Light perception and signalling in higher plants

446

Light perception and signalling in higher plants Pe´ter Gyula
y, Eberhard Scha¨ferz and Ferenc Nagy
§ Plants monitor changes in the ambient light environment using sensory photoreceptor families: the phototropins and cryptochromes, which absorb UV-A or blue light; the phytochromes, which sense red/far-red light; and the UV-B photoreceptors, which have not yet been identified. Recent advances suggest that photoreceptor-induced signalling cascades regulate light-modulated gene expression. These regulatory networks interact at the levels of transcription, posttranslational modification and nucleo-cytoplasmic compartmentalisation. Addresses
Institute of Plant Biology, Biological Research Centre of the Hungarian Academy of Sciences, Temesva´ri krt. 62, Szeged, H-6726, Hungary y e-mail: [email protected] § e-mail: [email protected] z Institute of Botany/Biologie II, University of Freiburg, Schanzlestrasse 1, D-79102, Freiburg, Germany e-mail: [email protected] Correspondence: Ferenc Nagy

Current Opinion in Plant Biology 2003, 6:446–452 This review comes from a themed issue on Cell signalling and gene regulation Edited by Kazuo Shinozaki and Elizabeth Dennis 1369-5266/$ – see front matter ß 2003 Elsevier Ltd. All rights reserved. DOI 10.1016/S1369-5266(03)00082-7

Abbreviations ARR4 ARABIDOPSIS RESPONSE REGULATOR 4 cop constitutive photomorphogenesis CRY cryptochrome det de-etiolated FR far-red fus fusca FyPP PHYTOASSOCIATED PROTEIN PHOSPHATASE HY5 ELONGATED HYPOCOTYL IN LIGHT 5 NPH3 NON-PHOTOTROPIC HYPOCOTYL 3 PHOT phototropin PHY phytochrome PIF3 PHYTOCHROME-INTERACTING FACTOR 3 PKS1 PHYTOCHROME KINASE SUBSTRATE 1 R red RPT2 ROOT PHOTOTROPISM 2 SPA1 SUPPRESSOR OF PHYTOCHROME A 1 UV-A/B ultraviolet-A/B ZTL ZEITLUPE

Introduction The photosensory system that plants have developed to monitor their light environment contains three known classes of photoreceptors — the phytochromes (PHY), the cryptochromes (CRY), and the phototropins (PHOT) — Current Opinion in Plant Biology 2003, 6:446–452

and the as yet unidentified ultraviolet-B (UV-B)-absorbing receptor molecules (Figure 1). Light-induced signal transduction starts with the perception of light by these specialised photoreceptors and culminates in the regulation of the expression of about 2500 genes in Arabidopsis thaliana, which eventually enables the plant to respond at the physiological level to changes in different modalities (directionality, intensity, colour, and diurnal and seasonal duration) of illumination. Recent studies have identified novel components of the signaling cascades and have unravelled molecular mechanisms that are involved in signal transduction and integration. This review gives a brief summary of these results and emphasises the most important features of the newly emerging concept of light-signal transduction.

The photoreceptors The phytochrome apoprotein is encoded by a small multigene family: in the model plant Arabidopsis thaliana this family consists of five genes (PHYA, PHYB, PHYC, PHYD and PHYE). All phytochromes exist as dimers that are composed of two 125-kDa polypeptides, each carrying a covalently linked open-chain tetrapyrrol chromophore. Phytochromes are synthesised in the dark in their physiologically inactive red (R)-light absorbing Pr form. After the absorption of a photon, this inactive Pr form is photoconverted into the physiologically active far-red (FR)-absorbing Pfr form, which in turn is transformed back into the Pr form upon absorption of FR. The Pfr form of PHYA is light labile, whereas the stability of the Pfr forms of PHYB–PHYE is not significantly affected by light. The carboxy-terminal domain of PHY functions in dimerisation and contains a region that resembles prokaryotic two-component histidine kinases. The aminoterminal region is thought to define the photosensory activity of the PHY molecule. Beyond inducing conformational change of the PHY molecule, light causes the autophosphorylation of PHYA [1] and the phosphorylation of other proteins by phytochrome [2]. Light also modulates the nucleo-cytoplasmic distribution of PHYA– PHYE by inducing their translocation into the nucleus in a light quality- and quantity-dependent fashion [3]. Cryptochromes (CRY1 and CRY2 in Arabidopsis) are flavoproteins that are found in various taxa and are thought to have evolved from photolyases. Unlike photolyases, however, CRY have no DNA-repair activity. The amino-terminal part of the CRY molecule binds two types of chromophore: pterin at one site and flavin adenine dinucleotide (FAD) at another. The carboxy-terminal parts of CRY1 and CRY2 contain a variable extension, which is not found in photolyases, and are essential for www.current-opinion.com

Light perception and signalling in higher plants Gyula, Scha¨ fer and Nagy 447

Figure 1

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?

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GI ELF3 SRR1 APRR1 APRR5 ? APRR9 ? ZTL pef2 pef3 red1

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Effectors Genotoxic stress response

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Photomorphogenesis

Current Opinion in Plant Biology

Photoreceptors and potential light-signalling intermediates. Cloned components are capitalised; those that have been genetically identified but not yet cloned are in lower case and italics. UV-B light is absorbed by unidentified receptor(s). High-fluence UV-B light damages DNA and elicits a series of protection responses. Low-fluence UV-B affects photomorphogenesis by enhancing PHYB-specific responses. UVB LIGHT INSENSITIVE 3 (ULI3) [41] is one of the signalling components that mediates these responses. The UV-A/blue part of the spectrum is monitored by phototropins (PHOT), cryptochromes (CRY) and PHYTOCHROME A (PHYA). Phototropins regulate the majority of phototropic responses and intracellular chloroplast movements. Cryptochromes provide the light signal for most of the blue-light-induced responses of photomorphogenesis. The CRY-induced signalling pathway is probably short; to date, only one positively acting intermediate has been identified [33]. Phytochromes are the most extensively studied photoreceptors. PHYB–E are the receptors that sense continuous red light, whereas PHYA (and to a smaller extent PHYE) responds to continuous farred and very low fluences of red and blue light. Signals from different photoreceptors are integrated by a complex regulatory network. This network inhibits the activity of the COP/DET/FUS class of proteins (which are negative regulators of photomorphogenesis) and induces the expression of downstream transcription factors, such as HY5 and HY5 HOMOLOGUE (HYH). The circadian clock affects this regulatory network at multiple levels. Components that are common to light-input pathways and the circadian clock are framed in a dashed-outline box. APRR1/5/9, ARABIDOPSIS PSEUDO-RESPONSE REGULATOR1/5/9; ARF7, AUXIN RESPONSE FACTOR7; COG1, COGWHEEL1; cp3, compacta3; EID1, EMPFINDLICHER IM DUNKELROTEN LICHT1; ELF3, EARLY FLOWERING3; FAR1, FAR-RED IMPAIRED RESPONSE; FHY1/2, LONG HYPOCOTYL IN FAR-RED LIGHT1/2; FIN219, FAR-RED INSENSITIVE219; GI, GIGANTEA; HFR1, LONG HYPOCOTYL IN FAR-RED LIGHT1; IAA1/3/4/9/17, INDOLE-3-ACETIC ACID RESPONSE FACTOR1/3/4/9/17; LAF1/6, LONG AFTER FAR-RED LIGHT1/6; NDPK2, NUCLEOSIDE DIPHOSPHATE KINASE2; PAT1, PHYA SIGNAL TRANSDUCTION1; PSI2, PHYTOCHROME SIGNALLING2; red1, red light elongated; srl1, short hypocotyl in red light; SRR1, SENSITIVITY TO RED LIGHT REDUCED1; SUB1, SHORT UNDER BLUE LIGHT1.

CRY function [4]. The photochemical mechanism of signal capture and transfer by CRY is likely to involve a redox reaction. Transcription of CRY1 and CRY2 is regulated by the circadian clock. The intracellular location of both cryptochromes is mostly nuclear: CRY2 is localised to the nucleus constitutively, whereas CRY1 is www.current-opinion.com

primarily found in the nucleus in the dark. The stability of CRY1 is not affected by light, whereas CRY2 is degraded rapidly upon blue-light illumination. Phototropins (PHOT1 and PHOT2 in Arabidopsis) are also flavoproteins. They carry two flavin mononucleotide Current Opinion in Plant Biology 2003, 6:446–452

448 Cell signalling and gene regulation

(FMN) chromophores that are associated with the LOV (light, oxygen, voltage)/PAS (PER, ARNT, SIM) domain in the amino-terminal part of the molecule. PHOT1 and PHOT2 are blue-light-sensitive receptor kinases, whose carboxy-terminal parts contain a classical Ser/Thr kinase domain. They mediate similar blue-light responses, but have different photosensitivities as determined by their amino-terminal domains. Besides controlling the phototropism of stem and root, phototropins also affect other physiological responses, namely chloroplast movement [5–7] and stomatal opening [8]. Upon signal capture, both PHOT1 and PHOT2 undergo autophosphorylation, and signal transfer from the activated receptors to downstream components likely involves a kinase reaction.

Signalling intermediates and molecular mechanisms involved in light-signal transduction After activation by light, receptors initiate downstream signal propagation that results in transient or sustained physiological responses. Classical genetic screens have yielded several possible light-signalling mutants (Figure 1) that can be classified into two major groups. Members of the first class belong to the constitutive photomorphogenesis (cop)/de-etiolated (det)/fusca (fus) group, which show signs of photomorphogenesis in complete darkness. The COP/ DET/FUS genes are therefore assumed to function as negative regulators of photomorphogenesis [9]. In harmony with the pleiotropic nature of cop mutants, it has become evident that the COP9 signalosome plays a central role in mediating the degradation of several regulatory proteins, thereby affecting light- and hormoneinduced signalling. In this review, we do not discuss the COP9 signalosome further_and refer to the COP/DET/ FUS pathway only in the context of light signalling. Members of the second class of possible light-signalling mutants develop normally in darkness but have disturbed responsiveness to light signals that are received by specific photoreceptors. Biochemical approaches and yeast two-hybrid screens coupled with reverse genetics have led to the identification of approximately 2500 genes in Arabidopsis.

Phytochrome signalling intermediates Until 1998, most of the available evidence suggested that phytochromes are localised and act primarily in the cytoplasm. Signal transduction from the cytosol to the nucleus was thought to be mediated by second messengers such as cyclic guanosine monophosphate (cGMP), Ca2þ and/or a phytochrome-induced phosphorylation cascade of regulatory proteins [10]. Recent data have radically changed this view. The emerging model postulates that phytochrome not only induces a signalling cascade mediated by Ca2þ and cGMP in the cytoplasm but also functions as a light-regulated kinase (Figure 2); its Pfr conformer can rapidly translocate into the nucleus, where it interacts with transcription factors and thus can directly regulate Current Opinion in Plant Biology 2003, 6:446–452

light-induced gene transcription [11]. This complex signalling network is attractive and is supported by a wealth of experimental data. PHYA is known to be autophosphorylated, and itself functions as a kinase that phosphorylates PHYTOCHROME KINASE SUBSTRATE 1 (PKS1) [2] and Aux/IAA (Auxin/Indoleacetic acid) proteins [12]. Moreover, a very recent report showed that PHYA can interact with the catalytic subunit of the Ser/ Thr-specific protein phosphatase FyPP, and that recombinant FyPP efficiently dephosphorylates oat PHYA in a conformation-dependent manner [13]. Casein kinase II (CKII)-mediated light-dependent phosphorylation has also been suggested to regulate the stability and transcriptional activity of ELONGATED HYPOCOTYL IN LIGHT 5 (HY5), a key component of phytochrome- and cryptochrome-controlled signalling cascades [14]. There is no evidence to show that the phosphorylation status and kinase activity of PHYB–E, in contrast to that of PHYA, affects light signalling. Moreover, a truncated PHYB molecule that lacks the entire postulated kinase domain efficiently restored wildtype red-light-inhibited hypocotyl elongation to a PHYB null mutant [15]. Light-induced change in the nucleo-cytoplasmic distribution of PHYA–E, that is, in their light-driven translocation into the nucleus, is an essential step in signalling. This process controls the availability of activated photoreceptors for interactions with other regulatory proteins in the nucleus. Nuclear PHYA–E is not evenly distributed: it is concentrated in subnuclear structures called nuclear speckles. Speckle formation exhibits a diurnal pattern in plants grown under Light/Dark cycles and is reversible by R/FR treatment [3,16]. Moreover, it seems to be restricted to biologically active photoreceptors: mutant PHYA and PHYB molecules that are unable to interact with other proteins are imported into the nucleus but fail to form these structures [3]. A missense mutation of PHYA impaired both the speckle formation of this photoreceptor and a subset of PHYA-controlled responses [17]. Co-localisation studies and fluorescence-resonance energy transfer (FRET) microscopy using PHYB::green fluorescent protein (GFP) and CRY2::red fluorescent protein (RFP) also demonstrated the formation of these subnuclear structures [18]. On the basis of these findings, it is tempting to postulate that PHYA- and/or PHYBcontaining speckles represent active transcriptional complexes, which possibly contain numerous physically and functionally interacting proteins (Figure 2). To corroborate this assumption, the molecular composition of these structures needs to be elucidated. Although it is well documented that all phytochrome species are imported into the nucleus in a manner that is affected by light quality and quantity [3], it should be noted that, even under inductive conditions, the majority of phytochromes remains cytosolic. The biological function of cytosolic phytochromes and the molecular www.current-opinion.com

Light perception and signalling in higher plants Gyula, Scha¨ fer and Nagy 449

Figure 2

Cytosol PKS1 P

Nucleus ?

PHYAr

P

Speckle

PK

FRc

S1

P P

PHYAfr

P

P

PHYAfr

PHYAfr

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mRNA

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1 KS

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Current Opinion in Plant Biology

Proposed model for light-regulated gene expression. Phytochromes (PHYs) are located in the cytosol in the dark. Upon appropriate light irradiation, they are converted to their active (Pfr) conformation and autophosphorylated. PHYs phosphorylate different proteins in the cytosol, including PKS1. PKS1 may function as a cytoplasmic-retention factor, whose activity is regulated by reversible phosphorylation. The phosphorylated Pfr forms of PHYs could have cytoplasmic functions. Dephosphorylation by a phosphatase (FyPP) may trigger the translocation of PHYs to the nucleus, where they interact with transcription factors and promote the formation of subnuclear bodies called ‘speckles’. Speckles are assumed to be higher order regulatory complexes that are involved in controlling the light-modulated transcription of genes. The level of transcription from promoters containing the light-responsive element (LRE) is determined by the concentration of active transcription factors at the specific site of action. Binding-site selection is achieved by extensive heterodimerization of transcription factors (e.g. PIF3, HFR1). PIF4, like PIF3, is probably bound to the promoter in the dark. In contrast to PIF3, however, PIF4 is probably displaced by activated PHYB. PHYs upregulate the expression of several transcription factors, including HY5. HY5 is a key regulator of photomorphogenesis, and its abundance is also regulated at the level of protein stability. In the dark, HY5 is targeted for proteolytic degradation by COP1. In light, this process is inhibited, in part, by the action of CRYs, possibly by purging COP1 from the nucleus. This allows active HY5 to accumulate and bind to light-responsive promoters that contain G-boxes. CKII, casein kinase II; CSN, COP9 signalosome; FRc, continuous far-red light; Rc, continuous red light.

mechanism that mediates their import into the nucleus and retention in the cytoplasm in the dark are unknown. It is interesting to note that no mutants have been described in which the nuclear import of PHYA–E is abolished or constitutive. Such mutants, unless lethal, would be expected to have a robust photomorphogenic phenotype that would be easily identifiable in a genetic screen. Molecular mechanisms that regulate the stability/ degradation of phytochromes in the nucleus and/or the cytoplasm are also largely unknown. The active conforwww.current-opinion.com

mation of PHYB is stabilised by the overexpression of the response regulator ARABIDOPSIS RESPONSE REGULATOR 4 (ARR4), a finding that opened the way to studies of possible interactions between light and cytokinin signalling pathways [19]. It is assumed that ubiquitin-mediated degradation is responsible for the light lability of PHYA. EID1 (EMPFINDLICHER IM DUNKELROTEN LICHT1), an F-box containing protein [20], and SUPPRESSOR OF Current Opinion in Plant Biology 2003, 6:446–452

450 Cell signalling and gene regulation

PHYTOCHROME A 1 (SPA1) are negatively acting factors that are possibly involved in the degradation of PHYA signalling intermediates. COP1, acting as an E3 ligase, induces the degradation of HY5 in the nucleus in the dark. On the basis of this finding, it is expected that COP1, a negative regulator of photomorphogenesis, acts by targeting certain proteins to the degradation machinery in the dark. Indeed it has been reported that COP1 interacts with SPA1 [21], CRY1 and PHYB in yeast [22,23]. There is no evidence, however, that the degradation of these proteins is mediated by COP1 in planta. In addition, the role of COP1-induced proteolytic degradation in light or at later stages of development is much less clear. Thus, the function of COP1 and the role of proteolytic degradation in phytochrome-initiated signal transduction, in contrast to CRY-induced signalling, is either minor or not yet understood. The most challenging findings of the past few years of research into phytochrome-induced signalling have provided evidence that PHYA and PHYB can interact directly, in a conformation-dependent manner, with the transcription factor PHYTOCHROME-INTERACTING FACTOR 3 (PIF3) bound to light-regulated promoters [24]. The significance of this type of regulation was further extended when other proteins were shown to heterodimerise with PIF3 [25,26]. More importantly, misexpression or mutation of the genes that encode these proteins was found to affect phytochrome-controlled aspects of photomorphogenesis. In addition, microarray studies have indicated that phytochrome-regulated signalling affects gene expression at the level of transcription [27–29]. Quail [30] proposes that phytochrome directly enhances the transcription of a set of master regulatory proteins in hierarchical order, which in turn trigger the expression of other regulators. This model proposes a relatively short, straightforward transcriptional cascade, which culminates in the light-modulated transcription of about 2500 genes in Arabidopsis [30].

Cryptochrome signalling intermediates According to our present interpretation, the signalling cascade controlled by CRY1 and CRY2 is organised differently from that controlled by PHY and can be relatively short. Recent studies have demonstrated that the overexpression of the carboxy-terminal parts of CRY1 and CRY2 induces a constitutive but still phytochromestimulatable photomorphogenesis. The cop1-like phenotype indicates that in the absence of an inhibitory aminoterminal domain, the carboxy-terminals of CRYs are constitutively active [4]. Moreover, CRY1 and CRY2 interact with COP1 in the nucleus in the dark [22,23]. It is postulated, therefore, that blue-light perception by CRY photoreceptors triggers the rapid deactivation/ degradation of COP1 by an unknown mechanism, allowing the accumulation of HY5 in the nucleus, which in turn enhances the transcription of target genes (Figure 2). Current Opinion in Plant Biology 2003, 6:446–452

This model emphasises the role of regulated proteolysis; it is certain, however, that other molecular mechanisms also play a significant role in CRY1- and CRY2-mediated signalling for the following reasons. First, microarray experiments have shown that blue light modulates the transcription of nearly as many genes as does red light. Thus, there must be key regulatory transcription factors other than HY5, for example HY5 HOMOLOGUE (HYH), that are involved in mediating this process [31]. Second, CRY2 is phosphorylated in vivo in a blue-light-dependent fashion [32], and furthermore, Moller and colleagues [33] provided evidence that a novel Ser/Thr protein phosphatase (AtPP7), which has high sequence similarity to the Drosophila retinal degradation C protein phosphatase, acts as a positive regulator in blue light signaling. Moreover, the interaction of CRY1 with proteins such as PHYA [34] and ZEITLUPE (ZTL; an F-box containing protein) [35] was demonstrated in yeast, and the interaction of CRY2 and PHYB in vivo in protoplasts was documented by FRET microscopy [18]. Remarkably, all of these interactions occur between cryptochromes and other photoreceptors, such as PHYA and PHYB, or putative receptors, such as ZTL. Although the molecular interpretation of these findings is still lacking, it is tempting to speculate that these interactions may mediate crosstalk between light-induced signalling cascades, and thus play a role in fine-tuning the response to the light environment. This hypothesis is supported by the fact that the absence of the Ca2þ-binding protein SUB1 in mutant Arabidopsis plants affected both cryptochrome- and phytochrome-mediated signalling [36].

Phototropin signalling intermediates The phototropin class of photoreceptors was identified only recently, yet in the past two years significant advances have been made toward identifying elements that mediate the phototropin-specific signalling cascade. PHOT1 and PHOT2 are bona fide receptor kinases and the BR-C, TTK, BAB (BTB)/pox virus, zinc-finger (POZ)domain proteins NON-PHOTOTROPIC HYPOCOTYL 3 (NPH3) [37] and ROOT PHOTOTROPISM 2 (RPT2) [38] have been identified as possible downstream signalling intermediates. PHOT1 and NPH3 interact physically and both are associated with the plasma membrane. Many BTB/POZ-domain proteins are known to interact with transcription factors. Therefore it is possible that RPT2 and NPH3 serve as relays between phototropin at the plasma membrane and transcription factors in the nucleus. One transcription factor that has been shown to act downstream from phototropins is an auxinresponse factor, NPH4/ARF7 [39]. The nph4 mutant lacks an auxin-responsive factor and displays impaired responsiveness to phototropic stimuli. These features suggest a link between PHOT1 signalling and auxinregulated transcription. However, further research is required to determine how the regulation of ion currents through the plasma membrane and the interaction of www.current-opinion.com

Light perception and signalling in higher plants Gyula, Scha¨ fer and Nagy 451

these receptors with different partners — for example, Hþ-ATPase in guard cells [8], ion transporters or channel proteins in other leaf cells [40], and maybe auxin transporters in stem cells — result in different movement responses in different parts of the plant.

7.

Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M, Okada K: Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 2001, 98:6969-6974.

8.

Kinoshita T, Doi M, Suetsugu N, Kagawa T, Wada M, Shimazaki K: phot1 and phot2 mediate blue light regulation of stomatal opening. Nature 2001, 414:656-660.

Conclusions

9.

Ma L, Gao Y, Qu L, Chen Z, Li J, Zhao H, Deng XW: Genomic evidence for COP1 as a repressor of light-regulated gene expression and development in Arabidopsis. Plant Cell 2002, 14:2383-2398.

Light-regulated signal transduction is mediated by a complex, integrated molecular network. Single or multiple photoreceptors can induce different signalling cascades that partly overlap. Several components of these cascades and some of the molecular mechanisms that mediate photoreceptor-controlled signal transduction have been identified. The terminal step of signalling, the regulation of target-gene expression, occurs predominantly at the level of transcription but signal relay is significantly affected by regulated degradation and the compartmentalisation of the signalling intermediates. Genetic screens and the analysis of mutants will undoubtedly lead to the identification of novel components of signalling cascades. Unravelling of the mode of action of these molecules and the molecular mechanisms by which they regulate signalling will, however, require advanced cell biological, biochemical and structural studies.

Acknowledgements The authors thank the members of our laboratory for stimulating discussions, E´ va A´ da´ m and La´ szlo´ Kozma-Bogna´ r for helpful comments on the manuscript, and Erzse´ bet Fejes for manuscript preparation and editing. Research was supported by grants from Howard Hughes Medical Institute (HHMI 55000325), the Hungarian Foundation for Basic Science (OTKA, T032565) and the Wolfgang Paul Award to Ferenc Nagy.

References and recommended reading Papers of particular interest, published within the annual period of review, have been highlighted as:  of special interest  of outstanding interest 1.

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Kircher S, Gil P, Kozma-Bogna´ r L, Fejes E, Speth V, HusselsteinMuller T, Bauer D, A´ da´ m E´ , Scha¨ fer E, Nagy F: Nucleocytoplasmic partitioning of the plant photoreceptors phytochrome A, B, C, D, and E is regulated differentially by light and exhibits a diurnal rhythm. Plant Cell 2002, 14:1541-1555. The paper demonstrates that light modulates nucleo/cytoplasmic compartmentalisation of PHYA–PHYE in a light-quality-dependent fashion and that the formation of PHYA–PHYE-containing sub-nuclear speckles exhibits a diurnal rhythm. 3. 

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