The Plant Journal (2010) 61, 982–991 doi: 10.1111/j.1365-313X.2009.04105.

ARABIDOPSIS: A RICH HARVEST 10 YEARS AFTER COMPLETION OF THE GENOME SEQUENCE

Light signal transduction: an infinite spectrum of possibilities

Joanne Chory*
Plant Biology Laboratory, The Salk Institute for Biological Studies, Howard Hughes Medical Institute, 10010 North Torrey
Pines Road, La Jolla, CA 92037, USA

Received 16 September 2009; revised 23 November 2009; accepted 25 November 2009.

*
For correspondence (fax +1 858 558 6379; e-mail chory@salk.edu).

SUMMARY

The past 30 years has seen a tremendous increase in our understanding of the light-signaling networks of
higher plants. This short review emphasizes the role that Arabidopsis genetics has played in deciphering this
complex network. Importantly, it outlines how genetic studies led to the identification of photoreceptors and
signaling components that are not only relevant in plants, but play key roles in mammals.

Keywords: Arabidopsis, light-signaling, photoreceptors.

INTRODUCTION

A few key events can shape a scientific life. For me, one of
these incidents occurred in 1987, after I had just given my
first job seminar. In it, I boldly claimed that I would use
Arabidopsis genetics to determine a complete signal trans-
duction pathway from phytochrome to the control of a light-
regulated gene. In 2010, this may not seem like an ambitious
goal, but in 1987, phytochrome was the only known receptor
in plants (Hershey et al., 1984), there was only a single report
of successful transformation of Arabidopsis (Lloyd et al.,
1986), and the Arabidopsis genetic map consisted of only
about 100 phenotypic markers (Koornneef et al., 1983).
It was still the days of slide projectors, so the lights in the
small seminar room were dimmed. My job talk was over and
it was time for probing questions, but the first speaker did
not ask me for clarification; rather, out of the darkness in the
back of the room came the proclamation ‘Why, you are a
very brave and naive girl! You know, there’s a reason that we
all fled from phytochrome research’. The speaker was
Harold William Siegelman, an icon in the phytochrome
field, who, in the 1960s, not only gave the intriguing
photoperiodic pigment its name, but also partially purified
‘holo-phytochrome’ and visualized the blue–green pigment
in a cuvette (Butler et al., 1959; Siegelman et al., 1966).
Dr Siegelman sat me down with his old notebooks and
showed me many puzzling results that scientists could not
explain from the 1960’s – observations that could not be
explained by the action of a single photoreceptor acting in a
linear signaling pathway. A perfect problem for a geneticist!
I left Brookhaven with words of encouragement from
Dr Siegelman and our agreement that the tools were in
place to unravel some of the paradoxes of light signaling. I
was extremely excited that I could make a difference in a
major area of plant physiology.
Fast forward to the bar at Cold Spring Harbor Laboratory
(CSHL) during the summer of 1993. I was with Elliot Meye-
rowitz, a guest speaker at the first Arabidopsis lab course, and
my fellow instructors, Joe Ecker and Sakis Theologis. We
were having beers after a long day in the lab. Joe and Sakis
were animatedly trying to convince Elliot that we needed to
sequence the Arabidopsis genome. Elliot was resisting the
idea, voting for individual investigator grants, rather than a
multi-national funding initiative. I don’t remember exactly
what happened, but at some point Elliot reversed his opinion,
and became enthusiastic that sequencing Arabidopsis would
be well worth the investment of tens of millions of dollars of
public funds. Jim Watson, then head of CSHL, together with
the leaders in Arabidopsis research, went on to lobby the US
National Science Foundation to take the lead in an initiative
that would fund three groups in the United States to
sequence chromosomes 1, 2 and 4. The rest is history….
These stories provide a major lesson for young scientists:
bringing new approaches to an old problem can lead to
major breakthroughs in a field. Mutants clarified the over-
lapping, and unique, functions of the various phytochromes
and led to the discovery of cryptochromes, phototropins and
other photoreceptors in plants. The availability of the fully

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sequenced and annotated genome of Arabidopsis gave us a
snapshot of what ‘makes a plant a plant’. It also provided the
framework for reverse genetic studies, and greatly facilitated
research in crop plants. I also learned that the leaders in a
field can provide guidance and advocacy for funding that
benefits an entire community.
In this review, I provide a brief history and summarize the
current state of knowledge of light-signaling research in
plants, focusing on how the sequence of Arabidopsis
enabled discovery of the principle components and dissec-
tion of the molecular mechanisms. My purpose is not to
review the many papers in the literature, but to recount the
chronology of some of the major discoveries in an effort to
uncover the role that Arabidopsis played in deconstruction
of one of the most complex signaling networks in plants.
Dissection of light-signaling networks has had profound
implications, not only for all flowering plants, but for human
biology as well.
A BRIEF HISTORY OF LIGHT SIGNAL TRANSDUCTION
PATHWAYS: THE 1980s
The early 1980s marked the dawn of modern plant molecular
biology. 1983 was an especially good year: the first reports
of stable plant transformation were published (Barton et al.,
1983; Caplan et al., 1983; Fraley et al., 1983; Herrera-Estrella
et al., 1983; Murai et al., 1983), maize transposons were
cloned (Burr and Burr, 1982; Geiser et al., 1982; Fedoroff
et al., 1983), and an Arabidopsis genetic map with 100 phe-
notypic markers scattered across the five chromosomes
became available (Koornneef et al., 1983). The icing on the
cake was Barbara McClintock’s Nobel prize, awarded for the
discovery of transposable elements. There was great
excitement regarding the potential for paradigm-shifting
discoveries in plant biology, so much that the US National
Science Foundation started a post-doctoral program spe-
cifically in the area of plant molecular biology. This program
was targeted to those new to the field, and would eventually
fund over 200 researchers.
It was a very exciting time in the light-signaling field as
well. After almost three decades of struggling, a full-length
phytochrome A holoprotein was purified from etiolated oat
seedlings by the Lagarias and Quail labs in 1983 (Litts et al.,
1983; Vierstra and Quail, 1983) (see Figure 1a for timeline).
This was followed a year later by cloning of the oat PHYA
gene (Hershey et al., 1984). Phytochrome, a red/far-red light
photoreceptor, thus became the first plant receptor whose
identity was known at the molecular level. Work at the other
end of the signal transduction pathway was also making
great progress. Several genes encoding the small subunit of
RuBisCO were cloned, as well as genes for the light-
harvesting chlorophyll a/b binding proteins. Work in multi-
ple laboratories led to the exciting discovery that light
positively regulates transcription of these genes (Simpson
et al., 1985; Timko et al., 1985; Gilmartin et al., 1990; Lam
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Light signal transduction 983
and Chua, 1990). The response was rapid (shorter than
15 min) and was universal among the angiosperms. Having
cloned phytochrome from oat, the Quail lab then went on to
show that light also negatively regulates transcription of this
gene (Bruce et al., 1989). Elaine Tobin’s lab weighed in with
the significant finding that light acts through phytochrome
to regulate gene expression in plants (Silverthorne and
Tobin, 1984).
By now, Agrobacterium-mediated transformation of the
solanaceous plants (tobacco, petunia, tomato, etc.) was
routine. The availability of histochemical markers such as
GUS, as well as facile transformation protocols, led to the
identification of multiple light-regulatory enhancers acting
in the promoters of these genes, such as the ‘L’, ‘I’ and ‘G’
boxes identified in Tony Cashmore’s lab, box II, and many
more (Donald and Cashmore, 1990). One principle soon
emerged: more than one light-regulatory enhancer was
required for a gene to become light-regulated (Donald and
Cashmore, 1990; Chattopadhyay et al., 1998). Yet, despite
these exciting advances, the events between photon excita-
tion of the photoreceptor and regulation of gene expression
remained a mystery (Figure 2).
Lurking in the shadows, a small, insignificant weed was
about to burst onto the scene. However, this insignificant
weed, Arabidopsis, had not yet made much of an impact on
the light-signaling field. A few papers, such as Koornneef’s
paper on long-hypocotyl mutants of Arabidopsis, are nota-
ble (Koornneef et al., 1980). In this paper, Koornneef
described the first large genetic screen for mutants with
reduced sensitivity to light. The mutants defined five
complementation groups, and led to the identification of
cryptochrome, phytochrome’s chromophore biosynthetic
enzymes, a downstream transcriptional regulator, and
phytochrome B (discussed in more detail below) (see
Figure 1b). Later, Arabidopsis genomic libraries proved
useful in identifying a phytochrome gene family (five
members in Arabidopsis) (Sharrock and Quail, 1989). The
decade ended with the description of a class of mutants
[de-etiolated (det) mutants] that developed like light-grown
plants even in the absence of light (Chory et al., 1989; Chory
and Peto, 1990). These loss-of-function mutations were
epistatic to the long-hypocotyl mutants, implying that
negative regulators existed downstream from light percep-
tion that prevented photomorphogenesis from occurring
when no light was available (Chory, 1992). Identification of
this class of mutants added an important regulatory
component to the pathway shown in Figure 2.
ARABIDOPSIS RULES THE 1990s: YOU CAN NEVER HAVE
TOO MANY MUTANTS
Arabidopsis dominated light-signaling research during the
1990s (Figure 1b). Mutants in both receptors and positively
acting signaling components were identified from genetic
screens for light-hyposensitive mutants (seedlings that have
984 Joanne Chory

(a)

(b)

Figure 1. A 30-year timeline of light-signaling research.

(a) Major discoveries in light signaling since 1980 that were made independently of the Arabidopsis system.
(b) Discoveries made during the same period using Arabidopsis.
Note that, during the past decade, it is hard to distinguish Arabidopsis-dependent contributions from independent ones.

long hypocotyls under various wavelengths and fluence
rates of light). Mutations in individual phytochromes were
characterized, solving some of the dilemmas in Dr Siegel-
man’s notebooks, while at the same time revealing even
more complexity in the light-signaling network (reviewed
by Neff et al., 2000; Briggs and Olney, 2001). Higher-order
genetic analysis revealed a complex web of interactions
within and between the various classes of photoreceptors,
including redundancy, antagonism and effector/modulator
relationships. Although the mechanisms of these interac-
tions are not all clear, there is mounting evidence for both
direct physical contacts between photoreceptors and
common interacting partners (Figure 3).
Unlike phytochrome, which was purified based on an
elegant photoreversibility assay, no receptor for blue light
had been identified at the end of the 1980s. Moreover,
researchers in this field were caught up in an abstract debate
as to what the chromophore for a blue light receptor might be

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Figure 2. Model for phytochrome signaling circa 1989.
(a carotenoid or a flavin-type molecule), a problem exacer-
bated by the erroneous notion that there was a single blue
light receptor. The first elusive blue/UV-A light photorecep-
tor, cryptochrome, was identified by cloning of the long
hypocotyl 4 (hy4) locus, originally reported in the Koornneef
et al., 1980 paper (Ahmad and Cashmore, 1993). HY4, which
was subsequently renamed cryptochrome 1 (CRY1), uses an
N-terminal domain that is shared with photolyases to bind
two chromophores, a flavin adenine dinucleotide with cata-
lytic functions and a deazaflavin or pterin for light harvesting
(Cashmore et al., 1999). However, CRY1 has no photolyase
activity. Cashmore and colleagues showed that Arabidopsis
has two cry-like genes, and performed a brute force screen to
identify cry2 mutants (Lin et al., 1998). Like CRY1, CRY2
appears to play a role in blue light perception in hypocotyls.
In addition to this role, CRY2 also plays a significant role in
flowering time. To date, the photochemistry of the crypto-
chromes has proven difficult to crack, although the prevalent
idea is that cryptochromes act through some sort of redox-
driven reaction. Very recently, Liu et al. identified the first
binding partner of CRY2, a nuclear protein called CIB1 that
binds to G-boxes in the promoters of light-regulated genes
(Liu et al., 2008).
The discovery of the blue light receptor family for
phototropism was a decade-long labor of love, mostly by
Winslow Briggs’ lab, that culminated in identification of
phototropin 1 in 1998 by cloning of the Arabidopsis nph1
locus (non-phototropic hypocotyl 1) (Liscum and Briggs,
1995; Christie et al., 1998). There is irony in this story. I have
it from good sources that Winslow strongly resisted working
on Arabidopsis, preferring larger plants, such as maize and
Figure 3. Genetic model for light signaling circa
2000.
Mutation in early signaling intermediates are
expected to have a phenotype only under the
specific light conditions activating their photore-
ceptor, and known molecules fitting this require-
ment include several transcription factors that
directly interact with photoreceptors, as well as
other molecules that are phosphorylated by
phytochromes. The subcellular localization of
phytochrome itself is light-regulated. Thus, in
light signaling, there are direct interactions of
photoreceptors, as well as cross-talk and inte-
gration of pathways both early and late in the
signaling network.
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Light signal transduction 985
pea. While these larger plants ultimately contributed to the
story, the discovery of phototropin would have been signif-
icantly delayed without Arabidopsis mutants. In 1988,
Gallagher et al. showed that blue light could activate phos-
phorylation of a plasma membrane protein from growing
regions of etiolated pea seedlings (Gallagher et al., 1988).
Various biochemical experiments suggested that this pro-
tein could autophosphorylate in response to blue light
(Short and Briggs, 1994). At the same time, genetic exper-
iments performed in Briggs’ lab and later in Liscum’s lab,
identified a number of phototropism-defective mutants,
nph1, 2, 3 and 4 (Motchoulski and Liscum, 1999; Harper
et al., 2000). The cloning of NPH1 suggested it to be the
photoreceptor for phototropism, as nph1 mutants are
impaired in light-activated phosphorylation and phototro-
pism (Christie et al., 1998). Arabidopsis has two phototro-
pins, PHOT1 and PHOT2. Genetic studies indicate that these
two phototropins have partially redundant functions. In
addition to controlling phototropism, characterization of
phot1 phot2 double mutants implied a role for phototropins
in blue light-dependent chloroplast relocation (Kagawa
et al., 2001), stomatal opening (Kinoshita et al., 2001) and
growth (Folta et al., 2003). Not only did the protein have a
canonical serine/threonine kinase domain, but it also con-
tained two repeated domains of 100 amino acids, with 40%
amino acid sequence identity to each other (Zhulin et al.,
1997). These domains also show sequence similarity to
domains found in a number of signaling proteins in organ-
isms from all kingdoms of life. Because all these proteins are
regulated by light, oxygen or voltage, the domains were
assigned the acronym LOV (Christie et al., 2002; Briggs,
2007). LOV domains are a subset of the PAS domain super-
family, which is known to mediate both ligand binding and
protein–protein interactions.
In addition to the work on photoreceptors, the 1990s was
a decade of discovery of light-signaling components
(Figure 3) (reviewed by Neff et al., 2000). Genetic and
molecular screens, most of which focused on seedling
986 Joanne Chory
responses, especially those that are part of de-etiolation,
identified many dozens of genes acting downstream of
photoreceptors. Because different spectral qualities trigger
the same developmental responses using different photo-
receptors, it was hypothesized that common late-acting
signaling intermediates are used. The best-studied class of
proteins that fit this description is the class of negative
regulators, which, when mutated, cause seedlings to de-
etiolate even in the absence of light (the det, cop and fus
class). The screen was performed to saturation in Xing-
Wang Deng’s lab, culminating in the identification of more
than ten ‘cop’ loci (‘constitutively photomorphogenic’)
(Kwok et al., 1996). Soon after, most of the COP genes had
been cloned. However, it was not until the Deng lab purified
the major ‘COP’ complex that it became apparent that these
proteins play a role in protein turnover (Chamovitz et al.,
1996). Eight of the proteins are members of an evolutionarily
conserved complex called the CSN (‘COP9 signalosome’)
(Wei et al., 1998). The CSN may have multiple activities, but
the best characterized is its ability to cleave and remove the
ubiquitin-like protein, Nedd8, from cullin ubiquitin ligase
subunits (Wei and Deng, 2003). COP1 is an E3 ligase that
targets both labile photoreceptors, e.g. PHYA, as well as
downstream effectors, e.g. HY5 (Figure 3) (Yi and Deng,
2005). More recently, several researchers have shown that
DET1 is also part of an E3 ligase that is in close association
with chromatin, and complexed with COP10, DDB1 and
CUL4 (Benvenuto et al., 2002; Schroeder et al., 2002; Yanag-
awa et al., 2004; Zhang et al., 2008). Also identified were
many positively acting signaling components, including
transcription factors, chaperones and scaffolds (reviewed by
Neff et al., 2000).
The decade ended with two remarkable discoveries. The
first is that phytochromes are light-regulated protein kinases.
With the discovery of cyanobacterial phytochromes in the
mid-1990s, Yeh et al. were able to show quite clearly that
bacterial phytochromes are light-regulated kinases (Yeh
et al., 1997). Higher-plant phytochromes also have a
histidine-kinase related domain, but no histidine kinase
activity could be found. Yeh and Lagarias showed that two
plant phytochromes are light- and chromophore-regulated
kinases, but, unlike their cyanobacterial counterparts, they
autophosphorylate on serine/threonine (Yeh and Lagarias,
1998). PHYA is a phosphoprotein in vivo , and at least one
serine is phosphorylated in a light-dependent manner. In
vitro kinase assays using phytochrome A identified other
substrates of PHYA, including CRY1 and CRY2, and some
newly discovered signaling proteins (Fankhauser et al., 1999;
Fankhauser, 2000).
Yeast two-hybrid screens identified the first potential
signaling partners of phytochrome. The first three included a
bHLH transcription factor, PIF3 (Ni et al., 1999), a cytoplas-
mic protein, PKS1 (Fankhauser et al., 1999), and a nucleoside
diphosphate kinase, NDPK2, which is localized to both
Journal compilation ª 2010 Blackwell Publishing Ltd, The Plant Journal, (2010), 61, 982–991
nuclear and cytoplasmic fractions (Choi et al., 1999). We
know now that PIF3 is a member of a sub-family of bHLH
proteins that bind preferentially to photo-activated phyto-
chrome through a phytochrome interaction domain (Huq
et al., 2004; Khanna et al., 2004, 2007; Al-Sady et al., 2006;
Monte et al., 2007; Shen et al., 2007). PIF family members
control light-regulated gene expression. Light induces the
phosphorylation of some PIFs, which is necessary for their
rapid degradation (Al-Sady et al., 2006; Shen et al., 2007);
however, ten years after their discovery, it is still unclear
whether PHY kinase activity is responsible for this degrada-
tion or whether phytochrome recruits another kinase to
perform the degradation (Castillon et al., 2007; Bae and
Choi, 2008).
LIGHT SIGNALING IN THE POST-SEQUENCE ERA: GENETIC
REDUNDANCY, MICROARRAYS, CELL AND STRUCTURAL
BIOLOGY
The completion of the Arabidopsis genome sequence in
2000 (Arabidopsis Genome Initiative, 2000) has facilitated
proteomic studies, design of gene expression and full-
genome tiling arrays for global gene expression and epige-
netic studies, as well as the positional cloning of genes
(Clark et al., 2007; Yazaki et al., 2007; Lister et al., 2009). This
greatly increased the speed of new discoveries in terms of
new signaling components; in addition, it helped to eluci-
date the degree to which these proteins may be redundantly
encoded (Alonso and Ecker, 2006).
A major step forward for those of us studying photomor-
phogenesis was the design and creation of various types of
platforms to interrogate transcription of the full genome of
Arabidopsis. A number of studies were published reporting
that hundreds, if not thousands, of genes were induced or
repressed by changes in light quality, intensity or dark/light
transitions (Tepperman et al., 2004, 2006). Judicious use of
various mutants in the analysis helped explain why different
photoreceptors have both overlapping and distinct func-
tions (Ma et al., 2003; Tepperman et al., 2004, 2006; Jiao
et al., 2007).
The Nagatani lab paper indicating that phytochromes
move to the nucleus from the cytosol after excitation by
light has completely changed researchers’ views of the
signaling pathway (Sakamoto and Nagatani, 1996; Yamag-
uchi et al., 1999; Nagatani, 2004). Within a few years, it was
noted that phytochromes are located in sub-nuclear parti-
cles, called phytochrome speckles or phytochrome nuclear
bodies (reviewed by Chen, 2008). These nuclear bodies
change in size and number with the fluence rate of red
light, the total number of photons or the time of day (an
indicator of how much active phytochrome there is) PHYB
has been found in the same nuclear body as CRY2, and
also in a NB with PIF3 (Mas et al., 2000). The current view
is that these nuclear bodies are sites of protein turnover,
and that turnover of transcription factors, such as the PIFs,
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as well as of some photoreceptors, is required to achieve a
light response.
NATURAL VARIATION IN LIGHT SIGNALING: A UNIQUE
SYSTEM FOR ELUCIDATING GROWTH REGULATORY
NETWORKS, AS WELL AS THE EVOLUTION OF SUCH
COMPLEX NETWORKS
The correct response to a specific light cue depends on the
environmental context. Thus, plants native to different light
environments have evolved different adaptive responses
(Maloof et al., 2000). Although mutational studies have
defined a number of genes involved in light perception and
signaling, the genes and molecular changes responsible for
adaptive changes in light response remain mostly unknown.
In a collaboration that has lasted more than a decade,
researchers in the labs of Detlef Weigel and myself have
shown that a wide range of heritable differences in light
response can be found among isolates of Arabidopsis thali-
ana (e.g. Maloof et al., 2001). Moreover, there is a significant
inverse correlation between latitude and light sensitivity,
suggesting adaptation to an environmental factor that varies
over latitudinal clines. Thus, natural variation studies in
Arabidopsis may be very informative, for both new gene
discovery (Loudet et al., 2008) and determining which
proteins in the signaling pathway may be under selection.
To date, these studies have identified that changes in
individual photoreceptor family members, including phyA,
phyB, phyC and cry2, are important determinants in the
natural variation of light sensitivity. One accession, Lm-2, is
insensitive to far-red light, similar to phytochrome A (phyA)
mutants. We found that Lm-2 does not complement phyA
due to a single amino acid change, and that this change
causes production of a protein that is less sensitive to light
(Maloof et al., 2001). In separate studies, we used QTL
mapping to identify loci involved in light-response variation
for seedling emergence between two other strains, Ler and
Cvi, and identified an average of four loci per light condition
examined (Borevitz et al., 2002). One QTL is the phyto-
chrome B gene, which is known to be important for
response to red light. Strikingly, association testing sug-
gests that the PHYB region is an important determinant of
the light response across many A. thaliana accessions
(Filiault et al., 2008). Finally, in support of a potential
adaptive role of PHYC, we found that the more active Col-0
PHYC haplotype group was more frequent at northern
latitudes (Balasubramanian et al., 2006). Combined with
the work of Koornneef and colleagues on CRY2 (El-Din
El-Assal et al., 2001; El-Assal et al., 2004), and Weinig et al.
on shade avoidance (Brock et al., 2007), these studies
demonstrate that Arabidopsis is an excellent organism for
studying the molecular basis of natural variation in light
response, and suggest that some changes in the light
response in Arabidopsis and its relatives are adaptive.
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Light signal transduction 987
BEYOND PLANTS
Studying the mechanisms by which plants respond to light
has had an impact beyond plants. In this section, I describe a
few examples of how plant research on light signaling has
had an impact on research in metazoans. Jones et al. (2008)
provide a more thorough treatment of this subject.
Protein turnover
The study of light signaling in plants has not only pro-
vided insight into plant growth and development, but has
also led to the discovery of conserved proteins that reg-
ulate transcription, tumorigenesis and lipid metabolism in
metazoans. Many of these proteins function in the regu-
lation of protein stability and are members of conserved
signaling modules found in both plants and animals.
Importantly, the COP9 signalosome (CSN), which shares
structural similarity with the lid sub-complex of the 26S
proteasome, was first recognized and purified from
plants, but is now known to play an essential role in
many aspects of both plant and animal development (Wei
et al., 1998; Menon et al., 2007). Similarly, the human
homologs of Arabidopsis COP1 and DET1 proteins were
recently shown to be important negative regulators of the
human tumor suppressor p53 (Yi and Deng, 2005). It was
a great personal satisfaction to me to open Science and
find a paper entitled: ‘Human De-etiolated-1 regulates
c-Jun by assembling a CUL4A ubiquitin ligase’ (Wertz
et al., 2004).
Cryptochrome and the circadian clock
Identification of Arabidopsis cryptochrome mutants enabled
identification of the many functions for cryptochromes in
plants, including its roles in photoperiodism and flowering,
seedling emergence, and as an input to the circadian clock.
Cloning the Arabidopsis gene allowed predictions of the
protein sequence, and enabled the discovery of crypto-
chromes from both flies and humans (Ceriani et al., 1999). In
flies, cryptochromes are both photoreceptors and compo-
nents of the circadian clock, while, in humans, crypto-
chromes appear to be solely clock components. A number of
diseases that depend on a functioning circadian clock (e.g.
cancer) are suspected to be caused by defects in the cryp-
tochrome pathway.
Phytochromes and phototropins as photoactivatable
switches
Over the past few years, a number of X-ray and NMR
structures for bacterial phytochromes and LOV domains
have been obtained, and have assisted in clarifying
how these photoreceptors work (Harper et al., 2004;
Rockwell et al., 2006; Chen et al., 2007; Wagner et al., 2007;
Cornilescu et al., 2008; Essen et al., 2008; Ogura et al., 2008;
988 Joanne Chory
Tokutomi et al., 2008; Yang et al., 2008; Hitomi et al., 2009).
These studies have enabled use of these two photoreceptors
as photo-activatable switches in mammalian systems. Two
recent papers explored actin dynamics using the chromo-
phore-binding domain of phytochrome B (Leung et al., 2008)
or the LOV domain of phototropin (Wu et al., 2009). A phy-
tochrome switch is being used to alter cell shape and
motility (Levskaya et al., 2009). LOV domain fusions are also
being used to probe conformational changes in proteins
(Strickland et al., 2008). Finally, fluorescent phytochromes
have allowed the live imaging of internal organs in intact
mice (Shu et al., 2009).
SUMMARY AND PROSPECTS FOR THE FUTURE
The past 30 years have seen a tremendous gain in our
understanding of the light-signaling networks of higher
plants. These networks allow plants to gauge their location,
monitor daily and seasonal time, and to adjust their growth
habit accordingly, thereby conferring a fitness advantage.
Because of the contributions of scientists using Arabidopsis,
we now have a mechanistic model for photomorphogenesis,
in which photoreceptors, mostly acting in the nucleus, reg-
ulate gene expression by initiating turnover of key tran-
scription factors. This triggers a transcriptional cascade,
leading to the regulated expression of thousands of nuclear
genes.
I think Bill Siegelman and his mentors would have been
proud of where their field has gone. Yet they would also be
shocked by the complexity, in terms of sheer numbers of
photoreceptors and their complex relationships with each
other. So, was sequencing the A. thaliana genome worth the
tens of millions of dollars? The answer is ‘yes’. Did a genetic
approach make a difference? Definitely ‘yes’. Arabidopsis
has truly risen to the ranks where it is on equal footing with
the other model genetic systems, e.g. yeast, Drosophila and
C. elegans, especially in terms of natural variation and as a
toolkit for molecular genetic studies.
Are the golden years of Arabidopsis over? My answer is a
resounding ‘no’! The functions of about 50% of Arabidopsis
genes are still unknown, and no other plant system comes
close to Arabidopsis in terms of gene discovery. Moreover,
we are just beginning to see the impact of 20 years of
Arabidopsis research on agriculture. The ease and power of
Arabidopsis transformation allows over- or under-expres-
sion of specific genes in various mutant backgrounds,
thereby conferring unique phenotypes. Moreover, knowing
the molecular defects of various Arabidopsis mutants has
explained traits that breeders have enriched for, such as the
high-pigment mutants of tomato (Lazarova et al., 1998;
Mustilli et al., 1999; Liu et al., 2004), or the sorghum
maturation genes (Finlayson et al., 1999, 2007). Reduction
of losses in yield due to shade avoidance in maize has
benefitted greatly from Arabidopsis research on shade
avoidance mutants (Kebrom and Brutnell, 2007).
Journal compilation ª 2010 Blackwell Publishing Ltd, The Plant Journal, (2010), 61, 982–991
In addition, using tissue- and cell type-specific Arabidop-
sis promoters to express components of light-signaling
pathways in a subset of cells is allowing us to understand
which portions of a plant’s response to light are cell
autonomous (Tanaka et al., 2002; Endo et al., 2005, 2007;
Endo and Nagatani, 2008). Arabidopsis is the only plant
system for which the tools are in place to successfully
perform such experiments.
The extensive set of mutants for Arabidopsis light,
disease and hormone responses will be put to good use
over the next decade to understand and test hypotheses
about fitness trade-offs during evolution of plants growing
in specific environments. Coupled with natural variation
studies (Weigel and Mott, 2009), and the Arabidopsis
molecular genetics toolkit (Lister et al., 2009), the possibil-
ities are limitless.
ACKNOWLEDGEMENTS
I thank Drs Eirini Kaiserli and Ullas Pedmale for reading this review
and verifying the facts. This review is not meant to cover all aspects
of light signaling (for instance, I did not even broach the exciting
fields of circadian biology, photoperiod and flowering). I have retold
events as I recall them, but bear in mind that my memories may be
distorted by more than 20 years of time. I thank my colleagues who
work on light signaling for stimulating discussions, and apologize to
those whose work I did not cite due to space constraints. Science is
truly a collective effort of many individuals who both compete and
collaborate with each other in search of the truth.
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