Phytochrome A-specific signaling in Arabidopsis thaliana

Plant Signaling & Behavior 6:11, 1714-1719; November 2011; ©2011 Landes Bioscience

Phytochrome A-specific signaling in Arabidopsis thaliana Stefan Kircher,1 Kata Terecskei,2 Iris Wolf,1 Mark Sipos2 and Eva Adam2,* Institute of Botany; Biology II; University of Freiburg; Freiburg, Germany; 2Plant Biology Institute; Biological Research Center; Szeged, Hungary

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Keywords: Arabidopsis, phyA, VLFR, HIR, signaling

Among the five phytochromes in Arabidopsis thaliana, phytochrome A (phyA) plays a major role in seedling deetiolation. Until now, more than 10 positive and some negative components acting downstream of phyA have been identified. However, their site of action and hierarchical relationships are not completely understood yet.

Introduction

response (VLFR) is saturated by a few Pfr-molecules per cell, thus it is apparently non-reversible. In some species seed germination displays extreme light-sensitivity typical of VLFR.5 In contrast, the low fluence response (LFR) depends on higher Pfr/Ptotal ratios, which then results in their classical photoreversible nature. Again, seed germination in species like Arabidopsis exhibit typical LFR characteristics.6,7 Interestingly, continuous irradiations with varying light quantities not affecting the Pfr/Ptotal ratio can result in gradual phy-mediated responses like hypocotyl growth inhibition. The phyA-dependent HIR (high irradiance response) in far-red light is the most prominent of this response category. In Arabidopsis, the phytochrome apoprotein is encoded by five different genes named PHYA to PHYE.8 PHYA and PHYB are the dominating members of this gene family and show different dynamics in their abundance.9 While VLFR and far-red HIR responses are mediated by the light-labile phyA mainly in early stages of development, the more stable phyB-E proteins represent the sensors for LFR and monitor the light conditions after seedling establishment. In this review we discuss the molecular mechanisms mediating phyA-dependent signaling.

©201 1L andesBi os c i enc e. Donotdi s t r i but e.

Higher plants have to cope with the environmental conditions at the place where they germinate and grow. Light plays a fundamental role in optimizing their adaptation and survival, thus plants have evolved multiple specialized photosensory systems to monitor changes in the surrounding light conditions. These photoreceptors include the recently discovered UVB-sensing UVR8,1 the blue/UVA sensory molecules cryptochromes, phototropins and LOV-domain proteins like Zeitlupe as well as the red/farred absorbing phytochromes.2,3 Phytochromes (phy) regulate all aspects of photomorphogenic development of plants throughout their whole life-cycle including seed germination, seedling development, the shade avoidance syndrome to detect and escape shading by photosynthetically active neighbors, entrainment of the circadian clock and the onset of flowering.4 Phytochromes have the capacity to steadily and rapidly sense changes in the incident light composition and thus play a key role in the dynamic adaptation of plants. On a molecular level this is achieved by the photoreversible nature of phy chromoproteins. The inactive Pr-form is converted maximally by red light (λmax 660 nm) into the physiologically active Pfr conformer, which can be reverted back into the inactive Pr conformer by absorption of a subsequent photon (λmax 720 nm). It is important to note that, due to the broad, distinct and partially overlapping absorbance spectra of Pr and Pfr, the entire light spectrum can be monitored by phytochromes, i.e., the action of these photoreceptors is not limited to the red and far-red parts of the spectrum. In consequence the qualitative and quantitative spectral composition of incident light establishes a photoequilibrium of conformers (Pfr/Ptotal ratio). The numerous physiological responses mediated by phy are categorized in three classes. The so-called very low fluence *Correspondence to: Eva Adam; Email: [email protected] Submitted: 07/25/11; Accepted: 07/26/11 DOI: 10.4161/psb.6.11.17509

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Mechanisms Controlling PhyA-Specific Signal Transduction Among the phytochrome receptors phyA displays unique properties. PhyA is present only as homodimers in planta10,11 and mediates two types of responses: it is the sole mediator of very low fluence responses (VLFR) detecting light conditions that the other phytochromes cannot distinguish from darkness, and the high irradiance response (HIR) requiring continuous high fluence FR light. Since phyA functions as an FR or dim light sensor, it shares little functional redundancy with the other Arabidopsis phytochromes. PhyA-controlled signaling is complex and mediated by a number of recently identified molecular components and mechanisms. A general scheme of the main phyA-controlled signaling cascades is illustrated in Figure 1. Light-induced nuclear import of phyA in its Pfr form is an early step in signaling. A single brief FR-, R- or B-light pulse induces nuclear import of phyA and subsequent formation of nuclear bodies (NB). In etiolated seedlings the nuclear import of phyA is a rapid process: it takes place within a few minutes after the inductive light pulse. An R pulse also promotes the rapid formation of phyA-containing cytosolic bodies, called sequestered areas of phytochromes (SAPs) which are thought to be the place of

Plant Signaling & Behavior

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REVIEW


Figure 1. A simplified model for phyA (phytochrome A) signaling pathways. After de novo synthesis in the cytosol, assembly of the chromophor and dimerization, light establishes a photoequilibrium (designated as λ) between Pr (red light absorbing form of phytochromes) and Pfr (far red light absorbing form of phytochromes). The Pfr form of phyA interacts with the transport helper proteins FHY1 (FAR-RED ELONGATED HYPOCOTYL 1) and FHL (FHY1-LIKE PROTEIN) and is imported into the nucleus by a piggyback mechanism. FHY1 and FHL can re-enter the cytosol and thus function as shuttleproteins for phyA (see Fig. 2 for details). Residual cytosolic phyA together with the blue light receptors PHOT1 and 2 (PHOTOTROPIC 1 and 2) trigger the phototropic response potentially via the PKS1 protein. In cytosol and nucleus phyA can become ubiquitinated in its Pfr form and is subsequently degraded, irrespective of its actual conformational state. Within the nucleus several phyA signal transduction pathways have been described. Phytochromes repress the (photomorphogenic repressor) COP1/SPA complex and thus enhance the nuclear accumulation of positive regulators such as HY5 (HYPOCOTYL 5), LAF1 (LONG AFTER FAR RED LIGHT1) and HFR1 (LONG HYPOCOTYL IN FAR RED 1). HY5 directly targets a number of genes important for photomorphogenesis. A second branch is that of the PIFs (PHYTOCHROME INTERACTING FACTORs), negative regulators of photomorphogenesis. Pfr induces the rapid degradation of these bHLH factors. A third pathway nearly exclusively responsible for the HIR (HIGH IRRADIANCE RESPONSE) includes the F-Box-protein EID1 (EMPFINDLICHER IM DUNKELROTEN LICHT 1). This protein targets a still unknown component of the phyA signaling network for degradation and functions as a repressor of phyA signaling. Not shown are the proposed effects on signaling of hypo- and hyperphosphorylated forms of phyA.

ubiquitination and degradation of phytochrome A. Continuous FR light also initiates nuclear transport and formation of phyA NBs, consequently phyA light-induced nuclear transport can be correlated with phyA-mediated VLFRs and HIRs.12-14 Within the nucleus phyA co-localizes with PHYTOCHROME INTERACTING FACTOR3 (PIF3) in the so-called early nuclear bodies and this interaction contributes to the degradation of PIF3.15 PhyA does not contain nuclear localization signal (NLS) motives, its light-dependent nuclear import depends on FAR-RED ELONGATED HYPOCOTYL1 (FHY1) and FHY1-LIKE (FHL). These plant-specific homologous proteins contain functional nuclear export (NES) and NLS sequences and both of them are needed for normal nuclear accumulation of phyA. FHY1 and FHL interact with phyA in R or FR light in yeast 2-hybrid assay in vitro and PhyA and FHY1 co-localize

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in nuclear complexes in planta.16,17 It has been shown that only the NLS and phyA-interaction domain of FHY1 are necessary for this interaction.18 fhy1/fhl double mutants are indistinguishable from the phyA null mutant with respect to hypocotyl growth inhibition, cotyledon expansion and apical hook opening.17 FHY3 (FAR-RED ELONGATED HYPOCOTYL 3) and FAR1 (FAR-RED IMPAIRED RESPONSE 1), two proteins related to Mutator-like transposases act together to modulate phyA signaling by directly activating the transcription of FHY1 and FHL and in this way indirectly controlling phyA nuclear accumulation.16,19 HY5 also directly binds to the FHY1 and FHL promoters a few base pairs away from the FHY3/FAR1 binding sites. In this way HY5 physically interacts with FHY3 and FAR1 and negatively regulates FHY3/FAR1-activated FHY1/FHL expression, providing a mechanism for fine-tuning phyA signaling.20


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©201 1L andesBi os c i enc e. Donotdi s t r i but e. Figure 2. Light-induced nuclear transport of PHYA. FHY1 and FHL are distributed in the cytosol and nucleus in the dark. Upon light irradiation phyA interacts with FHY1/FHL hetero- or homodimers in the cytosol. Functional NLS motifs of the FHY1/FHL are recognized by a cytosolic importin α protein. The IMPα-FHY1/FHL-phyA(Pfr) complex is transported through the nuclear pores to the nuclei, where importin dissociates from the complex. In the nucleus two proteins, FHY3 and FAR1, related to Mutator-like transposases, act together to modulate phyA signaling by directly activating the transcription of FHY1 and FHL in the dark, whose products are essential for light-induced phyA nuclear accumulation. Subsequent light responses mediated by phyA include the attenuation of COP1 level, accumulation of HY5 and feedback regulation of FHY3 and FAR1 transcript levels. HY5 downregulates FHY1/FHL transcription by modulating the activities of FHY3 and FAR1.

Figure 2 depicts the main components and molecular mechanisms regulating nuclear import of phyA. Interestingly, the Myb type LAF1 (LONG AFTER FAR-RED LIGHT) and a bHLH type transcription factor HFR1 (LONG HYPOCOTYL IN FAR-RED) independently transmit phyA signals downstream of FHY1 and FHL.21 Therefore, the authors propose that FHY1 and FHL are not only necessary to control nuclear accumulation of phyA, but are also involved in mediating interactions of phyA with these transcription factors to promote assembly of protein complexes important for phyA signaling. However, at least FHY1 must be dispensable in this aspect, because the phenotype of a fhy1/phyA background is rescued by a phyA molecule of constitutive nuclear localization.18 The fhy1/fhl double mutant

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was also used to determine the cytoplasmic function of phyA in R-induced phototropism, abrogation of gravitropism and inhibition of hypocotyl elongation in blue light.22 Accordingly, it is now generally accepted that there is an FR light induced phyA signaling that occurs via FHY1/FHL-dependent nuclear, and an FHY1/FHL independent cytoplasmic branch. In contrast to other phy Pfr-s, phyA Pfr is rapidly degraded.23,24 PhyA Pfr degradation is delayed but not abolished by blocking the proteasome with inhibitors.25-28 In the dark the CONSTITUTIVELY PHOTOMORPHOGENIC1/ SUPPRESSOR OF PHYA (COP1/SPA) complexes promote ubiquitination of the positive transcription factors HY5 and HYH by targeting them for degradation through the proteasome.29


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Action of COP1/SPA complexes in Arabidopsis is not limited to dark, as these complexes are also active in light. In light their targets, beside transcription factors, may also include phyA Pfr.26 The COP1/SPA1 complex also plays an important role in regulating protein levels of phyA signaling components like HFR1 and LAF1 via direct interaction with these transcription factors.30 Their COP1/SPA-mediated degradation is thought to prevent the light-signaling pathway from over-activation. PhyA degradation takes place both in the cytoplasm and in the nucleus.27,28 As a consequence, the total PHYA concentration and thereby phyA signaling is attenuated. An additional unique feature of phyA among the phy-s is that phyA autophosphorylates its own N-terminal domain31 and itself functions as a kinase that phosphorylates Aux/IAA (Auxin/ Indoleaceticacid) proteins32 and PHYTOCHROME KINASE SUBSTRATE1 (PKS1).33 Because PKS1 is associated with phototropin (phot) responses, the membrane-bound molecule could represent an important crosspoint for phyA and phot signal integration in phototropism.34 Several protein phosphatases that bind and dephosphorylate phyA are known. These include the FLOWER-SPECIFIC PHYTOCHROME-ASSOCIATED PROTEIN PHOSPHATASE (FyPP),35 the PHYTOCHROMEASSOCIATED PROTEIN PHOSPHATASE 5 (PAPP5) 36 and the PHYTOCHROME-ASSOCIATED PROTEIN PHOSPHATASE TYPE2C (PAPP2C).37 Phosphorylation of phyA has been shown to affect phyA signaling in different ways. For example, it has been documented that phosphorylated phyA preferentially associates with the COP1/SPA1 complex in the nucleus whereas the underphosphorylated form of phyA is protected by FHY3 and FHY1 from being recognized by the COP1/SPA1 complex.26 In general, this and other findings37 suggest that phosphorylation of phyA decreases, whereas dephosphorylation enhances the flux of signaling and thereby photoresponsiveness.36,38,39 PhyA of nuclear localization also initiates a recently discovered signaling pathway that involves physical interaction of this photoreceptor with members of the subfamily of bHLH transcription factors, the phytochrome interacting factors (PIFs). These transcription factors have been shown to act downstream of phyA and/or B mainly as negative components of various processes in de-etiolation.15,40,41 Mutations in their genes result in defective light-mediated responses; multiple PIF knockout plants exhibit even a COP-like phenotype.42 The physical interaction of phy-s with PIF proteins leads to the phosphorylation and degradation of these proteins and promotes turnover of phytochromes, thus provides a dual mechanism for regulating plant development.43,44 Comparative binding affinity studies with different members of the bHLH family suggests that PIF1 represents a major target for phyA Pfr-mediated regulation.45 Additionally, characterization of the eid1 mutant (empfindlicher im dunkelroten Licht 1) points to a third mode of action of phyA.46,47 This F-box protein is specific for phyA light signaling and part of a SCF complex,48 which is supposed to target a so far unknown phyA signaling component toward degradation. In contrast to SPA1, EID1 has high specificity for phyA HIR responses and almost no function in VLFR.49

PhyA Structure-Function Relations The overall domain structure of phyA is very similar to that of other members of the photoreceptor family. The N-terminal part consists of the N-terminal extension (NTE), PER, ARNT and SIM (PAS), cGMP phosphodiesterase, adenylate cyclase, FhlA (GAF) and phytochrome-specific GAF-related (PHY) domains and is responsible for defining the light sensing characteristics of the phytochromes.50,51 This region is homologous with the photosensory core of prokaryotic phytochromes, whose high-resolution structure has already been solved.52 It is necessary for photoreversibility and exhibits the full phyB activity when fused to a dimerizing domain and NLS.53 The C-terminal region of plant phytochromes comprises two PAS and a HKRD domain; the latter can be divided into the His kinase and ATPase domains. The C-terminal part contains sequences necessary for dimerization, nuclear translocation and for modulating phytochrome signaling.51 Within the NTE region the first 70 amino acids are important for the spectral integrity of phyA. Deletion or substitution of the serine-rich N-terminal stretch of oat phyA (aa 6–12) produced hyperactive photoreceptor in transgenic tobacco.54 Serine residues in this region are phosphorylated in vitro and in vivo.55 Arabidopsis PHYA with the corresponding amino acids deleted showed normal responses to pulses of FR light but impaired responses to cFR.56 The mutated phyA photoreceptor was less stable in cR or cFR light, which is in good agreement with the hypothesis that phyA turnover is regulated by phosphorylation. Mateos et al.57 reported that a constitutively nuclear localized fusion protein containing the 595 amino acid N-terminal fragment of oat phyA fused to the β-glucoronidase (GUS) reporter is light-stable and mediates VLFR but not HIR. In a recent publication Wolf et al.58 showed that the N-terminal 686 aa fragment of the Arabidopsis PHYA is not functional, either in nuclear VLFR, or in FR-HIR. The truncated phyA is degraded with similar kinetics in the nucleus and in the cytoplasm but more slowly than PHYA-YFP. When the same fragment carried only the dimerization domain, it retained the light-induced nuclear translocation and degradation. This means that the N-terminal fragment of phyA carries the recognition sequences necessary for the nuclear import and proteasomic degradation of phyA. Even a shorter (1–406 aa) fragment of the phyA photoreceptor showed light-induced and FHY1 dependent nuclear import in an in vitro assay system.59 Sequence alignments of the photosensory cores of plant and cyanobacterial phytochromes highlight sites of sequence differences that may have important roles in the functional divergence of phyA and phyB.60 In the case of phyA these sites occur in the PAS-GAF domains and are very close to known mutations. The PAS domain site D108T has a loss-of function mutation in oat phyA,61 and E121P is two residues away from an Arabidopsis mutant with reduced protein stability.62 Residues in the GAF domain might affect the light-sensing specificity of phyA. One site identified in the PHY region (K528G) is located in the tongue region that closes the chromophore pocket and stabilizes Pfr.52 Most of these amino acid




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substitutions are predicted to affect charge distribution within phyA and thus may influence the protein-chromophore interaction and/or the interaction of the photoreceptor with other proteins. Conclusions Phytochrome A mediates VLFR and FR-HIR responses in plants. At molecular level it was shown that phyA Pfr is rapidly degraded and that the phyA Pfr form is imported into the nuclei. Nuclear import of phyA is mediated by the FHY1/FHL proteins. In general, FR responsiveness derives from nuclear and cytoplasmic branches of phyA-controlled signaling cascades and the flux of signaling is regulated by the phosphorylation status. In addition to FHY1/FHL, several additional components acting References 1.

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downstream of phyA have been identified, but their precise molecular functions, sites of action and hierarchical relations are not yet well established. The basic structure of phyA and other phy-s does not explain the unique functional features of phyA.63 Recently phyA and phyB sequences from diverse plant species have been compared60 and amino-acid substitutions, presumed to be important for phyA evolution, were identified. These substitutions are localized in the N-terminal region and two of them are mapped in the light-sensing knot. However, it remains to be elucidated whether these specific changes indeed provide an explanation for the modified light sensing and functionality of phyA. Acknowledgments

Work of S.K. is supported by DFG (SFB592).

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