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First published online April 4, 2008; 10.1104/pp.108.118166 Plant Physiology 147:661-671 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
PHYTOCHROME KINASE SUBSTRATE4 Modulates Phytochrome-Mediated Control of Hypocotyl Growth Orientation1,[W],[OA]Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland (I.S., C.K., C.F.); and IFEVA, Facultad de Agronomía, Universidad de Buenos Aires and Consejo Nacional de Investigaciones Científicas y Técnicas, 1417-Buenos Aires, Argentina (H.E.B., J.J.C.)
Gravity and light are major factors shaping plant growth. Light perceived by phytochromes leads to seedling deetiolation, which includes the deviation from vertical hypocotyl growth and promotes hypocotyl phototropism. These light responses enhance survival of young seedlings during their emergence from the soil. The PHYTOCHROME KINASE SUBSTRATE (PKS) family is composed of four members in Arabidopsis (Arabidopsis thaliana): PKS1 to PKS4. Here we show that PKS4 is a negative regulator of both phytochrome A- and B-mediated inhibition of hypocotyl growth and promotion of cotyledon unfolding. Most prominently, pks4 mutants show abnormal phytochrome-modulated hypocotyl growth orientation. In dark-grown seedlings hypocotyls change from the original orientation defined by seed position to the upright orientation defined by gravity and light reduces the magnitude of this shift. In older seedlings with the hypocotyls already oriented by gravity, light promotes the deviation from vertical orientation. Based on the characterization of pks4 mutants we propose that PKS4 inhibits changes in growth orientation under red or far-red light. Our data suggest that in these light conditions PKS4 acts as an inhibitor of asymmetric growth. This hypothesis is supported by the phenotype of PKS4 overexpressers. Together with previous findings, these results indicate that the PKS family plays important functions during light-regulated tropic growth responses.
Plants have evolved sensitive mechanisms to detect and respond to their environment. Among the numerous environmental stimuli plants are particularly sensitive to light (Chen et al., 2004  ) and gravity (Esmon et al., 2005). While gravity is constant in intensity and is unidirectional, light is highly variable in direction, intensity, spectral composition, and duration (photoperiod). Our understanding of the molecular basis of light and gravity perception has considerably advanced over the past decades, however, we still know little about the mechanisms enabling plants to integrate all this information.
Light is critical for plants because they depend on it as a source of energy. To adjust growth and development to the environmental conditions plants sense UV-B, blue, red, and far-red signals (Chen et al., 2004
The perception of gravity typically directs root growth downwards while shoots grow upwards. These tropic growth responses maximize the acquisition of essential resources such as water, minerals, and light (Blancaflor and Masson, 2003
Light perceived by the phytochromes and the blue-light receptor cryptochromes induces the deviation from hypocotyl vertical growth (Poppe et al., 1996
Although initially identified for their function in phytochrome signaling (Fankhauser et al., 1999
The name PKS4 (At5g04190) is based on homology with the other members of the PKS gene family, but the ability to interact with phytochrome had not been tested previously (Lariguet et al., 2006 ). Here we show that, similarly to PKS1 and PKS2, PKS4 interacts with phyA and phyB in yeast two-hybrid analysis and in vitro pull-down assays (Supplemental Fig. S1).
To investigate whether the expression of PKS4 is regulated by light during deetiolation, 4-d-old seedlings were transferred from darkness to different light conditions (Supplemental Fig. S2). Red and blue light led to a rapid and transient decrease in transcript abundance whereas far-red light led to a slower and progressive decline of PKS4 mRNA levels (Supplemental Fig. S2). The reduced responses of the PKS4 mRNA level in the phyA mutant demonstrated a role for phyA in the regulation of PKS4 transcript abundance by light (Supplemental Fig. S2). PKS1 and PKS2 have distinct expression patterns in young seedlings, with PKS1 being expressed in the elongation zone of both hypocotyls and roots, and PKS2 being primarily expressed in the cotyledons (Lariguet et al., 2003
PKS4 Regulates VLFR, LFR, and HIR of Hypocotyl Growth
PKS1 and PKS2 negatively regulate one specific branch of phyA signaling, the VLFR (Lariguet et al., 2003
The analysis of double and triple mutants indicated a complex set of genetic interactions between the three members of the PKS gene family. We confirmed the reversion of the pks1 and pks2 mutant phenotypes in the pks1pks2 double mutant (Fig. 2; Lariguet et al., 2003 ). Generally speaking we observed no additive effects of the different pks phenotypes and the multiple mutants including pks4 essentially looked like the pks4 single mutant (Fig. 2). While the pks4 mutants showed enhanced VLFR and LFR, PKS4 overexpressing seedlings showed reduced VLFR and LFR (Fig. 3
). Double mutants between pks4 and phyA or phyB showed that the photoreceptor mutations were epistatic to the pks4 mutation under conditions where phyA or phyB mediates the light responses (Fig. 3). We conclude that PKS4 regulates phyA- and phyB-mediated deetiolation.
PKS4 Controls Light-Mediated Deviation from Vertical Hypocotyl Growth
The previously identified function of the PKS genes during phototropism prompted us to analyze the possible function of these genes during another light-controlled tropic response: phytochrome-mediated deviation from vertical hypocotyl growth (Poppe et al., 1996
Light Control of Hypocotyl Growth Orientation Depends on the Developmental Context Negative gravitropism of dark-grown hypocotyls is not simply a passive default state. To grow against the gravity vector, the hypocotyl must reorient, unless if by chance the seed position already aligns the hypocotyl growth axis with the gravity vector. In Figure 5A , the original orientation of the radicle and of the hypocotyl of a dark-grown seedling is essentially horizontal. After emergence, the root rapidly shifted the direction of growth following the gravity vector. The hypocotyl also changed the direction of growth very close to its point of emergence from the seed, adopting a near vertical position. If the seedling is exposed to light at early stages of development, the growth of the hypocotyl adopts a direction largely influenced by seed position (Fig. 5B). In Figure 5B the radicle emerged toward the right and the hypocotyl grew toward the opposite side. The effect of light can thus be seen as an inhibition of the hypocotyl asymmetric growth response required for gravitropism. To test this hypothesis we positioned seeds with the embryo (longest axis) oriented horizontally and the micropyl either toward the right- or the left-hand side. The micropyl is the place of radicle emergence and the shoot apical meristem is located at the opposite extreme of the longitudinal axis of the seed. We then recorded the final growth orientation of those two groups of seedlings separately after 4 d growth in continuous red light (Fig. 5C). The final growth orientation was largely influenced by the initial seed position: if the micropyl was toward the right, the hypocotyl grew toward the left and vice versa (Fig. 5C). Statistical analysis (contingency test) indicates that hypocotyl orientation is very significantly affected by seed position (P < 2.77 x 10–11).
When light was applied after a period of growth in darkness that allowed the hypocotyl to initiate negative gravitropism it induced bending of the hypocotyl at the level of the elongation zone leading to deviation from vertical growth (Fig. 5D). Thus, during early stages of hypocotyl elongation in darkness, gravity perception promoted asymmetric growth and vertically oriented the hypocotyl (Fig. 5A). At later stages light promoted asymmetric growth to cause deviation from vertical growth of a hypocotyl that was growing against the gravity vector prior to the light treatment (Fig. 5D).
Because the processes involved in light-mediated randomization of hypocotyl growth depend on the developmental context, we investigated the role of PKS4 in hypocotyl growth orientation in seedlings grown for various periods of time in darkness prior to the light treatment. To specifically address phytochrome control of this response, seedlings were transferred to red or far-red light, and growth orientation was recorded after a total of 5 d (Fig. 6 ). In accordance with the observations described above (Fig. 4), pks4 seedlings exposed to light shortly after stratification showed reduced deviation from vertical growth compared to the wild type (Fig. 6). Conversely, when the seedlings were grown for 48 h in darkness prior to illumination the pks4 mutants displayed a larger deviation from vertical growth than the wild type (Fig. 6). The deviation from vertical-growth orientation declined after prolonged periods of growth in darkness presumably because once the hypocotyls were almost fully expanded a change in growth direction could no longer occur (Fig. 6). These experiments suggested apparently opposite roles for PKS4 depending on the time of growth in darkness prior to illumination (Fig. 6). However, in both cases, PKS4 can be viewed as a negative regulator of asymmetric growth (see Fig. 5).
This effect of PKS4 on light-mediated deviation from vertical growth was tested at different fluence rates and both with seedlings that were grown in the light from the time of germination and seedlings that were pretreated with a prolonged growth period in the dark (48 h). Almost irrespective of the fluence rate, pks4 mutants displayed a greater randomization of hypocotyl orientation when the light was applied after 2-d growth in the dark and a more vertical orientation when they were grown in the light from the time of germination (Fig. 7).
In far-red light, where phyA is the only photoreceptor significantly contributing to the deetiolation response, the epistatic relationship between pks4 and phyA is easy to interpret. phyA was epistatic over pks4 under all conditions clearly positioning PKS4 in the phyA signaling branch (Fig. 8
). In red light, multiple phytochromes participate to the light-induced randomization of hypocotyl orientation (Poppe et al., 1996
Overexpression of PKS4 Leads to Constitutive Randomization of Hypocotyl Growth Orientation Our results based on the phenotype of pks4 loss-of-function alleles suggested that PKS4 may be necessary to inhibit asymmetric growth during phytochrome modulation of growth orientation. It was thus of interest to determine the growth orientation phenotype of PKS4 overexpressing seedlings. In agreement with our hypothesis such seedlings displayed an exaggerated randomization of growth orientation in seedlings continuously grown in red and far-red light (Fig. 9, B and C ). Interestingly overexpression of PKS4 led to inhibition of negative gravitropism in etiolated hypocotyls (Fig. 9A).
Light Does Not Reduce the Gravi-Reorientation of Etiolated Hypocotyls Although generally presented as inhibition of gravitropism, the actual mechanism leading to phytochrome-mediated deviation from vertical hypocotyl growth remains unclear. We investigated whether in 2-d-old etiolated seedlings the light-induced deviation from vertical hypocotyl growth is due to an inhibition of gravitropism. Two-day-old dark-grown seedlings were rotated by 90° and growth reorientation followed by time-lapse imaging over the following 18 h either in darkness or in the presence of red light (Fig. 10 ). The hypocotyls similarly (P > 0.05) reoriented their growth in response to the gravitropic stimulation both in darkness and in red light. However, several light-grown seedlings changed their growth direction after the initial gravi-reorientation and the response was significantly more variable in red-light-grown seedlings than in darkness (P < 0.05; Fig. 10, A and B). This variability of the response in red light is presumably related to the one observed in vertically grown seedlings exposed to red light (Fig. 5D). Interestingly, pks4 seedlings gravistimulated in red light had an early response similar to the wild type but at later time points (after 5 h) there was a greatly enhanced response (P < 0.005; Fig. 10B). Conversely, in pks4 seedlings gravistimulated in the dark, the early gravitropic response was somewhat delayed but reached the same amplitude than in the wild type at later time points. In summary, in hypocotyls displaying negative gravitropism red light caused the deviation of hypocotyl growth direction but it did not reduce the response to gravity stimulation.
PKS1 was identified as a protein interacting with and being phosphorylated by phytochrome A in vitro (Fankhauser et al., 1999 ). Physiological studies have shown that PKS1 and PKS2 are required for normal phytochrome-mediated responses (Fankhauser et al., 1999; Lariguet et al., 2003; Khanna et al., 2006). Two additional PKS1-related proteins, PKS3 (At1g18810) and PKS4 (At5g04190), have been identified in Arabidopsis, and PKS-like genes are present in all angiosperms investigated so far (Lariguet et al., 2006). Present data show that among the tested PKS genes (pks3 insertion mutants are not available yet), PKS4 has the strongest effect on phytochrome-mediated inhibition of hypocotyl elongation and cotyledon opening (Figs. 2 and 3). The expression of PKS4:GUS in the hypocotyl elongation zone (Fig. 1) correlates with these physiological responses. Similarly to pks1 and pks2 mutants, pks4 mutants show exaggerated phyA-mediated VLFR (Fig. 2). In addition, and in contrast to PKS1 and PKS2 (Lariguet et al., 2003), PKS4 also negatively regulates the phyA-mediated HIR as well as the phyB-mediated LFR (Figs. 2 and 3).
The phenotypes of pks4, pks1, and pks2 are not additive (Fig. 2). A possible explanation for this finding is that for these light responses the PKS proteins work as complexes and elimination of a single member would disrupt their function. Indirect support for this hypothesis comes from a previous study showing that PKS1 and PKS2 interact in vitro (Lariguet et al., 2003
In addition to a role in the control of hypocotyl elongation and cotyledon opening we show that PKS4 also regulates phytochrome-mediated control of hypocotyl orientation (Figs. 4–10
When light is applied to dark-grown seedlings that have already initiated negative gravitropism it also leads to deviation from the vertical growth orientation (Fig. 5D). However, the underlying mechanism is different because rather than simply interrupting the gravitropic response and causing the newly emerged hypocotyl to follow the orientation dictated by seed position, light causes the reorientation of distant portions of the hypocotyl that had been previously gravity oriented (Fig. 5D). This change in hypocotyl orientation cannot be fully accounted for by red-light inhibition of the gravitropic response. Actually, when 2-d-old etiolated seedlings were rotated by 90° and reorientation of the hypocotyl monitored either in darkness or light, red light did not inhibit gravi-reorientation (Fig. 10). Interestingly in rice coleoptiles red light does not inhibit the gravitropic response either (Yoshihara and Iino, 2005 The developmental control of light-mediated hypocotyl growth orientation allows us to propose a mode of action for PKS4. Our data suggest that PKS4 is an inhibitor of asymmetric growth in red- or far-red-grown hypocotyls. When seedlings are subjected to light during the phase of asymmetric growth in the hypocotyl elongation zone, removing an inhibitor of asymmetric growth leads to straighter hypocotyls (Fig. 4). In contrast, if light is applied when hypocotyl growth orientation is already aligned with the gravity vector, removing PKS4 (a negative regulator of asymmetric growth) leads to a greater randomization of hypocotyl orientation (Fig. 6). This hypothesis is also consistent with the gravi-reorientation experiments where the pks4 mutant shows greater reorientation in red light (Fig. 10). Moreover the phenotype of the PKS4 overexpressing seedlings, which show enhanced randomization of hypocotyl orientation is also consistent with this idea (Fig. 9). Our data from the pks4 mutants show that if any, PKS4 has a reduced role in the dark, suggesting that in the wild-type PKS4 must somehow be activated by phytochrome (directly or indirectly) to control hypocotyl growth orientation. However, hypocotyls of PKS4 overexpressing seedlings already show a deviation from vertical growth in darkness indicating that elevated levels or ectopic expression of PKS4 leads to light-independent negative regulation of asymmetric growth (Fig. 9).
A simple interpretation of the pks4 loss-of-function mutant phenotype during the control of hypocotyl elongation and cotyledon opening indicates that PKS4 is a negative regulator of phytochrome signaling (Figs. 2 and 3). The simplest interpretation of the pks4 loss- and gain-of-function mutants during the control of hypocotyl growth orientation suggests that PKS4 acts a negative regulator of asymmetric growth (Figs. 4–9
The role of the PKS genes in the phytochrome-mediated control of hypocotyl growth orientation (Figs. 4–10
Plant Material and Growth Conditions
Plant growth conditions and determination of light conditions were performed as described previously (Lariguet et al., 2003 PKS4 overexpressing plants were obtained by transforming Arabidopsis (Arabidopsis thaliana) ecotype Columbia (Col-0) seedlings with construct pIS007 that codes for the PKS4 complementary DNA driven by the cauliflower mosaic virus 35S promoter. PKS4 coding sequence flanked with BamHI (catalog no. R0136S; New England Biolabs) sites was amplified by PCR (IS01 5'-GGA TCC ATG GCG CAA ACT ACT GTC AC-3' and IS02 5'-GGA TCC TGG TAT CCA TCA TTG CCT TG-3'), the BamHI digested product was ligated using T4 DNA ligase (M0202S; New England Biolabs) into BamHI digested pCGN18 to yield pIS007. All PCR-generated constructs were verified by sequencing. Two single insertion lines expressing elevated levels of PKS4 RNA (data not shown) were selected for further analysis (IS07-5 and IS07-11).
Hypocotyl length and cotyledon opening measurements were performed as described in Lariguet et al. (2003)
The sterilized seeds were sown on agar plates (one-half strength MS with 0.8% [w/v] agar) and kept at 4°C for 3 d. Plates were subsequently transferred at 21°C ± 1°C and exposed to white light for 6 h to induce seed germination. Time-lapse images were acquired by using a CCD camera system composed of a binocular microscope (Nikon), monochrome CCD camera (CV-M50IR; JAI Japan), and infrared light-emitting diodes (FQ15603; Adlos AG; peak emission at 940 nm, half-bandwidth 50 nm) placed in an incubator (floraLEDS; CLF PlantClimatics GmbH). The MetaMorph software (Molecular Devices) was used to control the CCD camera system and to process images. The agar plates were set vertically and images were acquired every 30 min under darkness or in red-light condition at 21°C ± 1°C. To determine gravi-reorientation following 90° rotation of the seedlings we used stacked images (using National Institutes of Health ImageJ software version 1.38 [http://rsb.info.nih.gov/ij/]) as described by Folta et al. (2003)
Col-0 plants were transformed with construct pIS35. An SpeI genomic fragment obtained from BAC F21E1 was cloned into pBluescript II (Statagene), giving the construct pIS13. The SpeI-NheI fragment of pIS13 was then cloned into pPCB308 (Xiang et al., 1999 Materials and methods for the supplemental figures can be found online as Supplemental Data S1.
The following materials are available in the online version of this article.
We are grateful to Ariane Honsberger (University of Geneva), Angélique Vaucher and Martine Trevisan (University of Lausanne), Dany Rifat (University of Geneva), and Constanza Rossi (University of Buenos Aires) for technical support. We also thank the Arabidopsis stock center for providing the BAC clone. Received February 21, 2008; accepted March 25, 2008; published April 4, 2008.
1 This work was supported by the University of Lausanne, a grant from the Swiss National Science Foundation (grant no. 3100A0–112638 to C.F.), a grant from ANPCYT of Argentina (BID 1728/OC–AR PICT 32492) to J.J.C., and from University of Buenos Aires (G021) to J.J.C. I.S. was supported by long-term fellowships from the European Molecular Biology Organization and the Roche Foundation. C.K. was supported by a postdoctoral fellowship from the Toyobo Biotechnology Foundation. 
2 Present address: Clinique de Dermatologie, Hopitaux Universitaires de Geneve, rue Micheli-du-Crest 24, 1211 Geneva, Switzerland.
3 Present address: Cátedra de Química Orgánica y Biológica, Facultad de Ciencias Agrarias, Universidad Nacional de Cuyo, Almirante Brown 500, 5505, Chacras de Coria, Mendoza, Argentina. 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: Christian Fankhauser (christian.fankhauser{at}unil.ch).
[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.108.118166 * Corresponding author; e-mail christian.fankhauser{at}unil.ch.
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