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First published online April 29, 2009; 10.1104/pp.109.135988 Plant Physiology 150:1297-1309 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
The Histidine Kinase-Related Domain of Arabidopsis Phytochrome A Controls the Spectral Sensitivity and the Subcellular Distribution of the Photoreceptor1,[W],[OA]Albert-Ludwigs-Universität Freiburg, Institut für Biologie 2/Botanik, 79104 Freiburg, Germany
Phytochrome A (phyA) is the primary photoreceptor for sensing extremely low amounts of light and for mediating various far-red light-induced responses in higher plants. Translocation from the cytosol to the nucleus is an essential step in phyA signal transduction. EID1 (for EMPFINDLICHER IM DUNKELROTEN LICHT1) is an F-box protein that functions as a negative regulator in far-red light signaling downstream of the phyA in Arabidopsis (Arabidopsis thaliana). To identify factors involved in EID1-dependent light signal transduction, pools of ethylmethylsulfonate-treated eid1-3 seeds were screened for seedlings that suppress the hypersensitive phenotype of the mutant. The phenotype of the suppressor mutant presented here is caused by a missense mutation in the PHYA gene that leads to an amino acid transition in its histidine kinase-related domain. The novel phyA-402 allele alters the spectral sensitivity and the persistence of far-red light-induced high-irradiance responses. The strong eid1-3 suppressor phenotype of phyA-402 contrasts with the moderate phenotype observed when phyA-402 is introgressed into the wild-type background, which indicates that the mutation mainly alters functions in an EID1-dependent signaling cascade. The mutation specifically inhibits nuclear accumulation of the photoreceptor molecule upon red light irradiation, even though it still interacts with FHY1 (for far-red long hypocotyl 1) and FHL (for FHY1-like protein), two factors that are essential for nuclear accumulation of phyA. Degradation of the mutated phyA is unaltered even under light conditions that inhibit its nuclear accumulation, indicating that phyA degradation may occur mostly in the cytoplasm.
Light is an important exogenous factor that is essential for the survival of plants in their natural environment. To sense light quality, intensity, and direction, plants have evolved several classes of photoreceptors, including cryptochromes, phototropins, and phytochromes (Chen et al., 2004  ; Franklin et al., 2005). All phytochromes utilize covalently attached bilin chromophores, which enable light absorption and reversible photoconversion between two stable forms, Pr and Pfr. Upon absorption of red light, the Pr conformation converts to the Pfr conformation, and absorption of far-red light reconverts Pfr back to Pr. Phytochrome A (phyA), like most phytochromes, also exhibits dark reversion, in which the Pfr form reverts back to the more stable Pr conformation in the absence of light. Plant phytochromes are synthesized in the Pr conformation in the dark and remain inactive until light absorption, at which point the bioactive Pfr translocates into the nucleus (Møller et al., 2002; Chen et al., 2004; Rockwell et al., 2006).
Phytochromes constitute a small protein family in all analyzed plant species (Mathews and Sharrock, 1997
The subcellular partitioning of phytochromes in higher plants is regulated by light. The inactive Pr form accumulates in the cytoplasm, whereas the photoconverted Pfr form accumulates in the nucleus (Sakamoto and Nagatani, 1996
All phytochromes share a common architecture consisting of an N-terminal photosensory region, which binds the chromophore, and a C-terminal regulatory domain (CTD; Chen et al., 2004
The CTDs of all known phytochromes carry a His kinase-related domain (HKRD; Schneider-Poetsch et al., 1991
EID1 (for EMPFINDLICHER IM DUNKELROTEN LICHT1) is an F-box protein that functions as a negative regulator in phyA-specific light signaling (Büche et al., 2000 To identify factors involved in EID1-dependent light signaling, pools of ethylmethylsulfonate-treated eid1-3 seeds were screened for seedlings with a wild-type-like phenotype under weak far-red light, which normally induces a strong photomorphogenic response in the background line. Lines that exhibited a stable phenotype in a second round of screening were named rei for revertants of eid1-3. The phenotype of one of the rei mutants is presented here and is caused by a missense mutation in the HKRD of the phyA photoreceptor. This novel phyA allele shifts the action spectrum and persistence of HIR, making it uniquely useful among phyA alleles for understanding transduction mechanisms. Yellow fluorescent protein (YFP) fusion protein observations further indicate that the mutation causes an inhibition of nuclear accumulation under light conditions that normally adjust high levels of Pfr in the cytoplasm. Thus, our studies provide new insights into the functional role of the HKRD for the regulation of photomorphogenesis in higher plants.
Isolation of the phyA-402 Mutant To search for genes that are involved in EID1-dependent light signaling, suppressor mutants were screened from pools of ethylmethylsulfonate-treated eid1-3 seeds in a Wassilewskija background that exhibited reduced far-red light sensitivity compared with the hypersensitive mutant. One of the rei revertant lines was chosen for further analysis because of its strong suppressor phenotype. Under selective light conditions, F2 seedlings of backcrosses with eid1-3 exhibited a clear 3:1 (183:64) segregation for the Eid1-3 phenotype. Thus, the suppressor mutation behaved like a recessive monogenic locus. The mutant was crossed with the eid1-6 allele in a Columbia background for mapping. A tight linkage was detected to different markers that localize close to the PHYA gene on chromosome 1 (Supplemental Fig. S1A). This finding strongly suggested that the suppressor phenotype is caused by a mutation in the PHYA gene. This hypothesis was confirmed by experiments with rei eid1-3 mutants that had been transformed with a ProPHYA:PHYA:YFP construct; expression of the phyA-YFP fusion protein in the double mutant reinstated the initial hypersensitive Eid1-3 phenotype (Supplemental Fig. S1B). Sequence analysis of phyA in the rei mutant revealed a single C-to-T transition that leads to the exchange of Leu-946 for a Phe residue in the HA subdomain of the HKRD of PHYA (Fig. 1 ). The sequence polymorphism was used to create a cleavable amplified polymorphic sequence marker. No recombination was detected between the cleavable amplified polymorphic sequence marker and the mutation after the analysis of 90 F2 plants that displayed the revertant phenotype.
Both the Leu-946 residue and the surrounding sequence are highly conserved throughout plant evolution and could be identified in phytochrome sequences derived from mosses, liverworts, and green algae (Supplemental Fig. S2). The conserved Leu was only replaced by Val or Ile residues in some sequences belonging to the B and C subfamilies of higher plant phytochromes. Sequence alignments with the HA subdomain of Arabidopsis phyA, a fern phytochrome, and bacterial His receptor kinases with known structure exhibited a high degree of conservation for large aliphatic amino acid residues at the position of the mutated Leu (Fig. 1). When compared with the published structure of the HA subdomain of the osmoregulator EnvZ and the chemotaxis sensor CheA, the mutation falls into the hydrophobic core that stabilizes the HA loop structure formed by two  -helices. The new phyA allele was named phyA-402 according to the rules published by Quail et al. (1994).
Seedlings of the phyA-402 eid1-3 double mutant and the phyA-402 single mutant exhibited a phenotype that was nearly indistinguishable from the wild type under the weak far-red light used for screening, whereas eid1-3 seedlings showed a hypersensitive response (Fig. 2 ). No difference in seedling phenotypes was observed between the wild type, phyA-402, eid1-3, and phyA-402 eid1-3 under strong, saturating far-red light (Fig. 2). Thus, phyA-402 seedlings clearly differ from the phyA-211 knockout mutant that does not respond to far-red light. All tested lines exhibited very similar phenotypes under strong continuous red or white light and remained etiolated in darkness (Fig. 2). These data indicate that the phyA-402 allele encodes for a partially active photoreceptor that alters far-red light signaling.
The eid1-3 mutant displays a hypersensitive phenotype under continuous far-red light and extremely weak red light (Büche et al., 2000 ; Dieterle et al., 2001; Marrocco et al., 2006). To analyze whether the chosen revertant line suppresses the hypersensitive Eid1-3 phenotype under both light qualities, fluence rate response curves were measured for hypocotyl elongation and cotyledon opening (Fig. 3
). The phyA-402 mutation clearly suppressed the hypersensitive Eid1-3 phenotype under both light conditions. Interestingly, no differences in red and far-red light sensitivity were observed for inhibition of hypocotyl elongation between phyA-402 eid1-3, phyA-402, and the wild type (Fig. 3, A and B). The phyA-402 mutation also clearly reduced the effect of eid1-3 on cotyledon opening under continuous red and far-red light, even though suppression is not complete. The phyA-402 mutation also exhibited a weak hyposensitivity for cotyledon opening in the wild-type background under both light qualities tested (Fig. 3, C and D).
Up-regulation of anthocyanin accumulation is another far-red HIR in Arabidopsis (Kunkel et al., 1996 ). The phyA-402 allele also functions as a suppressor of eid1-3 with respect to anthocyanin biosynthesis. The mutated photoreceptor did not cause a reduction of anthocyanin accumulation in an EID1 wild-type or eid1-3 mutant background (Fig. 3E).
Because EID1 functions as an important negative regulator in far-red HIR (Büche et al., 2000 Wild-type seedlings exhibited a typical HIR action spectrum, with maximum light sensitivity at 720 nm (Fig. 4A). The maximum of the phyA-402 action spectrum is shifted from 720 to 716 nm, as light sensitivity is reduced at wavelengths above 716 nm. Thus, the HIR action spectrum of the mutant clearly differs from that of the wild type.
The release of HIR and the resulting hypocotyl elongation normally depend on strong continuous light irradiation and normally stop when dark phases are interposed (Büche et al., 2000 ). Seedlings were treated with multiple and strong 2.5-min far-red light pulses that were interrupted by dark phases of variable lengths. Decay kinetics were followed to estimate the apparent persistence of HIR signals installed by the light pulses.
The persistence of the far-red light signal in wild-type seedlings is about 9.1 min, and the HIR seemed to be nonexistent when dark phases exceeded 30 min (Fig. 4B). The phyA-402 line exhibited a reduction in the apparent half-life of the far-red light signal to about 6.2 min and a complete loss of HIR at about 15 min (Fig. 4B). The residual reduction of hypocotyl elongation remaining at prolonged dark phases has commonly been interpreted as a VLFR that does not depend on continuous light irradiation (Yanovsky et al., 1997 Comparable results were obtained for decay kinetics determined for cotyledon opening. The apparent half-life of the far-red light signal was shifted from 8.2 min in the wild type to 5.6 min in phyA-402 (Fig. 4C). Again, a residual difference in cotyledon opening was detected with prolonged dark phases between the wild type and phyA-402, indicative of a reduced VLFR in the mutant.
The observed weak loss-of-function phenotype of phyA-402 might be caused by a reduced level of the mutated phyA, an increased Pfr degradation rate, or a faster dark reversion from active Pfr to inactive Pr. To test for putative differences in phyA accumulation, the level of photoreversible phytochrome was measured with a dual wavelength ratio spectrophotometer (ratio-spec) in 4-d-old, dark-grown seedlings. No significant difference (P < 0.05) in phyA levels was detected between etiolated wild-type and phyA-402 seedlings (Table I ). Comparable results were also obtained by immunoblot analyses with protein extracts from etiolated seedlings (Fig. 5A ).
The phyA protein is typically degraded within the cell upon Pfr formation. No difference in wild-type phyA and phyA-402 protein degradation was detected upon irradiation of 4-d-old, dark-grown seedlings with strong continuous red and far-red light (Fig. 5, A and B). The levels of both proteins decreased quite rapidly under continuous red light and fell below the detection level by immunoblot analysis by 120 min (Fig. 5A). PhyA and phyA-402 degradation kinetics under continuous far-red light were followed by ratio-spec measurements. The degradation rate was slower in plants grown under far-red light because of the low Pfr levels caused by photoconversion by far-red light, and measurable amounts of phyA still remained detectable after 12 h of irradiation (Fig. 5B).
Pfr-A also shows dark reversion in many dicotyledonous plant species and some Arabidopsis ecotypes (Eichenberg et al., 2000
To study the subcellular localization of the mutated photoreceptor, ProPHYA:PHYA-402:YFP constructs were introduced into phyA-211 loss-of-function mutants. Whereas phyA-211 remained completely etiolated under continuous strong far-red light, transgenic phyA-211 seedlings expressing phyA-402-YFP exhibited a clear photomorphogenic phenotype similar to wild-type and phyA-211 plants expressing wild-type phyA-YFP (Supplemental Fig. S4). Therefore, the introduced PHYA-402:YFP construct can rescue the loss-of-function phenotype of phyA-211 and encodes for a functional photoreceptor molecule. The subcellular localization of the mutated YFP fusion protein was compared with a transgenic phyA-211 line that has been transformed with a wild-type ProPHYA:PHYA:YFP construct (Kircher et al., 2002
Similar to published results (Kim et al., 2000
Compared with the large, stable, and nearly immobile lNUS, early nuclear speckles (eNUS) are slightly smaller, very mobile, and appear quite rapidly upon red or white light irradiation of etiolated seedlings (Kircher et al., 2002 ; Chen et al., 2003; Bauer et al., 2004; Dieterle et al., 2005). Formation of eNUS can most easily be followed when seedlings are preirradiated with 8 to 10 h of far-red light before transfer to white light, because the pretreatment causes an enrichment of phyA in the nucleus. In the phyA-402-YFP- and phyA-YFP-expressing lines, a rapid aggregation of eNUS was observed that started between 2 and 10 min after the onset of microscopic light (Fig. 6, E, E', F, and F'). Etiolated seedlings were also transferred to strong red light to study the formation of sequestered areas of phyA-YFP and phyA-402-YFP (SAP). Rapid aggregation of SAP was observed in transgenic phyA-211 lines expressing both wild-type phyA-YFP and phyA-402-YFP starting at about 2 to 5 min after transfer to red light (Fig. 6, G, G', H, and H'). SAP disappeared in all tested lines after 30 min of continuous irradiation (Supplemental Fig. S4). These microscopic studies demonstrate that phyA-402-YFP exhibits normal cytoplasmic localization in darkness, normal nuclear accumulation under far-red light, and normal eNUS, lNUS, and SAP formation.
Similar to published results (Kim et al., 2000 To test whether red light preirradiation also blocks far-red light-induced nuclear accumulation of phyA-402-YFP, we applied a light treatment consisting of 20 min of strong red light followed by 20 min of strong far-red light. Etiolated seedlings were irradiated with four cycles of red/far-red light, and the subcellular localization of the YFP fusion proteins was analyzed at the end of the last far-red light pulse. Strong nuclear YFP fluorescence was observed in preirradiated transgenic phyA-211 lines expressing wild-type phyA-YFP, and red light-induced SAP were not detected (Fig. 6, I and I'). Thus, phyA-YFP exhibited a subcellular localization similar to seedlings treated with continuous far-red light alone (Fig. 6, C and C'). In striking contrast, phyA-402-YFP did not become visible inside the nucleus under the red/far-red light pulse treatment, although it did agglomerate at the nuclear envelope to some extent (Fig. 6, J and J'). Similar to phyA-YFP, SAP could no longer be observed after the multiple pulse treatment. These data demonstrate that a red light pretreatment can inhibit far-red light-triggered nuclear accumulation of phyA-402-YFP and that the red light-induced inhibition of phyA-402 nuclear accumulation does not depend on SAP formation.
To test whether impaired nuclear accumulation of phyA-402-YFP is caused by a reduced binding to the transport facilitators FHY1 and FHL, an established yeast two-hybrid assay was used (Hiltbrunner et al., 2005 Cell growth on selective medium was only observed with yeast strains that carry corresponding FHY1 or FHL and PHYA or PHYA-402 constructs. All transformed yeast strains were able to grow on L-W- medium, which only selects for the presence of two-hybrid vectors (Fig. 7 ). Interaction between FHY1 or FHL and the two phyA versions was strictly dependent on the presence of PCB and red light, demonstrating that Pfr is the state that interacts with both FHY1 and FHL. Both wild-type PHYA and mutant PHYA-402 strains grew equally well when combined with either FHY1 or FHL, indicating that the loss of nuclear accumulation under red light conditions is not likely attributable to a general loss of interaction between the transport facilitators and the Pfr form of phyA-402.
This study describes the identification and characterization of a weak loss-of-function phyA allele, phyA-402, that suppresses the far-red light-hypersensitive phenotype of eid1-3 and exhibits a strong inhibition of red light-induced nuclear transport in dark-grown seedlings. The phenotype is caused by the mutation L946F at a highly conserved residue in the HA subdomain of phyA, as determined by mapping analyses, by the rescue of the Eid1-hypersensitive phenotype by transformation with a functional ProPHYA:PHYA:YFP construct, and by sequencing of the respective gene (Fig. 1; Supplemental Figs. S1 and S2).
Whereas bacterial phytochromes function as light-regulated His kinases (Parkinson, 1993
Several of our observations clearly indicate that the mutation in the HA subdomain has very severe influences on light signal transduction events related to EID1, which functions as an important negative regulator in phyA-dependent HIR signaling (Büche et al., 2000
A unique feature of the eid1 mutant is a shift in the peak of the action spectra of phyA-mediated hypocotyl elongation, from 716 nm to 660 nm (i.e. from the far-red light to the red light part of the spectrum; Dieterle et al., 2001
Nevertheless, the most severe effect on the phyA-402 loss-of-function phenotype has been observed in the far-red light spectrum, and in that very spectrum the phyA-402-YFP fusion protein did not show detectable alterations in nuclear accumulation. Furthermore, the mutated photoreceptor also strongly suppressed the effect of eid1-3 under continuous far-red light. These data indicate that the effect of the phyA-402 mutation cannot solely be explained by an altered nuclear accumulation. The mutation leads to an exchange of a conserved amino acid in a protein domain that is thought to be important for both protein-protein interactions and phosphotransfer in bacterial His kinases, including prokaryotic phytochromes (Yeh and Lagarias, 1998
This assumption is further confirmed by the observed decrease in signal persistence in phyA-402. The decrease in signal persistence might look weak, but one has to take into account that full expression of HIR normally depends on continuous far-red light irradiation for several hours (Mancinelli, 1994
Experiments with spa1 (Hoecker et al., 1998
Our data further indicate that the mutation in the HKRD does not alter light-induced proteolysis of the photoreceptor, since analyses of degradation kinetics did not exhibit any difference between phyA-402 and wild-type phyA under all light conditions tested (Fig. 5). While red light induces phyA-YFP localization to the nucleus, microscopic studies revealed that nuclear accumulation of phyA-402-YFP is strongly inhibited, although total protein levels appear to be unadulterated (Fig. 6). The lack of differences in red light-induced proteolysis indicates that either phyA degradation takes place nearly exclusively in the cytoplasm or that cytoplasmic and nuclear degradation counterbalance each other and function with comparable efficiency under this light condition. This finding is in agreement with results obtained in fhy1 fhl double mutants, in which phyA degradation remains unaltered even though nuclear accumulation is blocked (Rösler et al., 2007
The mutation in the HKRD did not lead to detectable changes in speckle formation. Microscopic studies did not reveal any changes in the formation of cytoplasmic SAP, eNUS, or lNUS between wild-type phyA-YFP and phyA-402-YFP (Fig. 6). This finding differs from results obtained with other phyA loss-of-function alleles that carry missense mutations in the PAS2 domain and are impaired in NUS formation (Kircher et al., 2002
The most severe effect on subcellular localization has been observed upon red light irradiation of etiolated seedlings, which reveals a defect in the nuclear accumulation of phyA-402-YFP (Fig. 6; Supplemental Fig. S5). The Pfr form of the mutated photoreceptor is able to interact with FHY1 and FHL in yeast, similar to the wild-type molecule (Fig. 7). Therefore, the observed inhibition of phyA-402-YFP nuclear accumulation is not likely due to the loss of interaction with the two proteins that are essential for nuclear accumulation of phyA (Hiltbrunner et al., 2005 Models for the observed inhibition of nuclear accumulation of phyA-402 have to explain why this effect is most severe under red light treatments, whereas no differences have been observed under continuous far-red light. The observed block in red light-induced nuclear accumulation cannot fully be explained by reduced affinities to transport facilitators, because such a reduction would become most effective under low Pfr levels adjusted by far-red light but should be less important at high Pfr levels induced by red light.
One such process might be SAP formation, because it only occurs in etiolated seedlings that accumulate high levels of Pr-A, which are then photoconverted nearly completely to Pfr-A upon red light irradiation (McCurdy and Pratt, 1986a Another major difference between red and far-red light-treated seedlings occurs in the ratio Pfr/Ptot in the cell (approximately 0.87 in red light compared with approximately 0.05 in far-red light). An increased affinity of the Pfr form of phyA-402 toward FHY1 and FHL may result in a block in nuclear accumulation simply due to a reduction in the release from transport facilitators in the nucleus, thus decreasing further import. Deprivation of transport facilitators would be most effective under red light, because high levels of Pfr are formed and turnover from Pfr to Pr is low. The release process might be less important under far-red light, because Pfr is efficiently photoconverted back to Pr and, thus, a sufficient amount of transport facilitator molecules might be available in nuclear transport. However, the proposed delayed-release mechanism cannot fully explain why phyA-402-YFP nuclear accumulation is also blocked under repetitive red/far-red light treatments, because far-red light-induced conversion should detach the Pr molecule from its transport facilitators.
An alternative and more complex explanation for the observed effects of phyA-402 on nuclear localization and light responses involves several aspects of phyA function: the observed Pfr-stimulated autophosphorylation activity of phyA (Yeh and Lagarias, 1998
An enhanced phosphorylation state of phyA-402 explains the moderate reduction in physiological activity of the mutant in the wild-type background, which seems to mimic the effect seen with papp5 mutants (Ryu et al., 2005
To conclude, the strong Eid1-suppressor phenotype of phyA-402 clearly indicates that the HKRD of phyA has a severe influence on far-red HIR, since EID1 specifically functions as a negative regulator of this response mode but does not influence VLFR (Zhou et al., 2002
Plant Material and Mutagenesis
For genetic crossing and physiological analyses, the following ecotypes and photomorphogenic mutants of Arabidopsis (Arabidopsis thaliana) were used: Wassilewskija wild type, eid1-3 (ecotype Wassilewskija; Büche et al., 2000
Seeds were sown on four layers of Schleicher & Schüll 595 filter paper circles as described elsewhere (Büche et al., 2000
For hypocotyl length measurements and determination of cotyledon opening, seedlings were spread on water agar and photographed together with a size standard using a Zeiss Stemi SV6 binocular supplemented with a Zeiss AxioCam MRc 5 digital camera. Hypocotyl lengths and cotyledon angles were determined using ImageJ software (http://rsb.info.nih.gov/ij/). All data represent means ± SE of at least 40 seedlings analyzed in at least two independent experiments. Anthocyanin was extracted from 50 seedlings, and anthocyanin content was determined spectroscopically as described by Büche et al. (2000)
Revertant lines were crossed with eid1-6 in a Columbia background for mapping analyses. The phyA-402 mutant was mapped using PCR-based simple sequence length polymorphisms and cleavable amplified polymorphic sequence markers (Konieczny and Ausubel, 1993
Extraction of crude proteins and protein assays were performed as described by Dieterle et al. (2005)
Photoreversible phyA was measured in a dual wavelength ratio spectrophotometer at 5°C as described by Dieterle et al. (2005)
Construction of the ProPHYA:PHYA:YFP chimeric gene and isolation of transgenic lines carrying this gene have been described previously (Kircher et al., 2002
For epifluorescence and light microscopy, seedlings were transferred to glass slides under dim-green safelight and analyzed with an Axioskop microscope (Zeiss). The nuclei were located and searched under dim-green safelight, and except for the analysis of eNUS, only the first pictures taken with a digital Axiocam camera system (Zeiss) are presented. Excitation and detection of the fluorophore YFP was performed with a YFP-specific filter set (AHF Analysentechnik).
Yeast two-hybrid interaction assays and application of PCBs were done as described by Hiltbrunner et al. (2005)
The following materials are available in the online version of this article.
We thank Martina Krenz for her helpful technical assistance and Anita K. Snyder for her helpful comments on the manuscript. Received January 28, 2009; accepted April 26, 2009; published April 29, 2009.
1 This work was supported by the Deutsch Forschungsgemeinschaft (grant no. KR2020/2–3, "Analysis of Phytochrome A-Dependent Light Signalling in Arabidopsis thaliana") and the Human Frontier Science Program (postdoctoral fellowship no. LT 0063/2003–6 to A.H.). 
2 Present address: Umeå Plant Science Center, Department of Plant Physiology, Umeå University, SE–901 87 Umeå, Sweden. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Thomas Kretsch (thomas.kretsch{at}biologie.uni-freiburg.de).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.109.135988 * Corresponding author; e-mail thomas.kretsch{at}biologie.uni-freiburg.de.
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ABSTRACT
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max = 650 nm) and far-red light fields (20 µmol m–2 s–1;