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Plant Physiology 133:1979-1990 (2003) © 2003 American Society of Plant Biologists Light Control of Nuclear Gene mRNA Abundance and Translation in Tobacco1Department of Biochemistry and Molecular Biology, Oklahoma State University, Stillwater, Oklahoma 74078
Photosynthetic signals modulate expression of nuclear genes at the levels of mRNA transcription, mRNA stability, and translation. In transgenic tobacco (Nicotiana tabacum), the pea (Pisum sativum) Ferredoxin 1 (Fed-1) mRNA dissociates from polyribosomes and becomes destabilized when photosynthesis is inhibited by photosynthetic electron transport inhibitor 3-(3,4-dichlorophenyl)-1,1-dimethylurea. We used polymerase chain reaction suppressive-subtractive hybridization to identify similarly regulated endogenous tobacco genes. This screen identified 14 nuclear-encoded tobacco mRNAs whose light-induced increase in abundance is suppressed in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea. Sequence analysis of the cognate cDNAs revealed that nine of the mRNAs encode putative chloroplast-targeted proteins. We asked whether the abundance of these mRNAs was regulated transcriptionally or posttranscriptionally. Of the five mRNAs with sufficient abundance to detect using nuclear run-on assays, we observed transcriptional regulation of  -tubulin, thiazole biosynthetic enzyme, and pSKA10 (an unknown gene). Photosystem A subunit L and, to a lesser extent, -tubulin and pSKA10 mRNAs, may also be stabilized in the light. In contrast, Rubisco small subunit mRNA abundance appears to be transcriptionally up-regulated but posttranscriptionally down-regulated in the light. To determine whether, like Fed-1 mRNA, the mRNAs identified in this screen were translationally responsive to light, we characterized the polyribosome association of these mRNAs in the light and after a 15-min dark treatment. A subset of the mRNAs showed dramatic dark-induced polyribosome dissociation, similar to Fed-1 mRNA, and all of the mRNAs showed at least slight polyribosome dissociation. Thus, both posttranscriptional and translational regulation appear to be important mechanisms regulating the expression of many nuclear-encoded mRNAs encoding proteins involved in photosynthesis.
Plant fitness is enhanced by the ability to rapidly change light-harvesting capabilities in response to fluctuating light conditions (Kulheim et al., 2002  ). The genes for mRNAs encoding chloroplast proteins are divided between the nuclear and the chloroplast genome and are coordinately regulated in response to light, maximizing energy storage while minimizing photo-oxidative damage (for review, see Goldschmidt-Clermont, 1998; Barkan and Goldschmidt-Clermont, 2000; Brown et al., 2001; Rochaix, 2001). Photosynthetic control of the abundance of chloroplast-encoded mRNAs occurs at the levels of transcription, mRNA processing, and mRNA stability (Kubicki et al., 1994; Nickelsen et al., 1994; Alexciev and Tullberg, 1997; Deshpande et al., 1997; Yamamoto et al., 1997; Pfannschmidt et al., 1999; Tullberg et al., 2000). In addition, in depth study of many Chlamydomonas reinhardtii chloroplast-encoded mRNAs has revealed the importance of photosynthetic regulation of translation, often via binding of the encoded protein to the 5'- or 3'-untranslated region (UTR) of the corresponding chloroplast mRNA (for review, see Bruick and Mayfield, 1999). Light-regulated binding of proteins to mRNAs may be regulated, at least in part, by changes in redox state generated by photosynthesis (Kim and Mayfield, 1997; Yohn et al., 1998; Fong et al., 2000; Shen et al., 2001). Photosynthetic inhibitors have been used widely to distinguish redox regulators of chloroplastic gene expression, implicating the ferredoxin/thioredoxin, glutathione, and PRK/chloroplast protein 12 (CP12)/GAPDH complexes in the signal transduction chain within chloroplasts (Wedel et al., 1997; Vener et al., 1998; Irihimovitch and Shapira, 2000; Trebitsh and Danon, 2001).
Regulation of gene expression between the chloroplast and nucleus includes cross-signaling between the organelles. In addition to the complex effects of photoreceptor signals on nuclear mRNA transcription (for review, see Quail, 2002
To maintain appropriate stoichiometry between photosystems in response to light quality, promoters for a number of nuclear-encoded genes encoding chloroplast-localized proteins have differential responsiveness to oxidative and reductive signals (Pfannschmidt et al., 2001
As with chloroplast-encoded mRNAs, photosynthetic signals have been shown to regulate mRNA stability of a few nuclear-encoded mRNAs. Constitutively transcribed pea (Pisum sativum) Fed-1 mRNA in transgenic tobacco (Nicotiana tabacum) accumulates in the light. However, in the dark or in the presence of DCMU in the light, Fed-1 mRNA is destabilized (Petracek et al., 1998
In a few cases, photosynthetic signals have been shown to have profound effects on the translational regulation of nuclear-encoded genes. Darkness or treatment with DCMU induces a rapid (within 20 min) and reversible dissociation of Fed-1 mRNA from polyribosomes, with a concomitant decline in the in vivo translation rates of Fed-1 mRNA (Petracek et al., 1998
Little is known about the mechanisms by which light regulates cytoplasmic mRNA translation. However, recent results suggest the striking possibility that translation of the rye (Secale cereale) Cat1 mRNA may occur via direct modification of the mRNA. Rye Cat1 mRNA isolated from light-exposed leaves was translated more efficiently in vitro than Cat1 mRNA isolated from dark-exposed leaves (Schmidt et al., 2002 Here, we discuss the isolation of endogenous tobacco mRNAs whose abundance is either repressed or enhanced in the presence of DCMU. Strikingly, many of these mRNAs identified encode proteins involved in photosynthesis, suggesting that photosynthesis may regulate the mRNA levels of many genes involved in photosynthesis. In addition, we investigated the possibility that the mRNAs regulated at the level of abundance are also regulated at the level of translation. We examined the polyribosome loading profile of each of these mRNAs in the light and after a short dark treatment. A subset of the identified mRNAs showed substantial and rapid dark-induced dissociation from polyribosomes, suggesting that light has a substantial impact on the translation of many nuclear mRNAs encoding proteins involved in photosynthesis.
Isolation of Tobacco Leaf mRNAs Less Abundant in the Presence of Photosynthetic Electron Transport Inhibitor DCMU
Previously, we showed that the abundance of Fed-1 mRNA in transgenic tobacco is regulated by photosynthesis. Upon shift from dark to light, Fed-1 mRNA abundance increases 3- to 4-fold, and this increase is blocked by the addition of DCMU (Petracek et al., 1997 We used northern-blot analysis as an independent method to determine whether photosynthesis regulates the abundance of the identified mRNAs. Total RNA was extracted from plants transferred from darkness to light in the absence or presence of DCMU, transferred to nylon membrane, and hybridized with cDNA-specific probes. Examples of these analyses are shown in Figure 1, and a summary of the quantitative analyses is presented in Table I. Three cDNAs (not listed in Table I) were identified as differentially regulated in the secondary screen but were not detectable by northern analysis and thus were not analyzed further (pSK175, a putative 9-cis-epoxycarotenoid dioxygenase 4 [NCED1], and pSKD70). Of the detectable mRNAs, five showed a 3-fold or greater accumulation, and 14 showed at least a 1.4-fold greater accumulation in light versus light plus DCMU (Table I). Thus, this screen successfully identified mRNAs whose abundance is regulated by light in the absence, but not the presence, of DCMU.
Nine of the predicted proteins (LHC-I, ribosomal protein L29 [RPL29], CP12, photosystem II subunit X [PSII-X], PSAL, photosystem A subunit K [PSAK], PSAF, and the 33-kD precursor protein of oxygen-evolving complex [OEC 33 kDa]) contain a predicted chloroplast signal peptide (Table I) and localize to the chloroplast (Palomares et al., 1991
Four of the identified cDNAs (CAB16, CAB4, CAB10-like, and CAB36-like) represent light-harvesting complex II (B) mRNAs and were named in relation to genes already in GenBank. Northern-blot analyses (Fig. 1; Table I) indicate that DCMU has either little or no effect on the abundance of these mRNAs, or in some cases, DCMU may even slightly increase their abundance. Although such a category of mRNAs was unexpected based on our experimental design, these results are similar to previously published reports on the lack of effect of DCMU on CAB mRNA levels (Escoubas et al., 1995
Light regulation of mRNA abundance can occur either via regulation of promoter activity (transcriptional regulation) and/or regulation of mRNA stability (posttranscriptional regulation). We used nuclear run-on assays to determine whether light altered the rates of transcription of the genes we identified in our screen. Five-week-old 35S:Fed-1 transgenic tobacco plants were transferred to the dark for 40 h and then either brought to the light or left in the dark for an additional 6 h. Nuclei were isolated, and run-on nuclear RNAs were labeled with 32P and hybridized to each of the differentially expressed cDNAs. Run-on analysis of many of these RNAs was not possible because the signals were not sufficiently above background levels of hybridization to vector only (pKS-; Fig. 2) and salmon sperm DNA (S. Bhat, data not shown). However, five endogenous tobacco mRNAs and the Fed-1 RNA expressed from the transgene were clearly detectable above background (Fig. 2). These assays indicate that Fed-1 transcription rates are the same in the light and the dark (Fig. 2), whereas Fed-1 mRNA shows a 4-fold increase in the light compared with the dark (Fig. 1), consistent with our observation that dark results in a decreased half-life of Fed-1 mRNA (Petracek et al., 1998
As expected, we also identified genes that appear to be mainly regulated at the level of transcription by light. THI1 mRNA showed similar differences in run-on assays compared with steady-state mRNA accumulation between the light and dark, suggesting transcriptional control of THI1. In strong contrast to the other mRNAs, RBCS mRNA showed a dramatic 13-fold higher rate of transcription in the light compared with in the dark, but only a 2-fold difference in steady-state mRNA accumulation (P < 0.05; Table I; Fig. 2). These results suggest that transcription of RBCS mRNA is higher in the light but that the mRNA is destabilized in the light or stabilized in the dark, resulting in counterbalancing effects on RBCS mRNA accumulation.
In transgenic tobacco, Fed-1 mRNA expression is responsive to the dark at the levels of both abundance and translation (Dickey et al., 1992
To help define the mRNAs involved in the most rapid translational response to darkness, we asked whether the mRNAs we identified were represented among the mRNAs that rapidly dissociate from polyribosomes after a short dark treatment using polyribosome profile analyses. Leaves from 6-week-old tobacco grown in soil on a 12-h-light/12-h-dark cycle were harvested 6 h into the light cycle or after being transferred to the dark for 15 min. Crude extracts were resolved on Suc gradients, fractions were collected, and RNA was isolated and subjected to northern-blot analysis. During fractionation, the total UV254 absorbance profiles were recorded, allowing detection of RNA in polyribosomes (fractions approximately 8-12) and the free 80S monosome (Fig. 3A). As seen previously for a 20-min dark treatment (Hansen et al., 2001
The mRNAs we identified have different levels of reduced polyribosome dissociation after a 15-min dark treatment (Fig. 3, B and C; Table II). Figure 3B shows northern-blot hybridization of four representative mRNAs covering the range of dark-induced polyribosome dissociation, from the greatest to the least dissociation response. Figure 3C shows the quantitation of specific RNAs in the Suc gradient fractions. The gene-specific mRNAs showing the greatest to the least degree of polyribosome dissociation are arranged from the left to the right. All mRNAs examined after a short 15-min dark treatment show at least a slight dissociation from polyribosomes, with a shift primarily to fraction 2 (Fig. 3C; Table II). Furthermore, the degree of polyribosome dissociation in the dark seems to be independent of the level of initial polyribosome association in the light (e.g. compare PSAK and LHCI in Fig. 3B; Table II). By comparison with the overall UV profile (Fig. 3A), fraction 2 is likely to represent non-translated mRNP complexes, and an increase of many mRNAs in these fractions with a concomitant decrease in the polyribosome fractions suggests that there is a rapid but modest overall decrease of total translation in response to dark. Despite this general trend, the mRNAs show strikingly different degrees of response. Using a one-tailed two independent sample t test, we asked whether the observed increases in fraction 2 hybridizing mRNA in the dark or the decreases in polyribosomal hybridizing mRNA were statistically significant. In the dark, 15 of the mRNAs showed a statistically significant decrease in polyribosome association and eight of the mRNAs show statistically significant increases in fraction 2 hybridizing mRNA (Table II). Some mRNAs respond similarly to the transgenic Fed-1 mRNA (e.g. CAB10-like, CAB4, OEC 33 kDa, and pSKA10). These mRNAs exhibit a
We have identified endogenous tobacco nuclear-encoded mRNAs whose accumulation and/or translation is sensitive to photosynthesis. Photosynthesis regulates these mRNAs (to varying degrees) at the levels of transcription, mRNA stability, and translation. Surprisingly, it appears that these modes of regulation are sometimes in opposition to each other. As has been observed for the handful of previously studied nuclear-encoded mRNAs (Pfannschmidt, 2003 ), most of the DCMU-sensitive mRNAs we identified encode chloroplast-targeted proteins or stress-related proteins, suggesting a common signaling mechanism that regulates the production of these types of proteins in response to the quality and quantity of light (Table I).
All of the mRNAs isolated in this screen show at least a small decrease in accumulation in polyribosomal fractions in response to a short dark treatment (Fig. 3C; Table I). These data are consistent with our previous studies in which we observed an overall decrease in polyribosomes within 15 to 20 min in the dark, with increased time in the dark resulting in further dissociation of mRNAs from polyribosomes (Hansen et al., 2001
Whether or not the decreased polyribosome recruitment for the individual mRNAs is via the same mechanism or different mechanisms remains to be determined. One possibility is that the activity of a general factor involved in translation may be regulated by dark. For example, perhaps dark regulates the association of eIF3e with a component of the COP9 signalosome (Yahalom et al., 2001 Our data indicate that some mRNAs show a much more dramatic decline than other mRNAs in mRNA levels and/or shift off polyribosomes in response to a 15-min dark treatment (`Fig. 3, B and C). Thus, it is likely that there are also mRNA-specific dark-induced translational and mRNA abundance responses. Most of the nuclear mRNAs we identified encode proteins targeted to the chloroplast, strongly suggesting that many mRNAs of this category are dramatically regulated by dark and photosynthesis at the levels of mRNA abundance and, often, translation. The functional significance of this observation will require identification of the signaling pathways involved and the mechanisms of regulation of mRNA abundance and translation by light.
Related genes from different plant species may have different responses to dark or decreased photosynthesis. In transgenic tobacco, both the pea and tobacco ferredoxin genes show light-regulated translation (Hansen et al., 2001 That a number of mRNAs are considerably more translationally sensitive to dark than others suggests the presence of a common mechanism and, likely, common sequence elements mediate the conserved translational response. However, analysis of 5'-UTRs of this category of mRNAs does not reveal any clear conserved elements or structural patterns (data not shown). This suggests that the regulatory motifs may be complex and bipartite and/or involve sequences in addition to, or other than, those within the 5'-UTR.
The pea Fed-1 mRNA in transgenic tobacco shows similar posttranscriptional regulation both by dark and by DCMU in the light (Petracek et al., 1997
The mechanism(s) for photosynthetic regulation of nuclear gene expression is yet unclear, but it likely involves signals from the chloroplast. A number of molecules have been previously implicated in chloroplast-mediated signaling and are potential candidates for signaling pathways. First, a small redox molecule, such as oxygen, could diffuse across the chloroplast membranes and alter the redox state of regulatory proteins (Danon, 2002
How could chloroplastic signals alter mRNA stability or translation? First, mRNA binding proteins recognize a subset of mRNAs, and binding of these proteins to their target mRNAs may regulate their stability and translation. If the interaction of these mRNA-binding proteins is regulated by a photosynthesis-responsive, posttranslational modification (e.g. redox changes, phosphorylation, or methylation), then photosynthesis could affect mRNA abundance and/or translation. Alternatively, mRNA-specific binding proteins may not mediate regulation of mRNA abundance. Rather, perhaps photosynthetic metabolites, such as NADPH or DHAP, directly bind target mRNAs in a light-responsive manner, resulting in an altered structure of the mRNA resulting in regulation of mRNA abundance and/or translation. Consistent with this idea, in bacteria, signaling molecules and metabolites can bind directly and specifically to target mRNAs, resulting in regulation of gene expression (Mironov et al., 2002
Plant Growth
Tobacco seedlings were germinated in sterile Magenta boxes with membrane rafts (V8380 and M1917, Sigma-Aldrich, St. Louis) in sterile Murashige and Skoog medium (Invitrogen, Grand Island, NY) for the PCR-select library or on 0.5x Murashige and Skoog/1.5% (w/v) agarose petri plates for subsequent DCMU or light/dark mRNA abundance analysis, as described (Petracek et al., 1997
Plants were treated with DCMU as described (Petracek et al., 1997
Total RNA was prepared as described (Thompson et al., 1983
For cDNA library preparation, mRNA was isolated from 400 µg of total tobacco leaf RNA using the MicroPoly(A) Pure kit (Ambion, Austin, TX) following the manufacturer's instructions. Approximately 2 µg of the resulting poly(A) mRNA was then used to create a PCR-select cDNA library (BD Biosciences Clontech, Palo Alto, CA) following the manufacturer's instructions, using light-treated samples as the tester cDNA and DCMU/light-treated samples as the driver cDNA. The resulting PCR samples were cloned into pGEM-T (Promega Biotech, Madison, WI) or PCR-Script Amp (Stratagene, La Jolla, CA). The resulting cDNAs were screened with the reverse-subtracted cDNAs using the PCR-Select Differential Screening kit (BD Biosciences Clontech) to identify cDNAs likely to represent mRNAs differentially expressed in light-treated versus DCMU/light-treated plants. Positive candidate cDNAs were then used as probes in northern-blot hybridization analysis (Dickey et al., 1992
Upon request, all novel materials described in this publication will be made available in a timely manner for noncommercial research purposes, subject to the requisite permission from any third-party owners of all or parts of the material. Obtaining any permission will be the responsibility of the requestor.
Polyribosome analyses were performed as described (Petracek et al., 1997
Nuclei isolation was as described by Folta and Kaufman (2000 Two micrograms of each denatured cDNA-containing plasmid was dot blotted onto Gene Screen nylon membranes using a Hybri-Dot Manifold (Invitrogen). The membranes were prehybridized overnight at 42°C in 1 mL of 1.1x hybridization buffer and then probed with 32P-labeled run-on RNA for 72 h at 42°C. Membranes were washed twice in 2x SSC and 0.1% (w/v) SDS at 42°C for 15 min each, followed by three washes in 0.5x SSC and 0.1% (w/v) SDS at 68°C for 30 min each. Blots were exposed to Kodak XB-1 film with intensifying screens for 24 to 48 h at -70°C and to phosphor imager screens for quantitation.
We thank Tamyra Ravenel, Darnell Graham, Jennifer Barker, Xiao-Ping Guo, Angie Phillips, Claudia Dollins, and Sabith Erra for excellent technical assistance. We are appreciative of the help with the statistical analyses provided by Larry Claypool. Finally, we are grateful to Lynn Dickey for helpful discussions and to Mark Longtine for useful editorial comments. Received July 3, 2003; returned for revision August 4, 2003; accepted September 2, 2003.
1 This work was supported by the U.S. Department of Agriculture (grant no. 98-35301-7012 to M.E.P.) and by the Oklahoma Agricultural Experiment Station (project no. H-2427).  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.029686. * Corresponding author; fax 405-744-7799; e-mail marie_petracek{at}biochem.okstate.edu.
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ABSTRACT
RESULTS
6 L) or presence (40D
2-fold dissociation from polyribosomes (P < 0.01; 
-mercaptoethanol, and 1 mM aurin tricarboxylic acid [ATA; Sigma-Aldrich]). ATA was omitted from samples used for cDNA preparation. Samples were centrifuged at 11,000g for 30 min at 4°C, the supernatant was removed, and the pellet resuspended in 100 µM ATA in water or, in samples used to produce cDNA, in water alone. The resuspended RNA was then precipitated with ammonium acetate and ethanol at -80°C overnight and collected at 11,000g for 30 min at 4°C. The resulting pellet was resuspended in 100 µM ATA water or water alone. All water used was treated with DEPC. 
