Molecular Plant Advance Access published September 8, 2014 LETTER TO THE EDITOR
Molecular Plant
How Do Phytochromes Transmit the Light Quality Information to the Circadian Clock in Arabidopsis? directly interacts with various circadian clock components through direct protein–protein interaction. We systematically examined the interaction between PHYB and all of the major circadian clock components that comprise the circadian clock systems first using yeast two-hybrid assay. The nine clock components we examined include CIRCADIAN CLOCK ASSOCIATED 1 (CCA1), LONG ELONGATED HYPOCOTYL (LHY), PSEUDO RESPONSE REGULATOR 7 and 9 (PRR7 and PRR9), GI, TIMING OF CAB 1 (TOC1), LUX ARRHYTHMO (LUX), ELF3, and ELF4. In the yeast two-hybrid assays, we used full-length PHYB as prey and circadian clock components as baits; the full-length PHYB could not be used as bait due to its auto-activation. Through this yeast two-hybrid assay, we were able to find that four (CCA1, GI, TOC1, and ELF3) among the nine tested components showed a reproducible interaction (Figure 1A). The interaction between PHYB and ELF3 and TOC1 appeared weak. However, the binding of ELF3 with PHYB in yeast was previously reported (Liu et al., 2001). The interaction between TOC1 with PHYB was further confirmed using the co-immunoprecipitation experiment in the yeast (Supplemental Figure 1). PRR7, PRR9, and ELF4 did not show detectable interaction in this assay. LHY and LUX showed auto-activation activity and thus their interaction with PHYB could not be examined by this assay. We then reexamined the interaction between PHYB and all of the nine major circadian clock components by in planta pull-down assay. For the in planta assay, we used protoplast cells of a PHYB–GFP (Green Fluorescent Protein) overexpression line (PBG5) and a GFP overexpression line (a negative control), which were transfected with the clock component genes fused to a c-Myc tag. The protein extracts from these protoplast cells were then subjected to immunoprecipitation with anti-GFP antibody to pull down the clock component/PHYB–GFP complex. The pull-down precipitates were then probed with anti-MYC antibody to determine whether the clock components were coprecipitated with PHYB–GFP. This result showed that PHYB physically interacts with the six plant clock components, CCA1, LHY, GI, TOC1, LUX, and ELF3. Through this assay,
© The Author 2014. Published by the Molecular Plant Shanghai Editorial Office in association with Oxford University Press on behalf of CSPB and IPPE, SIBS, CAS. doi:10.1093/mp/ssu086 Received 8 April 2014; accepted 31 July 2014
Downloaded from http://mplant.oxfordjournals.org/ at Florida State University on October 6, 2014
Dear Editor, Plants use light as an environmental signal to coordinate diverse physiological and developmental processes, thereby increasing their fitness. Light quality, quantity, and photoperiod change periodically under natural conditions of daily and seasonal cycles. Plants have developed a circadian clock to respond to these predictable, periodic environmental changes, providing plants with the ability to anticipate daily and seasonal environmental changes. Conceptually, the circadian clock systems are composed of the environmental input pathways, circadian clock, and physiological outputs. An important input to the circadian clock in plants is the daily changes of light. Accordingly, the daily cycle of light and dark as an input entrains the rhythmic behavior of plant circadian clock. On the other hand, the circadian clock modulates the light responsiveness of physiological outputs at different times of the day through a gating mechanism. The intimate connection between the light and clock responses in plants renders the timely and prepared regulation of various physiological output processes to cope with the periodic environmental changes. How is the light input signal transmitted to the circadian clock? It has been known that light regulates circadian clock components at transcription, translation, and posttranslational levels, mostly through signal transduction cascades mediated by various signaling components (Martinez-Garcia et al., 2000; Kim et al., 2003; Yu et al., 2008). On the other hand, PHYTOCHROME B (PHYB), one of the red light photoreceptors, directly interacts with EARLY FLOWERING 3 (ELF3), one of the clock components (Liu et al., 2001). Furthermore, ZEITLUPE (ZTL), a blue light photoreceptor, directly interacts with GIGANTEA (GI), a clock component, leading to blue-light-dependent stabilization of GI (Kim et al., 2007). These reports prompted us to examine a possibility that direct interaction between photoreceptors and the circadian clock components may be a prevalent mechanism for connecting the light signaling input and the circadian clock system. Phytochromes play important roles in light-mediated physiological and developmental processes by absorbing red (R) and far-red (FR) lights. Among five phytochromes (PHYA, B, C, D, E) encoded in the Arabidopsis genome, PHYB has a major role in R light-mediated entrainment of the circadian clock (Somers et al., 1998). PHYB regulates light responses through direct physical interaction with several downstream signaling components (Ni et al., 1999; Yang et al., 2001). We thus investigated whether PHYB
2
Letter to the Editor
Molecular Plant
Downloaded from http://mplant.oxfordjournals.org/ at Florida State University on October 6, 2014
Figure 1 Phytochrome B (PHYB) Interacts with Variable Oscillators in Red and Far-Red Light. (A) Screening for physically interacting partners of PHYB among circadian clock proteins using the yeast two-hybrid assay. (B) Direct interaction between PHYB and clock proteins in planta. Transfected protoplasts were kept under diurnal conditions. Samples were harvested at 2 h after light on. * indicates a non-specific band. Loading control is tubulin. (C) Light quality alters the interactions of PHYB with clock proteins. Protoplasts transfected with clones were kept for 6 h in the light followed by 9 h in the dark. Protoplasts were treated with either red (13 μmol m–2 s–1) or far-red (4.5 μmol m–2 s–1) light for 4 h and then harvested. Blots are representative of several trials. Loading control is tubulin or blot stained coomassie blue dye. (D) Quantification of each clock protein and PHYB in IP of Supplemental Figure 5. The precipitates of clock proteins were quantified relative to immunoprecipitated PHYB and normalized to maximum value under either red or far-red light. Means of several biological experiments ± SE are shown. (E) Model for the light-quality-dependent interaction between PHYB and circadian clock proteins in Arabidopsis.
Molecular Plant
3
FACTOR 3 (PIF3) as a control (Ni et al., 1999). Our results showed that CCA1 interacts preferentially with the Pr-enriched PHYB in vitro, while PIF3 favors the Pfr-enriched conditions as reported (Supplemental Figure 6). PHYB plays a role in maintaining free-running rhythm of the circadian clock, as phyB mutation exhibits long period, under continuous R light (Somers et al., 1998). As PHYB showed a preferential binding with CCA1 in FR light, we tested whether PHYB may also play a role in FR light response of the free-running rhythm of the circadian clock. To test this idea, we measured the free-running rhythm of the clock-responsive chlorophyll a-b binding protein 2 (CAB2) promoter in a phyB null mutant under continuous FR light after entraining the mutant plants under a 12-h white light/12-h dark cycle. The result showed that the free-running period length is shorter in phyB-9 mutant than in WT (Supplemental Figure 7), indicating that PHYB plays a role in FR light-mediated response of the free-running rhythm. Here, we showed that PHYB interacts with various clock components and that the interaction is differential under R and FR light. The physiological significance and the detailed mechanism of this interaction remain to be elucidated. However, these observations lead to an interesting hypothesis that light input signal can be transmitted to circadian clock through direct interaction with various clock components, circumventing signaling cascades. The study on the interaction of light and the circadian clock has been mostly limited to the interaction between the photoperiod and the circadian clock but, along a daily cycle, the ratio of R/FR light cycles. We speculate that the differential binding of PHYB with various clock components under R and FR light may be a mechanism to transfer the environmental light quality information into the circadian clock. In an ecological setting, this mechanism would allow adjustment of the cyclic behaviors of output physiology, incorporating the R/FR ratio information.
SUPPLEMENTARY DATA Supplementary data are available at Molecular Plant Online.
FUNDING This research was supported by the Research Center Program of Institute for Basic Science (IBS; CA1208), Republic of Korea.
Miji Yeoma, Hyunmin Kima, Junhyun Limb, Ah-Young Shinc, Sunghyun Hongd, Jeong-Il Kimc, and Hong Gil Namd,e,1
Downloaded from http://mplant.oxfordjournals.org/ at Florida State University on October 6, 2014
we confirmed the in planta interaction of CCA1, GI, TOC1, and ELF3 with PHYB, as indicated in the yeast two-hybrid assay. This assay also showed that LHY and LUX can bind with PHYB in planta (Figure 1B and Supplemental Figures 2 and 3). The other three clock components, PRR7, PRR9, and ELF4, did not show reproducible difference between PBG5-expressing protoplast cells and GFP-expressing protoplast cells in their interaction with PHYB (Supplemental Figure 4). Combining the yeast two-hybrid data and the in planta pull-down data, we argue that the six clock components, CCA1, LHY, GI, TOC1, LUX, and ELF3, directly interact with PHYB. In Arabidopsis, the circadian clock consists of interconnected morning and evening loops (Locke et al., 2006). PHYB-interacting partners include the components in both the morning and the evening loops. PHYB physically interacts with CCA1 and LHY in the morning loop and with GI, TOC1, LUX, and ELF3 in the evening loop. It is notable that PHYB interacts with six out of the nine major clock components. The frequent interaction of PHYB with the clock components suggests that this interaction comprises a significant mechanism of interaction between the light signaling input and the circadian system. Spectral quality of light provides important environmental information to plants, such as for recognition of daily and seasonal information. Phytochromes recognize the change of the light quality in R and FR wavelengths through inter-conversion between Pr (R light absorbing form) and Pfr (FR light absorbing form). Accordingly, the interaction of PHYB with its signaling components is often dependent upon the spectral forms (Ni et al., 1999; Ryu et al., 2005). Therefore, we examined a possibility that the interaction between PHYB and circadian clock proteins changes dependent on light quality. To test this idea, we compared the in planta interaction of the six PHYBinteracting clock components with PHYB under R and FR lights. Our results showed that LUX preferentially interacts with PHYB in R light. In contrast, CCA1 and TOC1 showed a preferential interaction in FR light. LHY, GI, and ELF3 did not show a noticeable difference in R and FR lights (Figure 1C–1E and Supplemental Figure 5). The result with the PHYB–ELF3 complex is consistent with the previously reported in vitro assay (Liu et al., 2001). CCA1 and LHY are known to be functional redundant. Interestingly, their interactions with PHYB showed the different R and FR light responses, CCA being FR light preferential and LHY showing no differential binding. Interaction with many PHYB-interacting partners mostly is enhanced by R light (Ni et al., 1999; Ryu et al., 2005). In our case, CCA1 and TOC1 showed FR-preferential binding with PHYB. We further confirmed the FR-preferential binding of CCA1 with PHYB by an in vitro binding assay using recombinant Arabidopsis PHYB incorporated with phycocyanobilin. We also included PHYTOCHROME INTERACTING
Letter to the Editor
4
Letter to the Editor a Division of Molecular and Life Sciences, Pohang University of Science and Technology, Hyojadong, Pohang, Gyeongbuk, 790–784, Republic of Korea b Integrative Biosciences & Biotechnology in POSTECH, Hyojadong, Pohang, Gyeongbuk 790–784, Republic of Korea c Department of Molecular Biotechnology and Kumho Life Science Laboratory, Chonnam National University, Gwangju, 500–757, Republic of Korea d Center for Plant Aging Research, Institute for Basic Science, Daegu 711–873, Republic of Korea e Department of New Biology, DGIST, Hyeongpoong-Myun, Dalsung-gun, Daegu 711–873, Republic of Korea 1 To whom correspondence should be addressed. E-mail nam@ dgist.ac.kr, fax + 82-53-785-1819, tel. + 82-53-785-1800.
Kim, J.Y., Song, H.R., Taylor, B.L., and Carre, I.A. (2003). Lightregulated translation mediates gated induction of the Arabidopsis clock protein LHY. EMBO J. 22, 935–944. Kim, W.Y., Fujiwara, S., Suh, S.S., Kim, J., Kim, Y., Han, L., David, K., Putterill, J., Nam, H.G., and Somers, D.E. (2007). ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature. 449, 356–360. Liu, X.L., Covington, M.F., Fankhauser, C., Chory, J., and Wagner, D.R. (2001). ELF3 encodes a circadian clock-regulated nuclear
protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell. 13, 1293–1304. Locke, J.C., Kozma-Bognar, L., Gould, P.D., Feher, B., Kevei, E., Nagy, F., Turner, M.S., Hall, A., and Millar, A.J. (2006). Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol. Syst. Biol. 2, 59. Martinez-Garcia, J.F., Huq, E., and Quail, P.H. (2000). Direct targeting of light signals to a promoter element-bound transcription factor. Science. 288, 859–863. Ni, M., Tepperman, J.M., and Quail, P.H. (1999). Binding of phytochrome B to its nuclear signalling partner PIF3 is reversibly induced by light. Nature. 400, 781–784. Ryu, J.S., Kim, J.I., Kunkel, T., Kim, B.C., Cho, D.S., Hong, S.H., Kim, S.H., Fernandez, A.P., Kim, Y., Alonso, J.M., et al. (2005). Phytochrome-specific type 5 phosphatase controls light signal flux by enhancing phytochrome stability and affinity for a signal transducer. Cell. 120, 395–406. Somers, D.E., Devlin, P.F., and Kay, S.A. (1998). Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science. 282, 1488–1490. Yang, H.Q., Tang, R.H., and Cashmore, A.R. (2001). The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1. Plant Cell. 13, 2573–2587. Yu, J.W., Rubio, V., Lee, N.Y., Bai, S., Lee, S.Y., Kim, S.S., Liu, L., Zhang, Y., Irigoyen, M.L., Sullivan, J.A., et al. (2008). COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol. Cell. 32, 617–630.
Downloaded from http://mplant.oxfordjournals.org/ at Florida State University on October 6, 2014
References
Molecular Plant
Molecular Plant
How Do Phytochromes Transmit the Light Quality Information to the Circadian Clock in Arabidopsis? directly interacts with various circadian clock components through direct protein–protein interaction. We systematically examined the interaction between PHYB and all of the major circadian clock components that comprise the circadian clock systems first using yeast two-hybrid assay. The nine clock components we examined include CIRCADIAN CLOCK ASSOCIATED 1 (CCA1), LONG ELONGATED HYPOCOTYL (LHY), PSEUDO RESPONSE REGULATOR 7 and 9 (PRR7 and PRR9), GI, TIMING OF CAB 1 (TOC1), LUX ARRHYTHMO (LUX), ELF3, and ELF4. In the yeast two-hybrid assays, we used full-length PHYB as prey and circadian clock components as baits; the full-length PHYB could not be used as bait due to its auto-activation. Through this yeast two-hybrid assay, we were able to find that four (CCA1, GI, TOC1, and ELF3) among the nine tested components showed a reproducible interaction (Figure 1A). The interaction between PHYB and ELF3 and TOC1 appeared weak. However, the binding of ELF3 with PHYB in yeast was previously reported (Liu et al., 2001). The interaction between TOC1 with PHYB was further confirmed using the co-immunoprecipitation experiment in the yeast (Supplemental Figure 1). PRR7, PRR9, and ELF4 did not show detectable interaction in this assay. LHY and LUX showed auto-activation activity and thus their interaction with PHYB could not be examined by this assay. We then reexamined the interaction between PHYB and all of the nine major circadian clock components by in planta pull-down assay. For the in planta assay, we used protoplast cells of a PHYB–GFP (Green Fluorescent Protein) overexpression line (PBG5) and a GFP overexpression line (a negative control), which were transfected with the clock component genes fused to a c-Myc tag. The protein extracts from these protoplast cells were then subjected to immunoprecipitation with anti-GFP antibody to pull down the clock component/PHYB–GFP complex. The pull-down precipitates were then probed with anti-MYC antibody to determine whether the clock components were coprecipitated with PHYB–GFP. This result showed that PHYB physically interacts with the six plant clock components, CCA1, LHY, GI, TOC1, LUX, and ELF3. Through this assay,
© The Author 2014. Published by the Molecular Plant Shanghai Editorial Office in association with Oxford University Press on behalf of CSPB and IPPE, SIBS, CAS. doi:10.1093/mp/ssu086 Received 8 April 2014; accepted 31 July 2014
Downloaded from http://mplant.oxfordjournals.org/ at Florida State University on October 6, 2014
Dear Editor, Plants use light as an environmental signal to coordinate diverse physiological and developmental processes, thereby increasing their fitness. Light quality, quantity, and photoperiod change periodically under natural conditions of daily and seasonal cycles. Plants have developed a circadian clock to respond to these predictable, periodic environmental changes, providing plants with the ability to anticipate daily and seasonal environmental changes. Conceptually, the circadian clock systems are composed of the environmental input pathways, circadian clock, and physiological outputs. An important input to the circadian clock in plants is the daily changes of light. Accordingly, the daily cycle of light and dark as an input entrains the rhythmic behavior of plant circadian clock. On the other hand, the circadian clock modulates the light responsiveness of physiological outputs at different times of the day through a gating mechanism. The intimate connection between the light and clock responses in plants renders the timely and prepared regulation of various physiological output processes to cope with the periodic environmental changes. How is the light input signal transmitted to the circadian clock? It has been known that light regulates circadian clock components at transcription, translation, and posttranslational levels, mostly through signal transduction cascades mediated by various signaling components (Martinez-Garcia et al., 2000; Kim et al., 2003; Yu et al., 2008). On the other hand, PHYTOCHROME B (PHYB), one of the red light photoreceptors, directly interacts with EARLY FLOWERING 3 (ELF3), one of the clock components (Liu et al., 2001). Furthermore, ZEITLUPE (ZTL), a blue light photoreceptor, directly interacts with GIGANTEA (GI), a clock component, leading to blue-light-dependent stabilization of GI (Kim et al., 2007). These reports prompted us to examine a possibility that direct interaction between photoreceptors and the circadian clock components may be a prevalent mechanism for connecting the light signaling input and the circadian clock system. Phytochromes play important roles in light-mediated physiological and developmental processes by absorbing red (R) and far-red (FR) lights. Among five phytochromes (PHYA, B, C, D, E) encoded in the Arabidopsis genome, PHYB has a major role in R light-mediated entrainment of the circadian clock (Somers et al., 1998). PHYB regulates light responses through direct physical interaction with several downstream signaling components (Ni et al., 1999; Yang et al., 2001). We thus investigated whether PHYB
2
Letter to the Editor
Molecular Plant
Downloaded from http://mplant.oxfordjournals.org/ at Florida State University on October 6, 2014
Figure 1 Phytochrome B (PHYB) Interacts with Variable Oscillators in Red and Far-Red Light. (A) Screening for physically interacting partners of PHYB among circadian clock proteins using the yeast two-hybrid assay. (B) Direct interaction between PHYB and clock proteins in planta. Transfected protoplasts were kept under diurnal conditions. Samples were harvested at 2 h after light on. * indicates a non-specific band. Loading control is tubulin. (C) Light quality alters the interactions of PHYB with clock proteins. Protoplasts transfected with clones were kept for 6 h in the light followed by 9 h in the dark. Protoplasts were treated with either red (13 μmol m–2 s–1) or far-red (4.5 μmol m–2 s–1) light for 4 h and then harvested. Blots are representative of several trials. Loading control is tubulin or blot stained coomassie blue dye. (D) Quantification of each clock protein and PHYB in IP of Supplemental Figure 5. The precipitates of clock proteins were quantified relative to immunoprecipitated PHYB and normalized to maximum value under either red or far-red light. Means of several biological experiments ± SE are shown. (E) Model for the light-quality-dependent interaction between PHYB and circadian clock proteins in Arabidopsis.
Molecular Plant
3
FACTOR 3 (PIF3) as a control (Ni et al., 1999). Our results showed that CCA1 interacts preferentially with the Pr-enriched PHYB in vitro, while PIF3 favors the Pfr-enriched conditions as reported (Supplemental Figure 6). PHYB plays a role in maintaining free-running rhythm of the circadian clock, as phyB mutation exhibits long period, under continuous R light (Somers et al., 1998). As PHYB showed a preferential binding with CCA1 in FR light, we tested whether PHYB may also play a role in FR light response of the free-running rhythm of the circadian clock. To test this idea, we measured the free-running rhythm of the clock-responsive chlorophyll a-b binding protein 2 (CAB2) promoter in a phyB null mutant under continuous FR light after entraining the mutant plants under a 12-h white light/12-h dark cycle. The result showed that the free-running period length is shorter in phyB-9 mutant than in WT (Supplemental Figure 7), indicating that PHYB plays a role in FR light-mediated response of the free-running rhythm. Here, we showed that PHYB interacts with various clock components and that the interaction is differential under R and FR light. The physiological significance and the detailed mechanism of this interaction remain to be elucidated. However, these observations lead to an interesting hypothesis that light input signal can be transmitted to circadian clock through direct interaction with various clock components, circumventing signaling cascades. The study on the interaction of light and the circadian clock has been mostly limited to the interaction between the photoperiod and the circadian clock but, along a daily cycle, the ratio of R/FR light cycles. We speculate that the differential binding of PHYB with various clock components under R and FR light may be a mechanism to transfer the environmental light quality information into the circadian clock. In an ecological setting, this mechanism would allow adjustment of the cyclic behaviors of output physiology, incorporating the R/FR ratio information.
SUPPLEMENTARY DATA Supplementary data are available at Molecular Plant Online.
FUNDING This research was supported by the Research Center Program of Institute for Basic Science (IBS; CA1208), Republic of Korea.
Miji Yeoma, Hyunmin Kima, Junhyun Limb, Ah-Young Shinc, Sunghyun Hongd, Jeong-Il Kimc, and Hong Gil Namd,e,1
Downloaded from http://mplant.oxfordjournals.org/ at Florida State University on October 6, 2014
we confirmed the in planta interaction of CCA1, GI, TOC1, and ELF3 with PHYB, as indicated in the yeast two-hybrid assay. This assay also showed that LHY and LUX can bind with PHYB in planta (Figure 1B and Supplemental Figures 2 and 3). The other three clock components, PRR7, PRR9, and ELF4, did not show reproducible difference between PBG5-expressing protoplast cells and GFP-expressing protoplast cells in their interaction with PHYB (Supplemental Figure 4). Combining the yeast two-hybrid data and the in planta pull-down data, we argue that the six clock components, CCA1, LHY, GI, TOC1, LUX, and ELF3, directly interact with PHYB. In Arabidopsis, the circadian clock consists of interconnected morning and evening loops (Locke et al., 2006). PHYB-interacting partners include the components in both the morning and the evening loops. PHYB physically interacts with CCA1 and LHY in the morning loop and with GI, TOC1, LUX, and ELF3 in the evening loop. It is notable that PHYB interacts with six out of the nine major clock components. The frequent interaction of PHYB with the clock components suggests that this interaction comprises a significant mechanism of interaction between the light signaling input and the circadian system. Spectral quality of light provides important environmental information to plants, such as for recognition of daily and seasonal information. Phytochromes recognize the change of the light quality in R and FR wavelengths through inter-conversion between Pr (R light absorbing form) and Pfr (FR light absorbing form). Accordingly, the interaction of PHYB with its signaling components is often dependent upon the spectral forms (Ni et al., 1999; Ryu et al., 2005). Therefore, we examined a possibility that the interaction between PHYB and circadian clock proteins changes dependent on light quality. To test this idea, we compared the in planta interaction of the six PHYBinteracting clock components with PHYB under R and FR lights. Our results showed that LUX preferentially interacts with PHYB in R light. In contrast, CCA1 and TOC1 showed a preferential interaction in FR light. LHY, GI, and ELF3 did not show a noticeable difference in R and FR lights (Figure 1C–1E and Supplemental Figure 5). The result with the PHYB–ELF3 complex is consistent with the previously reported in vitro assay (Liu et al., 2001). CCA1 and LHY are known to be functional redundant. Interestingly, their interactions with PHYB showed the different R and FR light responses, CCA being FR light preferential and LHY showing no differential binding. Interaction with many PHYB-interacting partners mostly is enhanced by R light (Ni et al., 1999; Ryu et al., 2005). In our case, CCA1 and TOC1 showed FR-preferential binding with PHYB. We further confirmed the FR-preferential binding of CCA1 with PHYB by an in vitro binding assay using recombinant Arabidopsis PHYB incorporated with phycocyanobilin. We also included PHYTOCHROME INTERACTING
Letter to the Editor
4
Letter to the Editor a Division of Molecular and Life Sciences, Pohang University of Science and Technology, Hyojadong, Pohang, Gyeongbuk, 790–784, Republic of Korea b Integrative Biosciences & Biotechnology in POSTECH, Hyojadong, Pohang, Gyeongbuk 790–784, Republic of Korea c Department of Molecular Biotechnology and Kumho Life Science Laboratory, Chonnam National University, Gwangju, 500–757, Republic of Korea d Center for Plant Aging Research, Institute for Basic Science, Daegu 711–873, Republic of Korea e Department of New Biology, DGIST, Hyeongpoong-Myun, Dalsung-gun, Daegu 711–873, Republic of Korea 1 To whom correspondence should be addressed. E-mail nam@ dgist.ac.kr, fax + 82-53-785-1819, tel. + 82-53-785-1800.
Kim, J.Y., Song, H.R., Taylor, B.L., and Carre, I.A. (2003). Lightregulated translation mediates gated induction of the Arabidopsis clock protein LHY. EMBO J. 22, 935–944. Kim, W.Y., Fujiwara, S., Suh, S.S., Kim, J., Kim, Y., Han, L., David, K., Putterill, J., Nam, H.G., and Somers, D.E. (2007). ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature. 449, 356–360. Liu, X.L., Covington, M.F., Fankhauser, C., Chory, J., and Wagner, D.R. (2001). ELF3 encodes a circadian clock-regulated nuclear
protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell. 13, 1293–1304. Locke, J.C., Kozma-Bognar, L., Gould, P.D., Feher, B., Kevei, E., Nagy, F., Turner, M.S., Hall, A., and Millar, A.J. (2006). Experimental validation of a predicted feedback loop in the multi-oscillator clock of Arabidopsis thaliana. Mol. Syst. Biol. 2, 59. Martinez-Garcia, J.F., Huq, E., and Quail, P.H. (2000). Direct targeting of light signals to a promoter element-bound transcription factor. Science. 288, 859–863. Ni, M., Tepperman, J.M., and Quail, P.H. (1999). Binding of phytochrome B to its nuclear signalling partner PIF3 is reversibly induced by light. Nature. 400, 781–784. Ryu, J.S., Kim, J.I., Kunkel, T., Kim, B.C., Cho, D.S., Hong, S.H., Kim, S.H., Fernandez, A.P., Kim, Y., Alonso, J.M., et al. (2005). Phytochrome-specific type 5 phosphatase controls light signal flux by enhancing phytochrome stability and affinity for a signal transducer. Cell. 120, 395–406. Somers, D.E., Devlin, P.F., and Kay, S.A. (1998). Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science. 282, 1488–1490. Yang, H.Q., Tang, R.H., and Cashmore, A.R. (2001). The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1. Plant Cell. 13, 2573–2587. Yu, J.W., Rubio, V., Lee, N.Y., Bai, S., Lee, S.Y., Kim, S.S., Liu, L., Zhang, Y., Irigoyen, M.L., Sullivan, J.A., et al. (2008). COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol. Cell. 32, 617–630.
Downloaded from http://mplant.oxfordjournals.org/ at Florida State University on October 6, 2014
References
Molecular Plant
