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Plant, Cell and Environment (2008) 31, 667–678
Paths through the phytochrome network
EVE-MARIE JOSSE*, JULIA FOREMAN* & KAREN J. HALLIDAY
Institute of Molecular Plant Sciences, Edinburgh University, Kings Buildings, Mayfield Road, Edinburgh, EH9 3 JR, UK
ABSTRACT
Since the discovery of the physical interaction between
phytochrome B and the basic helix-loop-helix (bHLH) tran-
scription factor (TF) PIF3 a decade ago, plant phytochrome-
signalling research has largely focused on understanding the
mechanisms through which phytochromes and members of
this bHLH family signal. This concerted effort has revealed
how phytochrome and bHLH TF control gene expression
and plant growth, and has assigned precise roles to a number
of genes in the PIF3-like bHLH TF clade. This work has
focused largely on cell autonomous signalling events;
however, to synchronize plant growth and developmental
events at the tissue and organ level, temporal and spatial
signal integration is crucial. This review brings together
current knowledge of phytochrome signalling through
phytochrome-interacting factors (PIFs)/phytochrome-
interacting factor-like (PILs), and it evaluates the current
evidence for cross-tissue signal integration.
Key-words: bHLH transcription factor; circadian; gibberel-
lic acid signalling; inter-organ communication; light; photo-
receptor; PIF; PIL.
INTRODUCTION
Plant photoreceptors act at the interface of exterior and
internal molecular environments. Their job is to acquire
information on seasonal progression and on the condition
of the local habitat. This is achieved by detecting changes in
day length (photoperiod) and spectral light quality. Con-
stant surveillance provides a means for the plant to adjust
its growth and development so that it is in tune with the
seasons and the often dramatic accompanying changes in
local vegetation. Partly because light is a primary utility for
photosynthesizing plants, and partly because light cues can
provide an accurate readout of environmental change,
higher plants have evolved a whole suite of photoreceptors.
Subdivided into small gene families, these receptors absorb
light in both distinct and overlapping regions in the UV-B
to far-red (FR) (~280–800 nm) portion of the electromag-
netic spectrum. Detecting a broad spectral range has two
main advantages: (1) it ensures that vital responses, such as
chlorophyll production, are robustly triggered by a range of
wavelengths; and (2) it enables specialization, for instance,
Correspondence: K. J. Halliday. Fax: +44 131 650 6556; e-mail:
Karen.Halliday@ed.ac.uk
*Authors contributed equally to this manuscript.
© 2008 The Authors
Journal compilation © 2008 Blackwell Publishing Ltd
13653040, 2008, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1365-3040.2008.01794.x by NHS Education for Scotland NES, Edinburgh Central Office, Wiley Online Library on [17/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
doi: 10.1111/j.1365-3040.2008.01794.x
particular wavelengths trigger phototropic growth. In this
review, we will explore the emerging view of how phyto-
chromes (phy), the red (R) and far-red (FR) light-absorbing
photoreceptors, control the early stages of plant
development.
THE PHOTOREVERSIBLE PIGMENT
Phytochromes are large (~120 kD) protein dimers with
light-sensing phytochromobilin chromophores covalently
attached within the N-terminal region of each apoprotein
(Chen, Chory & Fankhauser 2004). These photoreceptors
exist as two interconvertible forms that toggle between
the biologically inactive R-absorbing Pr and active
FR-absorbing Pfr isoforms. R light irradiation induces a
conformational change that converts Pr into Pfr. This
photoconversion is reversible, following exposure to FR
wavelengths. Reversion to the inactive Pr form also occurs
during prolonged dark periods via a thermal process known
as dark reversion (Sineshchekov 1995; Braslavsky, Gartner
& Schaffner 1997). The absorption of light triggers the
translocation of phytochrome to the nucleus and the subse-
quent modification of gene transcription (Nagy & Schafer
2002; Huq, Al-Sady & Quail 2003; Nagatani 2004). These
early molecular events set in motion signalling pathways
that control an array of growth and developmental
responses including germination, seedling establishment,
elongation growth, apical dominance and flowering time
(Chory et al. 1996).
The antagonistic effects of R and FR light on plant
growth were first shown in the early 1950s. At this time,
Borthwick et al. (1952) demonstrated that R light induction
of lettuce seed germination could essentially be negated if
FR light was provided immediately after a R pulse. This led
to the development of the concept of a ’photoreversible
pigment’ (Butler et al. 1959) and to the idea of the existence
of two interconvertible forms of the phytochrome molecule
(Borthwick & Hendricks 1960). Suggestions were made
that the biologically inactive Pr and the active Pfr isoforms
resulted from the association of an apoprotein to a photo-
reversible pigment (Borthwick & Hendricks 1960). These
ideas were insightful as the phytochrome apoprotein was
later shown to attach the light-absorbing chromophore,
phytochromobilin (Elich & Lagarias 1987).
Initially, phytochrome was considered as a single molecu-
lar species. However, detailed spectrophotometric studies
suggested the existence of two forms of phytochrome with
different properties (Furuya, Hopkins & Hillman 1965).
These early studies lit the touch paper that eventually led to
667

668 E.-M. Josse et al.
the demonstration that phytochrome was divided into two
pools (Brockman & Schafer 1982; Abe et al. 1989; Furuya
1989; Nagatani et al. 1989). Type I, or light-labile phyto-
chrome, was abundant in etiolated seedlings, degrading
rapidly after exposure to light. In contrast, type II, or light-
stable phytochrome, was not degraded by light, persisting
in light-grown seedlings. Following the discovery of a small
gene family encoding five phytochromes in Arabidopsis,
named PHYA-E (Sharrock & Quail 1989; Clack, Mathews
& Sharrock 1994), phyA was assigned the light-stable, and
phyB-E the light-stable forms of phytochrome (Quail 1991;
Sharrock & Clack 2002).
As phyB-E Pfr and Pr are reasonably stable in light-
grown seedlings, the relative levels of these two isoforms
in planta are proportionate to the ratio of R and FR light
perceived. These characteristics mean that light-stable phy-
tochromes are exquisite sensors of light quality. They are
also robustly R/FR reversible, which is a key feature of the
so-called low fluence response (LFR) mode in which they
operate. The light-labile character of phyA-Pfr enables
phyA to work in quite a different manner. In etiolated
seedlings, phyA accumulates to very high levels, and
because of the overlapping absorption spectra of the Pr and
Pfr forms, even small amounts of R or FR light are sufficient
to generate phyA-Pfr (Shinomura et al. 1996). This triggers
responses in the so-called very low fluence response
(VLFR) mode, for example, germination. VLFRs are typi-
cally saturated at very low concentrations of Pfr and do not
show classical R/FR photoreversibility (Smith & Whitelam
1990). PhyA levels also accumulate under a continuous FR
or low R/FR ratio light where the majority of phyA is in the
Pr form. Under these conditions, a small proportion of
phyA will photoconvert to the Pfr form, which will then
either photorevert to Pr or degrade. This dynamic equilib-
rium will drive phyA action in the so-called high irradiance
response (HIR) mode, where the degree of the response is
highly dependent on the fluence rate and duration of the
FR light (Shinomura, Uchida & Furuya 2000). These char-
acteristics mean that phyA is, in some senses, more versatile
than the other phytochromes, regulating responses to FR as
well as R light.
GERMINATION AND SEEDLING
ESTABLISHMENT
Light is an extremely influential signal during both germi-
nation and seedling establishment. When germination
occurs in the absence of light, limited resources are used for
promoting elongation of the seedling hypocotyl in an effort
to reach light at the soil surface. Even very dim light can
trigger a whole series of events that dramatically alter the
developmental programme towards de-etiolation. Perhaps
the most important of these events is the rapid acquisition
of photosynthetic competence and the modification of
growth habit to maximize light and nutrient capture. In the
young seedling, light drives and coordinates a suite of
responses including inhibition of hypocotyl elongation,
cotyledon expansion, chlorophyll production and root
Journal compilation © 2008 Blackwell Publishing Ltd, Plant, Cell and Environment, 31, 667–678
13653040, 2008, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1365-3040.2008.01794.x by NHS Education for Scotland NES, Edinburgh Central Office, Wiley Online Library on [17/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
growth (Chen et al. 2004). The amplitude of this physiologi-
cal response is directly related to the fluence rate and spec-
tral quality of the ambient light environment.
Genetic studies in Arabidopsis have identified roles for
phyB and phyE in the R/FR reversible promotion of seed
germination (Shinomura et al. 1994; Hennig et al. 2002).
PhyA irreversibly triggers germination in both VLFR and
FR-HIR modes, and phyE appears to participate in this
response, regulating germination under a continuous FR
(Hennig et al. 2002). Mutant analysis has also shown that
phytochromes play a pivotal role in controlling the
de-etiolation switch and are intimately involved with fine-
tuning seedling establishment and development: for
example, phyA null mutants fail to de-etiolate and regulate
the requisite genes when grown under FR light (Nagatani,
Reed & Chory 1993; Parks & Quail 1993; Whitelam et al.
1993; Tepperman et al. 2001). These and associated experi-
ments show that, as for germination, phyA regulates early
development in response to FR light. While phyA is the
major regulator under FR light, R light responses are con-
trolled by multiple phytochromes, although phyB appears
to have a central role. This is highlighted by phyB mutant
alleles that fail to fully de-etiolate when grown under R
light. Mutant analysis has shown that phyC and phyD par-
ticipate, but have more minor roles in this process. phyC
mutants show a substantial increase in hypocotyl length
in R light, although no additional phenotype in a phyB
null background, suggesting that phyC controls extension
growth by modulating phyB function (Franklin et al. 2003a;
Monte et al. 2003). phyD mutants show a small or marginal
increase in hypocotyl elongation when grown under R light,
while phyE and phyA are indistinguishable from wild-type
seedlings (Aukerman et al. 1997). The effects of these muta-
tions do, however, become apparent when phyB levels
and/or levels of other phytochromes are also depleted
(Reed & Chory 1994; Devlin, Patel & Whitelam 1998;
Franklin et al. 2003a,b; Franklin, Allen & Whitelam
2007).Thus, all five phytochromes are involved in promot-
ing de-etiolation under a continuous R light.
Although mutant analysis suggests that phyB is the main
photoreceptor in R light, surprisingly, expression profile
experiments over 24 h demonstrate that a relatively small
portion of these genes is regulated in a phyB-dependent
manner (Tepperman et al. 2004). These data suggest that
some of the more visible phenotypes in the phyB null, for
example, hypocotyl elongation, are controlled by a distinct
subset of genes, and that the role of other phytochromes is
greater than originally expected. Kinetic studies of hypo-
cotyl growth inhibition have revealed temporal contribu-
tions of phyA and phyB to R-light-triggered de-etiolation
(Parks & Spalding 1999). This analysis has shown that upon
transfer to R light, phyA controls hypocotyl growth inhibi-
tion for the first 3 h. Thereafter, hypocotyl growth is mainly
controlled by phyB (Parks & Spalding 1999). This careful
study provided clear evidence for phyA action that is not
apparent in end-point studies where the phyA null has
no obvious phenotype. This central role for phyA in early
R light perception is consistent with microarray analysis
© 2008 The Authors

showing that 74% of early R-light-induced genes are phyA-
regulated, compared with 10% that are phyB-regulated
(Tepperman et al. 2001).
MAKING SENSE OF THE ENVIRONMENT
The spectral quality of the light environment can vary
greatly between habitats and seasons. Vegetation can
provide direct shade, thus reducing light availability, but
also altering the light spectrum in the immediate vicinity.
Photosynthetic pigments absorb light through the entire
visible electromagnetic spectrum, but less effectively in the
longer wavelength range, producing a light environment
that is FR enriched (Smith 1982). This reduction in the
R/FR ratio (low R/FR) alters the balance between Pr and
Pfr in favour of the biologically inactive Pr form, with a
consequential alteration of phytochrome signalling. Thus,
the balance between Pr and Pfr forms provides an accurate
and dynamic sensor of the presence and density of nearby
vegetation (Holmes & Smith 1975; Smith & Whitelam
1997). In the natural environment, this facility is essential as
the availability of nutrients, and most crucially, of light can
be dramatically reduced by competing plants. Reduced light
levels constrain photosynthetic productivity, limiting
carbon availability, which can impair growth, development,
and ultimately, threaten plant survival. Low R/FR ratios
trigger a wide range of responses that are collectively
referred to as ‘shade-avoidance responses’ (SARs) (Smith
& Whitelam 1997). These responses include an increased
elongation of petiole and stem, increased apical dominance,
altered chlorophyll levels, leaf hyponasty and early flower-
ing. The reallocation of plant resources to elongation
increases the likelihood of reaching unfiltered sunlight,
while acceleration of the life cycle maximizes survival
chances (Ballaré, Scopel & Sánchez 1990). The ability to
perceive and respond to environmental cues of this
nature is observed across many species (Casal, Sachez &
Deregibus 1987; Ballaré et al. 1990; Weijschede et al. 2006;
Kebrom & Brutnell 2007). Conserved through evolution,
this facility provides a vital readout of the changeable
habitat (Mathews 2006).
In Arabidopsis, the phyB mutant displays elongated
leaves and is early flowering, resembling wild-type plants
grown in low R/FR ratio light, implicating phyB as a core
mediator of SAR (Nagatani, Chory & Furuya 1991; Somers
et al. 1991; Reed et al. 1993). However, the retention of
responses to supplementary FR light and to end-of-day
(EOD) FR treatments in the phyB null mutant demon-
strates that other phytochromes also contribute to this
response (Goto, Kumagai & Koornneef 1991; Whitelam &
Smith 1991; Robson, Whitelam & Smith 1993; Halliday,
Koornneef & Whitelam 1994; Devlin et al. 1996). Analysis
of mutants carrying phyD and phyE null alleles in addition
to phyB has revealed apparent redundant roles for these
phytochromes in controlling shade avoidance (Aukerman
et al. 1997; Devlin et al. 1998, 1999). Further analysis has
shown that these are the only positive regulators of shade
avoidance, the phyBphyDphyE triple mutant being unable
© 2008 The Authors
Journal compilation © 2008 Blackwell Publishing Ltd, Plant, Cell and Environment, 31, 667–678
13653040, 2008, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1365-3040.2008.01794.x by NHS Education for Scotland NES, Edinburgh Central Office, Wiley Online Library on [17/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
The phytochrome network 669
to respond to either low R/FR or EOD-FR treatments
(Franklin et al. 2003b). Loss of phyC, even in the absence of
other phytochromes, does not impair R/FR perception, con-
sistent with phyC not regulating the SAR (Franklin et al.
2003a).
Interestingly, studies of phyA and phyAphyB mutants
have shown that phyA antagonizes SARs: in low R/FR ratio
light conditions, phyA mutants have enhanced hypocotyl
elongation, while phyAphyB double mutants display longer
hypocotyls than phyB (Johnson et al. 1994; Smith, Xu &
Quail 1997). These data are consistent with microarray
analysis revealing the antagonistic regulation by phyA of
many shade-responsive genes (Devlin, Yanovsky & Kay
2003). Under deep shade, de-etiolation is severely impaired
in phyA mutants, and many of these mutants die prema-
turely (Yanovsky, Casal & Whitelam 1995), suggesting that
in the natural environment, phyA is required to limit elon-
gation in shaded conditions.
SIGNALLING THROUGH PIFs
It has been shown that phytochromes in their Pfr form are
able to specifically and reversibly bind members of a group
of transcription factors (TFs) designated as phytochrome-
interacting factors (PIFs) (Ni, Tepperman & Quail 1998,
1999; Martinez-Garcia, Huq & Quail 2000; Huq & Quail
2002; Fujimori et al. 2004; Khanna et al. 2004; Oh et al.
2004). PIFs belong to the bHLH (basic helix-loop-helix) TF
superfamily of which 147 members have been identified.
PIFs cluster to subfamily number 15, which consists of 15
members (Toledo-Ortiz, Huq & Quail 2003). Sequence
alignments of these subfamily members have shown that 12
of the 15 members contain a conserved motif in their
N-terminal region, which is absent from the other members
of the superfamily. This motif, designated as active phyto-
chrome binding (APB) motif, is necessary and sufficient for
Pfr-specific binding of phyB to a subset of these bHLH TFs
(Khanna et al. 2004). The interaction of phyB with five of
these bHLH TFs (PIF1/PIL5, PIF3, PIF4, PIF5/PIL6, PIF6/
PIL2) has been shown in vitro (Ni et al. 1998, 1999; Huq &
Quail 2002; Khanna et al. 2004; Oh et al. 2004; Monte et al.
2007). An active phyA binding (APA) motif has also been
described for PIF3 (Al-Sady et al. 2006), and is necessary
for its binding to phyA. Such a motif has not yet been
reported in other bHLH members of subfamily 15.
Individual PIFs have different affinities for phyA and
phyB. For example, PIF3 preferentially binds phyB,
although a weak binding to phyA has been shown (Zhu
et al. 2000). PIF1/PIL5 also binds both phyA and phyB, but
while binding is weaker to phyA versus phyB, it has greater
than 10 times more affinity for phyA than PIF3 (Huq et al.
2004). Consistent with their binding affinities, PIF3 has been
shown to have a major role in phyB signalling and a minor
role in phyA signalling (Ni et al. 1998), while PIF1/PIL5
plays substantial roles in both phyA and phyB signalling
(Huq et al. 2004; Oh et al. 2004). Despite having roles in
phytochrome signalling, three members of this bHLH
TF subfamily, spatula (SPT), long hypocotyl in far-red1

670 E.-M. Josse et al.
(HFR1) and PIF3-like1 (PIL1), have been shown not to
directly interact with phytochrome in vitro (Fairchild, Schu-
maker & Quail 2000; Khanna et al. 2004). SPT and HFR1
lack the conserved APB motif, but the reason for the lack of
interaction between phytochrome and PIL1, which pos-
sesses an APB region, is as of yet unclear (Khanna et al.
2004), although it is of course possible that in vivo interac-
tions do occur.
PIFs/PILs have been shown to bind to G-box motifs,
which are present within the promoters of numerous light-
regulated genes. Furthermore, phyB was shown to bind
DNA-bound PIF3 specifically and reversibly upon transi-
tion to the active Pfr conformation (Martinez-Garcia et al.
2000). It is proposed that the phytochrome–PIF interaction
provides a direct means to modify transcription following
phytochrome translocation into the nucleus (Martinez-
Garcia et al. 2000; Tepperman et al. 2001). Additionally,
bHLH proteins in Arabidopsis and other organisms are
known to dimerize (Klemm, Schreiber & Crabtree 1998;
Fairchild et al. 2000; Firulli et al. 2000; Massari & Murre
2000; Khanna et al. 2004), providing a possible mechanism
for these TFs to moderate each other’s activity.
PIFs/PILs can act in concert with other TFs to regulate
development. PIF3 has been shown to act with elongated
hypocotyl 5 (HY5), a basic leucine zipper (bZIP) TF in the
regulation of gene transcription (Ang et al. 1998; Hardtke
et al. 2000; Osterlund et al. 2000; Shin, Park & Choi 2007).
PIF3 and HY5 can control the transcription in an antago-
nistic manner (e.g. during hypocotyl elongation), or in a
collaborative manner, to drive development in the same
direction (e.g. during FR-induced anthocyanin biosynthe-
sis) (Somers et al. 1991; Kim et al. 2003; Shin et al. 2007).
This collaborative action is achieved when PIF3 and HY5
bind separate sequence elements in the promoters of the
anthocyanin biosynthesis genes they control (Shin et al.
2007).
Many PIFs/PILs are described as negative regulators of
phytochrome signalling during long-term irradiation. For
instance, under a constant R light, the monogenic pif3, pif4
and pif5/pil6 mutants display short hypocotyl phenotypes
(Halliday et al. 1996; Huq & Quail 2002; Kim et al. 2003;
Bauer et al. 2004; Fujimori et al. 2004; Monte et al. 2004),
while the overexpression of PIF5/PIL6 and PIF1/PIL5
leads to excess elongation (Fujimori et al. 2004; Oh et al.
2004). Hence, for these physiological responses, PIF1/
PIL5, PIF3, PIF4 and PIF5/PIL6 are negative regulators of
phyB signalling. Likewise, under FR light, pif1/pil5 has a
short hypocotyl phenotype, while PIF1/PIL5 overexpres-
sion causes hypocotyl elongation (Oh et al. 2004), suggest-
ing that PIF1/PIL5 is a negative regulator of phyA
signalling. PIF3 appears to have an overlapping role with
PIF1/PIL5, as the pif3 mutant has expanded cotyledons
and PIF3 overexpressors have smaller cotyledons when
grown under FR light (Kim et al. 2003). In contrast, HFR1
and PIL1 appear to act as positive regulators of phyA
signalling, as mutant alleles have a long hypocotyl pheno-
types under FR light (Fairchild et al. 2000; Fankhauser
& Chory 2000; Soh et al. 2000; Khanna et al. 2006). The
Journal compilation © 2008 Blackwell Publishing Ltd, Plant, Cell and Environment, 31, 667–678
13653040, 2008, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1365-3040.2008.01794.x by NHS Education for Scotland NES, Edinburgh Central Office, Wiley Online Library on [17/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
biological rationale for these different modes of action is
discussed further below.
A BALANCE OF POWER
The stability of PIFs/PILs, and therefore their activity, is
subject to a close control by light. Some PIFs/PILs are more
stable in darkness, while others are stabilized by light. It has
been shown that nuclear-localized PIF3, PIF1/PIL5 or PIF5/
PIL6 is rapidly degraded by the proteasome when etiolated
seedlings are exposed to light (Bauer et al. 2004; Monte
et al. 2004; Park et al. 2004; Shen et al. 2005; Shen et al.
2007). Phytochromes play a major role in PIFs/PILs
stability. Indeed, phytochrome binding to PIF3 and to PIF5/
PIL6 is required for intranuclear phosphorylation. This
is thought to ‘label’ the protein for degradation via the
proteasome (Al-Sady et al. 2006; Shen et al. 2007). Analysis
of 35S:GUS:PIF3 and 35S:LUC:PIF1 transgenic lines sug-
gests that upon transfer to darkness, PIF3 and PIF1/PIL5
protein levels increase. This increase is greatly accelerated
when an FR light pulse is provided before transfer to
darkness, suggesting that phytochrome in its Pfr form is
required to maintain low levels of PIF3 and PIF1/PIL5
(Monte et al. 2004; Shen et al. 2005). As PIF3 and PIF1/PIL5
are under such close regulation by phyB-Pfr, they appear to
be good candidates for promoters of growth elongation
under low R/FR light. Studies using seedlings expressing
PIF3promoter-PIF3:YFP have suggested that PIF3 protein
abundance is also subject to diurnal control. When grown in
long-day cycles, PIF3 accumulates around the end of the
day (Viczian et al. 2005).Thus, PIF3 protein function may be
determined by both photoperiod and the relative propor-
tions of R and FR of the ambient light.
SPT and HFR1, in contrast to PIF3, PIF1/PIL5 and PIF5/
PIL6, are light stable (Duek et al. 2004; Penfield et al. 2005;
Yang et al. 2005b). While the mode of SPT protein regula-
tion has not yet been elucidated, we do have some insights
into HFR1 control. HFR1 is targeted for degradation by the
nuclear proteasome in the dark through a constitutive
photomorphogenic 1–suppressor of phyA 1 (COP1-SPA1)-
dependent process (Duek et al. 2004; Yang et al. 2005b).
COP1 and SPA1 physically interact to form the E3 ubiq-
uitin ligase complex, which mediates HFR1 degradation
(Hoecker & Quail 2001; Saijo et al. 2003; Yang et al. 2005a).
Light tempers this process by disrupting the COP1-SPA1
interaction and by triggering COP1 migration from the
nucleus (von Arnim & Deng 1994; von Arnim et al. 1997;
Stacey & von Arnim 1999; Hoecker & Quail 2001; Saijo
et al. 2003). The phenotypic similarity of the pil1 and hfr1
mutants (Salter, Franklin & Whitelam 2003; Sessa et al.
2005; Roig-Villanova et al. 2006) suggests that these bHLH
TFs may perform similar roles. HFR1 and PIL1 have been
shown to antagonize elongation growth under low R/FR
ratio light, conditions where phyA protein levels increase.
This provides a means for phyA to moderate elongation
growth under shade conditions. Moreover, transcriptomics
data have suggested a moderating role for phyA in the SAR
(Devlin et al. 2003). Thus, it appears that HFR1 and PIL1
© 2008 The Authors

may act as a counterbalance to PIF3 and PIF1/PIL5, which
promote elongation in low R/FR light.
PIFs MOVING THE HANDS OF TIME
When kept in a constant light (LL), hypocotyl elongation
growth in arrhythmic clock mutants is continuous, but wild-
type seedlings grow rhythmically, indicating that hypocotyl
growth is controlled by the circadian oscillator (Dowson-
Day & Millar 1999; Nozue et al. 2007). However, although
the clock is functional in darkness (Millar et al. 1995), dark-
grown seedlings grow rapidly and without a discernable
rhythm (Nozue et al. 2007). These observations suggest that
circadian growth control of hypocotyl elongation is light-
dependent. A series of experiments by Nozue et al. (2007)
reveal how this clock–light partnership operates. In contrast
to continuous light where hypocotyl growth peaks at sub-
jective dusk, under short-days conditions, the peak of hypo-
cotyl growth occurs at dawn (Dowson-Day & Millar 1999;
Nozue et al. 2007). Thus, photoperiodic conditions have a
dramatic effect on the phasing of this response. Genetic
studies have demonstrated that PIF4 and PIF5/PIL6 par-
ticipate in this process (Nozue et al. 2007). During the day,
light inhibits growth, at least partly, by reducing PIF4 and
PIF5/PIL6 protein levels. The clock appears to gate the
growth response by regulating the timing of PIF4 and PIF5/
PIL6 transcript levels. PIF4 and PIF5/PIL6 mRNA levels
start to rise from midway through the night and reach a
peak at dawn. In the absence of light, these protein products
are relatively stable, and therefore accumulate, driving
elongation during that latter portion of the night. At dawn,
light triggers the degradation of PIF4 and PIF5/PIL6 pro-
teins with a consequential slowing of elongation. These
experiments nicely illustrate the interplay between light
and the oscillator in the regulation of rhythmic hypocotyl
growth.
Although low R/FR ratio light triggers hypocotyl elonga-
tion, this response is circadian gated. Central to this SAR is
PIL1, a putative timing of CAB1 (TOC1) interacting PIF3-
like bHLH TF (Yamashino et al. 2003). PIL1 mRNA levels
are consistently low under white light (i.e. high R/FR), but
increase rapidly following exposure to low R/FR ratio light
(Salter et al. 2003). However, in wild-type seedlings grown
in LL, although pulses of low R/FR ratio light are able to
induce a rapid increase in PIL1 transcript levels, this
response appears to be circadian gated, with a maximal
response achieved at the start of the subjective day. Addi-
tionally, analysis of PIL1 mRNA levels in phytochrome null
mutants revealed that phyB, phyD and phyE are required
to repress PIL1 mRNA levels (Salter et al. 2003). Interest-
ingly, in wild-type seedlings, PIL1 is required to ensure
the correct phasing of hypocotyl elongation, as pil1 null
mutants show a 6 h phase-shift of hypocotyl elongation in
response to low R/FR light. As other circadian phenotypes
in pil1 are apparently unaltered, PIL1 may be involved in
rephasing an oscillator that regulates rhythmic growth in
young seedlings. This process may specifically require
TOC1, as toc1 mutant hypocotyls fail to respond to low
© 2008 The Authors
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13653040, 2008, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1365-3040.2008.01794.x by NHS Education for Scotland NES, Edinburgh Central Office, Wiley Online Library on [17/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
The phytochrome network 671
R/FR ratio pulses. This is a plausible proposition as PIL1
and TOC1 have been shown to interact in vitro (Yamashino
et al. 2003). However, detailed analysis is required to estab-
lish whether this interaction occurs in vivo, and if it does,
whether this interaction is relevant for this response. Other
studies have shown that PIF3 and PIF1/PIL5 protein levels,
which are subject to diurnal regulation, also accumulate
more rapidly following an EOD FR pulse (Monte et al.
2004; Shen et al. 2005), but it is not yet known whether the
activity of these proteins is gated by the circadian oscillator.
SIGNAL TRANSDUCTION
The molecular signalling events that are initiated by phyto-
chrome action have amazing complexity. Many light
responses are controlled by manipulating the master con-
trollers of physiology, growth and developmental responses:
the hormones. A wide range of studies have identified links
between light and several hormones including auxin, gib-
berellic acid (GA), ethylene, cytokinin and brassinosteroids
(Halliday & Fankhauser 2003). Perhaps the strongest con-
nections identified, thus far, are between auxin, GA and
phytochrome. Recent studies by our lab and others have
focused on the integration of light and GA pathways, high-
lighting the central role of PIF/PILs TFs in this light–
hormone interaction.
Seed fate is strongly affected by the balance of two hor-
mones with antagonistic effects: GA promotes germination,
and abscisic acid (ABA) maintains seed dormancy. Light
and temperature modulate both the synthesis and the per-
ception of these hormones in the seed (Penfield et al. 2005;
Oh et al. 2007). PIF1/PIL5 and SPT integrate light and
temperature signals to modulate germination, primarily
through the transcriptional regulation of GA and ABA
metabolism, catabolism and response genes. This provides a
means to modulate active GA and ABA levels in the seed,
and modulate responsivity to these powerful controllers of
germination (Oh et al. 2007). It was shown that in seedlings,
upon light activation and translocation to the nucleus,
phyB-Pfr binds PIF1/PIL5, targeting it for degradation
(Shen et al. 2005). In seeds, the depletion of PIF1/PIL5 (1)
elevates transcript levels of the GA biosynthetic genes
GA3ox1 and GA3ox2, (2) reduces levels of expression of
the GA catabolic gene GA2ox2, and (3) reduces transcript
levels of the ABA biosynthetic genes ABA1, NCED6 and
NCED9. These effects may, however, be indirect as PIF1/
PIL5 does not appear to bind directly to the promoter
regions of these genes to regulate transcription (Oh et al.
2007). The ABA catabolic gene CYP707A2 is also activated
by R light, through both PIF1/PIL5-dependent and PIF1/
PIL5-independent mechanisms (Oh et al. 2004, 2006, 2007;
Penfield et al. 2005; Seo et al. 2006). This leads to an accu-
mulation of GA and a depletion of ABA, which in turn
promotes germination.
SPT, unlike PIF1/PIL5, is light stable, and is required
to maintain dormancy in freshly harvested seed. This is
achieved by an SPT-mediated repression of GA3ox1
and GA3ox2 transcript abundance. A cold treatment

672 E.-M. Josse et al.
(stratification) represses SPT activity inducing an increase
in GA levels and relieving dormancy. Thus, SPT appears to
integrate light and temperature signals to control seed dor-
mancy (Penfield et al. 2005).
PIF1/PIL5 also regulates GA responsiveness by target-
ing DELLA growth regulators. DELLA genes comprise
a small clade [repressor of ga1-3 (RGA), GA-insensitive
(GAI), RGA-LIKE1 (RGL1), RGL2 and RGL3] within the
GRAS family [for review, Bolle (2004)]. DELLA proteins
are potent suppressors of growth, and GA exerts its promo-
tory effects on growth by triggering their degradation
through the E3 ubiquitin ligase SCFSLY1 (Itoh, Matsuoka &
Steber 2003). Interestingly, recent studies with green fluores-
cent protein (GFP)-RGA demonstrate that RGA stability is
also subject to ABA control (Penfield et al. 2006). In this
case, ABA prevents RGA degradation, suggesting that
DELLA stability may result from a balance of GA and ABA
levels (Achard et al. 2006). PIF1/PIL5 maintains dormancy
in the dark, not just by keeping the ABA:GA ratio high, but
by activating the transcription of the DELLA growth regu-
lators RGA and GAI. In contrast to the GA biosynthetic
genes, RGA and GAI appear to be direct targets, as PIF1/
PIL5 can bind both promoters (Oh et al. 2007).
An interesting observation that emerged from germina-
tion studies was the correlation between final cotyledon
size and dormancy in the della mutants. This correlation was
also broadly maintained when a larger range of mutants
with altered dormancy was examined. Further analysis
showed that cotyledon expansion is initiated prior to radicle
emergence, and as for germination, this process is anta-
gonistically regulated by GA and ABA. Thus, a light-,
temperature- and hormone-controlled DELLA-mediated
induction of cotyledon expansion prior to radicle emer-
gence could be a suitable strategy to overcome seed dor-
mancy by physically breaking the seed coat of Arabidopsis
seeds, leading to germination (Penfield et al. 2006).
When compared to the seed, the relationship between GA
and light is different in elongating tissues. Here, GA and light
act antagonistically, with light inhibiting and GA promoting
both hypocotyl and petiole elongation.When grown under R
light, RGA accumulates in hypocotyl cell nuclei in a phyB-
dependent manner (Achard et al. 2007).This suggests that, in
the hypocotyl, phyB and GA have opposing roles in regulat-
ing DELLA stability. The role of DELLAs in this process is
supported by the analysis of the della quadruple mutant
rga/gai/rgl1/rgl2 that has an elongated hypocotyl when
grown under R light (Achard et al. 2006). It is not yet known
how DELLA proteins mediate their control on growth, as
their proposed molecular function as TFs has not yet been
demonstrated (Jiang & Fu 2007; Ueguchi-Tanaka et al.
2007).A recent study using chromatin immunoprecipitation
on the promoters of a handful of DELLA target genes has
shown very weak interactions between RGA and those
promoters in vivo. This suggests the existence of an indirect
binding mechanism, possibly involving the association of
RGA with other DNA-binding proteins to control the
expression of its targets (Zentella et al. 2007). It is therefore
possible that DELLA control on elongation growth could be
Journal compilation © 2008 Blackwell Publishing Ltd, Plant, Cell and Environment, 31, 667–678
13653040, 2008, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1365-3040.2008.01794.x by NHS Education for Scotland NES, Edinburgh Central Office, Wiley Online Library on [17/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
executed by a secondary mechanism.As the PIF/PIL bHLH
TFs are known to regulate hypocotyl elongation, the
modification of PIF/PIL activity could provide one possible
mechanism via which DELLAs could impose control on
hypocotyl growth.
Consistent with a role in phytochrome signalling,
DELLA proteins and GA signalling have been implicated
in elongation growth during the SAR. Plants impaired in
GA biosynthesis, that is, the ga1-3 mutant or wild-type
plants treated with paclobutrazol, a GA biosynthesis inhibi-
tor, have a short hypocotyl that is less responsive to low
R/FR ratio. This suggests that the SAR is GA-dependent
(Achard et al. 2007; Djakovic-Petrovic et al. 2007). Interest-
ingly, the role of GA in the shade avoidance may be tissue-
specific as GA application phenocopies the response to low
R/FR ratio light in hypocotyls, but not petioles (Djakovic-
Petrovic et al. 2007).
INTER-ORGAN COMMUNICATION
To fully understand the intricacies of light signalling,
temporal and spatial elements need to be taken into con-
sideration. For example, light triggers opposing growth
responses in the hypocotyl and cotyledon, yet these spa-
tially separated pathways are completely synchronized. To
obtain a clear view of when and where signalling pathways
are initiated, organ- or tissue-specific analyses are required.
Recent transcriptomics studies in cotyledon and hypocotyl
provide a preliminary step towards understanding the dif-
ferences in the signalling pathways initiated in these two
tissues (Ma et al. 2005). Firstly, these data demonstrate that
the cotyledon expression profile of light-grown seedlings is
very close to that of both rosette and cauline leaves, but
shows little overlap with the hypocotyl gene expression
profile. Comparative analysis of light-responsive genes in
hypocotyls and cotyledons from this data set (Fig. 1) pro-
vides the following insights: (1) almost no light-responsive
genes are regulated antagonistically in hypocotyl versus
cotyledon tissue (Fig. 1a). This appears to rule out the pos-
sibility that target genes are simply subject to opposing
regulation in the two organs. (2) Light activates distinct
subsets of target genes in hypocotyl and cotyledon tissues
(Fig. 1b). These observations suggest that different path-
ways are activated in these two tissues, which is perhaps not
surprising as they perform different functions. We do not
yet have temporal resolution on these data sets, which will
provide the necessary detail to link components in the
network with confidence.
Early studies using microbeam irradiation of distinct
regions of the seedling provide evidence of phytochrome-
induced cell autonomous and transmissible signals (Nick
et al. 1993; Bischoff et al. 1997). We know now that the
markers used in these studies, anthocyanin and CAB2-
LUC, are PIF-regulated outputs of phytochrome signalling.
Nick et al. (1993) first showed that light triggers the accu-
mulation of anthocyanin at the site of light application and
at spatially separated sites. Furthermore, distinct patterns of
anthocyanin accumulation could be induced by applying
© 2008 The Authors
 13653040, 2008, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1365-3040.2008.01794.x by NHS Education for Scotland NES, Edinburgh Central Office, Wiley Online Library on [17/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
The phytochrome network 673

(a) UP DOWN DOWN UP control on root growth by long-distance signalling. In Ara-

489 792 503 853
4 12
cotyledon hypocotyl cotyledon hypocotyl
(b) UP DOWN
383 755 425 706
GAI 110 DFL1 HFR1 90
PKS2 PIL6 SPT
GH3-3 FLC
GA3ox2
SPA1
PHOT1
cotyledon hypocotyl
cotyledon hypocotyl
Figure 1. Diagrams comparing the profile of expression of
light-regulated genes in hypocotyl versus cotyledons as
determined from the microarray analysis performed by Ma et al.
(2005) in the Supplemental Tables 6 and 7. (a) Diagram
illustrating the number of light-regulated genes showing opposite
regulation in hypocotyl versus cotyledon. (b) Diagram illustrating
the overlapping and uniquely expressed light-regulated gene
numbers between hypocotyl and cotyledon. Genes having a
significant role in light signalling are mentioned within the area
representing the organ where they are specifically light-regulated.
the light beam to different areas of the cotyledon. Experi-
ments using a CAB2:LUC reporter construct led to similar
conclusions, that is, that both local cooperation and long-
range signalling influence the pattern of phytochrome-
regulated gene expression (Bischoff et al. 1997). Recent
work supports these earlier findings, demonstrating that
phyB can generate transmissible signals. For instance, the
expression of phyB solely in mesophyll cells in an otherwise
phyB null background can fully restore all aspects of the
wild-type phenotype (hypocotyl elongation, adult rosette
phenotype and flowering time). This does not preclude
phyB signalling in other tissues, but does support the notion
that a long-distance signal initiated in the leaf can trigger
responses in other tissues (Endo et al. 2005).
Reporter gene expression studies have demonstrated
that in Arabidopsis, phytochromes are expressed through-
out the seedling including the root (Toth et al. 2001;
Salisbury et al. 2007). Further evidence for phytochrome-
regulated long-distance signalling has come from studies of
roots. Phytochrome has a strong controlling influence on
roots, as mutants lacking phyA and phyB have reduced
responses to gravity, reduced primary root elongation and
fewer lateral roots (Kiss et al. 2003; Correll & Kiss 2005;
Salisbury et al. 2007). Studies have shown that root-located
phytochrome exhibits the same light-regulated cellular
dynamics as shoot phytochrome, and can regulate root
elongation (Usami et al. 2004; Correll & Kiss 2005;
Salisbury et al. 2007). However, in the natural environment,
where roots are mainly covered, phytochrome exerts
© 2008 The Authors
Journal compilation © 2008 Blackwell Publishing Ltd, Plant, Cell and Environment, 31, 667–678
bidopsis, this control appears to be achieved, at least in part
by regulating auxin transport (Salisbury et al. 2007).
Although the nature of many long-distance signals is
unclear, hormones and other small molecules are likely
candidates to fulfil this role. Auxin is transported from
the shoot apex and young leaves to the hypocotyl, and is
involved in light regulation of hypocotyl elongation (Jensen,
Hangarter & Estelle 1998; Blakeslee, Peer & Murphy 2005).
Photoreceptor-controlled inhibition of hypocotyl elonga-
tion and phytochrome control of lateral root development
are at least partially mediated by regulating auxin transport
HAT2 (Jensen et al. 1998; Salisbury et al. 2007). Furthermore, when
GA1
ELF3 FR irradiation is directed specifically at the cotyledon or the
CRY2 hypocotyl, auxin-responsive reporter gene expression in the
hypocotyl is only activated in response to cotyledon expo-
sure (Tanaka et al. 2002). These observations support the
role of auxin as part of a phytochrome-controlled long-
distance signal that coordinates plant development.
Other molecules, including mRNAs and proteins, have
been reported to travel long distances through the phloem
and to be essential for plant growth [for review, Wu, Weigel
& Wigge (2002)]. While we do not know whether molecules
of this nature operate during seedling development, we do
have some insights into a long-distance signal that regulates
flowering time. After much debate about the identity of the
florigen (Kobayashi & Weigel 2007), there is now good
evidence that FT (flowering locus T) protein acts as a long-
distance signal that triggers flowering (Corbesier et al.
2007). FT transcript levels are very sensitive to phyB status:
a reduction in phyB-Pfr enhances FT levels, and flowering is
accelerated as a consequence (Halliday et al. 2003; Endo
et al. 2005). Studies to date have shown that FT is most
abundantly produced in leaf tissue and is expressed highly
in the companion cells of the phloem (Wigge et al. 2005;
Mathieu et al. 2007). Following FT protein production, it is
uploaded into the phloem and travels towards the shoot
apical meristem. Flowering is then triggered by following
FT interaction with FD, which promotes expression of floral
meristem identity genes such as APETALA1 (Lifschitz
et al. 2006; Corbesier et al. 2007; Jaeger & Wigge 2007;
Tamaki et al. 2007). Work from Endo et al. (2005) demon-
strated that when expressed solely in vascular bundles,
phyB was not able to repress FT mRNA levels and to delay
flowering. In contrast, when expressed in mesophyll cells,
phyB was effective both in repressing FT expression in
companion cells and in delaying flowering time (Endo et al.
2005). The nature of the message between those two tissues
within the leaf is still unknown, yet it seems appropriate
that a plant would use its mesophyll cells, which are special-
ized to absorb light, to detect light-related information, and
use cells neighbouring the vascular tubes to relay this infor-
mation towards more distant organs. While we only have
sections of the picture, these studies illustrate well the
ability of organs to communicate in response to light per-
ception: a leaf-sensed stimulus can be propagated over long
distances to trigger specific physiological responses at the
apical meristem.

674 E.-M. Josse et al.
CONCLUSION
A desire to understand the mechanism of phytochrome
action has placed the spotlight on early signalling events.
This has paid dividends as we can now visualize the initial
steps following photoreceptor activation. Much of the
information gathered thus far represents, or has been
interpreted as, cell autonomous signalling. What we know
almost nothing about at this stage is the nature of
the light-driven signals that coordinate growth and
developmental events. Perhaps, mapping the long-distance
communication channels and analysing signalling in a
time- and tissue-specific manner will provide better reso-
lution on the complex network of phytochrome-signalling
components and greater insight into how light controls
plant development.
ACKNOWLEDGMENT
We would like to thank Dr. Paul Devlin for his helpful
comments during the preparation of this manuscript.
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Received 19 October 2007; received in revised form 23 January 2008;
accepted for publication 24 January 2008
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