Molecular Plant Advance Access originally published online on November 5, 2007
Molecular Plant 2008 1(1):68-74; doi:10.1093/mp/ssm008
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© The Author 2007. Published by Oxford University Press on behalf of CSPP and IPPE, SIBS, CAS.
Evidence of a Light-Sensing Role for Folate in Arabidopsis Cryptochrome Blue-Light Receptors
a Université Paris VI, Casier 156, 4 Place Jussieu, 75005 Paris, France
b Penn State University, 25 Yearsley Mill Road, Media, PA 19063, USA
1 To whom correspondence should be addressed, at address (a). E-mail ahmad{at}ccr.jussieu.fr, tel. 33(1)44272916, fax 33(1)44272916.
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Abstract |
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Arabidopsis cryptochromes cry1 and cry2 are blue-light signalling molecules with significant structural similarity to photolyases—a class of blue-light-sensing DNA repair enzymes. Like photolyases, purified plant cryptochromes have been shown to bind both flavin and pterin chromophores. The flavin functions as a light sensor and undergoes reduction in response to blue light that initiates the signalling cascade. However, the role of the pterin in plant cryptochromes has until now been unknown. Here, we show that the action spectrum for light-dependent degradation of cry2 has a significant peak of activity at 380 nm, consistent with absorption by a pterin cofactor. We further show that cry1 protein expressed in living insect cells responds with greater sensitivity to 380 nm light than to 450 nm, consistent with a light-harvesting antenna pigment that transfers excitation energy to the oxidized flavin of cry1. The pterin biosynthesis inhibitor DHAP selectively reduces cryptochrome responsivity at 380 nm but not 450 nm blue light in these cell cultures, indicating that the antenna pigment is a folate cofactor similar to that of photolyases.
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INTRODUCTION |
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TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODS |
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Cryptochromes are blue-light-sensing photoreceptors with significant structural similarity to photolyases—a class of blue-light-sensing DNA repair enzymes (Lin and Todo, 2005). Plant cryptochromes such as Arabidopsis cry1 and cry2 are most similar to microbial type I CPD photolyases, which repair cyclobutane pyrimidine dimers in UV-damaged DNA. A fully reduced flavin (FADH-) cofactor is bound to the C-terminus of the photolyase protein and participates in catalysis and DNA repair (Thompson and Sancar, 2002). In addition to flavin, photolyases bind a second chromophore, which is generally a pterin (folate) derivative, located near the surface of the protein. The pterin absorption peak lies between 377 and 415 nm, depending on the protein to which it is bound. The pterin cofactor functions by transfer of photon energy via FRET to flavin to initiate electron transfer to UV-damaged DNA (Carell et al., 2001). Energy is also transferred from pterin to oxidized or radical flavin during the process of photoreduction. Because pterin is bound near the surface of the molecule, it is often lost upon purification and therefore is lacking in typical preparations of purified photolyases (Sancar, 2003).
Although they are structurally related, cryptochromes differ from photolyases in that they do not repair DNA and, instead, are involved in multiple blue-light-sensing and signalling functions in plants and animals (Banerjee and Batschauer, 2005; Li and Yang, 2006). Like photolyases, cryptochromes bind flavin (FAD) (Lin et al., 1995; Malhotra et al., 1995). Action spectroscopy suggests that oxidized flavin by itself can act as a light sensor in Arabidopsis cryptochromes, as there is a pronounced peak of activity at 450 nm both in vivo (Ahmad et al., 2002) and during photoreduction of the purified protein in vitro (Zeugner et al., 2005; Bouly et al., 2007; Banerjee et al., 2007). However, the near-UV activity at 380 nm in the action spectrum (Ahmad et al., 2002) exceeds that of the corresponding absorption maximum of flavins, suggesting the possibility of a secondary chromophore with major absorption in this spectral region. It is plain that pterins are contenders for acting as light-harvesting antenna pigments in cryptochromes, as plant cryptochrome purified from E. coli expression systems have been shown to retain the pterin chromophore (Malhotra et al., 1995). Furthermore, a role for pterin as a light-sensing antenna pigment involved in energy transfer to flavin has been demonstrated in purified preparations of the cry-DASH-type cryptochromes which are similar to 6-4-type photolyases (Saxena et al., 2005; Klar et al., 2006). Although these cry-DASH cryptochromes are not related to plant cryptochromes cry1 and cry2, their overall structure is highly similar, suggesting that common mechanisms of light perception may occur.
In the present work, we seek to establish a role for a pterin specifically in plant cryptochromes. Since most photolyase preparations show absorption peaks in the near-UV wavelength (370–390 nm) as a result of pterin light absorption, we have re-investigated Arabidopsis cryptochrome responsivity at these wavelengths, both in plants and in heterologous in-vivo expression systems. In this study, we show a pronounced peak of cryptochrome activity at 380 nm, which is reduced in the presence of pterin biosynthesis inhibitors. Taken together, these data indicate a role for a pterin as a light-harvesting antenna pigment for cryptochrome in the near-UV wavelength range.
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RESULTS |
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TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODS |
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Action Spectrum of cry2
In a prior study, an action spectrum for Arabidopsis cryptochrome-1 (Ahmad et al., 2002) showed considerable responsivity in the near-UV wavelength (360–400 nm) but no clearly defined peak, such as that for folate in E. coli photolyase. However, the cry1 action spectrum was performed on the hypocotyl growth-inhibition response, which requires continuous irradiation over 3 d with resulting accumulation of anthocyanins and other stress-induced pigments. These pigments may have interfered with the response to UV/A light. We have therefore performed another action spectrum of a plant cryptochrome response—the blue-light-dependent degradation of cry2 protein, which occurs in etiolated seedlings on a much shorter time scale (Lin et al., 1998; Ahmad et al., 1998). Etiolated wild-type Arabidopsis seedlings were irradiated for 30 min by light at defined wavelengths of between 370 and 500 nm (Figure 1). Monochromatic light was generated by interference filters of approximately 10 nm half-bandwidth (see Methods). Seedlings were irradiated with light at multiple photon fluence rates within the sensitivity range of the photoreceptor at each wavelength. Western blot analysis was performed to determine the response (extent of cry2 degradation) at each wavelength and photon fluence. The signal of the cry2 band in the Western blots was quantitated digitally by imaging software to provide the values included in the graphs (Figure 1). For simplicity, the data presented in the plots (Figure 1) consist solely of the data points at which the rate of degradation of cry2 was proportional to the light intensity; additional data points at either lower fluence (showing no decrease in cry2 protein levels over 30 min of illumination) or higher photon fluence (with complete degradation and no detectable cry2 signal) at each wavelength are not shown.
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An action spectrum was derived from these plots as the photon fluence required to achieve 50% cry2 protein degradation at each wavelength. This value lies within the linear range of the dose–response curve and is therefore directly proportional to the degree of sensitivity of the photoreceptor to this wavelength (Figure 1). The derived action spectrum of cry2 (Figure 2) is consistent with that of cry1 (Ahmad et al., 2002) in the visible range, with a maximum at 450 nm, shoulders at around 415 and 480 nm, and a sharp decrease above 500 nm. In this respect, the action spectrum of cry2, like that of cry1, is consistent with a role for oxidized flavin as a primary light sensor. However, an additional peak of cry2 activation occurs at around 380 nm (Figure 2). This peak cannot be explained by absorption characteristics of any redox form of flavin. Therefore, an additional pigment absorbing in the near-UV region must be contributing to the activity spectrum of cry2. Responsivity at 380 nm is in fact higher than that at 450 nm at the same photon fluence rate.
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Photoreduction of cry1 Protein in Living Insect Cells Shows Peak Activity at 380 nm
It has been previously shown that plant cryptochrome overexpressed in insect cell cultures can be directly detected in living cells by fluorescence assay (Bouly et al., 2007). This is due to the high abundance of the recombinant protein, such that fluorescence emission of oxidized flavin bound to the apoprotein can be directly monitored. On the assumption that the intact unpurified cryptochrome in baculovirus-infected insect cell cultures may contain both pterin and flavin chromophores, we performed an excitation spectrum of cry1-expressing insect cell cultures extending into the UV/A wavelength range. As seen in prior studies, the excitation spectrum for emission at 525 nm showed a clearly defined peak at 450 nm, consistent with increased levels of protein-bound oxidized flavin (Figure 3A). However, an additional major peak appears at 380 nm (Figure 3A) that is much enhanced in cry1-overexpressing cells as compared with control cell cultures (Figure 3B). This peak cannot be explained from the absorption spectrum of any redox form of flavin, but nevertheless produces fluorescence emission at 525 nm consistent with excitation of oxidized flavin. Since folate derivatives absorb in this wavelength range (380 nm), a simple explanation would be that we have detected absorption of a pterin bound to cryptochrome, which acts as a light-harvesting antenna pigment for flavin excitation (hence the increased emission at 525 nm upon excitation at 380 nm).
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The flavin bound to Arabidopsis cryptochrome overexpressed in living insect cell cultures can be reduced in vivo subsequent to illumination (Bouly et al., 2007). Decrease in fluorescence emission at 525 nm occurs concomitantly with accumulation of radical intermediate in living insect cells, which represents the active state of the photoreceptor (Bouly et al., 2007; Banerjee et al., 2007). To determine the effect of UV/A light directly on the activation of cry1, living cells expressing cry1 were illuminated with a low intensity (2 µmol m–2 s–1) of UV/A (380 nm) light over time, and returned to the fluorimeter for measurement of excitation spectra at defined intervals. The values for emission at 525 nm (excitation at 450 nm) of these samples are plotted (Figure 4). The resulting progressive decrease in emission at 525 nm is due to decreased concentrations of oxidized flavin bound to cry1 as a result of photoreduction (Bouly et al., 2007). Interestingly, when illumination is performed at the same low photon fluence (2 µmol m–2 s–1) of blue light (450 nm), no decrease in the emission of samples at 525 nm in the fluorimeter is observed over time (Figure 4). Therefore, light at 380 nm is far more effective in activating the cryptochrome photocycle (initiating photoreduction) than blue light. This suggests the presence of an antenna pigment that is more light-sensitive (has higher extinction coefficient) than oxidized flavin, which is the case for the folate cofactor of E. coli photolyase (Sancar, 2003). In sum, our data provide evidence for a light-harvesting antenna pigment at 380 nm peak absorption which activates cryptochrome. The light sensitivity of this antenna pigment is higher than that of oxidized flavin, both in plants (degradation of cry2 response) and in insect cell cultures (cry1 in-vivo photoreduction response).
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A Pterin is Implicated in the Photo-Activation of Cryptochrome by UV/A Light
The inhibitor of pterin synthesis 2,4-diamino-6-hydroxyaminopyrimidine (DAHP) (Maier and Ninnemann, 1995) has been shown to inhibit the production and responsivity to pterins in several organisms (Portwich and Garcia, 2000). To determine whether DAHP affects the photoreaction of cryptochrome in insect cell cultures, the inhibitor was added to a final concentration of 5 mM during infection and production of recombinant cryptochrome proteins. Excitation spectra were taken of cultures either treated with DHAP or untreated control samples. When emission is monitored at 440 nm (the emission peak for pterins and folate derivatives), a pronounced peak of absorption at 380 nm is significantly reduced in cells treated with increasing concentrations of DHAP as compared with untreated control cells (Figure 5). Thus, DHAP selectively interferes with biosynthesis and accumulation of a species absorbing at 380 nm in this cell culture system, which is therefore likely to be a folate derivative.
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We next determined the effect of DHAP on the rate of flavin photoreduction (cryptochrome activation) in these cell cultures. Cry1-expressing cell cultures were irradiated at 10 µmol m–2 s–1 blue light (450 nm) over a time course of 200 min. At intervals, cell cultures were placed in the fluorimeter and emission was monitored at 525 nm for reduction in oxidized flavin. A plot of emission at 525 nm (excitation 450 nm) over time in these cultures (Figure 6) shows a gradual decrease in oxidized flavin, as previously shown (Bouly et al., 2007). The rate of photoreduction in response to blue light (450 nm) did not differ between cultures treated with DHAP and control cell cultures at the identical cryptochrome protein concentration (Figure 6). Therefore, the DHAP inhibitor does not induce cell death or prevent protein expression or assembly at this concentration in living insect cells. Furthermore, DHAP does not affect the responsivity of cry1 to blue light in vivo.
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We subsequently determined the effect of DHAP on the rate of flavin photoreduction (cry1 activation) at 380 nm. In this experiment, we used cell cultures of the identical age and concentration as those used for the blue-light treatments presented in Figure 6. Cry1-expressing cell cultures were irradiated at 2 µmol m–2 s–1 UV/A light (380 nm) over a time course of 200 min. At intervals, cell cultures were placed in the fluorimeter and emission was monitored at 525 nm for reduction of oxidized flavin. A plot of emission at 525 nm (for excitation at 450 nm) over time in these cultures (Figure 7) produces the gradual decrease in oxidized flavin, as previously determined (Figure 5), showing that 380 nm light is effective at stimulating cry1 activation. However, in contrast to the experiments in blue light (Figure 6), the rate of photoreduction in response to UV/A light (380 nm) was dramatically reduced in cultures treated with DHAP as compared with control cell cultures at the identical cryptochrome protein concentration (Figure 7). As DHAP does not affect cry1 activity at 450 nm light (Figure 6), this decreased efficiency cannot be due to loss of protein assembly or stability, but, instead, is due to loss of a light-harvesting antenna pigment.
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In sum, we have shown that an inhibitor of pterin biosynthesis reduces the response of cry1 to UV/A light but not to blue light. Taken together, these data indicate that there must be two distinct light-absorbing chromophores in Arabidopsis cryptochrome, one of which (peak efficiency at 380 nm) is a pterin and the other an oxidized flavin (peak efficiency at 450 nm). Since 380 nm light is more effective at inducing flavin photoreduction than 450 nm light, the role of the pterin is likely to act as a light-harvesting antenna by analogy with photolyases.
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DISCUSSION |
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TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODS |
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In this work, we provide evidence of a UV/A-sensing role for cryptochrome. We show a distinct UV/A-responsive peak at 380 nm in an Arabidopsis cry2-dependent response. A similar peak in responsivity is observed in insect cells overexpressing Arabidopsis cry1 protein. Because the observed peak of activity at 380 nm corresponds closely to the peak of wavelength sensitivity of folate bound to E. coli photolyases (Sancar, 2003) and because an inhibitor of pterin biosynthesis significantly reduces UV/A peak sensitivity of cry1 in insect cell cultures, we conclude that folate likely acts as a light-harvesting antenna pigment for plant cry1 and cry2 in vivo.
In prior studies, plant cryptochrome purified from an E. coli expression system was shown to bind pterin cofactor, similarly to E. coli photolyase (Malhotra et al., 1995). However, in this prior study, the peak of absorption in vitro was found to occur at around 410 nm, which is somewhat higher than the peak of cryptochrome activation (380 nm) determined in vivo in the present study. It is unclear whether this peak (410 nm) in fact resulted from absorption by pterin, as fluorescence emission studies of purified cryptochrome from E. coli showed no pronounced excitation peak at 410 nm (Malhotra et al., 1995). Possibly, the protein undergoes a conformational change upon cellular lysis or purification, resulting in a shift in folate absorbance from 380 to 410 nm.
The pterin cofactor is only loosely bound to cryptochrome, as evidenced by the fact that it is not present in preparations of either cry1 or cry2 protein after purification from baculovirus expression systems. Nevertheless, the pronounced peak of activity seen for cry2 response in living plants suggests that folate is acting as protein-bound cofactor. The peak of UV/A-sensitivity is less pronounced for the cry1 response (Ahmad et al., 2002). It seems unlikely that only cry2 (and not cry1) binds folate cofactor, as the native cry1 protein responds to 380 nm light in living insect cell cultures and is sensitive to folate biosynthesis inhibitors. Also, purified preparations of cry1 from E. coli expression systems bind folate (Malhotra et al., 1995). More likely, the difference in cry1 and cry2 action spectra is due to the production of shielding pigments during the cry1 assay (such as anthocyanins). Alternatively, prolonged irradiation at high light intensity, such as was used in determining cry1 responsivity in plants, may either destroy or cause release of loosely bound folate cofactor from the protein in vivo.
In photolyases, pterin is not essential for activity and can be lost without in any way affecting the DNA repair catalytic function. In Arabidopsis cryptochrome, the photoreceptor functions at wavelength ranges (above 450 nm) well beyond the absorption maximum observed at 380 nm of the putative pterin cofactor. Therefore, flavin must be able to act directly as a light sensor and catalytic cofactor in cryptochromes as well. The role of the pterin is therefore likely to broaden the range of wavelength sensitivity by acting as a light- harvesting antenna pigment in the near-UV range, by analogy with photolyases.
The pterin-binding site has been identified and disrupted by mutation in E. coli photolyase (Schleicher et al., 2005) and also for the cry-DASH cryptochrome cry3 of Arabidopsis (Klar et al., 2006). However, this deduced pterin-binding site is not precisely conserved in Arabidopsis cry1. Further studies are currently in progress to deduce and mutate the pterin-binding site in Arabidopsis cry1.
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METHODS |
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TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODS |
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Plant Culture Conditions and Irradiations
Arabidopsis germination, growth, and irradiation conditions for the action spectrum were carried out essentially as described (Ahmad et al., 2002). Arabidopsis thaliana seeds (ecotype WS) were surface-sterilized and sown on 1% agar plates containing
x MS salts, 2% sucrose, pH 5.5. Plates was placed at 4°C in the dark for 2 d to break dormancy, and then transferred at 22°C to constant white-light illumination until radicle emergence (36 h). Plates were returned to darkness for an additional 2 d at 22°C before light treatments. Average hypocotyl length was between 7 and 9 mm at the time of irradiation. Irradiations were performed using narrow-bandwidth interference filters from Schott industrie at the specified half-bandwidth: 380 ± 10 nm, 402 ± 12 nm, 418 ± 13 nm, 428 ± 10 nm, 438 ± 11 nm, 445 ± 10 nm, 466 ± 11 nm, 471 ± 16 nm, 492 ± 15 nm, 502 ± 15 nm, 515 ± 15 nm, 525 ± 12 nm. Plates were placed in stacks under the light-illumination source to generate a gradient of light intensities.
Western Blotting
Protein from plants was extracted and resolved on SDS gels essentially as described (Ahmad et al., 2002). Bradford assay was performed prior to loading to ensure equal protein concentration. Western transfer and antibody detection was performed by standard methods using anti-cry2 antibody as described (Ahmad et al., 2002). Equivalent load was verified by staining of gels for total protein. Quantification of cry2 protein bands on Western blots was performed by digital imaging techniques using the Shareware imaging software from Biorad, Inc.
Fluorescence Analysis of Arabidopsis cry1 in Living Insect Cells
Expression of Arabidopsis cry1 protein and analysis in the fluorimeter were performed essentially as described (Bouly et al., 2007). Confluent lawns of sf9 insect cells growing in culture flasks were transfected with concentrated supernatant of recombinant virus containing cry1 gene (Lin et al., 1995). Three days after infection, cultures were harvested and resuspended in PBS buffer at pH 7.4. Turbidity of the cells was adjusted to 1.0 OD for comparison with uninfected control cell cultures at the identical concentration. Irradiations were performed on these cells at the specified light intensities and wavelengths at 15°C. For fluorescence measurements, concentrated samples were placed directly in a Varian fluorescence spectrophotometer for analysis of excitation and emission spectra. To ensure that the instrument was correctly calibrated and did not produce artifactual peaks (e.g. at 380 nm), excitation and emission spectra were performed for pure flavin samples (FAD) and proved identical to published values (not shown). For DHAP inhibitor studies, the inhibitor at concentration of either 2 or 5 mM was added directly to growing cell cultures at the time of baculovirus infection. Untreated control-infected cultures were maintained in parallel for comparison of fluorescence excitation and emission spectra. Emission was monitored at 525 nm for detection of oxidized flavin and at 440 nm for detection of folate.
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Acknowledgements |
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We thank Jacqueline Vieira and Karamoko Sy for excellent technical assistance. This work was funded by the CNRS, the French Ministry of Education (contrat ACI) and NSF (0343737). N. Hoang is the recipient of an ACI/BCMS doctoral fellowship.
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