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First published online September 20, 2007; 10.1104/pp.107.103846 Plant Physiology 145:712-721 (2007) © 2007 American Society of Plant Biologists Phage-Type RNA Polymerase RPOTmp Transcribes the rrn Operon from the PC Promoter at Early Developmental Stages in Arabidopsis1,[C],[W]Laboratoire Plastes et Differenciation Cellulaire, Université Joseph Fourier and Centre National de la Recherche Scientifique, B.P. 53, F–38041 Grenoble, France
The plastid genome of higher plants is transcribed by two different types of RNA polymerases named nucleus encoded RNA polymerase (NEP) and plastid encoded RNA polymerase. Plastid encoded RNA polymerase is a multimeric enzyme comparable to eubacterial RNA polymerases. NEP enzymes represent a small family of monomeric phage-type RNA polymerases. Dicotyledonous plants harbor three different phage-type enzymes, named RPOTm, RPOTp, and RPOTmp. RPOTm is exclusively targeted to mitochondria, RPOTp is exclusively targeted to plastids, and RPOTmp is targeted to plastids as well as to mitochondria. In this article, we have made use of RPOTp and RPOTmp T-DNA insertion mutants to answer the question of whether both plastid-located phage-type RNA polymerases have overlapping or specific functions in plastid transcription. To this aim, we have analyzed accD and rpoB messenger RNAs (mRNA; transcribed from type I NEP promoters), clpP mRNA (transcribed from the –59 type II NEP promoter), and the 16S rRNA (transcribed from the exceptional PC NEP promoter) by primer extension. Results suggest that RPOTp represents the principal RNA polymerase for transcribing NEP-controlled mRNA genes during early plant development, while RPOTmp transcribes specifically the rrn operon from the PC promoter during seed imbibition.
Regulation of transcription in plant plastids is surprisingly complex (for review, see Shiina et al., 2005  ; Liere and Börner, 2006). Most of the genes that have been preserved during evolution from the cyanobacterial ancestor of plastids have been (Martin, 2003) and are still (Timmis et al., 2004) transferred to the nucleus, leaving only a limited number of genes (about 120) on the present day plastome. These genes encode a whole set of tRNAs and proteins functioning in photosynthesis, transcription, translation, RNA splicing, protein degradation, and lipid biosynthesis (for review, see Sugita and Sugiura, 1996). This small genome is transcribed by several RNA polymerases that are either nucleus encoded (nucleus encoded RNA polymerases [NEP]) or plastid encoded (plastid encoded RNA polymerase [PEP]). PEP is of eubacterial type, the core enzyme being composed of several subunits ( ,  , ', ''). The subunit composition is most comparable to that of cyanobacterial RNA polymerases where the -subunit is subdivided into two independent proteins when compared to RNA polymerases of other bacteria (Bergsland and Haselkorn, 1991; for review, see Igloi and Kössel, 1992). Promoter specificity and transcription initiation by PEP needs nucleus-encoded  -like factors (for review, see Allison, 2000; Lysenko, 2007).
NEP enzymes are single subunit phage-type RNA polymerases (Lerbs-Mache, 1993
Promoters that are recognized by NEPs have been characterized by using plant material lacking PEP activity (Allison et al., 1996
An exceptional promoter represents the rrn PC promoter. In spinach, this promoter is recognized by NEP2 with the help of CDF2 that binds immediately upstream of the transcription start site (Baeza et al., 1991
In this article, we have made use of Arabidopsis RPOTp and RPOTmp T-DNA insertion mutants to analyze which NEP recognizes in vivo the consensus-type promoters like accD and rpoB, the nonconsensus-type clpP –59 promoter, and the exceptional rrn PC promoter. To answer the question of whether the rrn PC promoter might be recognized by PEP, we have also grown wild-type plants in the presence of Tagetin, a specific inhibitor of PEP activity (Mathews and Durbin, 1990
Isolation of RPOTmp T-DNA Insertion Lines
Two different Arabidopsis RPOTmp T-DNA insertion lines have been obtained from the Salk collection (SALK_132842 and SALK_086115). They are named 842 and 115 in the following. The T-DNA is inserted in the third and fourth intron, respectively, of the RPOTmp gene, as indicated in Figure 1A
. Homozygous plants were selected by PCR screening using primer pairs 1 and 2 to reveal wild-type DNA and primer pairs 1 and left border (LB) to reveal the T-DNA insertion. After two successive backcrosses, one homozygous plant for each insertion mutant has been selected and the insertion has been further characterized by PCR using LB and 1, 2, 3 primers (Fig. 1B). Results indicate that, in both lines, two T-DNAs are inserted in head-to-tail orientation. Three-week-old wild-type and 115 plants, grown for 1 week on agar plates and subsequently transferred to soil, are shown in Figure 1C. The mutant line 115 shows a general reduction in growth as already reported for mutant lines 833 and 286E07 (Baba et al., 2004
Isolation of a RPOTp T-DNA Insertion Line
As RPOTp T-DNA insertion mutant, we have used the same mutant that has been recently described under the name sca3-3 (Hricova et al., 2006
Comparison of PEP- and NEP-Initiated Precursor RNAs in Wild-Type Plants and rpoTp and rpoTmp Mutants
As shown in Figures 1 and 2, both mutants are retarded in growth when compared to wild-type plants. To ensure that differences in precursor RNAs do not simply reflect changes in the developmental stage of the plants, we used plantlets of visually comparable developmental stages for further experiments, i.e. 2-d-old plantlets for wild type and 3- to 4-d-old plantlets for mutant plant material (Fig. 3
, stages that have been used for RNA extraction are boxed). We analyzed precursor RNA of two genes that are transcribed from consensus-type NEP promoters (accD and rpoB), two genes that are transcribed only from PEP promoters (rbcL and psbA), one gene that is transcribed from a nonconsensus-type NEP promoter (clpP), and finally the rrn operon that is transcribed from a PEP (P2, nomenclature of the rrn operon as in Lerbs-Mache, 2000
In the case of accD, we could only detect the –252 precursor RNA (Fig. 4A , left). The promoter that produces the –174 precursor RNA, recently described by Swiatecka-Hagenbruch et al. (2007) using 3-week-old plant material, is probably not active in 2- to 4-d-old plantlets. The –252 accD transcript is considerably diminished in rpoTp plants but not in rpoTmp plants, suggesting that the promoter is specifically recognized by RPOTp. When analyzing rpoB mRNAs, we detected several RNAs (Fig. 4A, middle). One of them corresponds to the recently described primary transcription product starting at position –300 from a type I NEP promoter (Swiatecka-Hagenbruch et al., 2007). The –538 transcript has not been described previously. Determination of the 5' end of this transcript by 5'-RACE using tobacco acid pyrophosphatase (TAP)-treated and nontreated RNA reveals this RNA as primary transcript (Fig. 4A, right top) and locates the transcription start site at position –538 (Fig. 4A, right bottom). The larger RNAs could not be detected by 5'-RACE and might therefore correspond to artefacts. Both rpoB mRNAs, –300 and –538, are strongly diminished in the rpoTp mutant, indicating that these two NEP promoters are also specifically recognized by RPOTp. The two mRNAs, rbcL and psbA, which are exclusively produced from PEP promoters, are also diminished in the rpoTp mutant (Fig. 4B). This might be explained as a secondary effect due to the general diminution of transcription of the rpo operon (Hricova et al., 2006), i.e. to a diminution of PEP enzyme. The –59 type II NEP promoter of the clpP gene is also specifically recognized by RPOTp, because transcripts starting at this position are only diminished in the rpoTp mutant but not in the rpoTmp mutant (Fig. 4C, left). In contrast to the type I and type II NEP promoters, the –136 rrn PC promoter seems to be activated in the rpoTp mutant (Fig. 4C, right, lanes 1–3). In general, in wild-type plants and the rpoTmp mutant, the amount of PC-initiated rrn transcripts is very low when compared to P2-initiated transcripts. A repetition of the experiment with longer exposure shows a slight diminution of PC transcripts in rpoTmp mutants when compared to wild type (Fig. 4C, right, lanes 1'–3'). Altogether, these results indicate that the exceptional NEP PC promoter is not under specific control of RPOTp. The PC promoter represents a likely candidate to be recognized specifically by RPOTmp, but RPOTp might recognize the promoter to some low extent in rpoTmp mutants.
We have recently shown that in Arabidopsis there is a tremendous rise in RNAs coding NEP, i.e. NEP enzymes should be highly active during the period of imbibition (Demarsy et al., 2006 ), and it has been known for a long time that 16S rRNA is highly expressed in the very early stages of plastid development (Baumgartner et al., 1993). A comparison of rrn precursor RNAs in very young seedlings and leaves of mature plants confirms these former observations (Fig. 5A
). To get a clearer picture on rrn transcription, we therefore reanalyzed PC-initiated rrn precursor RNAs by primer extension using dry seeds (stage 0), seeds after imbibition (stage 0+), and seedlings 2 d after germination (stage 2). The result shows an intermittent activation of the rrn PC promoter during the period of imbibition in wild-type plants. In the rpoTmp mutant, the PC-initiated transcript is absent in the two insertion lines, 115 and 842. Figure 5B (lanes 1–6) shows the result obtained with line 115. If we compare rrn transcripts of the same developmental stages from the rpoTp mutant with wild-type plants, we do not detect considerable differences in PC-initiated transcripts at stage 0+ (Fig. 5C, lanes 1–6). These experiments have been repeated several times showing the same result, i.e. we can conclude that RPOTmp specifically transcribes the rrn operon from the PC promoter during imbibition.
Finally, we wanted to assure that PC is indeed recognized by a NEP enzyme and not by PEP. For this objective, imbibition was performed using the transparent testa mutant having a highly permeable seed coat (tt2-1; Debeaujon et al., 2000 ; Rajjou et al., 2004) in the presence of Tagetin, a specific inhibitor of PEP (Mathews and Durbin, 1990, 1994) under the same experimental conditions as already described (Demarsy et al., 2006), and RNA was analyzed by primer extension 42 h after cold release of seeds (Fig. 5D). The PEP-initiated P2 transcript disappears after Tagetin treatment, while the PC transcript remains present at the same amount as in the untreated control (Fig. 5D, lanes 1 and 2 and 1' and 2').
Transcription of the plastid rrn operon is species specific. The rrn operon upstream sequence harbors multiple promoter elements that are differentially used in different plant species (for review, see Lerbs-Mache, 2000 ). In most of the already-analyzed plant species, transcription starts at the eubacterial type P2 promoter (for nomenclature of rrn promoters, see Lerbs-Mache, 2000) that can be considered as the principal rrn PEP promoter in most plant species. Exceptions are spinach and mustard in which the PC promoter represents the principal rrn operon promoter (Baeza et al., 1991; Pfannschmidt and Link, 1997). PC is located between P1 and P2, two initiation sites that are used by Escherichia coli RNA polymerase under in vitro transcription conditions (Iratni et al., 1994; Pfannschmidt and Link, 1997). More precisely, PC is located between the –10 and –35 consensus elements of the eubacterial type P2 promoter. This location excludes a priori that PC is used by an eubacterial type RNA polymerase because the P1 promoter is located too far upstream to allow initiation at PC. Nevertheless, the usage of the PC promoter is still ambiguous. In spinach, experiments using spectinomycin to induce ribosome depletion in chloroplasts and thus prevent the formation of PEP show a strong diminution of the PEP-transcribed rbcL transcript and a remarkable augmentation of NEP-initiated transcripts like clpP-59 and rrn 16S PC (Bligny et al., 2000). In mustard, rrn transcription starting at the PC promoter has been shown by in vitro transcription using two different RNA polymerase fractions, one of them being inhibited by rifampicin, a specific inhibitor of eubacterial-type multimeric RNA polymerases (Pfannschmidt and Link, 1997). By using biochemical fractionation of spinach chloroplast protein extracts, our group has obtained two different NEP activities; only one of them (NEP2) was able to correctly initiate at the PC promoter. This fraction did not react with antibodies that had been made against the C-terminal part of maize (Zea mays) RPOTp. From these results, it was not clear which RNA polymerase (PEP, RPOTp, or RPOTmp) initiates at the PC promoter. In addition, the existence of a fourth RNA polymerase of eukaryotic type in plastids could not be excluded (Bligny et al., 2000). The latter hypothesis was supported by several facts, such as the existence of internal promoter regions (Gruissem et al., 1986; Wu et al., 1997; Sriraman et al., 1998a), the importance of TATA-like sequence elements in plastid transcription (Link, 1984; Eisermann et al., 1990), plastid-associated location of eukaryotic-type transcription factors like TFIIS (da Costa e Silva, 2004) and pBrp (Lagrange et al., 2003), and bioinformatic prediction of plastid localization of at least 48 eukaryotic-type transcription factors (Wagner and Pfannschmidt, 2006; Schwanke et al., 2007). The recently discovered plant-specific RNA polymerase IV (RNAPIV; Pontier et al., 2005) would have been a likely candidate for a plastid-specific function, e.g. for PC transcription.
To answer the question of whether PC is transcribed by one of the two plastid localized phage-type RNA polymerases or by RNAPIV, we decided to analyze rrn precursor RNAs in wild-type and rpoTp and rpoTmp plants and also in the nrpd1 double mutant in which the two largest subunits of RNAPIV (NRPD1a and NRPD1b) are mutated (Pontier et al., 2005 Figure 3 shows that rpoTp and rpoTmp mutants are retarded in germination and early seedling outgrowth. To avoid that observed changes in promoter usage are simply due to the slower growth of the rpoT mutants, we have chosen wild-type and mutant plants having the same visible phenotype, i.e. 2-d-old wild-type plants and 3- to 4-d-old mutants (see Fig. 3) for primer extension analyses of some selected mRNAs. The abundance of rbcL and psbA mRNAs, two RNAs that are exclusively transcribed by PEP, is diminished in the rpoTp mutant (Fig. 4B). This diminution of PEP transcripts is probably due to a general diminution of PEP enzyme in rpoTp mutants because the rpoB/C1/C2 operon is transcribed by RpoTp (see Fig. 3A, rpoB). Type I and type II NEP promoters as shown by the accD –252 promoter, the rpoB –300 promoter, and the clpP –59 promoter, are all recognized mainly by RPOTp. By revealing the –538 rpoB transcript and confirming it as primary transcript by TAP RT-PCR, we detected an additional, as-yet-unknown rpoB promoter that is also under the control of RPOTp (Fig. 4A, middle and right). The only one of the analyzed RNAs that is specifically transcribed by RPOTmp is the PC-initiated rrn transcript (Fig. 5, B and C). This result already demonstrates that the PC promoter is recognized by RPOTmp. Nevertheless, as a supplementary control, we also analyzed rrn precursor RNAs in the nrpd1 double mutant in which the two largest subunits of RNAIV are inactivated by primer extension. The PC-initiated precursor RNA is not affected in this mutant, thus confirming specific recognition of PC by RPOTmp (data not shown).
Taken together, our results suggest that RPOTp is the principal NEP enzyme in Arabidopsis chloroplasts and RPOTmp seems to be highly active in transcribing the rrn operon at the PC promoter during seed imbibition. Both RNA polymerases, RPOTp and RPOTmp, have specific functions and cannot completely replace each other. However, RPOTmp seems to be able to transcribe from type I and type II NEP promoters with low efficiency. This can be supposed from the presence of low transcript levels in the RPOTp T-DNA insertion mutant (see Fig. 4) and from quantification of the precursor RNAs using ImageJ software that reveals a slight diminution of the transcripts also in RPOTmp mutants (Supplemental Table S1). Thus, RPOTmp probably contributes to a low extent also to the transcription of type I and type II NEP promoters. This low gene expression by RPOTmp seems to be sufficient to assure plant survival of RPOTp mutants (RPOTp/RPOTmp double mutants are lethal; see Hricova et al., 2006
These results suggest that RPOTmp is also present in chloroplasts in later developmental stages and not only in proplasts/amyloplasts of seeds. However, different reports show the absence or only very low quantities of PC-initiated transcripts in leaves and cotyledons (Sriraman et al., 1998b
From our results we can conclude that RPOTmp should be present and active in proplastid/amyloplasts of germinating seeds. In chloroplasts of mature plants, the quantity of the enzyme should be very low. Although it is still unclear whether transcription from the rrn PC promoter is the only really specific function of RPOTmp in dicotyledonous plants, such function would explain why monocotyledons exist quite well without RPOTmp. Up to now, the PC promoter has not been found in monocotyledons like rice (Oryza sativa; Silhavy and Maliga, 1998a
We have made use of rpoTp and rpoTmp mutants to analyze promoter usage of the two different NEP enzymes. While RPOTp seems to be the main mRNA transcribing NEP in Arabidopsis plastids during early seedling development, RPOTmp seems to have a specific function in rrn transcription during seed imbibition. Type I NEP promoters and the –59 type II clpP NEP promoter are principally recognized by RPOTp during early seedling development, while RPOTmp specifically recognizes the exceptional PC promoter during seed imbibition. From our results, we can conclude that the two NEP enzymes have different, development-related functions in plastids of Arabidopsis.
Plant Material and RNA Isolation
Surface-sterilized Arabidopsis (Arabidopsis thaliana) seeds (0) were spread on Murashige and Skoog agar plates, kept for 72 h at 4°C in darkness (0+), and then transferred into a growth chamber and grown for up to 3 d at 23°C under a 16-/8-h light/dark cycle at 70 µmol of photons m–2 s–1. tt2.1 seeds were spread on Murashige and Skoog agar plates containing 100 µM tagetin, kept for 24 h at 4°C in darkness, and then transferred into a growth chamber and grown for 42 h at 23°C as described previously (Demarsy et al., 2006
For all three mutants (RPOTmp: SALK_132842 and SALK_086115; RPOTp: SALK_067191) screening for the insertion and for homozygous plants has been done by PCR using the following primers (nos. correspond to those used in Figs. 1 and 2): (1) 5'-GCCTTTAGGGTTCCTTGATTGTC-3'; (2) 5'-GCGACATTCACATTTCCAACAA-3'; (3) 5'-ATGGCATCACTGCATATCTCCC-3'; (LB) 5'-GCGTGGACCGCTTGCTGCAACT-3'; (4) 5'-GAATCATACCCGAATCTCGTG-3'; and (5) 5'-CTGCAGCGAGAGGGTAACACG-3'.
Using isolated total DNA from Arabidopsis as template, the clpP, rpoB, accD, rbcL, psbA, and rrn promoter regions have been PCR amplified and cloned into pCRR2.1-TOPOR (Invitrogen) with the following primers: 5'-ATGTAACTTTATTGCATTGG-3' and 5'-TCATAGTTGCATTACT-3' (clpP), 5'-GGTATGCAATCGAATTGG-3' and 5'-CTTCTATTAAACCCTGATC-3' (rpoB), 5'-CTTTCGTGTCAGGGCTTG-3' and 5'-GAACGCTCATCCCAACC-3' (accD), 5'-GCATATCCGGTTATGCG-3' and 5'-GCCAAGATATCAGTATCC-3' (rbcL), and 5'-CCGTATCATCTTGACTTGG-3' and 5'-GGGCAGGTTCTTACGCG-3' (rrn). Primer extension experiments have been performed as described (Favory et al., 2005
The discrimination between transcription start sites and processing sites of precursor RNAs was done by RNA ligase-mediated (RLM) RACE (RLM-RACE kit, Ambion) without and with previous TAP treatment of RNAs. Reactions were performed according to the suppliers' protocol but without removal of free 5' phosphates by calf intestine alkaline phosphatase. PCR products were analyzed on agarose gels after two successive PCR amplifications, the first using two outer primers and the second using two inner primers. Primers are as follows: rpoB as outer: 5'-GAAATACCGCTGGAACTTACG-3', rpoB as inner: 5'-CCGCTGGAACTTACGGAG-3'. The inner and outer adapter primers are those of the RLM-RACE kit.
Two micrograms of DNase I-treated RNA was reverse transcribed using 400 units of Superscript II (Invitrogen SARL) according to the manufacturer's protocol. The reaction was performed in the presence of 1 µg random hexamers in a total volume of 60 µL at 42°C for 50 min. Aliquots of 3 µL of this reaction were afterward used as template for semiquantitative PCR in a 25-µL reaction mix containing 1 unit of BioTaq (Bioline). To ensure that amplification is in the linear range, the optimal number of cycles have been determined for each couple of primers separately.
PCR was carried out under the following conditions: 5 min denaturation at 94°C followed by n cycles of amplification (30 s at 94°C; 30 s at 55°C; 1 min at 72°C) and a final 10-min elongation step at 72°C. ADENINE PHOPHORIBOSYLTRANSFERASE (APT) mRNA amplification was used as an internal standard (Moffatt et al., 1994 Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers RPOTp (At2g24120) and RPOTmp (At5g15700).
The following materials are available in the online version of this article.
We are grateful to A. Cottet and E. Lambert for excellent technical assistance and to T. Lagrange and I. Debeaujon for kindly providing nrpd1 and tt2-1 seeds, respectively. Received June 12, 2007; accepted September 7, 2007; published September 20, 2007.
1 This work was supported by the European Community (grant no. FP6–2002–LifeSciHealth, PLASTOMICS, proposal no. 503238, L.M. was employed under this contract). 
2 These authors contributed equally to the article. 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: Silva Lerbs-Mache (silva.lerbs-mache{at}ujf-grenoble.fr).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.107.103846 * Corresponding author; e-mail silva.lerbs-mache{at}ujf-grenoble.fr.
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