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230

Seeing the world in red and blue: insight into plant vision and
photoreceptors
Margaret Ahmad
Plants see light through multiple photoreceptors, including
phytochromes and cryptochromes. Cryptochromes are
flavoproteins that participate in many blue-light responses,
including phototropism in plants and entrainment of circadian
rhythms in plants and animals. A novel flavoprotein, NPH1, is
also implicated in plant phototropism. Phytochromes function
as serine/threonine kinases whose potential interacting
partners include cryptochrome (CRY1 and CRY2).
Addresses
LPDP Universite Paris VI, UMR CNRS 7632, Tour 53 E5 Casier 156,
4 Place Jussieu, 75252 Paris Cedex 05, France;
e-mail: margaretahmad@hotmail.com
Current Opinion in Plant Biology 1999, 2:230–235
http://biomednet.com/elecref/1369526600200230
© Elsevier Science Ltd ISSN 1369-5266

Introduction
Light affects virtually all aspects of plant growth and development, from germination and de-etiolation to aspects of
vegetative morphology (stem growth and leaf expansion),
the onset of reproductive growth and floral initiation,
entrainment of circadian rhythms, gene expression, gravitropism and phototropism [1]. Plants respond to light
through photoreceptors which consist of light-absorbing
pigment, or chromophore, bound to a protein effector molecule, or apoprotein. Absorption of light by the
chromophore induces a chemical or confomational change
in the receptor apoprotein that is transmitted to downstream signalling molecules. All of the complex and diverse
responses to light are mediated by just a few different types
of photoreceptors. These include the phytochrome photoreceptors which absorb primarily in the red/far-red region
of the visible spectrum (600–800 nm wavelength) [2], and
specific blue/UV-A light absorbing photoreceptors
(350–500 nm) known as the cryptochromes [3]. There is in
addition evidence for specific UV-B absorbing photoreceptors [1], but the nature of these molecules is not known.
The structure and expression characteristics of the red-light
receptor phytochrome has been known for quite some
time; however its biochemical function and molecular targets have remained a mystery. Even less is known
concerning the molecular identity and mode of action of
the blue-light photoreceptors. In this review I will focus on

recent major progress in the characterization of red and
blue-light absorbing photoreceptors, their role in light signaling and their biochemical mechanisms of action.

CRY1, a plant blue-light photoreceptor related
to blue-light-activated DNA repair enzymes
Since the time of Darwin it has been known that plants
respond specifically to blue light and that distinct

blue-light absorbing photoreceptors must exist. This follows from the observation that certain plant resources, for
instance phototropsim — curvature towards the light —
are elicited preferentially or exclusively by blue light
(wavelengths less than 500 nm) and not by red light, eliminating phytochrome as a possible photoreceptor. Recently,
one such blue light photoreceptor was identified, by
cloning of hy4, a partially blue-light insensitive mutant of
Arabidopsis [4]. The structure of the HY4 protein, deduced
from the nucleotide sequence, revealed an amino-terminal
domain with significant homology to microbial DNA photolyases, which catalyze the blue-light dependent repair of
UV-damaged DNA [5]. In addition, there was a carboxyterminal extension of 180 amino acids, required for
photoreceptor function, which is not found in photolyases
(Figure 1). With some functional characteristics known,

the HY4 protein was then renamed CRY1 for cryptochrome, and proposed to function in plants as the elusive
and long sought-after blue-light photoreceptor.
Recombinant CRY1 protein purified from an E. coli
expression system bound two blue-light absorbing chromophores (a flavin and a pterin), and lacked detectable
DNA repair activity in vitro. Overexpression of CRY1 in
transgenic tobacco and Arabidopsis plants conferred hypersensitivity to blue light, shown particularly through the
inhibition of hypocotyl elongation and anthocyanin accumulation. It seems likely, therefore, that the CRY1 protein
evolved from a blue-light sensing DNA photolyase that
acquired a novel function as a photoreceptor in plants [3].

CRY1 is a member of a gene family with
homologues in animal systems
The hy4 mutant (lacking CRY1) is not completely blind to
blue light, and retains considerable blue-light responsiveness, arguing for the presence of additional blue-light
photoreceptors. It was, therefore, no surprise to find another sequence in the Arabidopsis genome with considerable
homology to CRY1, which was named CRY2 for cryptochrome-2 [3] (Figure 1). CRY2 overexpression studies in
transgenic plants, as well as the identification of null
mutant alleles in CRY2, revealed that CRY2 function is
essentially redundant to that of CRY1. For instance, CRY2
participates in inhibition of hypocotyl elongation, anthocyanin accumulation, and leaf and cotyledon expansion,

although to a reduced extent relative to CRY1 [6•,7].
Unlike CRY1, CRY2 protein is rapidly degraded in
seedlings upon irradiation by wavelengths of light (UV,
blue, green) that activate this receptor [6•,7]. Thus, CRY2
protein does not accumulate to high levels in bright white
light and may, therefore, play less of a role in many highirradiance responses. CRY2, like CRY1, contributes to
blue-light dependent promotion of floral initiation [8,9]. In
this response CRY2 contributes relatively more than

Plant vision and photoreceptors Ahmad

231

Figure 1
Domain structure and evolutionary relatedness
of cryptochromes and photolyases. The
amino-terminal 500 amino acids of CRY1
show 30% amino acid identity and 45%
similarity with E. coli photolyases; this is the
same as the relatedness of the various type 1

photolyases among themselves. A
dendrogram shows the relative evolutionary
relatedness of plant and animal
cryptochromes to type I (E. coli) and 6–4
photolyases; the distances of the lines are not
accurate with respect to evolutionary distance
and show relative relatedness only.

Cryptochromes and Photolyases

30% identity

E. coli

Photolyase

Pterin

Flavin

45% similarity
Plant
Pterin

Cryptochrome
carboxy-terminus

Flavin

Evolutionary relatedness of cryptochromes and photolyases

CRY 1

(Arabidopsis)

CRY 2

(Arabidopsis)

photolyase

(E. coli)

hCRY1

(human)

hCRY2

(human)

6-4 photolyase (Drosophila)
Current Opinion in Plant Biology

CRY1, and has been shown to be allelic to a previously
identified late-flowering mutant, fha. Whether the
increased role of CRY2 in floral initiation reflects increased
stability of CRY2 protein in floral organs, or differential tissue expression relative to CRY1, remains to be determined.
CRY1 and CRY2 proteins are highly homologous within
their amino-terminal chromophore-binding domain

(Figure 1) and indeed both CRY1 and CRY2 from mustard
bind the same chromophores when expressed in E. coli
[10]. The carboxy-terminal domains of CRY1 and CRY2,
by contrast, show almost no sequence relatedness.
Nevertheless, domain swap experiments show that all of
the domains of CRY1 and CRY2 proteins are functionally
interchangeable in chimeric photoreceptors. Therefore,
although the carboxy termini of the members of the cryptochrome gene family differ greatly in sequence, they
appear to have similar or idenitical function [6•]. This
would indicate that the reaction partners of both CRY1 and
CRY2 photoreceptors may also be identical. Additional

cryptochrome gene family members, have been identified
in numerous plant species including ferns and algae [3,11];
all sequences have considerable similarity in their chromophore-binding domains but divergent carboxy-termini.
By analogy with CRY1 and CRY2, it is likely that all these
proteins share considerable functional overlap, although
higher and lower plant transduction pathways may have
diverged somewhat in the course of evolution.
The discovery of cryptochrome in plants greatly stimulated the search for related sequences in other organisms that

might also function as photoreceptors. Interestingly, such
homologous genes were identified in mouse (mCRY1 and
mCRY2) and humans (hCRY1 and hCRY2) [12,13]. The
encoded proteins lack DNA repair activity in vitro, consistent with possible novel functions as blue-light
photoreceptors [14,15]. The mouse genes (mCRY1 and
mCRY2) are expressed in many tissues including the
suprachiasmatic nucleus, where the transcripts oscillate in
a circadian manner [16••]. Generation of knockout mice

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Physiology and metabolism

with a deletion of mCRY2 resulted in a one hour lengthening of the free-running period of behavioral rhythms
[17], consistent with a biological role in entrainment of circadian rhythms in mammals. Similarly in Drosophila, a
cryptochrome-like gene (cry) has been identified whose
transcript is regulated in a circadian and clock-gene dependent fashion [18 ••]. Null mutations within this
cryptochrome gene abolished light-dependent oscillation
in levels of per or timeless clock gene products in mutant
flies. Behavioral rhythms were also affected in cry mutant

flies, but only in those which had been visually blinded
(i.e. lacked functional eyes). Drosophila CRY, therefore,
mediates light-dependent entrainment of multiple cellular
circadian rhythms, although its role in behavioral rhythms
is redundant in visually intact flies [19••].
Interestingly, plant CRY1 also plays a role in entrainment of
circadian rhythms in Arabidopsis [20•], albeit a minor one
relative to that of phytochrome. It should be noted, however, that the mouse and fly cryptochrome gene sequences
are significantly more similar to a distinct class of DNA
photolyase repair enzyme than they are to the cryptochrome blue-light photoreceptor of plants (Figure 1) [21].
The animal photoreceptors, therefore, seem to have arisen
independently in the course of evolution from a different
ancestral photolyase enzyme, and do not share any direct
relatedness with the plant cryptochrome photoreceptors. It
will be interesting to see whether this convergent evolution
of animal and plant cryptochromes resulted in comparable
mechanisms of action and signaling pathways.

Cryptochrome and phototropism
One of the best-known, yet most elusive plant blue-light

responses has been the phenomenon of phototropism —
the curvature of plants towards a unilateral light source.
Elegant kinetic experiments in Arabidopsis have provided
compelling evidence that at least two different specific
blue-light photoreceptors are involved in mediating phototropic curvature [22]. As the wavelength specificity and
phytochrome modulation of phototropic curvature is very
similar to that seen for cryptochrome responses [3,22–24],
it was surprising that initial experiments with hy4 mutants
(lacking CRY1) showed normal phototropic curvature
[25]. Double mutants lacking both CRY1 and CRY2,
however, showed little detectable curvature in response
to single-pulse low fluence blue light (inducing the first
positive phototropic curvature) [26••]. Furthermore,
transgenic seedlings overexpressing either CRY1 or CRY2
genes had a lower fluence threshold for the onset of curvature, revealing hypersensitivity to blue light in the
phototropic response [26••]. These findings are consistent with a redundant role in phototropism for both CRY1
and CRY2, such that only in the absence of both of these
receptors is there a significant reduction in responsiveness. Under continuous blue-light irradiation, however,
even cry1 cry2 double mutant seedlings show considerable phototropic response (second positive phototropic
curvature). Cryptochrome, therefore, participates in

mediating phototropic curvature together with at least
one other, unrelated blue-light absorbing photoreceptor
in addition to CRY1 and CRY2.

NPH1, a novel flavoprotein implicated
in phototropism
The blue-light dependent phosphorylation of an approximately 120 kDa protein can be detected within minutes
after irradiation of etiolated seedlings in vivo or microsomal
extracts in vitro [27]. This phosphorylation reaction could
be induced in vivo by similar light intensities and wavelengths of blue light as induced phototropic curvature, and
was absent in a mutant of Arabidopsis that is null for phototropism in etiolated seedlings, designated nph-1 (for
non-phototropic hypocotyl) [28]. Thus, blue-light dependent autophosphorylation of a 120 kDa protein was
proposed as one of the early steps in the signaling pathway
mediating phototropism.
The NPH1 gene has been cloned by positional cloning
[29••] and encodes a protein (predicted MW 112 kDa)
whose carboxy-terminal domain had significant homology
to a serine-threonine protein kinase (falling into the
PVPK1 family within the protein kinase C group). In addition, the amino-terminus of NPH1 encodes two similar 107
amino acid sequences, which appear in a number of proteins determined to have a role in light, oxygen or voltage
sensing (hence named the LOV domain). Interestingly, at
least two of these proteins (prokaryotic NIFL and Aer)
function in redox sensing via oxidation or reduction of a
flavin, whereas a third (WC-1) is known by genetic evidence to be involved in blue-light sensing in Neurospora
(discussed in [29••]). Recombinant NPH1 protein was
expressed in a baculovirus system and shown to bind a
flavin, FMN, and a blue-light dependent phosphorylation
reaction occurred in crude insect cell extracts expressing
NPH1 consistent with its possible direct role in blue light
sensing. On the basis of these data, NPH1 has been proposed as a photoreceptor for phototropism [30••].
So, what could the relationship between the cryptochromes
and NPH1 in the phototropic response be? One possibility
is that the cryptochromes may function as light harvesting
molecules that pass light energy directly to NPH1 via an
electron transfer mechanism (NPH1 then presumably
transducing the light signal via a phosphorylation reaction
to an appropriate substrate). This possibility is supported
by the observation that blue-light dependent phosphorylation of NPH1 is impaired under low light intensities in
cry1 cry2 double mutants [26••]. Furthermore, the structure
of cryptochrome is that of a light-dependent redox donor
and NPH1 more similar to redox acceptors that function
independently of light [29••]. Interaction between photoreceptor pathways need not be simple, however, and may
well occur at multiple levels, not just at the point of photoreception (Figure 2). It will be of great interest to
establish the precise connection between these two classes
of blue-light signaling molecules in the years to come.

Plant vision and photoreceptors Ahmad

How does phytochrome work?
Phytochrome — the red/far-red light absorbing photoreceptor — was the first plant photoreceptor to be identified
and purified although for almost 40 years its mechanism of
action has remained a mystery. Phytochrome consists of an
amino-terminal chromophore-binding domain and a carboxy-terminal ‘effector’ domain important for dimerization
and protein/protein interactions. In Arabidopsis and other
higher plants, phytochrome is encoded by a gene family of
multiple members with considerable sequence similarity
within the amino-terminal chromophore-binding domain
and greater sequence divergence at the carboxy-termini.
Different members of the phytochrome gene family have
been implicated to different extents in the various
responses of the plant to red or far-red light; for instance
phyB, the most abundant phytochrome in light-grown
plants, has a predominant role in red-light dependent inhibition of hypcotyl elongation, stem and leaf expansion,
vegetative growth, and floral initiation while other less
abundant phytochrome gene family members appear to
play a minor and partially redundant role (phyC and
phyD). Phys A is photolabile and the active form (Pfr)
rapidly degraded in light, but accumulates to high levels in
dark-grown seedlings. PhyA participates in high-irradiance
responses under far-red light, as well as in shade-avoidance
responses and photoperiodic induction of flowering in
light-grown plants [2]. Elegant domain swap experiments
between phyA and phyB — two phytochrome gene family

233

members that are considerably diverged in apparent physiological function — demonstrate that the carboxy-terminal
domains of different phytochromes are fully functionally
interchangeable [31]. The biochemical mode of action and
immediate reaction partners of the many phytochrome
gene family members, therefore, are likely to be identical.
This interpretation is supported by identification of mutational hotspots in homologous regions of both phyA and
phyB carboxy-termini, consistent with similarity in biochemical function [2].
The first clue concerning the molecular function of phytochrome came from the observation that purified
preparations of higher plant phytochrome A displayed serine/threonine kinase activity [32]. This observation was
supported by sequence analysis of the carboxy-terminal
domains of several higher plant phytochromes, which
revealed significant homology to histidine kinase transmitter modules found on bacterial sensor proteins [33].
Moreover, a recently characterized prokaryotic phytochrome from Synechocystis PCC6803, when expressed in a
heterologous yeast system was demonstrated to have histidine kinase activity in vitro. The activity was inducible by
far-red light and reversible by red [34•], in contrast to higher plants where red light is inductive.
The breakthrough in determining the function of the higher plant phytochromes came from analysis of recombinant

Figure 2
Photoreceptors and models of signaling
pathways. The different photoreceptors
(cryptochrome, phytochrome and NPH1) have
domain structures comprising amino-terminal
chromophore-binding domains and carboxyterminal effector domains. Receptors
implicated in blue-light sensing bind flavins
and/or pterins; phytochrome binds a
tetrapyrrole chromophore. Phytochrome and
cryptochrome participate in
photomorphogenesis (germination, deetiolation, inhibition of hypocotyl elongation,
vegetative morphology and initiation of
reproductive growth), as well as in
phototropism. NPH1 seems more specifically
implicated in phototropism, although it may
also play a part in photomorphogenesis
(M Ahmad, unpublished data). Phytochrome
responds to red and far-red light, interacts
both directly and indirectly with cryptochrome
photoreceptors to potentiate blue-light
signaling, and impacts on phototropism
downstream of NPH1. Cryptochrome
functions in photomorphogenesis and
participates in phototropism through direct or
indirect interaction with the NPH1 mediated
signaling pathway.

UV-A
BLUE
GREEN

RED
FAR-RED

Phytochrome

Cryptochrome
P
e-

Pterin

Flavin

Ser–thr kinase

tetra
pyrrole

NPH1
Flavin

Ser–thr kinase

Phototropism

Photomorphogenesis
Current Opinion in Plant Biology

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Physiology and metabolism

oat phyA expressed in yeast, which led to the demonstration of the protein’s serine–threonine kinase activity in
vitro. Phosphorylation activity was dependent on proper
chromophore assembly and stimulated by red light. As the
properties of recombinant phyA were identical to those
described previously for purified plant phytochromes, the
kinase activity must be intrinsic to the photoreceptor. On
the basis of sequence homology data and the function of
cyanobacterial phytochromes, it is likely that all higher
plant phytochromes and the majority of lower plant phytochromes evolved from prokaryotic histidine kinase
two-component regulators that acquired a novel,
serine–threonine specificity during the course of evolution [35••].

Do the different photoreceptors speak to each
other?
Having at least two distinct sets of photoreceptors that
respond preferentially to red and blue light enables the
plant to maximize its responsivity throughout the visible
spectrum. Do these different visual pathways function
independently of each other, or is there communication
between them? In fact, reports of interactions between
blue and red-light sensing systems abound [36], and genetic evidence has shown significantly reduced CRY1 activity
in the absence of both phyA and phyB [24]. Remaining
CRY1 function in phyA phyB mutants [24,37–39] may be
potentiated by additional phytochrome gene family members that are found in Arabidopsis (phyD, E and F). The
cry1 cry2 double mutant (lacking cryptochrome but containing wild type levels of phytochrome) shows virtually no
blue-light responsiveness in this assay [26••]. The role of
phytochrome in blue-light dependent inhibition of
hypocotyl elongation is therefore solely to enhance the
activity of CRY1 and CRY2, and not to participate directly
as has been proposed by some authors [37–39].

Cryptochrome is a substrate for phytochromeassociated kinase activity
Given the involvement of phytochrome in cryptochromemediated signaling pathways, one possibility is that the
two different photoreceptors might interact directly.
Phosphorylation experiments in vitro with purified recombinant photoreceptors indeed showed that CRY1 serves as
a substrate for phytochrome-dependent kinase activity
[40••]. Phosphorylation occurred at the carboxy-terminus
of CRY1, in a serine-rich region that is conserved in all
higher plant cryptochromes that have been sequenced
[40••]. Thus, cryptochrome is one of the few biological
substrates proposed for phytochrome to date (Figure 2).
Given its function as a kinase, phytochrome may have
multiple substrates. Indeed, an Arabidopsis protein, PIF3,
which interacts with both phyA and phyB in yeast twohybrid interaction cloning experiments is another possible
reaction partner proposed for phytochrome [41••]. PIF3 is
a nuclear-localized basic helix-loop-helix protein that
appears to be involved in phytochrome responses in phyB

overexpressing and antisense transgenic plants. As phyB in
particular appears nuclear-localized, phyB may interact
directly with PIF3 in vivo, and possibly also with others of
the numerous transcription factors implicated in light
responses [42•,43]. It will be interesting to see whether
PIF3 serves as substrate for phosphorylation by phytochrome-associated kinase activity.

Emerging themes: simplicity
underlying complexity
The many diverse plant light responses are mediated by
only a handful of photoreceptors (principally cryptochrome
and phytochrome). These occur as families of homologues
whose members function similarly and may have identical
reaction partners. Complexity of response can result from
differential expression levels, localization, and accessibility
to signaling intermediates of the different members of a
photoreceptor gene family. Additional flexibility is
achieved by communication between the different classes
of photoreceptors and their transduction pathways.
NPH1 is a novel flavoprotein with serine–threonine kinase
activity that functions in phototropism, possibly in association with cryptochrome. Phytochrome functions as a
serine–threonine kinase with multiple possible substrates,
including cryptochrome and nuclear transcription factors.
In conclusion, the number and types of different photoreceptors, their mode of action and their inter-relationship in
various signaling pathways are beginning to come more
sharply into focus.

Acknowledgements
I am indebted to B Sotta, E Miginiac and J-C Kader for helpful comments
and critical reading of the manuscript.

References and recommended reading
Papers of particular interest, published within the annual period of review,
have been highlighted as:

• of special interest
•• of outstanding interest
1.

Kendrick RE, Kronenberg GHM: Photomorphogenesis in Plants, edn 2.
Dordrecht: Kluwer Academic Publishers; 1994.

2.

Quail PH: The phytochrome family: dissection of functional roles
and signalling pathways among family members. Philos Trans R
Soc Lond B Biol Sci 1998, 353:1399-1403.

3.

Ahmad M, Cashmore AR: Seeing blue: the discovery of
cryptochrome. Plant Mol Biol 1996, 30:851-861.

4.

Ahmad M, Cashmore AR: Hy4 gene of A. thaliana encodes a
protein with characteristics of a blue-light photoreceptor. Nature
1993, 366:162-166.

5.

Sancar A: Structure and function of DNA photolyase. Biochemistry
1994, 33:2-9.

Ahmad M, Jarillo JA, Cashmore AR: Chimeric proteins between cry1
and cry2 Arabidopsis blue light photoreceptors indicate
overlapping functions and varying protein stability. Plant Cell
1998, 10:197-208.
This paper explores the functional relatedness of cryptochrome gene family members and suggests a similar function and mechanism of action in Arabidopsis.

6.
•

7.

Lin C, Yang H, Guo H, Mockler T, Chen J, Cashmore AR:
Enhancement of blue-light sensitivity of Arabidopsis seedlings by
a blue light receptor cryptochrome 2. Proc Natl Acad Sci USA
1998, 95:7686-7690.

Plant vision and photoreceptors Ahmad

8.

Guo H, Yang H, Mockler TC, Lin C: Regulation of flowering time by
Arabidopsis photoreceptors. Science 1998, 279:1360-1363.

9.

Bagnall DJ, King RW, Hangarter RP: Blue-light promotion of
flowering is absent in hy4 mutants of Arabidopsis. Planta 1996,
200:278-280.

10. Malhotra K, Sang-Tae K, Batschauer A, Dawut L, Sancar A: Putative
blue-light photoreceptors from Arabidopsis thaliana and Sinapis
alba with a high degree of sequence homology to DNA
photolyase contain the two photolyase cofactors but lack DNA
repair activity. Biochemistry 1995, 34:6892-6899.
11. Kanegae T, Wada M: Isolation and characterization of homologues
of plant blue-light photoreceptor (cryptochrome) genes from the
fern Adiantum capillus-veneris. Mol Gen Genet 1998, 259:345-353.
12. van der Spek PJ, Kobayashi K, Bootsma D, Takao M, Eker APM,
Yasui A: Cloning, tissue expression, and mapping of a human
photolyase homolog with similarity to plant blue-light receptors.
Genomics 1996, 37:177-182.
13. Kobayashi K, Kanno S, Smit B, van der Horst GT, Takao M, Yasui A:
Characterization of photolyase/blue-light receptor homologs in
mouse and human cells. Nucleic Acids Res 1998, 26:5086-5092.
14. Todo T, Tsuji H, Otoshi E, Hitomi K, Kim ST, Ikenaga M:
Characterization of a human homolog of (6-4) photolyase. Mutat
Res 1997, 384:195-204.
15. Hsu DS, Zhao XD, Zhao SY, Kazantsev A, Wang RP, Todo T, Wei YF,
Sancar A: Putative human blue-light photoreceptors hCRY1 and
hCRY2 are flavoproteins. Biochemistry 1996, 35:13871-13877.
16. Thresher RJ, Vitaterna MH, Miyamoto Y, Kazantsev A, Hsu DS, Petit C,
•• Selby CP, Dawut L, Smithies O, Takahashi JS, Sancar A: Role of
mouse cryptochrome blue-light photoreceptor in circadian
photoresponses. Science 1998, 282:1490-1494.
This paper explores the circadian phenotype resulting from knockout of a
mouse cryptochrome gene. This is the first conclusive demonstration of a
role for cryptochrome photoreceptors in mammals.
17.

Miyamoto Y, Sancar: A vitamin B2-based blue-light photoreceptors
in the retinohypothalamic tract as the photoactive pigments for
setting the circadian clock in mammals. Proc Natl Acad Sci USA
1998, 95:6097-6102.

18. Emery P, So WV, Kaneko M, Hall JC, Rosbash M: CRY, a Drosophila
•• clock and light-regulated cryptochrome, is a major contributor to
circadian rhythm resetting and photosensitivity. Cell 1998,
95:669-679.
This paper characterizes a cryptochrome gene from Drosophila that is implicated in circadian rhythms.
19. Stanewsky R, Kaneko M, Emery P, Beretta B, Wagner-Smith K,
•• Kay SA, Rosbash M, Hall JC: The cryb mutation identifies
cryptochrome as a circadian photoreceptor in Drosophila. Cell
1998 95:681-692.
In this paper the circadian phenotypes of a fly with a mutation in the
Drosophila cryptochrome gene is analyzed, and a role in multiple circadian
rhythms of the fly established.
20. Somers DE, Devlin PF, Kay SA: Phytochromes and cryptochromes
•
in the entrainment of the Arabidopsis circadian clock. Science
1998, 282:1488-1490.
This paper demonstrates a role for CRY1 in entrainment of circadian rhythms
in Arabidopsis.
21. Kanai S, Kikuno R, Toh H, Ryo H, Todo T: Molecular evolution of the
photolyase-blue-light photoreceptor family. J Mol Evol 1997,
45:535-548.
22. Konjevic RB, Steinitz B, Poff KL: Dependence of the phototropic
response of Arabidopsis thaliana on fluence rate and wavelength.
Proc Natl Acad Sci USA 1989, 86:9876-9880.
23. Janoudi A-K, Konjevic R, Whitelam G, Gordon W, Poff KL: Both
phytochrome A and phytochrome B are required for the normal
expression of phototropism in Arabidopsis thaliana seedlings.
Physiologia Plantarum 1997, 101:278-282.
24. Ahmad M, Cashmore AR: The blue-light receptor cryptochrome 1
shows functional dependence on phytochrome A or phytochrome
B in Arabidopsis thaliana. Plant J 1997, 11:421-427.
25. Liscum E, Young JC, Poff KL, Hangarter RP: Genetic separation of
phototropism and blue light inhibition of stem elongation. Plant
Physiol 1992, 100:267-271.
26. Ahmad M, Jarillo J, Smirnova O, Cashmore AR: Cryptochrome blue
•• light photoreceptors of Arabidopsis implicated in phototropism.
Nature 1998, 392:720-723.
This paper establishes the role of the cryptochrome in phototropism, and is thereby the first report of a blue-light receptor implicated in the phototropic response.

27.

235

Short TW, Briggs WR: The transduction of blue-light signals in
higher-plants. Annu Rev Plant Physiol Plant Mol Biol 1994,
45:143-171.

28. Liscum E, Briggs WR: Mutations in the nph1 locus of Arabidopsis
disrupt the perception of phototropic stimuli. Plant Cell 1995,
7:473-485.
29. Huala E, Oeller PW, Liscum E, Han I-S, Larsen E, Briggs WR:
•• Arabidopsis NPH1: a protein kinase with a putative redox-sensing
domain. Science 1997, 278:2120-2123.
This paper describes the cloning of NPH1, a gene that has been implicated
in an early event in the phototropism signaling pathway and may thereby
define a novel blue-light photoreceptor.
30. Christie JM, Reymond P, Powell GK, Bernasconi P, Raibekas AA,
•• Liscum E, Briggs WR: Arabidopsis NPH1: a flavoprotein with the
properties of a photoreceptor for phototropism. Science 1998,
282:1698-1701.
This paper is a follow-up of the previous paper on cloning of NPH1, demonstrating that it binds flavin and particpates in blue-light dependent phosphorylation reaction in a heterologous system. These data are consistent with
function as a photoreceptor.
31. Wagner D, Fairchild CD, Kuhn RM, Quail PH: Chromophore-bearing
NH2-terminal domains of phytochromes A and B determine their
photosensory specificity and differential light lability. Proc Natl
Acad Sci USA 1996, 93:4011-4015.
32. Wong Y-S, Cheng H-C, Walsh DA, Lagarias JC: Phosphorylation of
Avena phytochrome in vitro as a probe of light-induced
conformational changes. J Biol Chem 1986, 261:12089-12097.
33. Schneider-Poetsch HAW, Braun B, Marx S, Schaumburg A:
Phytochromes and bacterial sensor proteins are related by
structural and functional homologies. FEBS Lett 1991,
281:245-249.
34. Yeh KC, Wu S-H, Murphy JT, Lagarias JC: A cyanobacterial
•
phytochrome two-component light sensory system. Science 1997,
277:1505-1508.
In this paper, a prokaryotic phytochrome (presumably ancestral to all plant
phytochromes) is demonstrated to have histidine kinase activity in vitro.
35. Yeh KC, Lagarias JC: Eukaryotic phytochromes: light-regulated
•• serine/threonine protein kinases with histidine kinase ancestry.
Proc Natl Acad Sci USA 1998, 95:13976-13981.
This paper provides conclusive evidence for the first time of the mechanism
of action of phytochrome, as a serine/threonine dependent protein kinase.
36. Mohr H: Coaction between pigment systems. In Photomorphogenesis
in Plants, edn 2. Edited by Kendrick RE, Kronenberg GHM. Kluwer
Academic Publishers: Dordrecht; 1994:353-372.
37.

Casal JJ, Mazella MA: Conditional synergism between
cryptochrome 1 and phytochrome B is shown by the analysis of
phyA, phyB, and hy4 simple, double, and triple mutants in
Arabidopsis. Plant Physiol 1998, 118:19-25.

38. Neff MM, Chory J: Genetic Interactions between phytochrome A,
phytochrome B, and cryptochrome 1 during Arabidopsis
development. Plant Physiol 1998, 118:27-36.
39. Poppe C, Sweere U, Drumm-Herrel H, Schafer E: The blue-light
receptor cryptochrome 1 can act independently of phytochrome A
and B in Arabidopsis thaliana. Plant J 1998, 16:465-471.
40. Ahmad M, Jarillo J, Smirnova O, Cashmore AR: The CRY1 blue light
•• photoreceptor of Arabidopsis interacts with phytochrome A
in vitro. Mol Cell 1998, 1:939-948.
This paper demonstrates that cryptochrome is a substrate for phosphorylation by phytochrome in vitro. This is the first report of a possible biological
substrate for photochrome-associated phosphorylation activity, and also
defines a possible means by which these two major photoregulatory systems
within the plant may communicate.
41. Ni M, Tepperman JM, Quail PH: PIF3, a phytochrome-interacting
•• factor necessary for a normal photoinduced signal transduction,
is a novel basic helix-loop-helix protein. Cell 1998, 95:657-667.
In this paper, a possible interacting factor for phytochrome is identified in
yeast two-hybrid interaction studies, and implicates a transcription factor
directly in the phytochrome response.
42. Fankhauser C, Chory J: Light control of plant development. Annu
•
Rev Cell Dev Biol 1997, 13:203-229.
This paper demonstrates that a transcription factor implicated in phytochrome responses may participate in the entrainment of circadian rhythms.
43. Wang ZY, Tobin EM: Constitutive expression of the CIRCADIAN
CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms
and suppresses its own expression. Cell 1998, 93:1207-1217.