Download Intracellular redistribution of phytochromes

COMMENTARY
475
Intracellular trafficking of photoreceptors during lightinduced signal transduction in plants
Ferenc Nagy1,2, Stefan Kircher3 and Eberhard Schäfer3,*
1Plant Biology Institute, Biological Research Centre, H-6701 Szeged, PO Box 521, Hungary
2Agricultural Biotechnology Centre, H-2101 Godollo, PO Box 411, Hungary
3Institut für Biologie II/Botanik, Universität Freiburg, Schänzlestrasse 1, D-79104 Freiburg, Germany
*Author for correspondence
Journal of Cell Science 114, 475-480 © The Company of Biologists Ltd
Summary
Plants monitor changes in the ambient light environment
by highly specialised photoreceptors, which include the
red/far-red photoreversible phytochromes, the blue-lightabsorbing cryptochromes and phototropin and the so-farunidentified UVB photoreceptor(s). Light easily penetrates
plant organs/tissues and reaches even the subcellular
compartments of various cell types. Therefore, it is not
surprising that the determination of the intracellular
localisation of photoreceptors has been, for many years,
a major, and often controversial, subject of plant
photobiology and cell biology research. Phototropin, one of
the blue-light photoreceptors of higher plants, controls
phototropism by monitoring the direction of light, and
it is localised in or at the plasmalemma. In contrast,
the subcellular localisation of phytochromes changes
Introduction
Plants are sessile organisms; therefore optimal adaptation to
changes in the natural environment is an essential strategy.
Light is a dominant but broadly variable environmental factor.
It is not only an energy source but also an essential signal for
adaptation and regulation of plant growth and development.
The most dramatic developmental switch occurs at the point of
transition from skotomorphogenesis (development in darkness)
to photomorphogenesis (development in light). Light-mediated
signal transduction starts with the absorption of light by
specialised photoreceptors. Several classes of photoreceptors
that monitor the quality, quantity and the temporal and spacial
pattern of light have evolved: the UVB photoreceptors (as
yet unidentified), red/far-red photoreversible phytochromes
(Clack et al., 1994), and the blue-light-absorbing proteins
cryptochromes (Cashmore et al., 1999) and phototropin
(Christie et al., 1998; Christie et al., 1999).
Being an electromagnetic wave, light can easily penetrate
plant tissues. Red and far-red light can even pass through
compact organs, such as stems or leaves, and activate
phytochromes deep within cells. Physiological experiments,
in vivo spectroscopy, immunocytochemical studies and
ubiquitous activities of phytochrome promoters in transgenic
plants indicate that phytochromes are present in all tissue types
examined. Therefore, each cell is likely to contain at least one
type of phytochrome at any stage of development.
Until 1999, however, the intracellular localisation of most
of these photoreceptors, including phytochromes, remained
dynamically and exhibits a very complex pattern. These
photoreceptors are localised in the cytosol in darkgrown tissues. Irradiation, however, induces import of
phytochromes into the nucleus. The import occurs in a
light-quality- and light-quantity-dependent fashion and, as
such, seems to be unique to higher plants. Light-induced
accumulation of phytochromes in the nuclei correlates well
with various physiological responses mediated by these
photoreceptors. These observations indicate that lightdependent intracellular redistribution of phytochrome
photoreceptors is one of the major regulatory steps in
photomorphogenesis.
Key words: Phytochrome, Nuclear import, Signalling
largely obscure. In the case of phytochromes, a controversial
debate about their exact intracellular localisation erupted nearly
20 years ago and has lasted until very recently. Phytochromes
and cryptochromes were generally thought to be cytosolic, and
this view became even more prevalent after the first sequence
information became available. Phototropin was thought to be an
exception and localised in/at the plasmalemma.
Phototropin
Darwin’s pioneering work revealed that phototropism of plants
is mediated by a blue-light-absorbing pigment; however, the
photoreceptor involved, phototropin, was identified only a few
years ago. Physiological and biochemical data showed a strong
correlation between phototropism and a blue-light-mediated
phosphorylation of a 120 kDA protein associated with plasma
membranes (Short and Briggs, 1994). Using a genetic
approach, it has been shown (Huala et al., 1997) that the
nonphototropic hypocotyl locus (NPH1) encodes a serine/
threonine kinase that contains two N-terminal domains
characteristic of proteins mediating light-, oxygen- and
voltage-dependent responses (LOV domains). Expression of
NPH1 in baculovirus allowed the authors to demonstrate
binding of flavin mononucleotide (FMN) to the LOV
domains and blue-light-mediated autophosphorylation of the
photoreceptor (Christie et al., 1998; Christie et al., 1999).
However, it remains to be seen whether phototropin is a
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JOURNAL OF CELL SCIENCE 114 (3)
A) PHYA
light
synthesis
Pr
P fr
signaling
VLFR
HIR
gene
regulation
photomorphogenesis
gene
regulation
photomorphogenesis
destruction
B) PHYB
light
synthesis
Pr
P fr
signaling
LFR
cR
dark reversion
Fig. 1. Modes of action of (A) PHYA and (B) PHYB. Red-light-absorbing (Pr) and far-red-light-absorbing forms (Pfr) of PHYA and PHYB are
shown. Signal transduction competes with proteolytic degradation of Pfr (PHYA) or dark reversion of Pfr back to Pr (PHYB). Four different
modes of action leading to regulation of gene expression can be distinguished: (1) the very-low-fluence response (VLFR), a response that is
saturated at about 1% of Pfr and involves PHYA; (2) the high irradiation response (HIR), a response to continuous irradiation with maximal
responsiveness in far-red (~720 nm) light that also involves PHYA; (3) the low fluence response (LFR), a response to red light pulses that can
be reverted by far-red light and involves PHYB; and (4) the continuous red light response (cR), a response that can not be induced by red light
pulses (not discussed in this review) and involves PHYB.
membrane-associated protein, as was inferred by the early
biochemical studies.
Jarillo et al. recently identified a new NPH1-like protein,
NPL1 (Jarillo et al., 1998), that shows significant structural
similarity to NPH1. We speculate that NPL1 and NPH1
together are probably the most important photoreceptors
controlling phototropism in higher plants.
Cryptochromes
Ahmad and Cashmore (Ahmad and Cashmore, 1993) cloned
the HY4 gene, identifying the first member of the long-sought
blue-light-absorbing photoreceptor family. HY4 encodes the
cryptochrome 1 (CRY1) photoreceptor. CRY1 displays striking
similarity to photolyases; however, it has a unique C-terminal
extension and lacks photolyase activity. FADH is its
catalytically active chromophore; the second chromophore
could be either a pterin or a deazoflavin (Malhotra et al.,
1995). The second member of this subclass of blue-light
photoreceptor, CRY2, has also been identified and contains a
different C-terminal extension (Lin et al., 1998).
Results of biochemical studies employing CRY1overexpressor lines were interpreted as indicating that this
photoreceptor is cytosolic (Lin et al., 1996a; Lin et al., 1996b).
In contrast, experiments on transiently transformed plant
cells expressing the CRY1-GFP fusion protein indicated that
CRY1 is localised in the nucleus in the dark (Cashmore et al.,
1999). Moreover, analysis of the cellular distribution of the
CRY2-GUS or CRY2-GFP fusion proteins in transgenic plants
showed that the CRY2 photoreceptor is constitutively localised
in the nucleus (Kleiner et al., 1999; Guo et al., 1999). A more
complex picture is emerging in lower plants, especially in fern
gametophytes. Microbeam irradiation indicates that fern
homologues of higher-plant CRY photoreceptors are present in
the cytosol but also associated with the nucleus (Wada and
Sugai, 1994). Recent studies showed that at least two members
of the CRY family in Adiantum capillus-veneris are indeed
localised in the nucleus and that the nucleo/cytoplasmic
distribution of these receptors is not influenced by light
(Imaizumi et al., 2000).
Phytochromes
In Arabidopsis, phytochromes are encoded by five genes
(PHYA-PHYE) (Clack et al., 1994). PHYA (and probably
all phytochrome types) binds an open chain tetrapyrol
(phytochromobilin), which is covalently linked by a thioetherlinkage to the apoprotein, as a functional chromophore
(Lagarias et al., 1980; Kunkel et al., 1995; Kunkel et al., 1996).
In general, the photosensory function of phytochromes is based
on their capacity to perform reversible interconversion between
the red-light-absorbing Pr form and the far-red-light-absorbing
Pfr form following sequential absorption of red and far-red
light. However, the different phytochromes are not only
encoded by different genes but also have different modes of
action (Fig. 1).
PHYA is the most specialised phytochrome. It is responsible
for the very low fluence rate response (VLFR) and the high
Intracellular redistribution of phytochromes
irradiance response (HIR) (Furuya and Schäfer, 1996). The
extraordinary responsiveness of PHYA allows it to control
germination of seeds buried in the soil and to induce
germination when seeds are exposed to star light (Hartmann et
al., 1998). The other phytochromes control, to different extents,
the classical red/far-red reversible induction, the so-called lowfluence-rate responses (LFRs) and responses to continuous redlight (Furuya and Schäfer, 1996).
All phytochromes are synthesised in the biologically
inactive, red-light-absorbing Pr forms. The half-life of the
physiologically active form of PHYA is extremely short, and
proteolytic degradation of the Pfr form is believed to be
responsible for termination of signalling. In the case of the
light-stable phytochromes, especially PHYB, termination of
signalling is not yet understood. Regulation of the dark
reversion of the Pfr to the Pr form is thought to be the most
likely mechanism, since proteolytic degradation of the Pfr form
of PHYB clearly cannot play a major role (Fig. 1).
Computational analysis of phytochrome sequences and
structures from a variety of species, including ferns, mosses
and algae, indicates that they are cytosolic: no motif, domain
or even secondary structure that could facilitate insertion into
or association with any type of membrane has been identified.
This contrasts with in vivo observations of lower plants, in
which microbeam irradiation has revealed a very localised
response and an action dichroism for phytochrome-mediated
growth responses and chloroplast re-orientation (Kraml, 1994).
These observations suggest that phytochromes associate, at
least in lower plants, with the plasma membrane and that this
probably involves as-yet-unknown protein-protein interactions.
In higher plants, early immunocytochemical analysis of
the subcellular distribution of PHYA demonstrated only
cytosolic localisation of the photoreceptor. Therefore,
until recently, in the absence of any other indication,
phytochromes of higher plants were thought to be localised
in the cytosol and/or associated with cell membranes.
Intracellular localization of PHYB in light and
darkness
PHYB is the most ancient type of phytochrome present in
higher plants. Given the observations outlined above, it
was therefore fairly surprising when, in 1996, Sakamoto
and Nagatani reported the enrichment of PHYB in nuclear
fractions isolated from light-grown trabidopsis seedlings
(Sakamoto and Nagatani, 1996). They also showed that a
fusion protein consisting of the C-terminal part of the A.
thaliana PHYB fused to GUS is constitutively localised to
nuclei in transgenic plants.
Despite the potential importance of these data, they were
largely ignored. However, recent studies by Nagatani
and co-workers (Yamaguchi et al., 1999) and ourselves
(Kircher et al., 1999), which showed that chimeric proteins
consisting of full-length PHYB fused to GFP can
complement PHYB mutations, substantiated the earlier
findings. These later reports showed convincingly that
the PHYB-GFP fusion protein is a biologically active
photoreceptor, that the PHYB contains a functional NLS
and that the NLS motif is localised in the C-terminal part
of the photoreceptor. More importantly, these reports
documented unambiguously that the PHYB-GFP fusion
477
protein is localised in the cytosol in the dark and that
accumulation of the tagged photoreceptor in the nucleus is a
light-driven process. Nuclear translocation is induced by
repeated pulses of or continuous red light and reversed by farred light. After light treatment, PHYB-GFP is detectable
mainly in the form of speckles, and these speckles are present
only in nuclei (Fig. 2). Upon transfer to dark, the structures
gradually dissolve, and nuclei become diffusely stained and
finally free of any detectable fluorescence, which indicates that
the PHYB-GFP fusion protein has disappeared.
Intracellular localization of PHYA in light and
darkness
PHYA is a highly specialised photoreceptor that has
physiology and biochemistry markedly different from those of
other phytochromes. Therefore, it was expected that the lightdependent intracellular redistribution of PHYA, if it occurs and
plays a role in PHYA-mediated signalling, would exhibit
characteristics quite different from those of PHYB. It has been
demonstrated (Kircher et al., 1999; Kim et al., 2000) that lightdependent intracellular redistribution of PHYA indeed takes
place, and PHYA, similarly to PHYB, is imported into the
nucleus. These studies clearly established that the PHYA-GFP
fusion protein is a functional photoreceptor. In darkness it is
localised exclusively in the cytosol, and light induces its
translocation to the nucleus (Fig. 2).
The kinetic, light-quality and -quantity requirements of the
redistribution of PHYA are sharply different from those of
PHYB. Import of the PHYA-GFP fusion protein is an order of
Fig. 2. Localisation of PHYA-GFP (a and b) and PHYB-GFP fusion
proteins (c and d) in Arabidopsis seedlings grown for 7 days darkness and
kept in darkness (a and c) irradiated for 24 hours with far-red light (b) or
irradiated for 6 hours with red light (d), before analysis by epifluorescence
microscopy. Nuclei (nu) and selected plastids (pl) are indicated.
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JOURNAL OF CELL SCIENCE 114 (3)
FHY1
SPA1
FAR1
EID1
FR/R
PHYApr
PHYApfr
PHYApfr
PIFX
mRNA
LRE 1
R
Cytosol
Nucleus
RED1
photomorphogenesis
PHYBpr
PHYBpfr
PHYBpfr
PIF3
mRNA
LRE 2
Fig. 3. A model depicting molecular components and cellular processes involved in PHYA- and PHYB-mediated phototransduction in higher
plants. PHYApr and PHYBpr represent red-light-absorbing forms of phytochrome-A and phytochrome-B, respectively. PHYApfr and PHYBpfr
represent far-red-light-absorbing forms of phytochrome A and phytochrome B, respectively. FHY1, SPA1, FAR1 and EID1 are shown to effect
PHYA-mediated signalling; RED1 is known to modulate PHYB-mediated signalling; PIF3 binds to different LREs (cis-acting light regulatory
elements) required for light-induced transcription of target genes and interacts selectively with the pfr form of PHYB. PIFX is a postulated
nuclear protein that is involved in PHYA-mediated phototransduction.
magnitude faster, easily detectable within a minute and
induced by pulses of or continuous far-red light. Although
PHYA-GFP imported into the nucleus forms speckles, these
speckles are smaller and more numerous when compared with
those formed by PHYB-GFP. In addition, the speckles are not
restricted to nuclei: they are easily detectable in the cytosol,
and formation of these structures in the cytosol precedes
their appearance in the nucleus. The PHYA–GFP-containing
speckles formed in the cytosol are reminiscent of sequestered
areas of phytochrome (SAPs) thought to represent
intermediates or products of ubiquitin-mediated proteolytic
degradation of PHYA (Speth et al., 1986).
Intracellular localization of PHYC-PHYE
To analyse intracellular localisation of the other three members
of the phytochrome photoreceptor family, we chose an
approach similar to that used for PHYA and PHYB, analysing
the nucleo/cytoplasmic distribution of PHYC-GFP, PHYDGFP and PHYE-GFP fusion proteins in transgenic tobacco and
Arabidopsis seedlings. Interpretation of the emerging data
seems to be rather difficult for several reasons. First, in sharp
contrast to PHYA-GFP and PHYB-GFP, the PHYC-GFP,
PHYD-GFP and PHYE-GFP fusion proteins are always
detectable in the nuclei in dark-grown seedlings in all lines
tested so far. Import of these proteins into nuclei might
therefore be light independent and constitutive. Second, in
etiolated seedlings, staining of the nuclei is always diffuse:
speckles do not form. Finally, red-light treatment induces
formation of speckles in the nuclei (which can be reversed by
far-red light) but does not significantly affect the diffuse
fluorescence. The kinetics of the appearance/disappearance of
these speckles is, however, comparable to that of PHYB–GFPcontaining speckles. These results might indicate that PHYCPHYE, in contrast to PHYA and PHYB, can be imported into
the nucleus in their biologically inactive Pr (dark) form, and
yet the speckle formation is dependent on the presence of the
Pfr form (Kircher et al., unpublished data). Why might the
regulation of PHYC-PHYE import into the nucleus be so
different? Is the import of these photoreceptors indeed
regulated differentially or is there an active retention
mechanism that ensures efficient cytosolic retention of PHYA
and PHYB but not that of PHYC-PHYE in the dark? If so, what
is the biological function of PHYC-PHYE accumulated in
nuclei in the dark, and why is speckle formation a strictly lightinduced phenomenon for all phytochromes?
Conclusions and perspectives
The localisation of photoreceptors in algae, ferns and mosses
is still not clear, but we expect that a specific mechanism to
recruit photoreceptors to the plasma membrane exists.
Intracellular redistribution of phytochromes
Whether this is completely lost in higher plants or whether
there are still traces of this type of regulation mediating some
of the known light-dependent membrane responses (such as
regulation of ion channels in guard cells and pulvini) remains
to be elucidated.
In higher plants, all photoreceptors, except NPH1-like
receptors, are imported into nuclei, and their nucleo/
cytoplasmic partitioning is regulated by light, albeit to different
degrees. It is well documented that light, in a quality- and
quantity-dependent fashion, induces transport of PHYA-GFP
and PHYB-GFP into nuclei and that the import is accompanied
by spot formation within the nucleus. What is the biological
relevance, if any, of these speckles? Recent experiments show
that PHYB and CRY2 physically interact in these spots (Más
et al., 2000). In addition, Quail and co-workers have provided
compelling evidence that PHYB interacts in vitro with a variety
of nuclear proteins, mainly transcription factors. These
interactions are light reversible, specific to the physiologically
active Pfr form of PHYB (Ni et al., 1998; Ni et al., 1999), and
one of these interacting proteins, PIF3, an HLH-type factor,
binds to the promoters of several but not all light-regulated
genes tested (Martinez-Garcia et al., 2000). Taken together
these results indicate that, at least for some PHYB-mediated
responses, a very short signal transduction chain can be
envisaged: light absorption leads to Pfr formation, which
promotes import of the protein into the nucleus and interaction
with promoter-bound transcription factors. Do the nuclear
speckles whose appearance is strictly light induced and which
are quite different for the different phytochromes, by analogy
with PHYB-CRY2, reflect different functional complexes that
contain, for example, PHYB-PIF3? We were currently trying
to answer these questions.
After light-to-dark transitions, the phytochrome-containing
speckles dissolve, producing a diffuse staining that is followed
by a complete loss of fluorescence in the nucleus. Is this due
to degradation – even for the stable phytochromes PHYBPHYE – or to export into the cytosol? Notwithstanding these
and many more questions, it is safe to say that light-qualityand light-quantity-dependent import of the different
phytochromes into the nuclei is a key regulatory step in
controlling the transition from skoto- to photo-morphogenesis
(Fig. 3).
Such a conclusion is further supported by the fact that the
specific functions of the different phytochromes clearly
manifest themselves at the level of light-dependent import into
the nuclei. The wavelength- and fluence-rate dependence of
PHYA and PHYB nuclear import correlates well with the
established physiological functions of these receptors. PHYA
regulates VLFR and far-red HIR, and nuclear import of PHYA
is also induced by VLFR and far-red high irradiance (Kim et
al., 2000). Likewise, PHYB mediates the low fluence rate
response (LFR), and nuclear import of PHYB is also induced
by LFR (Gil et al., 2000). It follows that, in far-red light, only
import of PHYA into the nuclei is observed, whereas in red
light the appearance of PHYA in the nuclei is only transient;
thus, PHYB cannot be a physiological far-red-light-activated
photoreceptor, and PHYA cannot be a red-light-activated
photoreceptor.
The work in Freiburg was supported by funding from the
Graduiertenkolleg, SFB 388, Human Frontier Science Programme to
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E.S and a Humboldt Stiftung Award to F.N. Work in Hungary was
supported a Howard Hughes International Scholarship (55000325)
and by Human Frontier Science Programme and OTKA T-032565
grants to F.N.
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