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GENETICS, GENOMICS, AND MOLECULAR EVOLUTION

Transcriptional Gene Silencing Mediated by a Plastid Inner Envelope Phosphoenolpyruvate/Phosphate Translocator CUE1 in Arabidopsis^1,[OA]

State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100193, China (J.S., X.R., R.C., J.L., Z.G.); China Agricultural University-University of California Riverside Center for Biological Sciences and Biotechnology, Beijing 100193, China (Z.G.); and National Center for Plant Gene Research, Beijing 100193, China (Z.G.)

	ABSTRACT

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Mutations in REPRESSOR OF SILENCING1 (ROS1) lead to the transcriptional gene silencing (TGS) of Pro_RD29A:LUC (LUCIFERASE) and Pro_35S:NPTII (Neomycin Phosphotransferase II) reporter genes. We performed a genetic screen to find suppressors of ros1 that identified two mutant alleles in the Arabidopsis (Arabidopsis thaliana) CHLOROPHYLL A/B BINDING PROTEIN UNDEREXPRESSED1 (CUE1) gene, which encodes a plastid inner envelope phosphoenolpyruvate/phosphate translocator. The cue1 mutations released the TGS of Pro_35S:NPTII and the transcriptionally silent endogenous locus TRANSCRIPTIONAL SILENCING INFORMATION in a manner that was independent of DNA methylation but dependent on chromatin modification. The cue1 mutations did not affect the TGS of Pro_RD29A:LUC in ros1, which was dependent on RNA-directed DNA methylation. It is possible that signals from chloroplasts help to regulate the epigenetic status of a subset of genomic loci in the nucleus.

ROS1 encodes a DNA glycosylase/lyase, and its mutations lead to TGS of originally active Pro_RD29A:LUC (LUCIFERASE) and Pro_35S:NPTII (Neomycin Phosphotransferase II) reporter genes in a T-DNA region. Screening for suppressors of the ros1 mutant using silenced Pro_35S:NPTII as a selection marker has identified two genes encoding RPA2A/ROR1 and TSL in previous studies (Kapoor et al., 2005; Xia et al., 2006; Wang et al., 2007). An independent screening for ros1 suppressors using silenced Pro_RD29A:LUC as a selection marker has identified several genes, including NUCLEAR RNA POLYMERASE D (NRPD1/NRPD1a), NUCLEAR RNA POLYMERASE E (NRPE1/NRPD1b), NRPD2a, RNA-DIRECTED DNA METHYLATION2 (RDM2), ARGONAUTE4 (AGO4), HUA ENHANCER1 (HEN1), DEFECTIVE IN RNA-DIRECTED DNA METHYLATION1 (DRD1), and HISTONE DEACETYLASE6 (HDA6; He et al., 2009). Mutations in RDM2, NRPD1, NRPE1, NRPD2a, HEN1, and DRD1 release the TGS of only Pro_RD29A:LUC but not Pro_35S:NPTII, suggesting the biological roles of these genes in the small interfering RNA (siRNA)-directed DNA methylation pathway. Mutations in HDA6 and AGO4 reactivate the expression of both silenced Pro_RD29A:LUC and Pro_35S:NPTII, suggesting that the two proteins mediate TGS in both siRNA-directed DNA methylation-dependent and -independent pathways (He et al., 2009). Here, we characterized two new alleles of the Arabidopsis CHLOROPHYLL A/B BINDING PROTEIN UNDEREXPRESSED1 (CUE1) gene encoding a plastid inner envelope phosphoenolpyruvate/phosphate translocator (PPT; Li et al., 1995; Streatfield et al., 1999). cue1 mutations release the TGS of TSI and silenced Pro_35S:NPTII in ros1, but not Pro_RD29A:LUC, suggesting that the possible signals from chloroplasts not only regulate nuclear gene expression but also modulate nuclear epigenetic status in an siRNA-directed DNA methylation-independent manner in Arabidopsis.

	RESULTS

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cue1 Mutants Show a Release of TGS of Pro_35S:NPTII

The ros1-1 mutant was isolated in a previous study in the C24 background, which carries a T-DNA insertion with silenced Pro_RD29A:LUC and Pro_35S:NPTII genes. Two allelic mutants, named cue1-101 and cue1-102, were isolated during a genetic screening for suppressors of ros1-1 on Murashige and Skoog (MS) agar medium containing 40 mg L^–1 kanamycin. Both mutants showed a similar reticulate leaf phenotype. We used map-based cloning to identify the CUE1 gene encoding a plastid inner envelope PPT with six transmembrane domains that imports phosphoenolpyruvate into plastids (Fischer et al., 1997; Streatfield et al., 1999; Knappe et al., 2003). After sequencing the CUE1/AT5G33320 gene, we found a G₁₆₃₉-to-A₁₆₃₉ point mutation that changed Gly-251 to Glu-251 in ros1-1 cue1-101. Gly-251 lies between transmembrane domains III and IV in a region that is highly conserved in different PPTs from Arabidopsis, cauliflower (Brassica oleracea), tobacco (Nicotiana tabacum), and maize (Zea mays) and also in other chloroplast triose phosphate/phosphate translocators (Fischer et al., 1997). In cue1-102 ros1-1, a G₈₈₆-to-A₈₈₆ point mutation that disrupts the acceptor splicing site in the first intron of the CUE1 gene was found. This mutation is expected to produce an abnormal mRNA that would be translated into a truncated protein due to a putative early stop codon. As shown in Figure 1B , cue1-101 ros1-1 and cue1-102 ros1-1 seedlings were more resistant than ros1-1 seedlings to kanamycin but less resistant than the wild type, suggesting that the cue1 mutations only partially released the TGS of Pro_35S:NPTII. Northern-blot analysis indicated that both cue1-101 ros1-1 and cue1-102 ros1-1 expressed more NTPII transcripts than ros1-1 but less than the wild type (Fig. 1E), which is consistent with the phenotypes of the seedling growth on kanamycin. However, a ddm1 mutant allele (named ddm1-101) isolated during our ros1 suppressor screening increased the NPTII expression at a much higher level even than wild-type C24 (Fig. 1E). Because Pro_RD29A:LUC and endogenous RD29A are silenced in the ros1 mutant, we also analyzed their gene expression. COR47 and RD29A are two stress-inducible genes with similar inducible patterns under abscisic acid (ABA) or other abiotic stress treatments (Xia et al., 2006). Under 100 µM ABA treatment for 3 h, the silenced Pro_RD29A:LUC or endogenous RD29A was reactivated in the C24 wild type, but not in ros1-1, cue1-101 ros1-1, or cue1-102 ros1-1 based on bioluminescence analysis (Fig. 1D) and northern blot (cue1-101 ros1-1; Fig. 1F). As a control, the COR47 gene was expressed at similar levels in the wild type, ros1-1, and cue1-101 ros1-1 (Fig. 1F).

View larger version (126K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 1. cue1 mutations released TGS of 35S-NPTII but did not affect the expression of RD29A-LUC or endogenous RD29A gene. A, Seedling growth on MS agar medium. WT, C24 wild type, which carried a T-DNA insertion locus; ros1-1, a mutation in the ROS1 gene that led to TGS of ProRD29A:LUC and Pro35S:NPTII in the T-DNA region as well as to TGS of the endogenous RD29A gene; cue1-101 ros1-1 and cue1-102 ros1-1, two mutant alleles isolated in this study. B, Wild-type, ros1-1, cue1-101 ros1-1, and cue1-102 ros1-1 seedlings grown for 2 weeks on MS agar medium supplemented with 40 mg L–1 kanamycin. C and D, Seedlings grown on MS agar medium were treated with 100 µM ABA for 3 h (C), and then the expression of ProRD29A:LUC was imaged by luminescence analysis (D). Luminescence was not detected in ros1-1, cue1-101 ros1-1, or cue1-102 ros1-1 but was detected in the C24 wild type. E, NPTII expression in the wild type (lane 1), ros1-1 (lane 2), cue1-101 ros1-1 (lane 3), cue1-102 ros1-1 (lane 4), and ddm1-101 ros1-1 (lane 5). The ddm1-101 ros1-1 mutant was isolated during our ros1 suppressor screening. rRNAs were used as a loading control. F, RD29A and LUC expression under no stress conditions (wild type [lane 1], ros1-1 [lane 2], and cue1-101 ros1-1 [lane 3]) or after 100 µM ABA treatment for 3 h (wild type [lane 4], ros1-1 [lane 5], and cue1-101 ros1-1 [lane 6]). COR47 was used as a control for ABA-inducible gene expression, and Tubulin was used as a loading control.

TSIs are silenced markers frequently used in TGS analysis (Steimer et al., 2000). The expression of TSIs was barely detected in the wild type or ros1-1. TSI transcripts were expressed at higher levels in cue1-101 ros1-1 and cue1-102 ros1-1 than in the wild type or the ros1-1 single mutant, although the expression in the suppressor mutants was much lower than in ddm1-101 (Fig. 2A ). TSI transcripts were increased slightly more in cue1-101 and cue1-102 single mutants than in cue1-101 ros1-1 and cue1-102 ros1-1 double mutants (Fig. 2A). These results indicate that cue1 mutations release the TGS of not only a transgene but also endogenous genes in Arabidopsis.

View larger version (85K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 2. cue1 mutations released the TGS of TSI but did not affect DNA methylation. A, TSI expression in different plants. ACTIN was used as a loading control. cue1 single mutations tended to increase TSI transcripts more than the cue1 ros1-1 double mutation. B, The expression of TSI and NPTII genes in cue1-101 ros1-1 seedlings was partially rescued by feeding different aromatic amino acids. cue1-101 ros1-1 seedlings were grown on MS agar medium or MS agar medium containing 1 mM Phe, 1 mM Trp, 1 mM Tyr, or all three aromatic acids (1 mM for each) together for 10 d. Total RNAs were isolated and used for northern blot with 32P-labeled NTPII or TSI probes. rRNAs were used as loading controls. C, Bisulfite sequencing analysis of DNA methylation in endogenous RD29A promoter and transgenic RD29A promoter. No DNA methylation difference was found between ros1-1 and cue1-101 ros1-1. D, DNA methylation analysis in the wild type, ros1-1, cue1-101 ros1-1, and cue1-102 ros1-1 at rDNA and centromeric DNA (cen-DNA) digested with HpaII or MspI. WT, C24 wild type.

TGS is mediated by both DNA methylation and/or histone modifications. We analyzed the DNA methylation status of RD29A promoters in both the T-DNA region and in the endogenous gene by bisulfite sequencing. There is no evidence for a DNA methylation difference between cue1-101 ros1-1 or cue1-102 ros1-1 and ros1-1 (Fig. 2C). We also analyzed the centromeric DNA and 180-bp rDNA regions using DNA methylation-sensitive restrictive enzymes but found no difference in DNA methylation (Fig. 2D). These results suggest that the cue1 mutation releases TGS in a siRNA-directed DNA methylation-independent pathway.

cue1 Mutations Decrease H3K9m2 But Do Not Change the Overall Heterochromatin Status

We then performed a chromatin immunoprecipitation (ChIP) assay to determine the effect of cue1 mutations on histone modifications in different genomic regions. Histone H3 acetylation (H3Ac) is a marker for transcriptional activation, while histone H3 Lys-9 dimethylation (H3K9m2) is a transcriptional silencing marker. We chose the ACTIN promoter as a control for active genes. When no antibodies were added, no PCR products were amplified (Fig. 3A ). Consistent with previous results, the ros1 mutation increased H3K9m2 at the 35S promoter, TSI, and LUC regions compared with the wild type (Xia et al., 2006). H3K9m2 was reduced at both the TSI and 35S promoter regions but was not changed at the Pro_RD29A:LUC locus in cue1-101 ros1-1. For histone H3Ac, we observed a clear decrease at 35S and LUC in ros1-1 and similar levels at 35S in the wild type and cue1-101 ros1-1, but no difference was seen at TSI among the three genotypes. Although a minor change in H3Ac levels at LUC in cue1-101 ros1-1 was detected, we did not detect a change in RD29A expression in our experimental conditions. Monomethylated and dimethylated histone H3K9 are enriched around Arabidopsis pericentromeric heterochromatin (Naumann et al., 2005). We performed an immunostaining assay to detect the distribution of H3K9m2 in nuclei using anti-H3K9m2 antibodies. As shown in Figure 3B, no apparent difference was found for immunostaining of H3K9m2 among the wild type, ros1-1, and cue1-101 ros1-1. The above results indicate that the cue1 mutation affects TGS of some loci by changing chromatin modifications but does not influence the global H3K9m2.

View larger version (48K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 3. ChIP analysis of TSI, 35S promoter, and ProRD29A:LUC regions and dimethylated H3K9 immunostaining in nuclei. A, ChIP analysis in partial TSI as well as in LUC and 35S promoter regions using specific antibodies against dimethylated H3K9 (anti-H3K9m2) and histone H3 acetylation (anti-H3Ac). PCR amplification of ACTIN was used as a control. No-antibody precipitation was used as a mock control. B, Immunostaining with anti-dimethylated H3K9 antibody and 4',6-diamino-phenylindole (DAPI) counterstaining in nuclei. No heterochromatin difference was found among the wild type, ros1-1, and cue1-101 ros1-1. WT, Wild type.

Previous studies indicated that plants with mutant alleles for several genes (BRU1, FAS1, RPA2A/ROR1, TSL, and others) affecting TGS are also sensitive to the DNA-alkylating agent methylmethane sulfonate (MMS; Takeda et al., 2004; Xia et al., 2006; Wang et al., 2007). These genes are all thought to be involved in DNA repair. In order to determine whether cue1 mutations influence DNA repair, we examined the sensitivity of cue1 seedlings to different concentrations of MMS. Five-day-old seedlings were transferred to MS medium containing different concentrations of MMS and cultured for an additional 7 d. As shown in Figure 4 , cue1 seedlings were smaller than the wild type under normal growth conditions (Li et al., 1995; Streatfield et al., 1999). MMS treatment inhibited the growth of all plants and caused yellowing of the leaves. However, the yellowing of leaves was more severe in the C24 wild type and ros1-1 than in cue1-101 ros1-1 or cue1-101, suggesting that cue1 seedlings are more resistant to MMS. These results suggest that the biological role of CUE1 in DNA repair is different from that of other known proteins (Takeda et al., 2004; Xia et al., 2006; Wang et al., 2007).

View larger version (52K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 4. cue1 seedlings were more resistant to MMS treatment than the wild type (WT) and ros1-1. Five-day-old seedlings were transferred to MS agar medium containing different concentrations of MMS and were photographed 7 d later. Different seedlings treated with the same concentration of MMS were grown on the same plate for comparison.

	DISCUSSION

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The TGS mechanism at the Pro_35S:NPTII locus differs from that at Pro_RD29A:LUC (Xia et al., 2006; He et al., 2009). The TGS at the Pro_RD29A:LUC locus is caused by small RNA-directed DNA methylation (Gong et al., 2002), while the TGS of Pro_35S:NPTII is not related to siRNA-directed DNA methylation but likely results from a heterochromatin-spreading pathway (Kapoor et al., 2005; Xia et al., 2006; Wang et al., 2007; He et al., 2009). Blocking small RNA production in ros1 releases the TGS of Pro_RD29A:LUC but not that of Pro_35S:NPTII, suggesting that these two loci possess different TGS mechanisms (Kapoor et al., 2005; Xia et al., 2006; Wang et al., 2007; He et al., 2009). Mutations in CUE1 influenced the histone H3K9 dimethylation and H3 acetylation only at some loci, suggesting that these signals produced by CUE1 mutations influence TGS independent on DNA methylation, probably by modulating histone modifications in the affected loci, but did not affect global histone modifications.

Proteins such as BRU1, FAS1, FAS2, RPA2A/ROR1, ABO4/DNA polymerase , TSL, and MORPHEUS' MOLECULE1 (MOM1) are required for maintenance of TGS at TSI independent of DNA methylation (Takeda et al., 2004; Elmayan et al., 2005; Kapoor et al., 2005; Shaked et al., 2006; Xia et al., 2006; Wang et al., 2007). Except for MOM1, all other proteins also function in DNA repair, as plants with mutations in these genes are sensitive to DNA damage regents (Takeda et al., 2004; Elmayan et al., 2005; Kapoor et al., 2005; Shaked et al., 2006; Xia et al., 2006; Wang et al., 2007). cue1 mutants were more resistant to MMS than the wild type. Clearly, CUE1 affects nuclear genome stability through a different new pathway. Our studies suggest that signals from chloroplasts might be essential for coordinating both gene expression and chromatin structures. Such coordination may be required for appropriate short-term responses to environmental changes and possibly also for long-term, evolutionary adaptation to environmental stresses by eliciting epigenetic changes (Yin et al., 2009).

	MATERIALS AND METHODS

TOP ABSTRACT RESULTS DISCUSSION MATERIALS AND METHODS LITERATURE CITED

 

Plant Materials and Growth Conditions

Arabidopsis (Arabidopsis thaliana) seedlings were grown on MS (Sigma) medium supplemented with 3% Suc and 0.8% agar in a growth chamber using a 16-h-light/8-h-dark cycle at 22°C with light intensity of 50 µmol m^–2 s^–1 and 70% relative humidity. For aromatic amino acid feeding assay, seeds were sown on MS agar medium or MS agar medium supplemented with 1 mM Phe, 1 mM Trp, 1 mM Tyr, or all three aromatic acids (1 mM for each) together and cultured in a growth chamber for 10 d.

Mutant Screening, Genetic Analysis, and Position Cloning

Ethyl methanesulfonate mutagenesis and screening of mutants were performed as described before (Xia et al., 2006). We identified two allelic mutants that showed similar kanamycin sensitivity and exhibited reticulate leaf phenotypes. Each of the two mutants was backcrossed to ros1-1, and the F2 population showed 1:3 segregation of kanamycin-resistant to kanamycin-sensitive phenotype. All kanamycin-resistant mutants also had the reticulate leaf phenotype, suggesting that the kanamycin-resistant phenotype was linked to the reticulate leaf phenotype. The reticulate leaf phenotype was used to isolate the mutants. The simple sequence-length polymorphisms were used to map the gene. We narrowed the mutation around CUE1/AT5G33320. The mutations were found by sequencing the full-length AT5G33320 from two mutants.

Nucleic Acid Isolation and Gel-Blot Analysis

Total genomic DNA was digested by methylation-sensitive restriction enzymes HpaII and MspI. DNA methylation analysis was performed as described previously using rDNA and 180-bp centromere DNA as probes by Southern-blot analysis (Xia et al., 2006). For northern-blot analysis, 20 µg of total RNAs isolated from 2-week-old seedlings (treated or not with 100 µM ABA for 3 h) were resolved on 2% formaldehyde gels and blotted onto Hybond N+ membranes (Amersham). NPTII, TSI, rDNA, and the 180-bp centromeric repeat were labeled with [-³²P]dCTP using a random priming labeling kit (Takara) as described previously (Xia et al., 2006).

Bisulfite Sequencing

Genomic DNA (2 µg) was digested with EcoRI, EcoRV, and HindIII. Digested DNA was used for bisulfite treatment as described previously (Wang et al., 2007). Bisulfite-treated DNA was amplified using endogenous and transgenic RD29A promoter primer pairs (Xia et al., 2006). Amplified PCR fragments were cloned into pMD18-T vector (Takara). About 15 randomly selected clones were sequenced for each genotype. The sequences of the different genotypes were compared, and the percentage of methylation at endogenous and transgenic RD29A promoters was calculated.

ChIP Assay

ChIP assays were performed using a previously described method (Xia et al., 2006). Chromatins were immunoprecipitated with anti-H3 dimethyl K9 antibodies (Upstate) and anti-H3 acetyl antibodies (Upstate). Immunoprecipitated DNA was purified and analyzed with PCR using primer pairs TSI, LUC, 35S promoter, and ACTIN promoter as described (Xia et al., 2006). At least three independent experiments were done and showed similar results.

MMS Treatment

Five-day-old seedlings were transferred to MS agar medium supplemented with different concentrations of MMS. Seedlings were photographed 7 d later.

Immunostaining

Preparation of plant nuclei and immunostaining experiments were performed as described before (Probst et al., 2004). Anti-Lys-9 dimethylated H3 (Upstate; 07-441) antibody was diluted 1:100 and incubated with the blocked slides in the solution of 1% bovine serum albumin in phosphate-buffered saline (overnight at 4°C). An anti-rabbit fluorescein isothiocyanate-coupled antibody was applied to detect the signals (Molecular Probes; 1:100, 37°C, 40 min) in 0.5% bovine serum albumin in phosphate-buffered saline, and DNA was counterstained with 4',6-diamino-phenylindole.

Sequence data from this article can be found in the GenBank/EMBL data libraries under accession number NM_122856.

	ACKNOWLEDGMENTS

 
We thank Dr. Jian-Kang Zhu for critically reading and commenting on the manuscript.

Received April 13, 2009; accepted June 4, 2009; published June 10, 2009.

	FOOTNOTES

 
¹ This work was supported by the National Natural Science Foundation of China (grant nos. 30630004 and 30421002) and the 111 Project (grant no. B06003) to Z.G.

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: Zhizhong Gong (gongzz{at}cau.edu.cn).

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.109.139626

^* Corresponding author; e-mail gongzz{at}cau.edu.cn.

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