected by light in vitro, and
AtCry2 displays no detectable kinase activity in Rhodopsin Photochemistry
the light or dark (108). Blue-light-dependent
As in bacteriorhodopsin, the retinal chro-
phosphorylation of AtCry1 and AtCry2 in vivo
mophore of algal rhodopsins adopts the all-
may arise from other light-dependent kinases
trans conformation in its dark-adapted state
for which the disordered CCT domain is a
D470 (56, 80). Upon blue-light absorption
substrate.
around 470 nm, the retinal moiety isomerizes
Like other plant photoreceptors, AtCry1
to the 13-cis form (56, 80) (Figure 1f ). Long
and AtCry2 form homodimers in vivo and in
hampered by limited protein availability, de-
vitro (119). Dimerization is mediated by the
tailed spectroscopic studies of the photocycle of
PHR domain and appears to be essential for
Volvox carteri channelrhodopsin became feasible
signaling in AtCry1 and AtCry2 (116). AtCry3
recently (35). Briefly, the initial photoexcited
and photolyases, however, appear to be mostly
state P500 interconverts to the P510 state within
monomeric in solution (75).
200 μs through an intermediate with a depro-
tonated Schiff base. Based on electrophysio-
logical experiments, P510 is the major signal-
RHODOPSINS ing, ion-conducting state (35). P510 thermally
In contrast to the five other water-soluble relaxes to the ground state through a spectro-
photoreceptor classes, rhodopsins are integral scopically silent intermediate denoted N with

36 Möglich et al.
 time constants of 20 and 100 ms, respectively. cations (102). These properties are exploited
The quantum yield for retinal isomerization in in so-called optogenetic applications in neuro-
rhodopsins is typically high, e.g., 0.64 in bacte- science (31), where channelrhodopsin-2 (102)
riorhodopsin (140). is largely used because it achieves higher pho-
tocurrents than channelrhodopsin-1 (101).
The gating mechanism of channel-
Rhodopsin Structure rhodopsins is little understood but certain as-
In the absence of high-resolution structures, pects might be shared with bacteriorhodopsin.
plant rhodopsins are expected to structurally Specifically, channelrhodopsin-2 also displays
resemble homologous microbial rhodopsins H+ pumping activity and could thus be
(57). As shown for bacteriorhodopsin in considered a “leaky proton pump” (39). In
Figure 3f (91), microbial rhodopsins belong native algae, part of the channelrhodopsin
to the large family of seven-helix transmem- photoreceptor function might be mediated
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

brane proteins (41). Seven α helices connected by regulation of as yet unidentified down-
by short loops traverse the plasma membrane stream proteins (128, 129) similar to microbial
and assemble into a barrel-like bundle. The sensory rhodopsins (120). Such a function
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retinal chromophore is embedded in the middle might reside in the long C-terminal half of
of this bundle through residues that are largely channelrhodopsins, which is not required for
conserved in algal rhodopsins (101). Studies by light-gated channel activity (101). Related
crystallography and cryoelectron microscopy scenarios may also apply to the less studied
on bacteriorhodopsin revealed in great detail enzymerhodopsins (55, 70). The observation
its structure and light-induced conformational that transmembrane rhodopsin photoreceptors
changes throughout the photocycle (57, 90, 91). can be linked to the same types of effector
However, these findings may not fully apply to domains (e.g., histidine kinases) as soluble pho-
algal rhodopsins, and corresponding homology toreceptors is intriguing. Certain principles
models are almost certainly deficient in their and mechanisms of signal transduction might
molecular details (55). Reliable answers will be be shared among quite disparate photoreceptor
provided by three-dimensional structures of classes.
plant rhodopsins, the prospects for which ap-
pear improved by recent advances in the recom-
binant production of channelrhodopsins (35). COMMON STRUCTURAL AND
SIGNALING PRINCIPLES
All photoreceptors face the same principal task:
Rhodopsin Signal Transduction the information provided by absorption of a
We focus on key aspects of rhodopsin func- photon must be efficiently converted into pro-
tion and refer to Reference 55 for a current and ductive “jiggling and wiggling of atoms” (40)
authoritative treatment. Phototaxis in Chlamy- to elicit the appropriate physiological response.
domonas and related algae involves photocur- Our analysis of the six photoreceptor classes re-
rents driven by cation influx across the plasma veals certain recurring principles of structure
membrane (88). Such photocurrents depend on and signal transduction mechanisms.
the action of channelrhodopsins (44, 129) and Photoreceptors of the LOV, PYP, phy-
appear within microseconds after light excita- tochrome, and BLUF classes are based on the
tion (55). Heterologous expression of channel- same modular domain architecture in which a
rhodopsin in oocytes established their function photosensor domain is covalently linked, usu-
as light-gated ion channels (101, 102). Although ally to the N terminus but occasionally to the
in algae the photocurrent is mainly carried by C terminus of an effector domain. Strikingly,
Ca2+ and H+ (59, 88), channelrhodopsins are different sensor domains can regulate the same
also permeable for other mono- and divalent type of effector domain and in some proteins

www.annualreviews.org • Structure and Function of Plant Photoreceptors 37

 several photosensors occur in combination, their photoreactions, structures, and signaling
e.g., in neochromes. These classes bury their mechanisms have recently enabled applica-
chromophores, inaccessible to solvent, within tions in biotechnology and protein engineer-
a core consisting of a central β sheet and sev- ing. As natural photoreceptors frequently em-
eral α helices. The structural similarity among ploy near-ubiquitous metabolites such as flavins
them and resemblance to certain chemosensor and bilins as cofactors and spontaneously incor-
domains may reflect a common evolutionary porate them to form a functional photosensor,
origin (5, 99). The modular structure appears photoreceptors can readily be deployed in vivo
to have evolved by fusion of individual domains in heterologous systems. For example, a plant-
characterized by distinct functions, e.g., signal derived photoreceptor may be functionally ex-
sensing, catalysis or propensity to oligomer- pressed in Xenopus (101) or Mus (50).
ize, and which retain those functions, albeit in Because most current biotechnological ap-
modified form, in the multidomain photorecep- proaches are based on plant photoreceptors, we
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

tors we see today. These photoreceptors usually summarize these approaches briefly and loosely
form dimers or higher-order oligomers, which group them into four categories (Figure 7).
introduces the possibility of quaternary struc- First, various efforts are directed at altering
by National Taiwan University on 06/01/10. For personal use only.

tural changes. Linkers or extensions at the N or properties of photoreceptors such as their ab-
C termini of the sensor domains are mainly α- sorption, action and emission spectra, quantum
helical, often located at a dimer (or oligomer) yield, or photocycle kinetics (Figure 7a). Ex-
interface and involved in signal transduction. amples include spectral tuning in rhodopsins
Their conformations are light dependent and (162), incorporation of alternate chromophores
may take the form of order-disorder transitions, into LOV domains (95), and mutant photosen-
which in turn may modulate quaternary struc- sors with altered photocycle kinetics (22).
ture. Thus, changes in quaternary structure and Second, photoreceptor domains were engi-
dynamics often form part of the signal transduc- neered to act as fluorophores (Figure 7b). As
tion mechanism (99). noted in the Introduction, natural photorecep-
However, cryptochromes and rhodopsins tors are evolutionarily optimized to efficiently
differ architecturally from the other photore- undergo productive photochemistry upon light
ceptors, lack a clear modular structure, and absorption and conversely unproductive de-
incorporate their chromophores into a compact excitation pathways such as internal conversion
unit that also contains an enzyme active site or or fluorescence are minimized. If productive
ion channel. This architecture almost certainly photochemistry is blocked, e.g., in mutant
reflects their evolution from light-absorbing proteins, other processes of de-excitation such
proteins that utilize photons primarily as a as fluorescence can become dominant. For
source of energy rather than for their informa- example, removal of their active-site cysteine
tion content. However, the recent discovery renders LOV domains fluorescent (19, 34).
of enzymerhodopsins implies that to some Similarly, several bacteriophytochromes have
extent signaling strategies are shared between been made fluorescent by mutating key residues
the integral membrane rhodopsins and several in such a way as to block efficient Pr↔Pfr pho-
of the water-soluble, modular photoreceptor toconversion (42, 127). High-resolution crystal
classes. structures of photoreceptors guide the rational
design of variants with impaired photochem-
istry and increased fluorescence. Fluorescent
PHOTORECEPTOR photoreceptor variants represent interesting
BIOTECHNOLOGY alternatives to the widely used jellyfish fluores-
The identification of photoreceptors and cent proteins for which GFP is the paradigm
elucidation—even in its earliest stages—of (141). The orthogonal chromophores and

38 Möglich et al.
 a Optimized photoreceptors b Fluorescent photoreceptors

hν hν

* *
kp kF kp kF

c Heterologous expression d Artificial light switches

Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

Off
by National Taiwan University on 06/01/10. For personal use only.

hν hν
+

On
Effector protein

Figure 7
Application of plant photoreceptors in biotechnology and protein engineering in four general areas.
(a) Alteration and improvement in properties of photoreceptors such as action and fluorescence spectra,
quantum yield, and lifetime of the signaling state. (b) Upon light absorption, a photoreceptor efficiently
undergoes productive photochemistry (kp ) (left). Competing de-excitation processes such as radiative decay
(fluorescence, kF ) are minimized but may become dominant in mutant proteins with impaired
photochemistry (right). (c) Natural photoreceptors, e.g., channelrhodopsin, were isolated from plants
(Chlamydomonas) and expressed in other organisms (Mus) to control their behavior by light. (d ) Design of
modular photoreceptors by fusion of effector proteins ( green triangle) with photosensor domains.

photochemistry in photoreceptors differ because the underlying photoreceptors need

greatly from GFP and its variants in important not be added exogenously but can be genetically
properties such as fluorescence emission encoded and endogenously expressed in the de-
spectrum (127). sired cellular location. This facilitates noninva-
Third, (plant) photoreceptors were heterol- sive and reversible control over physiological
ogously expressed to control behavior of cells processes with excellent spatial and temporal
and even of entire organisms (Figure 7c). resolution. Most versatile are those photore-
Based on their ability to elicit action poten- ceptors that regulate elementary processes of
tials in neurons, channelrhodopsins (101) have importance in diverse cell types and organisms
found widespread use (e.g., Reference 50), thus (cf. channelrhodopsins).
spawning the vibrant field of optogenetics (31). Fourth, artificial photoreceptors were de-
Photoactivated adenyl cyclase (65) was em- signed (Figure 7d ) via approaches that ex-
ployed to increase cellular levels of the sec- ploit the modularity of photoreceptors to be-
ond messenger cAMP (3 ,5 -cyclic adenosine stow light sensitivity on effector proteins by
monophosphate) upon light absorption (123). covalently linking them to suitable photo-
These approaches are particularly powerful sensor domains. For example, LOV domains

www.annualreviews.org • Structure and Function of Plant Photoreceptors 39

 were fused (carefully) to regulate, in a blue- A major challenge is to extrapolate from
light-dependent manner, the activities of a data at the molecular level to the physiology
DNA-binding protein (133), dihydrofolate re- of living plants. In the following, we highlight
ductase (81), histidine kinases (98), and most some of the difficulties and how they might
recently and spectacularly, the small GTPase be addressed. Recently, microbial proteins have
Rac1 (154). A bacteriophytochrome was used served as powerful model systems to study
to bestow control by red light on histidine ki- photoreceptor structure, photochemistry, and
nase activity (83). Further, the light-dependent signaling mechanisms. Although the primary
association of plant phytochromes with their in- photochemical events are expected to be closely
teracting factors (PIF) was harnessed to regu- similar in plants, that is very unlikely to be the
late actin metabolism (82). A key challenge to case for downstream events. At the physiolog-
designers is to efficiently couple photosensor ical level, photoreceptors such as phototropins
and effector domains, thus translating a signif- and phytochromes occur as several subtypes
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

icant portion of the free energy available from with partly overlapping, partly differing func-
photon absorption into a change of biological tions. Photoreceptor function may vary in dif-
activity (99). The nature of the linker between ferent cell compartments (e.g., cytosol versus
by National Taiwan University on 06/01/10. For personal use only.

sensor and effector domain is therefore crucial nucleus) or tissues (e.g., root versus leaf ), and
in determining the extent of light regulation may further depend upon time of day and de-
(83, 98, 133). Knowledge of natural photore- velopmental stage.
ceptors, their structures, and signaling mecha- As we note in the Introduction and in the
nisms informs the design of artificial photore- section on LOV photoreceptors, sensor and
ceptors (99); and vice versa, the properties of effector domains are frequently studied in isola-
artificial photoreceptors yield insights relevant tion and their properties can differ from that of
for natural systems (98). the full-length protein. It is not fully known for
any plant photoreceptor how multiple domains
are arranged in space and how they interact with
FUTURE CHALLENGES each other. To give one example, there is no
AND OUTLOOK detailed information on the atomic structure of
The identity, structure, and photochemistry any plant phytochrome. We therefore strongly
of many photoreceptors have only been elu- advocate structural studies on full-length pro-
cidated recently. Advances in DNA technol- teins (10), preferably at atomic but also at lower
ogy have greatly facilitated the identification of resolution.
new members of known photoreceptor families Experimental results would be invaluable—
(e.g., References 101, 138). Although perhaps and far superior to any model—but one has to
less likely, completely new photoreceptor fami- be realistic. Such studies place high demands
lies based on novel photochemistry may remain on sample quality (purity) and quantity. They
to be discovered, as may combinations of pho- are complicated by the structural heterogene-
tosensors with other metabolic sensors. For ex- ity of signaling proteins: Structural changes in
ample, flavin cofactors serve as redox sensors in response to relatively small inputs of free energy
many proteins (124). It has long been known are inherent in all signaling systems, and flex-
that light can lead to photoreduction of the ibility forms an essential aspect of their func-
flavin ring, though in most cases photoreduc- tion (99). A further challenge derives from the
tion processes appear to be of no physiolog- fact that in vivo photoreceptors do not act in
ical relevance. However, a recent report sug- isolation but in concert with other sensors and
gests that the Oryza sativa protein HAL3 acts cellular components, many of which are as yet
as a combined redox and light sensor in vivo unidentified. Nevertheless, one should not be
(134). deterred.

40 Möglich et al.
 DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.

LITERATURE CITED
1. Ahmad M, Cashmore AR. 1993. HY4 gene of A. thaliana encodes a protein with characteristics of a
blue-light photoreceptor. Nature 366:162–66
2. Ahmad M, Lin C, Cashmore AR. 1995. Mutations throughout an Arabidopsis blue-light photoreceptor
impair blue-light-responsive anthocyanin accumulation and inhibition of hypocotyl elongation. Plant J.
8:653–58
3. Alexandre MT, Arents JC, van Grondelle R, Hellingwerf KJ, Kennis JT. 2007. A base-catalyzed mech-
anism for dark state recovery in the Avena sativa phototropin-1 LOV2 domain. Biochemistry 46:3129–37
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

4. Anantharaman V, Balaji S, Aravind L. 2006. The signaling helix: a common functional theme in diverse
signaling proteins. Biol. Direct. 1:25
5. Anantharaman V, Koonin EV, Aravind L. 2001. Regulatory potential, phyletic distribution and evolution
by National Taiwan University on 06/01/10. For personal use only.

of ancient, intracellular small-molecule-binding domains. J. Mol. Biol. 307:1271–92

6. Andel F 3rd, Murphy JT, Haas JA, McDowell MT, van der Hoef I, et al. 2000. Probing the photoreaction
mechanism of phytochrome through analysis of resonance Raman vibrational spectra of recombinant
analogues. Biochemistry 39:2667–76
7. Anderson S, Crosson S, Moffat K. 2004. Short hydrogen bonds in photoactive yellow protein. Acta
Crystallogr. D 60:1008–16
8. Anderson S, Dragnea V, Masuda S, Ybe J, Moffat K, Bauer C. 2005. Structure of a novel photoreceptor,
the BLUF domain of AppA from Rhodobacter sphaeroides. Biochemistry 44:7998–8005
9. Banerjee R, Schleicher E, Meier S, Viana RM, Pokorny R, et al. 2007. The signaling state of Arabidopsis
cryptochrome 2 contains flavin semiquinone. J. Biol. Chem. 282:14916–22
10. Barends TR, Hartmann E, Griese JJ, Beitlich T, Kirienko NV, et al. 2009. Structure and mechanism of
a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature 459:1015–18
11. Bogomolni RA, Spudich JL. 1982. Identification of a third rhodopsin-like pigment in phototactic
Halobacterium halobium. Proc. Natl. Acad. Sci. USA 79:6250–54
12. Borgstahl GE, Williams DR, Getzoff ED. 1995. 1.4 Å structure of photoactive yellow protein, a cytosolic
photoreceptor: unusual fold, active site, and chromophore. Biochemistry 34:6278–87
13. 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. 284:26005–16
14. Borucki B, von Stetten D, Seibeck S, Lamparter T, Michael N, et al. 2005. Light-induced proton release
of phytochrome is coupled to the transient deprotonation of the tetrapyrrole chromophore. J. Biol. Chem.
280:34358–64
15. Bouly JP, Giovani B, Djamei A, Mueller M, Zeugner A, et al. 2003. Novel ATP-binding and autophos-
phorylation activity associated with Arabidopsis and human cryptochrome-1. Eur. J. Biochem. 270:2921–28
16. Bouly JP, Schleicher E, Dionisio-Sese M, Vandenbussche F, Van Der Straeten D, et al. 2007. Cryp-
tochrome blue light photoreceptors are activated through interconversion of flavin redox states. J. Biol.
Chem. 282:9383–91
17. Brautigam CA, Smith BS, Ma Z, Palnitkar M, Tomchick DR, et al. 2004. Structure of the photolyase-like
domain of cryptochrome 1 from Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 101:12142–47
18. Brudler R, Hitomi K, Daiyasu H, Toh H, Kucho K, et al. 2003. Identification of a new cryptochrome
class. Structure, function, and evolution. Mol. Cell 11:59–67
19. Chapman S, Faulkner C, Kaiserli E, Garcia-Mata C, Savenkov EI, et al. 2008. The photoreversible
fluorescent protein iLOV outperforms GFP as a reporter of plant virus infection. Proc. Natl. Acad. Sci.
USA 105:20038–43
20. Chen M, Chory J, Fankhauser C. 2004. Light signal transduction in higher plants. Annu. Rev. Genet.
38:87–117

www.annualreviews.org • Structure and Function of Plant Photoreceptors 41

 21. Christie JM. 2007. Phototropin blue-light receptors. Annu. Rev. Plant Biol. 58:21–45
22. Christie JM, Corchnoy SB, Swartz TE, Hokenson M, Han IS, et al. 2007. Steric interactions stabilize
the signaling state of the LOV2 domain of phototropin 1. Biochemistry 46:9310–19
23. Christie JM, Reymond P, Powell GK, Bernasconi P, Raibekas AA, et al. 1998. Arabidopsis NPH1: a
flavoprotein with the properties of a photoreceptor for phototropism. Science 282:1698–701
24. Christie JM, Swartz TE, Bogomolni RA, Briggs WR. 2002. Phototropin LOV domains exhibit distinct
roles in regulating photoreceptor function. Plant J. 32:205–19
25. Cornilescu G, Ulijasz AT, Cornilescu CC, Markley JL, Vierstra RD. 2008. Solution structure of a
cyanobacterial phytochrome GAF domain in the red-light-absorbing ground state. J. Mol. Biol. 383:403–
13
26. Crosson S, Moffat K. 2001. Structure of a flavin-binding plant photoreceptor domain: insights into
light-mediated signal transduction. Proc. Natl. Acad. Sci. USA 98:2995–3000
27. Crosson S, Moffat K. 2002. Photoexcited structure of a plant photoreceptor domain reveals a light-driven
molecular switch. Plant Cell 14:1067–75
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

28. Crosson S, Rajagopal S, Moffat K. 2003. The LOV domain family: photoresponsive signaling modules
coupled to diverse output domains. Biochemistry 42:2–10
29. Dasgupta J, Frontiera RR, Taylor KC, Lagarias JC, Mathies RA. 2009. Ultrafast excited-state isomer-
by National Taiwan University on 06/01/10. For personal use only.

ization in phytochrome revealed by femtosecond stimulated Raman spectroscopy. Proc. Natl. Acad. Sci.
USA 106:1784–89
30. Davis SJ, Vener AV, Vierstra RD. 1999. Bacteriophytochromes: phytochrome-like photoreceptors from
nonphotosynthetic eubacteria. Science 286:2517–20
31. Deisseroth K, Feng G, Majewska AK, Miesenböck G, Ting A, Schnitzer MJ. 2006. Next-generation
optical technologies for illuminating genetically targeted brain circuits. J. Neurosci. 26:10380–86
32. Demarsy E, Fankhauser C. 2009. Higher plants use LOV to perceive blue light. Curr. Opin. Plant Biol.
12:69–74
33. Domratcheva T, Grigorenko BL, Schlichting I, Nemukhin AV. 2008. Molecular models predict light-
induced glutamine tautomerization in BLUF photoreceptors. Biophys. J. 94:3872–79
34. Drepper T, Eggert T, Circolone F, Heck A, Krauss U, et al. 2007. Reporter proteins for in vivo fluo-
rescence without oxygen. Nat. Biotechnol. 25:443–45
35. Ernst OP, Sánchez Murcia PA, Daldrop P, Tsunoda SP, Kateriya S, Hegemann P. 2008. Photoactivation
of channelrhodopsin. J. Biol. Chem. 283:1637–43
36. Essen LO. 2006. Photolyases and cryptochromes: common mechanisms of DNA repair and light-driven
signaling? Curr. Opin. Struct. Biol. 16:51–59
37. Essen LO, Mailliet J, Hughes J. 2008. The structure of a complete phytochrome sensory module in the
Pr ground state. Proc. Natl. Acad. Sci. USA 105:14709–14
38. Fedorov R, Schlichting I, Hartmann E, Domratcheva T, Fuhrmann M, Hegemann P. 2003. Crystal
structures and molecular mechanism of a light-induced signaling switch: the Phot-LOV1 domain from
Chlamydomonas reinhardtii. Biophys. J. 84:2474–82
39. Feldbauer K, Zimmermann D, Pintschovius V, Spitz J, Bamann C, Bamberg E. 2009. Channelrhodopsin-
2 is a leaky proton pump. Proc. Natl. Acad. Sci. USA 106:12317–22
40. Feynman RP. 1963. The Feynman Lectures on Physics. Menlo-Park, CA: Addison-Wesley
41. Finn RD, Mistry J, Schuster-Böckler B, Griffiths-Jones S, Hollich V, et al. 2006. Pfam: clans, web tools
and services. Nucleic Acids Res. 34:D247–51
42. Fischer AJ, Lagarias JC. 2004. Harnessing phytochrome’s glowing potential. Proc. Natl. Acad. Sci. USA
101:17334–39
43. Foerstendorf H, Lamparter T, Hughes J, Gärtner W, Siebert F. 2000. The photoreactions of recom-
binant phytochrome from the cyanobacterium Synechocystis: a low-temperature UV-Vis and FT-IR
spectroscopic study. Photochem. Photobiol. 71:655–61
44. Foster KW, Saranak J, Patel N, Zarilli G, Okabe M, et al. 1984. A rhodopsin is the functional photore-
ceptor for phototaxis in the unicellular eukaryote Chlamydomonas. Nature 311:756–59
45. Fuhrmann M, Stahlberg A, Govorunova E, Rank S, Hegemann P. 2001. The abundant retinal protein
of the Chlamydomonas eye is not the photoreceptor for phototaxis and photophobic responses. J. Cell Sci.
114:3857–63

42 Möglich et al.
 46. Gauden M, van Stokkum IH, Key JM, Lührs DC, van Grondelle R, et al. 2006. Hydrogen-bond switching
through a radical pair mechanism in a flavin-binding photoreceptor. Proc. Natl. Acad. Sci. USA 103:10895–
900
47. Gauger MA, Sancar A. 2005. Cryptochrome, circadian cycle, cell cycle checkpoints, and cancer. Cancer
Res. 65:6828–34
48. Gomelsky M, Kaplan S. 1998. AppA, a redox regulator of photosystem formation in Rhodobacter sphaeroides
2.4.1, is a flavoprotein. Identification of a novel FAD binding domain. J. Biol. Chem. 273:35319–25
49. Gomelsky M, Klug G. 2002. BLUF: a novel FAD-binding domain involved in sensory transduction in
microorganisms. Trends Biochem. Sci. 27:497–500
50. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K. 2009. Optical deconstruction of
parkinsonian neural circuitry. Science 324:354–59
51. Grinstead JS, Hsu ST, Laan W, Bonvin AM, Hellingwerf KJ, et al. 2006. The solution structure of the
AppA BLUF domain: insight into the mechanism of light-induced signaling. ChemBioChem 7:187–93
52. Halavaty AS, Moffat K. 2007. N- and C-terminal flanking regions modulate light-induced signal trans-
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

duction in the LOV2 domain of the blue light sensor phototropin 1 from Avena sativa. Biochemistry
46:14001–9
53. Harper SM, Christie JM, Gardner KH. 2004. Disruption of the LOV-Jalpha helix interaction activates
by National Taiwan University on 06/01/10. For personal use only.

phototropin kinase activity. Biochemistry 43:16184–92

54. Harper SM, Neil LC, Gardner KH. 2003. Structural basis of a phototropin light switch. Science 301:1541–
44
55. Hegemann P. 2008. Algal sensory photoreceptors. Annu. Rev. Plant Biol. 59:167–89
56. Hegemann P, Gärtner W, Uhl R. 1991. All-trans retinal constitutes the functional chromophore in
Chlamydomonas rhodopsin. Biophys. J. 60:1477–89
57. Henderson R, Baldwin JM, Ceska TA, Zemlin F, Beckmann E, Downing KH. 1990. Model for the
structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 213:899–
929
58. Hoang N, Bouly JP, Ahmad M. 2008. Evidence of a light-sensing role for folate in Arabidopsis cryp-
tochrome blue-light receptors. Mol. Plant 1:68–74
59. Holland EM, Braun FJ, Nonnengässer C, Harz H, Hegemann P. 1996. The nature of rhodopsin-
triggered photocurrents in Chlamydomonas. I. Kinetics and influence of divalent ions. Biophys. J. 70:924–
31
60. Huang Y, Baxter R, Smith BS, Partch CL, Colbert CL, Deisenhofer J. 2006. Crystal structure of cryp-
tochrome 3 from Arabidopsis thaliana and its implications for photolyase activity. Proc. Natl. Acad. Sci.
USA 103:17701–6
61. Hughes J, Lamparter T. 1999. Prokaryotes and phytochrome. The connection to chromophores and
signaling. Plant Physiol. 121:1059–68
62. Ihee H, Rajagopal S, Šrajer V, Pahl R, Anderson S, et al. 2005. Visualizing reaction pathways in pho-
toactive yellow protein from nanoseconds to seconds. Proc. Natl. Acad. Sci. USA 102:7145–50
63. Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA. 2003. FKF1 is essential for photoperiodic-
specific light signalling in Arabidopsis. Nature 426:302–6
64. Inoue S, Kinoshita T, Matsumoto M, Nakayama KI, Doi M, Shimazaki K. 2008. Blue light-induced
autophosphorylation of phototropin is a primary step for signaling. Proc. Natl. Acad. Sci. USA 105:5626–
31
65. Iseki M, Matsunaga S, Murakami A, Ohno K, Shiga K, et al. 2002. A blue-light-activated adenylyl cyclase
mediates photoavoidance in Euglena gracilis. Nature 415:1047–51
66. Iwata T, Yamamoto A, Tokutomi S, Kandori H. 2007. Hydration and temperature similarly affect light-
induced protein structural changes in the chromophoric domain of phototropin. Biochemistry 46:7016–21
67. Jung A, Domratcheva T, Tarutina M, Wu Q, Ko WH, et al. 2005. Structure of a bacterial BLUF photore-
ceptor: insights into blue light-mediated signal transduction. Proc. Natl. Acad. Sci. USA 102:12350–55
68. Jung A, Reinstein J, Domratcheva T, Shoeman RL, Schlichting I. 2006. Crystal structures of the AppA
BLUF domain photoreceptor provide insights into blue light-mediated signal transduction. J. Mol. Biol.
362:717–32

www.annualreviews.org • Structure and Function of Plant Photoreceptors 43

 69. Kasahara M, Swartz TE, Olney MA, Onodera A, Mochizuki N, et al. 2002. Photochemical properties
of the flavin mononucleotide-binding domains of the phototropins from Arabidopsis, rice, and Chlamy-
domonas reinhardtii. Plant Physiol. 129:762–73
70. Kateriya S, Nagel G, Bamberg E, Hegemann P. 2004. “Vision” in single-celled algae. News Physiol. Sci.
19:133–37
71. Kennis JT, Crosson S, Gauden M, van Stokkum IH, Moffat K, van Grondelle R. 2003. Primary reactions
of the LOV2 domain of phototropin, a plant blue-light photoreceptor. Biochemistry 42:3385–92
72. Kim WY, Fujiwara S, Suh SS, Kim J, Kim Y, et al. 2007. ZEITLUPE is a circadian photoreceptor
stabilized by GIGANTEA in blue light. Nature 449:356–60
73. Kinoshita T, Emi T, Tominaga M, Sakamoto K, Shigenaga A, et al. 2003. Blue-light- and
phosphorylation-dependent binding of a 14–3-3 protein to phototropins in stomatal guard cells of broad
bean. Plant Physiol. 133:1453–63
74. Kita A, Okajima K, Morimoto Y, Ikeuchi M, Miki K. 2005. Structure of a cyanobacterial BLUF protein,
Tll0078, containing a novel FAD-binding blue light sensor domain. J. Mol. Biol. 349:1–9
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

75. Klar T, Pokorny R, Moldt J, Batschauer A, Essen LO. 2007. Cryptochrome 3 from Arabidopsis thaliana:
structural and functional analysis of its complex with a folate light antenna. J. Mol. Biol. 366:954–64
76. Kneip C, Hildebrandt P, Schlamann W, Braslavsky SE, Mark F, Schaffner K. 1999. Protonation state
by National Taiwan University on 06/01/10. For personal use only.

and structural changes of the tetrapyrrole chromophore during the Pr → Pfr phototransformation of
phytochrome: a resonance Raman spectroscopic study. Biochemistry 38:15185–92
77. Kottke T, Heberle J, Hehn D, Dick B, Hegemann P. 2003. Phot-LOV1: photocycle of a blue-light
receptor domain from the green alga Chlamydomonas reinhardtii. Biophys. J. 84:1192–201
78. Koyama T, Iwata T, Yamamoto A, Sato Y, Matsuoka D, et al. 2009. Different role of the Jalpha helix in
the light-induced activation of the LOV2 domains in various phototropins. Biochemistry 48:7621–28
79. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, et al. 2001. Initial sequencing and analysis of
the human genome. Nature 409:860–921
80. Lawson MA, Zacks DN, Derguini F, Nakanishi K, Spudich JL. 1991. Retinal analog restoration of
photophobic responses in a blind Chlamydomonas reinhardtii mutant. Evidence for an archaebacterial like
chromophore in a eukaryotic rhodopsin. Biophys. J. 60:1490–98
81. Lee J, Natarajan M, Nashine VC, Socolich M, Vo T, et al. 2008. Surface sites for engineering allosteric
control in proteins. Science 322:438–42
82. Leung DW, Otomo C, Chory J, Rosen MK. 2008. Genetically encoded photoswitching of actin assembly
through the Cdc42-WASP-Arp2/3 complex pathway. Proc. Natl. Acad. Sci. USA 105:12797–802
83. Levskaya A, Chevalier AA, Tabor JJ, Simpson ZB, Lavery LA, et al. 2005. Synthetic biology: engineering
Escherichia coli to see light. Nature 438:441–42
84. Li QH, Yang HQ. 2007. Cryptochrome signaling in plants. Photochem. Photobiol. 83:94–101
85. Lim WA. 2002. The modular logic of signaling proteins: building allosteric switches from simple binding
domains. Curr. Opin. Struct. Biol. 12:61–68
86. Lin C, Shalitin D. 2003. Cryptochrome structure and signal transduction. Annu. Rev. Plant Biol. 54:469–
96
87. Lin C, Todo T. 2005. The cryptochromes. Genome Biol. 6:220
88. Litvin FF, Sineshchekov OA, Sineshchekov VA. 1978. Photoreceptor electric potential in the phototaxis
of the alga Haematococcus pluvialis. Nature 271:476–78
89. Losi A, Polverini E, Quest B, Gärtner W. 2002. First evidence for phototropin-related blue-light recep-
tors in prokaryotes. Biophys. J. 82:2627–34
90. Luecke H, Schobert B, Richter HT, Cartailler JP, Lanyi JK. 1999. Structural changes in bacterio-
rhodopsin during ion transport at 2 angstrom resolution. Science 286:255–61
91. Luecke H, Schobert B, Richter HT, Cartailler JP, Lanyi JK. 1999. Structure of bacteriorhodopsin at
1.55 Å resolution. J. Mol. Biol. 291:899–911
92. Más P, Kim WY, Somers DE, Kay SA. 2003. Targeted degradation of TOC1 by ZTL modulates
circadian function in Arabidopsis thaliana. Nature 426:567–70
93. Masuda S, Bauer CE. 2002. AppA is a blue light photoreceptor that antirepresses photosynthesis gene
expression in Rhodobacter sphaeroides. Cell 110:613–23

44 Möglich et al.
 94. Masuda S, Hasegawa K, Ishii A, Ono TA. 2004. Light-induced structural changes in a putative blue-light
receptor with a novel FAD binding fold sensor of blue-light using FAD (BLUF); Slr1694 of Synechocystis
sp. PCC6803. Biochemistry 43:5304–13
95. Mathes T, Vogl C, Stolz J, Hegemann P. 2009. In vivo generation of flavoproteins with modified cofac-
tors. J. Mol. Biol. 385:1511–18
96. Matsuoka D, Iwata T, Zikihara K, Kandori H, Tokutomi S. 2007. Primary processes during the light-
signal transduction of phototropin. Photochem. Photobiol. 83:122–30
97. Matsuoka D, Tokutomi S. 2005. Blue light-regulated molecular switch of Ser/Thr kinase in phototropin.
Proc. Natl. Acad. Sci. USA 102:13337–42
98. Möglich A, Ayers RA, Moffat K. 2009. Design and signaling mechanism of light-regulated histidine
kinases. J. Mol. Biol. 385:1433–44
99. Möglich A, Ayers RA, Moffat K. 2009. Structure and signaling mechanism of Per-ARNT-Sim domains.
Structure 17:1282–94
100. Müller M, Carell T. 2009. Structural biology of DNA photolyases and cryptochromes. Curr. Opin. Struct.
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

Biol. 19:277–85
101. Nagel G, Ollig D, Fuhrmann M, Kateriya S, Musti AM, et al. 2002. Channelrhodopsin-1: a light-gated
proton channel in green algae. Science 296:2395–98
by National Taiwan University on 06/01/10. For personal use only.

102. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, et al. 2003. Channelrhodopsin-2, a directly
light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 100:13940–45
103. Nakasako M, Zikihara K, Matsuoka D, Katsura H, Tokutomi S. 2008. Structural basis of the LOV1
dimerization of Arabidopsis phototropins 1 and 2. J. Mol. Biol. 381:718–33
104. Nakasone Y, Eitoku T, Matsuoka D, Tokutomi S, Terazima M. 2006. Kinetic measurement of transient
dimerization and dissociation reactions of Arabidopsis phototropin 1 LOV2 domain. Biophys. J. 91:645–53
105. Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B. 2000. FKF1, a clock-controlled gene that
regulates the transition to flowering in Arabidopsis. Cell 101:331–40
106. Oesterhelt D, Stoeckenius W. 1973. Functions of a new photoreceptor membrane. Proc. Natl. Acad. Sci.
USA 70:2853–57
107. Ogura Y, Komatsu A, Zikihara K, Nanjo T, Tokutomi S, et al. 2008. Blue light diminishes interaction of
PAS/LOV proteins, putative blue light receptors in Arabidopsis thaliana, with their interacting partners.
J. Plant Res. 121:97–105
108. Özgür S, Sancar A. 2006. Analysis of autophosphorylating kinase activities of Arabidopsis and human
cryptochromes. Biochemistry 45:13369–74
109. Partch CL, Clarkson MW, Özgür S, Lee AL, Sancar A. 2005. Role of structural plasticity in signal
transduction by the cryptochrome blue-light photoreceptor. Biochemistry 44:3795–805
110. Pawson T, Nash P. 2003. Assembly of cell regulatory systems through protein interaction domains.
Science 300:445–52
111. Pokorny R, Klar T, Hennecke U, Carell T, Batschauer A, Essen LO. 2008. Recognition and repair of
UV lesions in loop structures of duplex DNA by DASH-type cryptochrome. Proc. Natl. Acad. Sci. USA
105:21023–27
112. Rockwell NC, Lagarias JC. 2006. The structure of phytochrome: a picture is worth a thousand spectra.
Plant Cell 18:4–14
113. Rockwell NC, Su YS, Lagarias JC. 2006. Phytochrome structure and signaling mechanisms. Annu. Rev.
Plant Biol. 57:837–58
114. Rohmer T, Lang C, Hughes J, Essen LO, Gärtner W, Matysik J. 2008. Light-induced chromophore
activity and signal transduction in phytochromes observed by 13C and 15N magic-angle spinning NMR.
Proc. Natl. Acad. Sci. USA 105:15229–34
115. Rohmer T, Strauss H, Hughes J, de Groot H, Gärtner W, et al. 2006. 15N MAS NMR studies of
cph1 phytochrome: chromophore dynamics and intramolecular signal transduction. J. Phys. Chem. B
110:20580–85
116. Rosenfeldt G, Muñoz-Viana R, Mootz HD, von Arnim AG, Batschauer A. 2008. Chemically induced
and light-independent cryptochrome photoreceptor activation. Mol. Plant 1:4–14
117. Salomon M, Eisenreich W, Dürr H, Schleicher E, Knieb E, et al. 2001. An optomechanical transducer
in the blue light receptor phototropin from Avena sativa. Proc. Natl. Acad. Sci. USA 98:12357–61

www.annualreviews.org • Structure and Function of Plant Photoreceptors 45

 118. Sancar A. 2003. Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors.
Chem. Rev. 103:2203–37
119. Sang Y, Li QH, Rubio V, Zhang YC, Mao J, et al. 2005. N-terminal domain-mediated homodimerization
is required for photoreceptor activity of Arabidopsis CRYPTOCHROME 1. Plant Cell 17:1569–84
120. Sasaki J, Spudich JL. 2008. Signal transfer in haloarchaeal sensory rhodopsin- transducer complexes.
Photochem. Photobiol. 84:863–68
121. Sawa M, Nusinow DA, Kay SA, Imaizumi T. 2007. FKF1 and GIGANTEA complex formation is
required for day-length measurement in Arabidopsis. Science 318:261–65
122. Schleicher E, Kowalczyk RM, Kay CW, Hegemann P, Bacher A, et al. 2004. On the reaction mechanism
of adduct formation in LOV domains of the plant blue-light receptor phototropin. J. Am. Chem. Soc.
126:11067–76
123. Schröder-Lang S, Schwärzel M, Seifert R, Strünker T, Kateriya S, et al. 2007. Fast manipulation of
cellular cAMP level by light in vivo. Nat. Methods 4:39–42
124. Senda T, Senda M, Kimura S, Ishida T. 2009. Redox control of protein conformation in flavoproteins.
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

Antioxid. Redox Signal. 11:1741–66

125. Shalitin D, Yang H, Mockler TC, Maymon M, Guo H, et al. 2002. Regulation of Arabidopsis cryptochrome
2 by blue-light-dependent phosphorylation. Nature 417:763–67
by National Taiwan University on 06/01/10. For personal use only.

126. Shalitin D, Yu X, Maymon M, Mockler T, Lin C. 2003. Blue light-dependent in vivo and in vitro
phosphorylation of Arabidopsis cryptochrome 1. Plant Cell 15:2421–29
127. Shu X, Royant A, Lin MZ, Aguilera TA, Lev-Ram V, et al. 2009. Mammalian expression of infrared
fluorescent proteins engineered from a bacterial phytochrome. Science 324:804–7
128. Sineshchekov OA, Govorunova EG, Spudich JL. 2009. Photosensory functions of channelrhodopsins in
native algal cells. Photochem. Photobiol. 85:556–63
129. Sineshchekov OA, Jung KH, Spudich JL. 2002. Two rhodopsins mediate phototaxis to low- and high-
intensity light in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 99:8689–94
130. Somers DE, Schultz TF, Milnamow M, Kay SA. 2000. ZEITLUPE encodes a novel clock-associated
PAS protein from Arabidopsis. Cell 101:319–29
131. Spudich JL, Yang CS, Jung KH, Spudich EN. 2000. Retinylidene proteins: structures and functions from
archaea to humans. Annu. Rev. Cell Dev. Biol. 16:365–92
132. Strauss HM, Hughes J, Schmieder P. 2005. Heteronuclear solution-state NMR studies of the chro-
mophore in cyanobacterial phytochrome Cph1. Biochemistry 44:8244–50
133. Strickland D, Moffat K, Sosnick TR. 2008. Light-activated DNA binding in a designed allosteric protein.
Proc. Natl. Acad. Sci. USA 105:10709–14
134. Sun SY, Chao DY, Li XM, Shi M, Gao JP, et al. 2009. OsHAL3 mediates a new pathway in the light-
regulated growth of rice. Nat. Cell Biol. 11:845–51
135. Suzuki T, Yamasaki K, Fujita S, Oda K, Iseki M, et al. 2003. Archaeal-type rhodopsins in Chlamydomonas:
model structure and intracellular localization. Biochem. Biophys. Res. Commun. 301:711–17
136. Swartz TE, Corchnoy SB, Christie JM, Lewis JW, Szundi I, et al. 2001. The photocycle of a flavin-
binding domain of the blue light photoreceptor phototropin. J. Biol. Chem. 276:36493–500
137. Swartz TE, Tseng TS, Frederickson MA, Paris G, Comerci DJ, et al. 2007. Blue-light-activated histidine
kinases: two-component sensors in bacteria. Science 317:1090–93
138. Takahashi F, Yamagata D, Ishikawa M, Fukamatsu Y, Ogura Y, et al. 2007. AUREOCHROME, a
photoreceptor required for photomorphogenesis in stramenopiles. Proc. Natl. Acad. Sci. USA 104:19625–
30
139. Taylor BL, Zhulin IB. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol.
Mol. Biol. Rev. 63:479–506
140. Tittor J, Oesterhelt D. 1990. The quantum yield of bacteriorhodopsin. FEBS Lett. 263:269–73
141. Tsien RY. 2009. Constructing and exploiting the fluorescent protein paintbox (Nobel Lecture). Angew.
Chem. Int. Ed. Engl. 48:5612–26
142. Tsunoda SP, Ewers D, Gazzarrini S, Moroni A, Gradmann D, Hegemann P. 2006. H+ –pumping
rhodopsin from the marine alga Acetabularia. Biophys. J. 91:1471–79

46 Möglich et al.
 143. Ulijasz AT, Cornilescu G, von Stetten D, Kaminski S, Mroginski MA, et al. 2008. Characterization of
two thermostable cyanobacterial phytochromes reveals global movements in the chromophore-binding
domain during photoconversion. J. Biol. Chem. 283:21251–66
144. Ulrich LE, Koonin EV, Zhulin IB. 2005. One-component systems dominate signal transduction in
prokaryotes. Trends Microbiol. 13:52–56
145. The UniProt Consortium. 2008. The universal protein resource (UniProt). Nucleic Acids Res. 36:D190–95
146. van der Horst MA, Hellingwerf KJ. 2004. Photoreceptor proteins, “star actors of modern times”: a review
of the functional dynamics in the structure of representative members of six different photoreceptor
families. Acc. Chem. Res. 37:13–20
147. van Thor JJ, Borucki B, Crielaard W, Otto H, Lamparter T, et al. 2001. Light-induced proton release
and proton uptake reactions in the cyanobacterial phytochrome Cph1. Biochemistry 40:11460–71
148. van Thor JJ, Mackeen M, Kuprov I, Dwek RA, Wormald MR. 2006. Chromophore structure in the
photocycle of the cyanobacterial phytochrome Cph1. Biophys. J. 91:1811–22
149. Vierstra RD, Davis SJ. 2000. Bacteriophytochromes: new tools for understanding phytochrome signal
Annu. Rev. Plant Biol. 2010.61:21-47. Downloaded from arjournals.annualreviews.org

transduction. Semin. Cell Dev. Biol. 11:511–21

150. 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 438:325–31
by National Taiwan University on 06/01/10. For personal use only.

151. Wagner JR, Zhang J, von Stetten D, Günther M, Murgida DH, et al. 2008. Mutational analysis of
Deinococcus radiodurans bacteriophytochrome reveals key amino acids necessary for the photochromicity
and proton exchange cycle of phytochromes. J. Biol. Chem. 283:12212–26
152. Wang H, Ma LG, Li JM, Zhao HY, Deng XW. 2001. Direct interaction of Arabidopsis cryptochromes
with COP1 in light control development. Science 294:154–58
153. Wu Q, Gardner K. 2009. Structure and insight into blue light-induced changes in the BlrP1 BLUF
domain. Biochemistry 48:2620–29
154. Wu YI, Frey D, Lungu OI, Jaehrig A, Schlichting I, et al. 2009. A genetically encoded photoactivatable
Rac controls the motility of living cells. Nature 461:104–108
155. Yang HQ, Tang RH, Cashmore AR. 2001. The signaling mechanism of Arabidopsis CRY1 involves direct
interaction with COP1. Plant Cell 13:2573–87
156. Yang HQ, Wu YJ, Tang RH, Liu D, Liu Y, Cashmore AR. 2000. The C termini of Arabidopsis cryp-
tochromes mediate a constitutive light response. Cell 103:815–27
157. Yang X, Kuk J, Moffat K. 2008. Crystal structure of Pseudomonas aeruginosa bacteriophytochrome: pho-
toconversion and signal transduction. Proc. Natl. Acad. Sci. USA 105:14715–20
158. Yang X, Kuk J, Moffat K. 2009. Conformational differences between the Pfr and Pr states in Pseudomonas
aeruginosa bacteriophytochrome. Proc. Natl. Acad. Sci. USA. 106:15639–44
159. 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 104:12571–76
160. Yuan H, Bauer CE. 2008. PixE promotes dark oligomerization of the BLUF photoreceptor PixD. Proc.
Natl. Acad. Sci. USA 105:11715–19
161. Zeugner A, Byrdin M, Bouly JP, Bakrim N, Giovani B, et al. 2005. Light-induced electron transfer in
Arabidopsis cryptochrome-1 correlates with in vivo function. J. Biol. Chem. 280:19437–40
162. Zhang F, Prigge M, Beyriere F, Tsunoda SP, Mattis J, et al. 2008. Red-shifted optogenetic excitation: a
tool for fast neural control derived from Volvox carteri. Nat. Neurosci. 11:631–33
163. Zoltowski BD, Schwerdtfeger C, Widom J, Loros JJ, Bilwes AM, et al. 2007. Conformational switching
in the fungal light sensor Vivid. Science 316:1054–57

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 Annual Review of
Plant Biology

Contents Volume 61, 2010

A Wandering Pathway in Plant Biology: From Wildflowers to

Phototropins to Bacterial Virulence
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Winslow R. Briggs p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Structure and Function of Plant Photoreceptors
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Auxin Biosynthesis and Its Role in Plant Development
Yunde Zhao p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p49
Computational Morphodynamics: A Modeling Framework to
Understand Plant Growth
Vijay Chickarmane, Adrienne H.K. Roeder, Paul T. Tarr, Alexandre Cunha,
Cory Tobin, and Elliot M. Meyerowitz p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p65
Female Gametophyte Development in Flowering Plants
Wei-Cai Yang, Dong-Qiao Shi, and Yan-Hong Chen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p89
Doomed Lovers: Mechanisms of Isolation and Incompatibility in Plants
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Chloroplast RNA Metabolism
David B. Stern, Michel Goldschmidt-Clermont, and Maureen R. Hanson p p p p p p p p p p p p p p 125
Protein Transport into Chloroplasts
Hsou-min Li and Chi-Chou Chiu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 157
The Regulation of Gene Expression Required for C4 Photosynthesis
Julian M. Hibberd and Sarah Covshoff p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 181
Starch: Its Metabolism, Evolution, and Biotechnological Modification
in Plants
Samuel C. Zeeman, Jens Kossmann, and Alison M. Smith p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 209
Improving Photosynthetic Efficiency for Greater Yield
Xin-Guang Zhu, Stephen P. Long, and Donald R. Ort p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 235
Hemicelluloses
Henrik Vibe Scheller and Peter Ulvskov p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 263
Diversification of P450 Genes During Land Plant Evolution
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v
 Evolution in Action: Plants Resistant to Herbicides
Stephen B. Powles and Qin Yu p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 317
Insights from the Comparison of Plant Genome Sequences
Andrew H. Paterson, Michael Freeling, Haibao Tang, and Xiyin Wang p p p p p p p p p p p p p p p p 349
High-Throughput Characterization of Plant Gene Functions by Using
Gain-of-Function Technology
Youichi Kondou, Mieko Higuchi, and Minami Matsui p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 373
Histone Methylation in Higher Plants
Chunyan Liu, Falong Lu, Xia Cui, and Xiaofeng Cao p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 395
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Genetic and Molecular Basis of Rice Yield

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Genetic Engineering for Modern Agriculture: Challenges and

Perspectives
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Metabolomics for Functional Genomics, Systems Biology, and
Biotechnology
Kazuki Saito and Fumio Matsuda p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 463
Quantitation in Mass-Spectrometry-Based Proteomics
Waltraud X. Schulze and Björn Usadel p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 491
Metal Hyperaccumulation in Plants
Ute Krämer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 517
Arsenic as a Food Chain Contaminant: Mechanisms of Plant Uptake
and Metabolism and Mitigation Strategies
Fang-Jie Zhao, Steve P. McGrath, and Andrew A. Meharg p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 535
Guard Cell Signal Transduction Network: Advances in Understanding
Abscisic Acid, CO2 , and Ca2+ Signaling
Tae-Houn Kim, Maik Böhmer, Honghong Hu, Noriyuki Nishimura,
and Julian I. Schroeder p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 561
The Language of Calcium Signaling
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Mitogen-Activated Protein Kinase Signaling in Plants
Maria Cristina Suarez Rodriguez, Morten Petersen, and John Mundy p p p p p p p p p p p p p p p p p 621
Abscisic Acid: Emergence of a Core Signaling Network
Sean R. Cutler, Pedro L. Rodriguez, Ruth R. Finkelstein, and Suzanne R. Abrams p p p p 651
Brassinosteroid Signal Transduction from Receptor Kinases to
Transcription Factors
Tae-Wuk Kim and Zhi-Yong Wang p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 681

vi Contents
 Directional Gravity Sensing in Gravitropism
Miyo Terao Morita p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 705

Indexes
Cumulative Index of Contributing Authors, Volumes 51–61 p p p p p p p p p p p p p p p p p p p p p p p p p p p 721
Cumulative Index of Chapter Titles, Volumes 51–61 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 726

Errata
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