Plant photoreceptors- their structure, function and signalling mechanisms.

Anushka Mondal(am18ms205)
Introduction:

Photoreceptor proteins are light-sensitive proteins that are involved in sensing and giving
response to light in plants. Photoreceptor proteins usually consist of a protein which is attached
to a non-protein photopigment that reacts to light via photoreduction.This initiates a change of
the receptor protein that further triggers a signal transduction cascade. Light influences vital
aspects of the development, morphology, and metabolism of plants by generating an initial signal
by absorbing a photon of visible light, and transmitting this signal via intricate molecular and
metabolic pathways. These features are perceived by Signaling photoreceptors which use the
information contained in the absorption of a photon to modulate biological activity in plants and
a wide range of organisms[1]. There are six classes of photoreceptors that are known:
light-oxygen-voltage (LOV) sensors, phytochromes, xanthopsins, blue-light sensors using flavin
adenine dinucleotide (BLUF), cryptochromes, and rhodopsins. They are all water-soluble
proteins except for rhodopsins, which are an integral part of membrane proteins. The absorption
characteristics of photoreceptors are similar to the spectrum of light that falls on them, usually,
the sun's spectrum in the Earth's range from the nearest UV (∼350 nm) to blue to very red/red
(∼750 nm), which is filtered, for example, a canopy of leaves. Because the polypeptide backbone
and amino acid chains do not absorb this visible spectrum, all photoreceptors contain an organic,
non-protein compound known as chromophore that acts as the primary source of photon
absorption and may be bound together with or without protein synthesis. The larger the
chromophore, the greater the degree of electron delocalization and the longer the wavelength it
will absorb. Changes in affinity are basically thermodynamic in nature; therefore the signal has
both thermodynamic as well as structural features [2]. Each chromophore represents
photochemistry and photophysics, and some photoreceptors use different chemical processes.
There are 2 characteristic features of both photoreceptors and chemoreceptors that are both
modular in their architecture, and each of the modules is associated with a different aspect of
receptor function [3]. Usually, a photoreceptor consists of several discrete protein units known as
modules or domains, each of which forms a cohesive component sequence. When the domains
are mixed up during evolution it conferred greater phenotypic complexity in signalling and
regulation[4]. This is the reason why a single class of photosensor domain such as the LOV
Bluelight sensors is found attached to a very wide range of effector domains covalently that
differ in their tertiary structure and biological activity as well [5]. Now their structure, function
and signalling mechanisms will be discussed below.

Light-oxygen-voltage (LOV) sensors: Light-oxygen-voltage (LOV) receptors are sensory

proteins that control a wide range of organismal adaptations in different kingdoms of life. Since
they have a modular nature, LOV domains can be used as optogenetic actuators. A flavin
chromophore is a protein that absorbs blue light, forms a bond that has a proximal cysteine
residue, and induces changes in its surroundings. Light perception is very crucial to most
organisms, and thus several families of photoreceptor proteins exist to sense this environmental
cue. Among these photoreceptors, LOV photoreceptors respond to blue light and help in
mediating diverse processes such as phototropism in plants[6]. To carry on this broad range of
biochemical modes of action, the proteins consist of LOV photo sensor domains, which are
functionally coupled to a variety of specialized transducer and effector modules[7]. This
modularity of LOV receptors makes them vital for the construction of genetically encoded
light-sensitive proteins[8]. In the photosensor domains of LOV, signals are generated via
absorption of blue light which is 450 nm by a flavin nucleotide chromophore, that can be a flavin
mononucleotide (FMN) or a flavin adenine dinucleotide in Fig.1. [9].
 Fig.1.
After the photon is absorbed by the dark-adapted state (FMNA450), an exciting flavin singlet
state (FMN*) is populated at a time scale of picosecond [10]. This state then decays into a triplet
state(FMNT) over several nanoseconds[11]. Within a few microseconds, a covalent thiol adduct
is being formed between a flavin atom C4a and a cysteine residue of the LOV photosensor[12]
through a radical intermediate. The flavin-cysteinyl photoproduct is usually metastable whose
lifetimes range from seconds to hours depending on the chromophore environment, temperature,
and solvent conditions[13]. The conserved glutamine residue rotates by around 180 in response
to N5 protonation and is constituted by a focal point of signal transduction[13]. Although the
mechanism of photochemistry appears conserved across all known LOV receptors, depending on
the protein architecture, LOV activation can take place resulting in dimerization or
monomerization[14] of the whole photoreceptor protein.

Fig.2.
LOV domains usually constitute a subclass of a family known as the PerARNT-Sim (PAS)
family whose members can serve as versatile sensors as well as perform interaction domains in
diverse groups of signalling proteins[15]. The first structure of a LOV domain and that of the
LOV2 domain of Adiantum capillus-veneris neochrome 1[16], is found in the canonical PAS
fold. The LOV2 domain of Avena sativa phototropin 1, the domain of PAS core comprises a
five-stranded antiparallel β sheet, which has strands that are in the topological order
BβAβ-Iβ-Hβ-Gβ (such that, 2-1-5-4-3), and several α helices (Cα, Dα, Eα, Fα) are packed on
either side of the sheet in Fi.3.
 Fig.3.

The flavin nucleotide cofactor, a flavin mononucleotide (FMN) in the LOV plant proteins, is
bound to a ridge formed by a central β sheet and helices Eα and Fα. A separate series of nearby,
stored glutamine residues is proposed to rotate and thus alter its hydrogen-bonding pattern [17].
In the domain of A. sativa phototropin 1 LOV2, other structural changes occur within the β sheet
and the C-terminal Jα helix from the middle [18] (Figure 4).

Fig.4.
The nuclear magnetic resonance (NMR) data suggest that this Jα helix is ​open [19]. Infrared
spectroscopic results suggest that these reactions persist with different moderate structures [20]
remaining for full visualization. Light-induced structural changes are usually relatively small and
(with the exception of Jα helix) are mainly confined to the surrounding flavin area, which may be
for a number of reasons. Light-induced light-induced changes may be affected by quality or
reduction in crystal clear or by photoreceptor separation, or changes may be naturally strong, and
may be associated with greater atomic translation.
Functions:-
Light-oxygen-voltage (LOV) domains use flavin nucleotide cofactors to detect blue light.
Originally detected as tandem sensory domains in plant photoreceptor phototropin [21], LOV
domains have since been found in a few plants, fungi, and bacterial proteins [22]. In plants, to
date, three families of bona fide photoreceptors using LOV domains have been identified. First,
phototropin 1 and 2 mediate a variety of rapid reactions, caused by light in plants, including
phototropism, chloroplast and leaf movements, and diarrhoea. Second, the proteins of the
ZEITLUPE family regulate slower light reactions such as circadian clock entry and flowering
[23]. Third, autochromes emerge from photosynthetic stramenopiles and regulate morphogenesis
features in light response [24]. The basis for this variation may be linked to protein mutations, or
solvent access, and a specific flavin chromophore [25], in which genetic mutations can
significantly affect photocycle kinetics [26]. Phototropins, a combination of protein-regulated
proteins, are important in the signal transmission of the ZEITLUPE family protein [27].

Phototropins: Phototropins usually comprise two LOV domains, LOV1 and LOV2, and a
serine/threonine kinase domain[ 28]. Itundergo autophosphorylation at several serine and
threonine residues but no other physiological phosphorylation target has been identified[29.
Recent research data on phototropins indicate that autophosphorylation is essential for a
particular serine residue in the kinase activation loop. This is true for all phototropin-dependent
responses; phosphorylation at other sites may be required for specific phototropin-dependent
responses[30] . Repressing the phototropin kinase activity in the dark is relieved upon blue-light
absorption by the LOV2 domain[31] . However, the photochemically identical LOV1 domain is
not at all important for the regulation of light kinase activity. It attenuates the effect of LOV2 and
it may also contribute to dimerization. Structural[32] and functional[33] data implicate the
unfolding of the Jα helix in the light regulation of phototropin kinase activity. Though the
molecular details remain elusive, light-dependent interactions both among individual phototropin
domains[34] and between other proteins and phototropin, such as 14–3-3 proteins[35] and
presumably the unidentified phosphorylation targets of phototropin, play key roles in signalling.
ZEITLUPE family: The A. thaliana ZEITLUPE, FKF1, LKP2 and proteins is comprised of a
LOV domain which is followed by an F-box domain and several Kelch repeats in Fig.5. [36].
The ubiquitin-dependent protein degradation is maintained by these proteins in a light-controlled
manner[37], ultimately leading to photoperiodic expression and/or accumulation[38] of key
proteins involved in regulating the circadian clock and flowering onset. Structural information is
not available on ZEITLUPE proteins, and their detailed mechanism of action is only beginning
to be understood[39] . As for phototropin, light-regulated protein interactions are crucial for
signal transduction of the ZEITLUPE-family proteins[40].

Fig.5.
Autochromes: Stramenopile autochromes are transcription factors that comprise an N-terminal
basic-zipper DNA-binding domain and a C-terminal LOV domain, thus resembling the modular
composition of bacterial one-component systems[41] . Bluelight absorption increases the affinity
of the basic-zipper domain for DNA. The autochromes also regulate cell branching and
differentiation [42].

Xanthopsins:
The family of the xanthopsins is the photoreceptor family that carries trans-p-coumaric acid,
through a thiol-ester linkage, as its light-sensitive chromophore. It is sensitive to yellow light.
PYP displays a typical R/β fold, with a central five-stranded β-sheet and helical segments on
either side, which has become the prototype for the PAS domain, key element in biological signal
transfer. Photoactive yellow protein or PYP is a small, cytoplasmic photoreceptor that is made up
of 126 amino acids that, upon absorbing blue light, usually undergoes a reversible photocycle
that span [43]. PYP thus represents an isolated sensor domain in Fig.6., demonstrating the
xanthopsin class of photoreceptors.

Fig.5.

Plants don't have any homolog of PYP. PYP usually serves as the structural paradigm for the
PAS domain family, of which LOV domain forms a significant part. Through the application of
time-resolved crystallography, ultrafast spectroscopic techniques, and NMR PYP has the ability
to provide the results in details about the photocycle of any photosensor domain at the atomic
level. The PYP contains a 4-hydroxycinnamic acid chromophore, which is covalently attached
by a thioester bond to a cysteine residue and is completely buried in the interior part of the
protein in Fig.7.

Fig.7.

The most vital photochemical event is the isomerization of trans to cis about the double bond
which lies in the tail part of its chromophore. Generally, in the dark ground state, the phenolate
anion at the head of the chromophore is stabilized by unusually short hydrogen bonds[44] to the
nearest glutamic acid as well as tyrosine side chains. The partial unfolding of the Cα helix, which
contains these glutamic acids and tyrosine residues; and, ultimately, unfolding of a pair of short,
N-terminal α helices packed on the distal side of the β sheet, which forms the structural core of
all PAS and LOV domains including PYP. These intermediates differ in tertiary structure. Each,
therefore, represents a distinct structural signal, which could differ in affinity for another protein
to which the signal could be transmitted. More recent studies have extended the time resolution
toward 100 picoseconds to explore isomerization itself and characterize earlier stages of the
photocycle. Although ultimately unsatisfying from a physiological standpoint, these studies on
PYP point the way to an understanding at the atomic level of the generation of a structural signal
in an isolated photo sensor domain. But small is not simple; even PYP turns out to be deceptively
complicated when studied in detail.

Rhodopsins:
Rhodopsins are an integral membrane proteins. Light detection is achieved via retinal
chromophore that is covalently attached to a lysine residue as protonated Schiff base. It is long
recognized as the photoreceptor in animal vision, related rhodopsins were subsequently
identified as photoreceptors in algae [45] and microorganisms [46]. Known plant rhodopsins
belong to the microbial type-1 rhodopsins [47], which are exemplified by bacteriorhodopsin[48].
Channelrhodopsins mediate phototaxis in flagellate algae[49], and were first identified in
Chlamydomonas reinhardtii as light-gated cation channels[ 50 ] in Fig.8. Chlamydomonas also
expresses other kinds of rhodopsins for which no clear functional role has yet been ascertained .
The first identified chlamyopsins 1 and 2 are prevalent in the Chlamydomonas eyespot but their
physiological role is unclear [51] . In chlamyopsins 5– 7, renowned as the enzyme rhodopsins,
rhodopsin sensor domains are covalently linked to response regulator, histidine kinase, or
adenylate cyclase / guanylate cyclase effector domains[52] . Other algal rhodopsins [53]
function as light driven H+ pumps similar to bacteriorhodopsin though their physiological role
remains mysterious in photosynthetic organisms [54].

Fig.8
Rhodopsin Photochemistry: Like in bacteriorhodopsin, the retinal chromophore of algal
rhodopsins adopts the alltrans conformation in its dark adapted state D470 [55]. Upon blue light
absorption around 470 nm, the retinal moiety isomerizes to the 13-cis form [56]. Long hindered
by limited protein availability, indetailed spectroscopic studies of the photocycle of Volvox
carteri channelrhodopsin became achievable recently [57]. Briefly, the initial photoexcited state
P500 interconverts to the P510 state within 200 μsec through an intermediate with the help
deprotonated Schiff base.

Fig.9.
Rhodopsin Structure: In the lack of high resolution structures, plant rhodopsins are expected to
structurally mirror homologous microbial rhodopsins[58]. As shown for bacteriorhodopsin [59],
microbial rhodopsins belong to the large family of seven helix transmembrane proteins[60] .
Seven alpha helices connected by short loops traverse the plasma membrane and congregate into
a barrel-like bundle. The retinal chromophore is embedded in the middle of the bundle through
the residues that are highly conserved in algal rhodopsins[61]. Studies by cryoelectron
microscopy and crystallography on bacteriorhodopsin revealed in great detail its structure and
light induced conformational changes throughout the photocycle [62] . However, these findings
may not fully apply to algal rhodopsins, and corresponding homology models are almost
certainly deficient in their molecular details [63]. More informative answers will be provided by
3-dimensional structures of the plant rhodopsins, which are improved by recent advances in
recombinant production of channelrhodopsins[57] .
 Fig.10
Rhodopsin Signal Transduction: Phototaxis in Chlamydomonas and related algae involves
photocurrents driven by cation influx across the plasma membrane [64] . Such photo currents
depend on the action of channelrhodopsins [65] and appear within microseconds after light
excitation [66]. Heterologous expression of channelrhodopsin in the oocytes established their
function as light gated ion channels [67]. Although in algae the photocurrent is majorly carried
by Ca2+ and H+ [68], channelrhodopsins are also permeable for other mono and divalent cations
[69] . These properties are exploited in so called optogenetic applications in the field of
neuroscience [70], where channelrhodopsin-2 [72] is highly used because it achieves higher
photo currents than channelrhodopsin-1 [73]. The gating mechanism of channelrhodopsins was
not understood completely but certain aspects might be shared with bacteriorhodopsin.
Particularly, channelrhodopsin-2 also displays H+ pumping activity and could thus be considered
as a “leaky proton pump” [74]. In native algae, part of the channelrhodopsin photoreceptors
function might be mediated by regulation of unidentified downstream proteins similar to
microbial sensory rhodopsins [75]. Such function might reside in the long C terminal half of
channelrhodopsins, which is not required for light gated channel activity [76].

Phytochromes: In 1959 phytochromes were first discovered in plants as photoreceptors.

Phytochromes mediate plant growth and development in response to long-wavelength visible
light [77]. These are red/far-red photochromic biliprotein photoreceptors in plants regulating
about 20% of all genes and mediating fundamental effects of light on development such as
germination, de-etiolation, and flowering[78]. Higher plant phytochromes are soluble
chromoproteins that exist as homo- or heterodimers of two 125 kD polypeptides, each with a
covalently attached linear tetrapyrrole bilin chromophore to sense red/far-red light Absorption of
a photon causes the inactive red-absorbing inactive Pr spectroscopic form to photo-convert to the
far-red-absorbing active Pfr spectroscopic form; absorption of a second photon causes reversion
to the inactive Pr form[79]. During these transitions, structural changes occur in the protein, on
the micro-and millisecond time scale, and proton uptake and release reactions[80]. The canonical
phytochromes have a conserved N-terminal photosensory core and a C-terminal regulatory
region, typically including a histidine-kinase-related domain. Two N-terminal domains PAS and
GAF, form a chromophore binding module or CBM that displays only limited photoconversion
from the dark state. However, the addition of the phytochrome-specific (PHY) domain yields the
three-domain, PAS-GAF-PHY, photosensory core module (PCM) that retains the fundamental
photoconversion properties of total length proteins . The C-terminal effector domain in
bacteriophytochromes is a histidine kinase (HK) domain and forms part of a two-component
signaling system). In all five classes of plant phytochromes, denoted as phyA, phyB, phyC,
phyD, and phyE, the C terminus contains a histidine-kinase-related domain or HKRD in place of
an authentic HK domain, and between the PCM and HKRD, there are two additional PAS
domains.

Fig.11

Accordingly, phyB-phyE mediates, in a reversible fashion, the so-called low fluence response or
LFR, which is triggered by R light and terminated by FR-light[81]. PhyB is more abundant than
phyC–E, but its mRNA levels are typically only ~1% of those of phyA mRNA in the dark and in
sunlight. However, phyB is the most abundant phytochrome due to phyA degradation[82].

Phytochrome Structure: Plant phytochromes or Phys, Fig. 12

. cyanobacterial phytochromes or Cphs, and most
bacteriophytochromes or BphPs share a typical architecture
consisting of an N-terminal photosensory region with three conserved domains (termed P2 or
PAS domain, P3 or GAF domain, and P4 or PHY domain) and a C-terminal regulatory histidine
kinase-related domain (HKRD). Plant phytochromes have an additional N-terminal extension
termed P1 known to inhibit dark reversion, and two additional regulatory PAS domains recently
shown to be essential for nuclear localization[77]. The PAS, GAF, and PHY domains share a
common core fold defined by a central, antiparallel β sheet with the strands in the order of
2–1-5–4-3 and a connecting element between strands 2 and 3 containing an α helix(3). Although
the overall spatial arrangement of these three domains is linear in a beads-on-a-string fashion,
they are closely integrated via the N-terminal extension of the PAS domain, a highly unusual
knot, and an arm extending from the PHY core domain[78].
Phytochrome Photochemistry: All four pyrrole nitrogens in the bilin chromophore are
protonated in both the Pr and Pfr states. The primary photochemical event in the reversible
Pr↔Pfr photoconversion in Phys and BphPs is Z/E isomerization around the C15-C16 double
bond between rings C and D in the bilin chromophore(1). However, ring D remains nearly
unchanged between the Pr and Pfr structures of the GAF domain of a “PAS-less”
phytochrome[79].

Phytochrome signal perception and transduction: Phytochromes (Phys) synthesized in

seedlings germinated in darkness and mainly localized in the cytoplasm to the inactive Pr form.
Due to red-light irradiation, the photoreceptors get converted to the active Pfr conformation and
translocate into the nucleus. Direct interaction happens with a subfamily of basic
helix-loop-helix or bHLH transcription factors, termed PIFs or Phytochrome-Interacting Factors;
PIF1–8 [83]. These PIFs act to repress seed germination, promote seedling skotomorphogenesis
and promote shade-avoidance through regulated expression of over a thousand genes and
light-activated phytochrome molecules directly reverse these activities by inducing
phosphorylation, ubiquitination, and degradation of the PIFs, thereby regulating the expression
of a large number of PIF target genes within minutes[84] .

Cryptochromes: Cryptochromes are photosensory receptors, mediate light regulatory growth

and developments in plants. In 1993 Arabidopsis CRY1 protein (encoded by genes Cry1 gene
which regulates the circadian clock in a light-dependent fashion)[85] get isolated. Since then
cryptochromes have been found in every multicellular eukaryote[86] . Cryptochromes are the
oldest family of flavin (a class of yellow water-soluble nitrogenous pigments)-containing
photoreceptors . We can classify the cryptochrome superfamily into five families: (i)CPD
(cyclobutane pyrimidine photolyase) photolyase, (ii)6–4 photolyase, (iii)CRY-DASH (probably a
single-stranded DNA repairing enzyme), (iv)plant cryptochromes, and (v)animal
cryptochromes[86]. All members of the cryptochrome superfamily have an N-terminal
photolyase homology or the PHR domain, can bind to the flavin adenine dinucleotide or FAD
cofactor and a light-harvesting chromophore[87] but lack photolyase activity, and a
carboxyl-terminal extension that contains a DQXVP-acidic-STAES (DAS) domain conserved
from moss to fern, to angiosperm. Proteins from the photolyase/cryptochrome family share their
three-dimensional fold, sequence homology, and the redox-active flavin adenine dinucleotide or
FAD cofactor but exhibit diverse activities. In response to blue light or UV-A light, they function
physiologically in DNA repair, entrainment of the circadian clock, or other processes. Plants
Arabidopsis thaliana cryptochrome 1 and 2 (AtCry1 and AtCry2) entrain the circadian clock and
trigger developmental processes such as de-etiolation and flower induction.

Fig. 13.

Cryptochrome Structure: One prominent feature of a photolyase structure is a positively

charged groove running through the enzyme, the DNA-binding site. We can see a cavity in the
center of the groove opposing the flavin-binding site. The CPD of bound DNA can fit into the
hole to accept the electron from the flavin. The PHR domain [PAM (protein associated with
Myc)-HIW (Highwire)-RPM-1 (regulator of presynaptic morphology 1)] of Arabidopsis cry2 is
relatively hydrophobic, and the positively charged groove found in photolyase is partially
conserved in cry2. However, the groove in cry2 appears shorter, more comprehensive, and with a
relatively lower surface electrostatic potential than that of the photolyase(10). The photosensory
PHR domains in AtCry1 and AtCry3 share the same architecture with DNA photolyases,
composed of an N-terminal α/β domain and a C-terminal α-helical domain[87]. The α/β domain
adopts a dinucleotide-binding fold consisting of a five-stranded parallel β sheet surrounded by
five helices. The helical domain consists of 16 helices and non-covalently binds the FAD
chromophore in a U-shaped conformation. The linker region between the α/β and helical
domains is extended and largely unstructured, with conformations that vary among photolyase
and cryptochrome structures. The nucleotides ATP or AMP-PNP [adenosine 5
-(β,γimido)triphosphate] bind to AtCry1-PHR near the FAD chromophore, like the binding of the
substrate cyclobutane pyrimidine dimers to photolyase. Secondary structure prediction and
circular dichroism (CD) and NMR spectroscopy suggest that the isolated AtCry1-CCT domain
mainly adopts a flexible, extended structure with short stretches of helices[88] . However, in the
case of the full-length protein, it adopts a more stable conformation through interaction with its
cognate PHR domain(3).

Fig.14.

Cryptochrome Photochemistry: Absorption of light by DNA photolyases causes

photoreduction of the oxidized ground state of FAD to a fully reduced, catalytic FADH−, the
light-activated state, which further enables electron transfer to DNA to split and repair the UV
lesions. The absorption of blue light by the oxidized ground state of FAD in AtCry1 and AtCry2
induces the formation of a radical intermediate state (semiquinone), FADH·, that accumulates in
the activated signaling state. Absorption of green light by FADH· causes further reduction to
FADH−, which abrogates signaling. FADH− reoxidizes to the fully oxidized form during dark
reversion[89].
In the vicinity of the FAD chromophore, a chain of three tryptophan residues and antenna
pigments such as MTHF or 8-hydroxy-5-deazariboflavin or 8-HDF are conserved among DNA
photolyases and cryptochromes. This Trp triad is required for FAD reduction in AtCry1 and
participates in intramolecular electron transfer to the FAD chromophore upon photoactivation.
Cryptochrome Signal Transduction: The CRY1 protein detects blue light and initiates
downstream signals that effect photomorphogenic changes in the plant. Photoreception by plant
CRYs occurs in the PHR domain, and the cryptochrome C-terminal extensions or CCT region
contacts the constitutive photomorphogenesis 1 or COP1, the E3 ubiquitin ligase protein, that is
downstream in the blue-light signaling pathway(13). The CCT domain undergoes a light-induced
order-to-disorder transition, particularly in the serine-rich region of the DAS motif . The crystal
structures of AtCry1-PHR at 2.6Å- and 2.45-Å resolution reveal that CRY1-PHR binds Mg·ATP
at an unconventional site.

Fig.15.
Overexpression of the C-terminal domains of AtCry1 and AtCry2 results in a constitutive
photomorphogenic phenotype. For this, transgenic plants exhibit the light-driven inhibition of
hypocotyl growth even in darkness, suggesting that Arabidopsis cryptochromes achieved the
signaling mechanism by regulating the accessibility or conformation of the C-terminal domain to
COP1 in a light-dependent manner. Studies of the interaction between Arabidopsis
cryptochromes and COP1 suggest a mechanism driven by a light-dependent conformational
rearrangement in the C-terminus since the interaction occurs through the C-terminal domain of
cryptochromes, independent of light, and only after light irradiation inhibition of COP1 function
occurs. The loss-of-function cop1 mutant exhibits constitutive photomorphogenic phenotypes,
leading to the hypothesis that COP1 is a central repressor of plant photomorphogenesis[90].
UVR8: UVR8: Arabidopsis UVR8 was originally identified through a for mutants which are
hypersensitive to UV-B[87] . UVR8 plays a physiological role in UV-B tolerance which was
further demonstrated by the sensitivity of uvr8 mutants compared to wild type under simulated
sunlight[88] . UVR8 is a seven-folded β-propeller protein made up of 440 amino acids[89].
Molecular and biochemical studies have demonstrated that in light conditions devoid of UV-B,
the UVR8 photoreceptor exists as homodimer which undergoes instant monomerization
following UV-B exposure, a process dependent on an intrinsic tryptophan residue that serves as
an UV-B chromophore.

Structure : Many photoreceptors make use of bound cofactors as chromophores, for example
phytochromobilin for phytochromes, flavin mononucleotide (FMN) for phototropins, and flavin
adenine nucleotide (FAD) and possibly a pterin for cryptochromes. In the case of UVR8, a set of
biochemical and genetic data strongly indicated that an intrinsic tryptophan, namely tryptophan-285
(Trp-285 or W285), functions as a chromophore for UV-B perception[90] . In agreement, purified
UVR8 dimer devoid of any form of prosthetic chromophore is able to perceive UV-B and
monomerize in vitro[90]. Several recent works have revealed much about how UVR8 exists as a
homodimer capable of monomerization upon UV-B exposure. These publications present UVR8
predictive models arising from biochemical and structural analysis followed up by systematic
mutational analysis of key residues. Of the 14 UVR8 tryptophans mentioned above, six are located
within the protein core contributing to maintain the β-propeller structure, one is situated in the
C-terminal part that was not included in the core structure, and seven are found at the homodimeric
interface. Amongst the tryptophans at the dimer interface, mutational analysis showed that Trp-233,
Trp-285, Trp-337 and Trp-94 of the opposing UVR8 monomer contribute to exciton coupling within
the structure . These four residues were thus proposed to form a cross-dimer “tryptophan pyramid”
involved in UV-B sensing. Trp-285 in particular as well as Trp-233 play important roles in UV-B
perception, and that Trp-337 contributes to but is not essential for this same process. Concurrently,
mutation of Trp-94 did not affect UVR8 monomerisation upon UV-B indicating that a tryptophan

“pyramid” structure per se is not required for UV-B perception. Interestingly, UVR8W285F was found
to be weakly responsive to UV-C in vitro which is not the case for wild type UVR8[90] . This is in
accordance with the absorption properties of phenylalanine versus tryptophan.

Signaling pathway: Once UV-B is perceived and the UVR8 dimer is monomerized, a molecular
signaling pathway is initiated that transduces this initial event into appropriate changes in gene
expression. For this to occur, action needs to take place within the nucleus. In agreement, and as
mentioned in a previous section, UVR8 partially shifts from the cytoplasm to the nucleus upon UV-B
exposure . However, one cannot assume by any means that UVR8 acts alone in UV-B signaling. This
section describes the currently known UVR8-interacting proteins, such as the E3 ubiquitin ligase
COP1, and the WD40-repeat β-propeller proteins RUP1 and RUP2. COP1 plays a pivotal role in
signaling for visible light qualities. Via interaction with SPA family members, COP1 acts as an E3
ubiquitin ligase and facilitates select protein ubiquitination and degradation. In darkness, this process
modulates the abundance of light signaling proteins, including the transcription factor HY5, to
suppress seedling photomorphogenesis. It is for this reason that cop1 seedlings are referred to as
constitutively photomorphogenic and display a light-grown phenotype even when grown in darkness.
cop1 seedlings present an exaggerated photomorphogenic and severely dwarf phenotype when grown
in light but interestingly do not seem to deploy typical photomorphogenic or molecular responses to
UV-B . Although it is difficult to compare with wild type directly since cop1 seedlings already
exhibit constitutively short hypocotyls, cop1 seedlings do not display the typical reduced hypocotyl
elongation under UV-B compared to white-light-grown seedlings . This lack of UV-B-induced
photomorphogenesis in cop1 seedlings, alongside the absence of UV-B-induced flavonoid
accumulation, gene expression changes, and accumulation of HY5 supports the notion that COP1
plays a promotive role in UV-B responses This contrasts with the repressive role COP1 is known to
play in visible light signaling where HY5 is degraded through COP1 ubiquitination in darkness, but
is able to accumulate in cop1 seedlings leading to the constitutive photomorphogenic mutant
phenotype [91] . COP1 in UV-B signaling displays further contrasting properties in that, alongside
UVR8 and HY5, COP1 accumulates in the nucleus following UV-B exposure and UV-B responses
are independent of SPA proteins . Thus, an unique feature of HY5 in UVR8-mediated UV-B
signaling is that HY5 is used in maintaining a functional significance even in older seedlings and
mature plants.
Reference
1. Möglich, A., Yang, X., Ayers, R. A., & Moffat, K. (2010). Structure and function of plant
photoreceptors. Annual review of plant biology, 61, 21-47.
2. Moglich A, Ayers RA, Moffat K. 2009. Structure and signaling mechanism of
Per-ARNT-Sim domains. ¨ Structure 17:1282–94
3. Pawson T, Nash P. 2003. Assembly of cell regulatory systems through protein interaction
domains. Science 300:445–52
4. Lim WA. 2002. The modular logic of signaling proteins: building allosteric switches from
simple binding domains. Curr. Opin. Struct. Biol. 12:61–68
5. Crosson S, Rajagopal S, Moffat K. 2003. The LOV domain family: photoresponsive
signaling modules coupled to diverse output domains. Biochemistry 42:2–10
6. Conrad, K. S., Manahan, C. C., & Crane, B. R. (2014). Photochemistry of flavoprotein
light sensors. Nature chemical biology, 10(10), 801-809.
7. Glantz, S. T., Carpenter, E. J., Melkonian, M., Gardner, K. H., Boyden, E. S., Wong, G.
K. S., & Chow, B. Y. (2016). Functional and topological diversity of LOV domain
photoreceptors. Proceedings of the National Academy of Sciences, 113(11),
E1442-E1451.
8. Wu, Y. I., Frey, D., Lungu, O. I., Jaehrig, A., Schlichting, I., Kuhlman, B., & Hahn, K. M.
(2009). A genetically encoded photoactivatable Rac controls the motility of living cells.
Nature, 461(7260), 104-108.
9. Herrou, J., & Crosson, S. (2011). Function, structure and mechanism of bacterial
photosensory LOV proteins. Nature reviews microbiology, 9(10), 713-723.
10. Berntsson, O., Diensthuber, R. P., Panman, M. R., Björling, A., Hughes, A. J., Henry, L.,
... & Westenhoff, S. (2017). Time-resolved X-ray solution scattering reveals the structural
photoactivation of a light-oxygen-voltage photoreceptor. Structure, 25(6), 933-938.
11. Swartz, T. E., Corchnoy, S. B., Christie, J. M., Lewis, J. W., Szundi, I., Briggs, W. R., &
Bogomolni, R. A. (2001). The photocycle of a flavin-binding domain of the blue light
photoreceptor phototropin. Journal of Biological Chemistry, 276(39), 36493-36500.
12. Šali, A., & Blundell, T. L. (1993). Comparative protein modelling by satisfaction of
spatial restraints. Journal of molecular biology, 234(3), 779-815.n
13. Zoltowski, B. D., & Gardner, K. H. (2011). Tripping the light fantastic: blue-light
photoreceptors as examples of environmentally modulated protein− protein interactions.
Biochemistry, 50(1), 4-16.
14. Conrad, K. S., Bilwes, A. M., & Crane, B. R. (2013). Light-induced subunit dissociation
by a light–oxygen–voltage domain photoreceptor from Rhodobacter sphaeroides.
Biochemistry, 52(2), 378-391.
15. Moglich A, Ayers RA, Moffat K. 2009. Structure and signaling mechanism of
Per-ARNT-Sim domains. ¨ Structure 17:1282–94
16. 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
17. 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
18. Halavaty AS, Moffat K. 2007. N- and C-terminal flanking regions modulate
light-induced signal transduction in the LOV2 domain of the blue light sensor
phototropin 1 from Avena sativa. Biochemistry 46:14001–9
19. Harper SM, Neil LC, Gardner KH. 2003. Structural basis of a phototropin light switch.
Science 301:1541– 44
20. Iwata T, Yamamoto A, Tokutomi S, Kandori H. 2007. Hydration and temperature
similarly affect lightinduced protein structural changes in the chromophoric domain of
phototropin. Biochemistry 46:7016–21
21. 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
22. Losi A, Polverini E, Quest B, Gartner W. 2002. First evidence for phototropin-related
blue-light recep- ¨ tors in prokaryotes. Biophys. J. 82:2627–34
23. 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
24. 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
25. Alexandre MT, Arents JC, van Grondelle R, Hellingwerf KJ, Kennis JT. 2007. A
base-catalyzed mechanism for dark state recovery in the Avena sativa phototropin-1
LOV2 domain. Biochemistry 46:3129–37
26. 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
27. . 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
28. 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
29. Christie JM. 2007. Phototropin blue-light receptors. Annu. Rev. Plant Biol. 58:21–45
30. 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
31. Matsuoka D, Tokutomi S. 2005. Blue light-regulated molecular switch of Ser/Thr kinase
in phototropin. Proc. Natl. Acad. Sci. USA 102:13337–42
32. Harper SM, Neil LC, Gardner KH. 2003. Structural basis of a phototropin light switch.
Science 301:1541– 44
33. Harper SM, Christie JM, Gardner KH. 2004. Disruption of the LOV-Jalpha helix
interaction activates phototropin kinase activity. Biochemistry 43:16184–92 54.
34. 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
35. 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
36. Somers DE, Schultz TF, Milnamow M, Kay SA. 2000. ZEITLUPE encodes a novel
clock-associated PAS protein from Arabidopsis. Cell 101:319–29
37. Mas P, Kim WY, Somers DE, Kay SA. 2003. Targeted degradation of TOC1 by ZTL
modulates ´ circadian function in Arabidopsis thaliana. Nature 426:567–70
38. 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
39. Demarsy E, Fankhauser C. 2009. Higher plants use LOV to perceive blue light. Curr.
Opin. Plant Biol. 12:69–74
40. 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
41. Ulrich LE, Koonin EV, Zhulin IB. 2005. One-component systems dominate signal
transduction in prokaryotes. Trends Microbiol. 13:52–56
42. 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
43. 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
44. Anderson S, Crosson S, Moffat K. 2004. Short hydrogen bonds in photoactive yellow
protein. Acta Crystallogr. D 60:1008–16
45. . 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
46. 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
47. Bogomolni RA, Spudich JL. 1982. Identification of a third rhodopsin-like pigment in
phototactic Halobacterium halobium. Proc. Natl. Acad. Sci. USA 79:6250–54
48. Deisseroth K, Feng G, Majewska AK, Miesenbock G, Ting A, Schnitzer MJ. 2006.
Next-generation ¨ optical technologies for illuminating genetically targeted brain circuits.
J. Neurosci. 26:10380–86
49. Domratcheva T, Grigorenko BL, Schlichting I, Nemukhin AV. 2008. Molecular models
predict lightinduced glutamine tautomerization in BLUF photoreceptors. Biophys. J.
94:3872–79
50. Ernst OP, Sanchez Murcia PA, Daldrop P, Tsunoda SP, Kateriya S, Hegemann P. 2008.
Photoactivation ´ of channelrhodopsin. J. Biol. Chem. 283:1637–43
51. Feldbauer K, Zimmermann D, Pintschovius V, Spitz J, Bamann C, Bamberg E. 2009.
Channelrhodopsin2 is a leaky proton pump. Proc. Natl. Acad. Sci. USA 106:12317–22
52. Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, et al. 2006. Pfam:
clans, web tools ¨ and services. Nucleic Acids Res. 34:D247–51
53. Foster KW, Saranak J, Patel N, Zarilli G, Okabe M, et al. 1984. A rhodopsin is the
functional photoreceptor for phototaxis in the unicellular eukaryote Chlamydomonas.
Nature 311:756–59
54. 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
55. Gauden M, van Stokkum IH, Key JM, Luhrs DC, van Grondelle R, et al. 2006.
Hydrogen-bond switching ¨ through a radical pair mechanism in a flavin-binding
photoreceptor. Proc. Natl. Acad. Sci. USA103:10895– 900
56. Gomelsky M, Kaplan S. 1998. AppA, a redox regulator of photosystem formation
inRhodobacter sphaeroides 2.4.1, is a flavoprotein. Identification of a novel FAD binding
domain. J. Biol. Chem. 273:35319–25
57. Gomelsky M, Klug G. 2002. BLUF: a novel FAD-binding domain involved in sensory
transduction in microorganisms. Trends Biochem. Sci. 27:497–500
58. 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
59. Hegemann P. 2008. Algal sensory photoreceptors. Annu. Rev. Plant Biol. 59:167–89
60. Hegemann P, Gartner W, Uhl R. 1991. All-trans retinal constitutes the functional
chromophore in ¨ Chlamydomonas rhodopsin. Biophys. J. 60:1477–89
61. 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
62. Holland EM, Braun FJ, Nonnengasser 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
63. Jung A, Domratcheva T, Tarutina M, Wu Q, Ko WH, et al. 2005. Structure of a bacterial
BLUF photoreceptor: insights into blue light-mediated signal transduction. Proc. Natl.
Acad. Sci. USA 102:12350–
64. Kateriya S, Nagel G, Bamberg E, Hegemann P. 2004. “Vision” in single-celled algae.
News Physiol. Sci. 19:133–37
65. 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
66. Litvin FF, Sineshchekov OA, Sineshchekov VA. 1978. Photoreceptor electric potential in
the phototaxis of the alga Haematococcus pluvialis. Nature 271:476–78
67. Luecke H, Schobert B, Richter HT, Cartailler JP, Lanyi JK. 1999. Structural changes in
bacteriorhodopsin during ion transport at 2 angstrom resolution. Science 286:255–61
68. Luecke H, Schobert B, Richter HT, Cartailler JP, Lanyi JK. 1999. Structure of
bacteriorhodopsin at 1.55 A resolution. ˚ J. Mol. Biol. 291:899–911
69. Moglich A, Ayers RA, Moffat K. 2009. Structure and signaling mechanism of
Per-ARNT-Sim domains. ¨ Structure 17:1282–94
70. 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
71. 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
72. Oesterhelt D, Stoeckenius W. 1973. Functions of a new photoreceptor membrane. Proc.
Natl. Acad. Sci. USA 70:2853–57
73. Sasaki J, Spudich JL. 2008. Signal transfer in haloarchaeal sensory rhodopsin-
transducer complexes. Photochem. Photobiol. 84:863–68
74. . Sineshchekov OA, Govorunova EG, Spudich JL. 2009. Photosensory functions of
channelrhodopsins in native algal cells. Photochem. Photobiol. 85:556–63
75. Tittor J, Oesterhelt D. 1990. The quantum yield of bacteriorhodopsin. FEBS Lett.
263:269–73
76. 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
77. Yuan H, Bauer CE. 2008. PixE promotes dark oligomerization of the BLUF
photoreceptor PixD. Proc. Natl. Acad. Sci. USA 105:11715–19
78. PHYTOCHOME STRUCTURE AND SIGNALING MECHANISMS; Nathan C.
Rockwell, Yi-Shin Su, and J. Clark Lagarias* Section of Molecular and Cellular Biology,
University of California, Davis, CA 95616.
79. Dynamic Nuclear Polarization Provides New Insights into Chromophore Structure in
Phytochrome Photoreceptors; International Edition: DOI: 10.1002/anie.201608119
80. Structure and Function of Plant Photoreceptors; Annu. Rev. Plant Biol. 2010. 61:21–47;
Andreas Moglich, ¨ 1,∗ Xiaojing Yang,1,∗ Rebecca A. Ayers,1 and Keith Moffat1,2
81. MICHAEL A. VAN DER HORST AND KLAAS J. HELLINGWERF 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. 2004, 37, 13-20
82. Molecular mechanisms for mediating light-dependent nucleo/ cytoplasmic partitioning of
phytochrome photoreceptors; New Phytologist (2015) 206: 965–971 doi:
10.1111/nph.13207
83. Phytochrome-mediated photoperception and signal transduction in higher plants Eberhard
Schäfer & Chris Bowler1,+ Universitat Freiburg, Institut fur Biologie II/Botanik,
 Schanzlestrasse 1, D-79104 Freiburg, Germany and 1Molecular Plant Biology
Laboratory, Stazione Zoologica ‘Anton Dohrn’, Villa Comunale, I-80121 Naples, Italy
Received July 1, 2002; revised September 30, 2002; accepted October 1, 2002
84. 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;
85. PIFs: pivotal components in a cellular signaling hub; Trends Plant Sci. 2011 January ;
16(1): 19–28. doi:10.1016/j.tplants.2010.08.003.
86. PPKs mediate direct signal transfer from phytochrome photoreceptors to transcription
factor PIF3; DOI: 10.1038/ncomms15236
87. Chentao Lin and Dror Shalitin. CRYPTOCHROME STRUCTURE AND SIGNAL
TRANSDUCTION. Annu. Rev. Plant Biol. 2003. 54:469–96
88. The photolyase/cryptochrome superfamily is classified into five families: CPD
(cyclobutane pyrimidine photolyase) photolyase, 6–4 photolyase, CRY-DASH (probably
a single-stranded DNA repairing enzyme), plant cryptochromes, and animal
cryptochromes
89. Direct Observation of a Photoinduced Radical-Pair Intermediate in a Cryptochrome
DASH Blue-Light Photoreceptor; Angew Chem Int Ed Engl. 2009 ; 48(2): 404–407.
doi:10.1002/anie.200803102.
90. . Chad A. Brautigam*, Barbara S. Smith*†, Zhiquan Ma*, Maya Palnitkar*†, Diana R.
Tomchick*, Mischa Machius*, and and Johann Deisenhofer*†‡. August 17, 2004.
Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana.
91. Kliebenstein, D. J., Lim, J. E., Landry, L. G., & Last, R. L. (2002). Arabidopsis UVR8 regulates ultraviolet-B
signal transduction and tolerance and contains sequence similarity to human regulator of chromatin condensation
1. Plant physiology, 130(1), 234-243.
92. Favory, J. J., Stec, A., Gruber, H., Rizzini, L., Oravecz, A., Funk, M., ... & Ulm, R. (2009). Interaction of
COP1 and UVR8 regulates UV‐B‐induced photomorphogenesis and stress acclimation in Arabidopsis.
The EMBO journal, 28(5), 591-601
93. Wu M., Grahn E., Eriksson L.A., Strid A. Computational evidence for the role of Arabidopsis
thaliana UVR8 as UV-B photoreceptor and identification of its chromophore amino acids. J.
Chem. Inf. Model. 2011;51:1287–1295.
94. Osterlund, M. T., Hardtke, C. S., Wei, N., & Deng, X. W. (2000). Targeted destabilization of HY5 during
light-regulated development of Arabidopsis. Nature, 405(6785), 462-466.