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Molecular and Cellular Biology, April 2006, p. 2869-2876, Vol. 26, No. 7
0270-7306/06/$08.00+0 doi:10.1128/MCB.26.7.2869-2876.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.
Heike Lange,1,
Kristina Kühn,2
Malek Alioua,1
Thomas Börner,2 and
Dominique Gagliardi1*
Institut de Biologie Moléculaire des Plantes, CNRS UPR2357, 12 Rue du Général Zimmer, 67084 Strasbourg Cedex, France,1 Institut für Biologie/Genetik, Humboldt-Universität zu Berlin, Chausseestr. 117, D-10115 Berlin, Germany2
Received 26 September 2005/ Returned for modification 30 November 2005/ Accepted 9 January 2006
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ABSTRACT |
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INTRODUCTION |
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Exoribonucleases are major players in RNA 3' processing and degradation processes. We have recently characterized an A. thaliana nuclear gene (At5g14580) that encodes a mitochondrial exoribonuclease belonging to the polynucleotide phosphorylase (PNPase) family (17). The mt PNPase is essential for viability in Arabidopsis, in contrast to the chloroplast PNPase-like protein encoded by the At3g03710 gene. Down-regulation of the mt PNPase results in the accumulation of unprocessed RNAs, such as atp9 and orfB mRNA and 18S rRNA precursors (16, 17). Moreover, RNA species that are quickly turned over in wild-type (WT) plants accumulate in the absence of PNPase. Such RNAs include, for instance, 18S rRNA degradation intermediates and the leader of the 18S rRNA, which is removed by an endonuclease from the primary transcript. These initial studies revealed that PNPase is essential for several aspects of mt RNA metabolism, including 3' processing and degradation processes. Interestingly, all RNA substrates of PNPase that we have investigated so far are polyadenylated. Although mature RNAs are not constitutively polyadenylated in plant mitochondria, poly(A) tails trigger rapid exonucleolytic degradation by PNPase, similar to the situation reported first for Escherichia coli and later for chloroplasts (1, 3).
To determine new substrates, and thus novel biological roles, of PNPase, we cloned about 300 polyadenylated mt RNAs from plants down-regulated for PNPase (PNP– plants). These sequences were considered degradation tags, as they allowed the identification of different classes of transcripts requiring PNPase for their degradation as judged by their accumulation in PNP– versus WT plants. Our results indicate that maturation by-products such as rRNA leaders or tRNA intergenic sequences are generally degraded by PNPase. In addition, we show that a major role for PNPase is the degradation of transcripts that are, in some cases, expressed to surprisingly high levels from regions lacking known genes. Some of these RNAs, which include transcripts of chimeric open reading frames (ORFs) created by mt DNA recombination events or antisense (AS) RNA transcribed from the opposite DNA strand of a known gene, could have a deleterious effect on mitochondrial function. These data show that the lack of tight transcriptional control in Arabidopsis mitochondria is counterbalanced by polyadenylation-mediated decay by PNPase.
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MATERIALS AND METHODS |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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RNA extraction and analysis.
RNA was extracted from either whole seedlings or mitochondria isolated from suspension cell culture by using the TRI-reagent (Molecular Research Center) according to the manufacturer's instructions. For Northern blot analysis, 5 µg of total or mt RNA was fractionated using 6% (wt/vol) acrylamide-bisacrylamide (19:1)-7 M urea-1x Tris-borate-EDTA gels or 1% agarose-3% formaldehyde gels. RNA was then transferred to a Hybond-N+ membrane (Amersham). Probes consisted of either primers labeled with [
-32P]ATP and polynucleotide kinase or antisense RNA transcribed in vitro by T7 RNA polymerase in the presence of [
-32P]UTP, as indicated in the figure legends. Prehybridization and hybridization were performed in 7% (wt/vol) sodium dodecyl sulfate (SDS)-0.5 M NaPi, pH 7.2, at 45°C or 65°C for primer and RNA probes, respectively. Filters hybridized with primer probes were washed three times at 45°C in 2x SSC (1x SSC is 0.15 M NaCl plus 0.015 M sodium citrate)-0.1% (wt/vol) SDS for 20 min. Filters hybridized with RNA probes were washed for 30 min in 2x SSC, 1x SSC, 0.5x SSC, and 0.1x SSC solutions, each containing 0.1% (wt/vol) SDS. Mapping of poly(A) sites by oligo(dT) adapter-primed reverse transcription-PCR (RT-PCR) was carried out as described previously (16). Identification of primary transcripts was performed by 5' rapid amplification of cDNA ends (RACE) RT-PCR following tobacco acid pyrophosphatase (TAP) treatment as described previously (11).
Small polyadenylated RNA library construction. Total RNA (5 µg) from PNP– plants was fractionated on 6% (wt/vol) acrylamide-bisacrylamide (19:1)-7 M urea-1x Tris-borate-EDTA gels. RNAs of 100 to 150 nucleotides (nt) were eluted from the gel in 0.5 M ammonium acetate, 0.1% SDS, and 1 mM EDTA for 1.5 h at 50°C. RNAs were extracted using phenol-chloroform-isoamylic alcohol (25:24:1) and then ethanol precipitated. Full-length cDNAs were synthesized using the cDNA SMART synthesis kit (Clontech) according to the manufacturer's instructions. This protocol allows the incorporation of sequence tags at both the 3' and 5' ends of polyadenylated RNA. Total cDNAs were amplified by PCR according to the cDNA SMART synthesis kit (Clontech) protocol, using the PCR Advantage II kit (Clontech) for 19 cycles (15 s at 94°C, 15 s at 65°C, and 15 s at 68°C). PCR products were cloned using the TOPO cloning kit (Invitrogen). Inserts were amplified by PCR and sequenced without further purification.
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RESULTS |
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In summary, 70% of the clones analyzed match the Arabidopsis mt genome indicating that the experimental strategy was successful. To date, the only known role for polyadenylation in plant mitochondria is to target RNA for degradation. Therefore, we considered it likely that these polyadenylated RNA species correspond to RNA degradation tags that would accumulate in PNP– compared to WT plants. This assumption was confirmed experimentally by Northern blot analysis of the investigated transcripts reported below. A detailed list of all degradation tags is given in Table S1 in the supplemental material. All nucleotide coordinates in that table and hereafter refer to the Arabidopsis complete mitochondrial genome sequence (ecotype C24, accession number NC_001284).
PNPase degrades maturation by-products. We obtained 17 and 20 clones corresponding to mt rRNAs (8 in 26S rRNA and 9 in 18S rRNA) and mRNAs, respectively (see Table S1 in the supplemental material). These sequences represent fewer than 13% of the clones assigned to the mt genome. By contrast, 143 degradation tags (47% of the mt sequences) correspond to sequences 5' and 3' to rRNA and tRNA (Fig. 1; see Table S1 in the supplemental material). As an example we show the positions of degradation tags located downstream of the 5S rRNA (Fig. 1A). The locations of several degradation tags downstream of the 5S rRNA confirm that in Arabidopsis mitochondria, transcription does not stop close to the 3' end of the 5S rRNA and that RNA corresponding to sequences downstream of the 5S rRNA can be polyadenylated (Fig. 1A). Numerous degradation tags map in the leader region of the 26S rRNA (see Table S1 in the supplemental material), suggesting the involvement of PNPase in degrading this maturation by-product, as previously shown for the 18S rRNA leader (16). A region of about 230 nt containing the promoter of the 26S rRNA is duplicated in the Arabidopsis mt genome. The degradation tags matching this duplicated region could be transcribed from either region. However, in both cases, specific sequences downstream of the duplicated region were found in our screen, indicating that both regions are expressed (Fig. 2A; see Table S1 in the supplemental material).
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In summary, the characterization of degradation tags 5' and 3' to tRNA and rRNA indicates a general role for PNPase in the degradation of maturation by-products in plant mitochondria.
Editing of tRNA maturation by-products. Intriguingly, C-to-U editing sites were observed in expressed trn intergenic regions. As shown in Fig. 1B, five putative editing sites were detected in degradation tags matching the trnS-trnY-trnP-trnC-trnN-trnY cluster. These C-to-U conversions are not present at a given position in all degradation tags, excluding a possible microgenetic variation between C24 and col-0 ecotypes. In addition, the C-to-U editing site at nucleotide 106058 downstream of tRNAAsn was observed at the same position in degradation tags of different lengths (i.e., not identical cDNA clones) (Fig. 1B). These new sites did not exhibit clear sequence homologies with previously known editing sites. So far, editing sites have been characterized only for known genes in Arabidopsis mitochondria, and their number has been estimated at 441 (6). The biological significance, if any, of these novel editing sites remains unknown. However, our results suggest that more sites than previously thought are edited or, at least, that these sites are "editable" as long as the target RNA is stabilized by the lack of PNPase.
PNPase degrades expressed regions lacking known genes. The Arabidopsis mt genome contains a large number of predicted ORFs exhibiting no significant homology to known genes. Moreover, these ORFs are not conserved between plant species and thus are unlikely to represent functional genes. In Arabidopsis, ORFs larger than 100 codons represent up to 10% of the genome. We found several degradation tags corresponding to such nonfunctional ORFs in our screen (orf315, orf275, orf240a, orf135b, orf106f, orf294, and orf145c) (see Table S1 in the supplemental material). These results indicate that these nonfunctional ORFs are indeed expressed and are degraded by the polyadenylation decay pathway in Arabidopsis mitochondria.
We have also characterized degradation tags that match the Arabidopsis mt genome in regions that do not contain any known genes or predicted ORFs. Some of these regions are probably expressed at low levels as indicated by the low number and scattered distribution of degradation tags (see Table S1 in the supplemental material). These may reflect a basal expression of the mt genome, probably due to relaxed transcription. In contrast, other regions are highly expressed. These include a region containing the rrn26 promoter, which has been duplicated in the genome by a recombination event (Fig. 2A). This duplicated promoter is functional, given the high number of degradation tags found in its vicinity. However, it does not seem to drive the expression of a functional RNA, as we could not detect corresponding transcripts in WT plants by Northern blot analysis (Fig. 2B). By contrast, RNA species of different lengths, and therefore detected as a smear, can be observed by Northern analysis in the absence of PNPase (Fig. 2B). Taken together, our results show that this region is highly expressed but that the resulting RNA is quickly degraded by PNPase.
Another region characterized by a high number of degradation tags, and thereby evidently highly expressed, is a part of repeat I (Fig. 3A). Repeat I is one of two large repeated regions in the Arabidopsis mt genome that are active in recombination (10). No known genes are present in repeat I. Most tags were identified downstream of a putative promoter that fulfils previously established criteria for plant mt promoters. However, some degradation tags were also found 5' of this putative promoter, indicating that transcription may also start upstream (Fig. 3A). The high number of degradation tags in repeat I prompted us to analyze by Northern blot analysis a possible accumulation of RNA species transcribed from this region. These experiments were conducted using WT mt RNA and several reverse primers spanning this region (Fig. 3A). A 500-nt transcript could clearly be detected using primers P2 and P3 (Fig. 3B), whereas no signal was detected using primers P1 and P4 (data not shown). This 500-nt transcript in WT plants was further characterized by mapping its 5' and 3' extremities by circular RT-PCR. The 5' and 3' ends were localized at nt 47019 to 47024 and 47518 to 47521, respectively. The 5' ends map downstream of a sequence, named Ath-59 (Fig. 3C), that was previously identified in a screen aimed at identifying small noncoding RNAs from Arabidopsis (15). Ath-59 is not known to be a functional RNA to date, but it exhibits features of a tRNA-like structure (L. Maréchal-Drouard, personal communication). Thus, it is likely that it is recognized by the tRNA processing machinery, which might generate the 5' end of the 500-nt transcript. We could not detect the accumulation of Ath-59 by Northern blotting, showing that Ath-59 does not accumulate to the same levels as the 500-nt transcript. Northern blot analysis using total RNAs from WT and PNP– plants shows an extraordinarily high accumulation of the 500-nt transcript in PNP– plants (Fig. 3D). Taken together, these data show that a novel transcript is transcribed from repeat I to high levels but that PNPase actively degrades this transcript, thereby preventing its accumulation.
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PNPase degrades antisense transcripts. One degradation tag is in the AS orientation to the 500-nt transcript locus described above (Fig. 3A). This sequence is complementary to the part of the 500-nt transcript that is edited to 100% in PNP– plants, but it exhibits a G at the relevant position. Thus, it is unlikely that it corresponds to an experimental artifact but rather is likely that the AS RNA originates from transcription on the opposite strand. To determine if transcription can be initiated on the strand opposite to the 500-nt transcript, we used a modified 5' RACE technique that allows the identification of primary transcripts. In plant mitochondria, primary transcripts carry triphosphates at their 5' ends and are thus poorly ligated by T4 RNA ligase to the RNA adapter used in 5' RACE experiments. Treatment of the RNA samples with tobacco acid pyrophosphatase will convert 5' triphosphates to monophosphates and thus enhance the efficiency of ligation to the RNA primer. Primary transcripts can be identified by comparing 5' RACE RT-PCR profiles obtained with or without TAP treatment. As shown in Fig. 4A, primary transcripts were detected in AS orientation to the 500-nt transcript.
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The presence of these AS RNAs prompted us to look for putative AS RNAs to known transcripts. We thus used oligo(dT) adapter-primed RT-PCR to detect polyadenylated atp9 AS transcripts (Fig. 5A). Sequence analysis of the PCR products confirmed the existence of atp9 AS transcripts for the following two reasons. First, most poly(A) tails were longer than the oligo(dT)12 used for cDNA synthesis, indicating that these cDNAs indeed originate from polyadenylated transcripts (Fig. 5A). The locations of the poly(A) tails confirm the AS orientation of these transcripts. Second, the position corresponding to editing sites in sense atp9 mRNA harbored a guanosine in all AS clones. An adenosine would have been expected if the AS RNA were synthesized from sense transcripts due to an experimental artifact. These results strongly suggest that a promoter is active in the AS orientation to the atp9 gene. Indeed, such a promoter can be experimentally detected (Fig. 5B). However, detection of the primary transcripts corresponding to AS atp9 RNA required nested PCR, suggesting a relatively weak activity of the promoter. This is supported by the fact that the atp9 AS RNAs do not accumulate to sufficient levels to be detected by Northern blotting (data not shown). Promoters driving AS RNA synthesis could also be detected for three other genes tested, i.e., nad4, nad5, and nad7, through 5' RACE directed at primary transcripts being generated from the nad4, nad5, and nad7 AS strands (Fig. 5B). An nad4 AS transcript which is initiated at a sequence displaying similarity to the Arabidopsis mitochondrial promoter Prps3-1053 was amplified, and an RNA that is complementary to nad5 was found to be transcribed from a motif reminiscent of the Prps3-1133 promoter (Fig. 5B; compare reference 11). An nad7 AS RNA whose 5' end maps to a sequence containing common promoter elements gave rise to a strong 5' RACE signal (Fig. 5B). These results indicate that AS RNAs to known genes are common in Arabidopsis mitochondria. In addition, we show that AS RNAs to atp9 and the 500-nt transcript can be polyadenylated. Their polyadenylated status suggests that these RNAs are degraded by PNPase in Arabidopsis mitochondria. This was indeed confirmed for the AS RNAs to the 500-nt transcript, which accumulate in PNP– compared to WT plants.
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DISCUSSION |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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To detect novel RNAs that accumulate in PNP– plants, we first identified RNA degradation tags in the range of 100 to 150 nt. This size limit was essential to prevent contamination by cytoplasmic mRNA. The sequence information generated by the degradation tags was then used to determine the sizes of the RNA species accumulating in PNP– plants by Northern blot analysis (Fig. 1 to 4). This analysis showed that transcripts such as tRNA maturation by-products or the 500-nt transcript accumulate as full-length RNA in PNP– plants. However, shorter RNA species could also be detected in PNP– plants by Northern experiments but required prolonged exposures of the RNA filters (see, for instance, Fig. 3). In addition, several degradation tags were arranged in a consecutive manner and are thus likely generated by an endonuclease. These results imply that an alternative degradation pathway involving a yet-unidentified endonuclease could operate in plant mitochondria. Nevertheless, the accumulation of mostly full-length RNA in PNP– plants is consistent with the fact that degradation of plant mitochondrial RNA is mostly exonucleolytic and performed by PNPase.
We have identified a novel 500-nt RNA transcribed from repeat I in Arabidopsis mitochondria (Fig. 3). We so far have no indication that this RNA plays a functional role, even though it shares features common to mitochondrial RNA, such as having defined 5' and 3' ends, exhibiting editing sites, and accumulating to sufficient levels in WT plants to be detected by Northern blotting. The transcript contains about 70 nt of the 18S rRNA, followed by 27 nt similar to tRNATyr and a 28-nt chloroplast sequence. Thus, this gene is unlikely to encode a functional RNA but rather seems to be the result of duplication and recombination events, which are often observed in plant mt genomes. It is unknown at present whether the high accumulation of the 500-nt transcript could be detrimental to mt function. One possible deleterious effect would be the mobilization of part of the editing machinery to the detriment of endogenous RNA substrates. Such a type of competition has recently been reported to occur in chloroplasts (8).
Other expressed RNAs that we have characterized here could also have deleterious effects. These RNAs include AS transcripts to known genes and expressed unknown ORFs such as chimeric ORFs. Chimeric ORFs, created by recombination events, are constituted of a fragment of a known gene fused in frame to an originally noncoding sequence. Expression of chimeric ORFs can have profound biological importance, as most cytoplasmic male sterility (CMS) systems are associated with the expression of such an ORF. CMS is a maternally inherited phenotype in which plants are not affected in vegetative and female development but fail to set viable pollen. The expression of chimeric ORFs also in some cases results in homeotic conversion of floral whorls, underlying the impact of mt function on plant development (13; see references cited in reference 24). The mitochondrial dysfunction linked with CMS-associated genes is clearly under nuclear control, as the CMS phenotype can often be reverted by the introduction in a cross of so-called restorer-to-fertility genes (21). In sunflower PET1-CMS, restoration of fertility is achieved by the specific destabilization of the CMS-associated transcript via the polyadenylation-dependent decay pathway (5). Our results show that in Arabidopsis some of the expressed chimeric ORFs are also degraded through PNPase and polyadenylation, thereby preventing the accumulation of these transcripts.
Other RNAs potentially deleterious to mitochondrial function are AS RNAs, which, as we show here, are commonly produced in Arabidopsis mitochondria. Indeed, we found AS RNAs in all five regions that we investigated, i.e., nad4, nad5, nad7, atp9, and repeat I. The AS RNAs are produced by transcription from the opposite strand of the corresponding gene and provide another proof of the relaxed control of transcription initiation in Arabidopsis mitochondria. The polyadenylation status of the atp9 and the 500-nt transcript AS RNAs, as well as the high accumulation of the latter in PNP– plants, clearly indicates that PNPase is involved in degrading these AS RNAs. There is no information about the effect of the accumulation of AS RNA in plant mitochondria due to the lack of an in vivo transformation method for mitochondria. However, it has been recently reported that expression of an AS RNA to the rpoB transcript in the chloroplast results in severely abnormal development of the transgenic plants (8). The molecular reason for this impairment in growth and development is unknown at present, as neither the editing status nor steady-state levels of the RpoB protein or its transcripts was affected. However, this example illustrates the potentially deleterious effect of AS RNAs in a plant organelle.
Considerable attention has recently been given to systematic analyses of transcription of whole or large parts of genomes using microarray experiments. These experiments, conducted with E. coli, human, Drosophila melanogaster, Saccharomyces cerevisiae, or Arabidopsis thaliana genomes, revealed that large regions between predicted genes are expressed (reviewed in reference 9). In addition, AS transcripts were found for most known genes. For instance, more than 3,000 out of 4,000 ORFs in E. coli are also transcribed in the antisense orientation (18). A similar situation was observed for about 30% of the annotated genes in Arabidopsis (19, 23). In some cases, AS transcription is even higher than sense transcription of a characterized gene (19). Thus, the occurrence of numerous noncoding RNAs from intergenic regions and AS RNAs to known genes is not a peculiarity of the Arabidopsis mt genome but seems to be a widespread phenomenon observed in different organisms or genetic compartments. The polyadenylated status of these RNA species is apparently conserved, as the aforementioned microarray experiments were conducted with polyadenylated RNA. Polyadenylation has long been considered to have opposite effects on RNA stability in E. coli, Trypanosoma brucei mitochondria, and plant organelles on the one hand and nucleus-encoded RNA on the other. However, this view has been challenged by the recent discovery that an RNA quality control mechanism involving polyadenylation is present in the yeast nucleus. Indeed, RNAs transcribed from intergenic regions in the nuclear genome of Saccharomyces cerevisiae are rapidly degraded by the nuclear exosome following polyadenylation of the target RNA by the TRAMP complex (12, 22). Again, this type of nuclear RNA quality control strongly resembles the pathway that we described here for plant mitochondria, although the proteins involved are not related. Relaxed transcription being counterbalanced by polyadenylation-dependent decay thus seems to be a conserved mechanism among distinct genetic systems.
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ACKNOWLEDGMENTS |
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We thank Philippe Giegé for critical reading of the manuscript and Théophile Ofodo for technical assistance.
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FOOTNOTES |
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Supplemental material for this article may be found at http://mcb.asm.org/.
These authors contributed equally to this work.
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