From the Department of Molecular Biology, University of Geneva, 1211 Geneva 4, Switzerland
Because plants are photo-auxotrophic they are
particularly sensitive to their light environment. To fine-tune their
development according to light intensity, direction, spectral quality,
and periodicity they possess a multiplicity of light sensors (1). In
Arabidopsis there are eight identified photoreceptors, but this list is still incomplete. It includes three UV-A/blue light receptors (phototropin, a photoreceptor to sense light direction, and
two cryptochromes that mediate many photomorphogenic responses (2, 3))
and five phytochromes (phy)1
named phyA-phyE that absorb mainly red/far-red light, with phyA also
responding to broad-spectrum light (UV-A to far-red) of very low
intensity (4). All these photoreceptors bind to a chromophore, which
for the phytochromes is a linear tetrapyrrole (phytochromobilin) (5).
Because many light effects are induced by the co-action of several
photoreceptors and because some photoreceptors regulate multiple
aspects of photomorphogenesis, a genetic approach was instrumental for
dissecting the specific roles of individual photoreceptors (1). As
a consequence, research has concentrated on a few species that are
particularly well suited for molecular genetic studies, in particular
Arabidopsis (6).
Phytochromes were originally defined as the receptors responsible
for red, far-red reversible, plant responses (7-9).
Photobiological experiments led to the proposal that phy exists in two
spectral forms: the inactive Pr form (red light absorbing)
phototransforms into the active Pfr form (far-red light absorbing) upon
absorption of red light. This reaction can be reversed when Pfr is
converted to Pr upon absorption of far-red light. Purification of phy
from plants confirmed the existence of those two spectrally
interconvertible forms (10). phy are classified into two groups; type I
(phyA in Arabidopsis) is light-labile and type II
(phyB-phyE in Arabidopsis) is light-stable (11). Numerous
recent reviews cover phy-mediated photomorphogenesis in detail
(12-19).
Photobiological and genetic studies have revealed that this small gene
family plays important roles in seed germination, seedling de-etiolation, neighbor perception and avoidance, and the transition from vegetative to reproductive growth (induction of flowering). At the
molecular and cellular level phy responses include: development of the
chloroplast, inhibition or promotion of cell growth (depending on the
organ), ion fluxes at the plasma membrane, and gene expression responses (1). Genetic screens to identify loci implicated in phy
responses have yielded four apoprotein mutants (phyA,
phyB, phyD, and phyE), two chromophore
mutants (hy1 and hy2), and numerous mutants
implicated in phy-mediated signaling. The analysis of these mutants
highlighted the role of phytochromes in sensing light quality,
intensity, and the duration of the light cycle and revealed that type I
and type II phy have distinct modes of photoperception (14, 15).
Light-stable phy are responsible for the classical red/far-red
reversible phy responses. In Arabidopsis phyB plays the most prominent role; it is the major red light receptor for seedling de-etiolation, and it affects many light-regulated cell elongation responses, shade avoidance, and the regulation of flowering time by day
length (20). phyD and phyE mutants have more
subtle phenotypes that are only revealed in double or triple mutant
combinations (21-23). Because certain phytohormone mutants also
display similar phenotypes, a subset of phy responses might be mediated
by light-regulated hormonal signaling (14, 24-26).
phyA, the only type I phy in Arabidopsis, plays a major role
in gene expression and germination in response to very low fluences of
broad spectrum light as well as in sensing day-length extension (27-30). phyA is also essential for de-etiolation in far-red enriched light (31-33). Such conditions are found when a young seedling develops under a dense canopy of plants. This is a particularly interesting phy function because, contrary to most phy responses, it is
induced by far-red light and inhibited by red light (see above) (34).
This high irradiance response to far-red light identifies a novel form
of active phy, Pr, that has been cycled through Pfr, which will be
referred to as Pr*. Pr* has acquired novel properties that are distinct
from Pr and Pfr, but the molecular nature of the distinction between
Pr* and Pr is unknown (34). As illustrated above, type I and type II
phy play distinct roles; however, it must be pointed out that depending
on the responses their role can be overlapping, coordinated, or even
antagonistic (35-39).
Phytochromes bind phytochromobilin (P
Plants Possess Multiple Photoreceptors
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Multiple Phytochromes Have Overlapping and Distinct
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Molecular Properties of Phytochromes and Bacteriophytochromes
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B) via a thioether linkage
to a cysteine residue in the most conserved domain among phy (Fig.
1). The first committed step in
chromophore biosynthesis is the cleavage of the tetrapyrrole ring of
heme (Fig. 1A). This reaction is catalyzed by a heme
oxygenase encoded by the HY1 gene in Arabidopsis
(40, 41). Hy2 mutants are most probably defective in the
P
B synthase enzyme; this step is followed by an isomerization in the
C-3 double bond of P
B (42). The nature of the P
B isomerase is
still unclear, but phy itself is capable of catalyzing this reaction
(42). phy chromophore mutants can be mimicked by overexpression of a
mammalian biliverdin reductase (43). phy apoprotein binds to the
3E-P
B in the cytoplasm to yield the Pr form of the photoreceptor. This reaction requires the bilin lyase domain (BLD) of the
photoreceptor. Absorption of red light triggers a "Z" to "E"
isomerization in the C-15 double bond between the C and D rings of the
linear tetrapyrrole, resulting in the far-red light-absorbing form Pfr
(44) (Fig. 1A). Conformational changes in the protein
backbone are required to maintain this high energy state of the
photoreceptor (45). Pfr can be converted to Pr either by a slow
non-photoinduced reaction (dark reversion) or much faster upon
absorption of far-red light. It is generally assumed that all phy have
the same chromophore. Because of the very low levels of type II phy
this has not been verified in vivo. Analysis of
reconstituted recombinant phyA, phyB, phyC, and phyE reveals that they
have similar but not identical spectral properties (46-48).
View larger version (19K):
[in a new window]
Fig. 1.
Structural domains and spectral properties of
phytochromes. A, biosynthetic pathway of the
phytochrome chromophore. Enzymes are indicated in red, and
the Arabidopsis genes are indicated. Note that chromophore
binding is autocatalytic; it requires the bilin lyase domain of the
phytochrome; phytochromes also possess P B isomerase activity. The
arrow indicates the site of chromophore attachment to a
cysteine in the bilin lyase domain. Absorption of red light triggers a
"Z" to "E" isomerization in the C-15 double bond between the C
and D rings (indicated in bold). The absorption spectra of
Pr and Pfr are indicated. BVR, biliverdin reductase.
B, structural domains of prokaryotic and plant phytochromes.
PAS is the acronym from the founding members of this protein domain
(Per/Arndt/Sim). Cph1,
cyanobacterial phytochrome 1 from Synechocystis sp. PCC6803;
RcaE, regulator of chromatic adaptation E from
Fremyella diplosiphon; BphP,
bacteriophytochrome 1 from Deinococcus radiodurans;
Ppr, PYP-phytochrome-related from Rhodospirillum
centenum.
Phytochromes are soluble homodimers composed of two functional domains: an N-terminal light-sensing domain and a C-terminal signaling domain (Fig. 1). The N-terminal portion is necessary and sufficient for photoperception and possesses the bilin lyase activity allowing attachment of the chromophore to the apoprotein (42). The minimal BLD is actually less than 200 amino acids long (49). The first 70 amino acids of the protein are dispensable for chromophore binding; they constitute the N-terminal extension (ATE). The ATE is poorly conserved, possibly accounting for some functional differences among phy. Structure function analysis has revealed that in phyA, the ATE is composed of two subdomains (50, 51). The ATE might be implicated in stabilization of the Pfr form of the photoreceptor, which is particularly interesting in view of the large structural changes observed in this part of the protein upon Pr to Pfr phototransformation (45).
The importance of the C-terminal half of plant phytochromes is highlighted by the numerous missense mutations affecting this portion of the protein (4, 52). This signaling domain is composed of a PAS (Per/Arndt/Sim)-related domain (PRD) and a histidine kinase-related domain (HKRD) (Fig. 1) (53, 54). PAS domains have diverse functions; they can be used either as protein-protein interaction platforms or as co-factor binding domains (55). Interestingly such modules are used to bind the chromophore in various blue light receptors (2). In phytochromes, the PRD domain is required for interaction with phy signaling partners but might also play a role in stabilization of the Pfr form of phyB (4, 47, 56, 57). Interestingly a mutation in the BLD domain of phyB has the opposite effect, leading to a phyB protein locked in the Pfr conformation (58).
The discovery of phytochromes in prokaryotes had two important
consequences: they provided a phylogenetic origin for plant phy and
suggested a biochemical mechanism for phy signaling (59-61). Cyanobacterial phytochrome 1 (Cph1) is composed of a BLD and a histidine kinase domain (Fig. 1B). Cph1 autophosphorylates
and phosphorylates the Rcp1 response regulator in a light-regulated fashion (Fig. 2A) (61). It is
noteworthy that in several cases response regulators are encoded in the
same operon as the photoreceptor, suggesting that light-regulated
protein phosphorylation is a common theme in bacteriophytochrome
signaling. More complex structures have been found in the purple
bacteria Rhodospirillum centenum where the photoreceptor has
an additional photoactive yellow protein (PYP) domain, which is highly
related to the PAS domains present in plant phy (62).
Bacteriophytochromes have been discovered in non-photosynthetic
organisms as well (63). Their biological function is not always
understood, but they play rather diverse roles depending on the
species, including chromatic adaptation, resetting of the circadian
clock, and regulation of pigment biosynthesis (59, 62-64).
Interestingly, some of these functions have been conserved in plant phy
(38, 65).
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The HKRD domain of plant phytochromes is only distantly related to bacterial histidine kinases, and several residues essential for kinase activity are absent in plant phy (66). In fact, work over the past 20 years has indicated that oat phyA might be a Ser/Thr kinase, and this has been confirmed convincingly quite recently (19, 54). Recombinant oat phyA is a light and chromophore-modulated protein kinase with Pfr being a more active form than Pr (Fig. 2C) (54). Oat phyA is a phosphoprotein in vivo; two phosphorylation sites have been mapped, and interestingly they correspond to residues phosphorylated after in vitro kinase assays (67). Ser-7 is constitutively phosphorylated, and mutagenesis studies suggest that phosphorylation of this residue is implicated in down-regulation of phyA signaling (50). Ser-599 phosphorylation is only observed in phyA extracted from light-treated plants (67). Phosphorylation of this residue might therefore be a molecular tag distinguishing between different forms of phy. The importance of this residue has been demonstrated in vitro because a S599K mutant loses light-regulated kinase activity (68). The cryptochromes and PKS1 (phytochrome kinase substrate 1) are also substrates of phyA as a protein kinase, but the role of phosphorylation during phy-mediated light signaling remains to be determined in vivo (68, 69). Based on reverse genetic studies it has been proposed that PKS1 acts as a negative regulator of phyB and phyA signaling (68).2 The phyA-cryptochrome interaction might be the molecular basis for the co-action between those photoreceptors (69). These studies suggest a role for phy-mediated phosphorylation; quite surprisingly, however, deletion of the HKRD domain of phyB has a milder phenotype than certain point mutations in the HKRD (52).
All five members of the phy family are widely expressed (70, 71). PHYA transcription is negatively regulated by light through a negative feedback loop dependent on both phyA and phyB (72). phyB mRNA is under circadian regulation; however, this regulated gene expression has only a minor impact on the steady state level of the protein (73). The stability of the phyA protein is greatly dependent on the light conditions. PfrA is selectively ubiquitinated leading to proteolytic degradation, phyA protein levels being therefore about 100-fold lower in the light than in the dark (Fig. 2C) (74). Interestingly PrA* (PrA which has been cycled through Pfr) has a half-life similar to the one of PfrA. Ubiquitination of PrA* might therefore be the molecular tag distinguishing it from PrA. It is noteworthy that the PrA* form of phy (just like the signal generated by PrA*) is very short lived (34, 74, 75).
Subcellular localization is probably a major level of regulation for
plant phytochrome action. Both phyA and phyB are cytoplasmic in the
dark, and appropriate light treatments trigger their translocation into
the nucleus (Fig. 2B) (12). This relocation takes several hours for phyB in contrast with the more rapid translocation of phyA.
This differential behavior correlates well with the sequential action
of those phy during light-induced inhibition of hypocotyl growth (39).
The slow nuclear translocation of phyB implies that PfrB will be
present in the cytoplasm where it could also play a role. Several rapid
phy effects, such as ion fluxes at the plasma membrane, have been
reported; they could be induced by the cytoplasmic pool of PfrB
(76).
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Signaling, What Happens after Photoperception? |
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Pharmacological studies using microinjection of a tomato phy
mutant have identified heterotrimeric G proteins, cGMP and
Ca2+, as second messengers in phy signaling (77). Genetic
screens have identified two classes of signaling components, those
acting downstream of a single photoreceptor and those acting downstream of multiple photoreceptors (Fig. 3). This
presumably reflects the fact that light signals perceived by different
photoreceptors must be integrated (14, 15). The latter class (light
signal integration, see Fig. 3) includes both positively acting factors (i.e. HY5) and a large group of negative regulators of
photomorphogenesis (DET/COP/FUS) (16, 17). Mutants with phenotypes
under specific light conditions (i.e. only red light) are
considered as acting early in the cascade. The study of such mutants
and of phy interacting proteins reveal a complex signaling web (Fig. 3)
(14, 15, 26, 78-82). These loci can be classified into three groups:
those acting specifically downstream of phyA, downstream of phyB, or downstream of both. Interestingly both nuclear and cytoplasmic factors
have been identified, and these signaling branches include positive and
negative regulation (Fig. 3). Most of the cloned genes code for
proteins with poorly defined biochemical functions. It is currently
quite hard to propose a model that integrates all those factors,
particularly because the relative position of these elements in the
chain of events is still largely unknown.
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Paradoxically the best understood branch of phy signaling appears to be
rather simple (Fig. 2B). PfrB is selectively imported into
the nucleus where it interacts with PIF3, a bHLH transcription factor.
This interaction occurs specifically with PfrB but not PrB and
irrespective of DNA binding by PIF3 (Fig. 2B) (83). How
interaction with phyB affects PIF3 activity remains to be solved.
RSF1/HFR1/REP1 is another bHLH transcription factor that is quite
related to PIF3 and also plays an important role in phy signaling (82,
84-86). RSF1/HFR1/REP1 is, however, implicated in phyA- and not
phyB-mediated signaling (82, 84-86). There is currently no data
indicating a direct interaction between RSF1/HFR1/REP1 and phyA (85).
The presence of bHLH transcription factors in both phyA and phyB
signaling is particularly noteworthy in view of the recently uncovered
convergence of multiple phy signaling pathways on a single promoter
(87). Genetic studies for both PIF3 and RSF1/HFR1/REP1 have revealed
that they play important roles in phy signaling, but they also indicate
that these transcription factors only account for part of the response
initiated by the phy (82, 83, 85, 86). These recent studies illustrate the potentially very short signaling chain initiated by the
phytochromes, but we should keep in mind that much remains to be done
to have a global view of the multiple events initiated by those photoreceptors.
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ACKNOWLEDGEMENTS |
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I thank Jorge Casal, Masaki Furuya, Enamul Huq, Clark Lagarias, Pill Soon Song, Rick Vierstra, and Jim Weller for communicating results prior to publication; Miguel Blazquez, Michel Goldschmidt-Clermont, and Patricia Lariguet for helpful comments on the manuscript, and Nicolas Roggli for artwork.
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FOOTNOTES |
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* This minireview will be reprinted in the 2001 Minireview Compendium, which will be available in December, 2001. This is the second article of three in the "Light Minireview Series."
Supported by a grant from the Swiss National Science Foundation.
To whom correspondence should be addressed: Dept. of Molecular Biology,
University of Geneva, 30 quai E. Ansermet, 1211 Geneva 4, Switzerland.
E-mail: Christian.Fankhauser@molbio.unige.ch.
Published, JBC Papers in Press, February 16, 2001, DOI 10.1074/jbc.R100006200
2 J. Casal, J. Chory, and C. Fankhauser, unpublished data.
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ABBREVIATIONS |
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The abbreviations used are: phy, phytochrome(s); BLD, bilin lyase domain; ATE, N-terminal extension; PRD, PAS (PER/ARNT/SIM)-related domain; HKRD, histidine kinase-related domain; PYP, photoactive yellow protein; bHLH, basic helix-loop-helix.
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