Department of Biology, Indiana University, Bloomington
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Abstract |
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Introduction |
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Although mitochondrial gene content is highly variable in angiosperms, the sizes of these genes are generally well conserved. Two exceptions to this pattern are the cytochrome c biogenesis gene ccb577 (equivalent to the N-terminal portion of the bacterial ccl1 gene) and the ribosomal protein gene rpl2. Ccb577 has been characterized from the mitochondrion of six diverse angiosperms. In four cases (Oenothera, carrot, wheat, and beet), the gene is present as a single open reading frame (ORF) (Gonzalez, Bonnard, and Grienenberger 1993
; Schuster et al. 1993
; Kubo et al. 2000b
). However, in the crucifers Brassica and Arabidopsis, ccb577 is split into two widely separated and independently transcribed ORFs (Handa, Bonnard, and Grienenberger 1996
; Unseld et al. 1997
). Thus, the ccb577 gene was split relatively recently during eudicot evolution, as discussed by Handa, Bonnard, and Grienenberger (1996)
.
The locus for the ribosomal protein gene rpl2 has been sequenced from the mitochondrial DNA of five flowering plants. In both Arabidopsis (Sunkel, Brennicke, and Knoop 1994
; Unseld et al. 1997
) and Oenothera (EMBL accession number X80170), rpl2 is missing about 550 bp at the 3' end of the gene that are present in rpl2 from rice (Kubo et al. 1996
), the liverwort Marchantia (Oda et al. 1992
), and the protist Reclinomonas (Lang et al. 1997
). The missing region is not present elsewhere in the completely sequenced Arabidopsis mitochondrial genome (Unseld et al. 1997
), but it is present in the nucleus of Arabidopsis (EMBL accession number X82556).
Wheat mitochondrial DNA contains only a small fragment of rpl2, from the 3' end of the gene, and the rpl2 fragment is cotranscribed with another gene (Subramanian, Fallahi, and Bonen 2001
). rpl2 has been transferred to the nucleus in wheat, where two copies are expressed (Bonen, Carrillo, and Subramanian 1998
). The first exon of rpl2 has been sequenced from the mitochondrion of potato (Loessel et al. 1999
), although the sequenced region does not extend to the 3' end of the gene.
In this study we show that the 5' rpl2 gene in mitochondrial DNA was created by the formation of a stop codon in the common ancestor of core eudicots, and that this event was probably allowed by the slightly earlier transfer of the 3' end of rpl2 to the nucleus and its establishment there as a functional gene. The two resulting functional rpl2 genes are present in different cellular compartments in some core eudicots, and in the same compartment (the nucleus) in others.
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Materials and Methods |
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The mitochondrial 3' rpl2 sequence was PCR-amplified from several core eudicot DNAs using the following primers: forward (5'-GAAGCRGGYAADATGGTGAT-3') and reverse (5'-GTGGGGAAACGCACAATTTAG-3). The mitochondrial 5' rpl2 gene was PCR-amplified from several core eudicot genomic DNAs or cDNAs using the primer F1 (5'-GAGCRCTTAGACAWTTCACT-3') and one of the following reverse primers: R1 (5'-ACAGGTGCACGATCKACTTTG-3'), R2 (5'-GRCGTGGCCAAGAAGCAGC-3'), or R4 (5'-CYGCCCAGAATGCYCATMCAT-3'). Most of exon 2 was PCR-amplified from three basal eudicot DNAs using the primers F1 (5'-GAGCRCTTAGACAWTTCACT-3') and Rev (5'-GTGGGGAAACGCAGAATTTAG-3'). All PCR products were sequenced directly on both strands using an ABI 3700 DNA sequencer. Mitochondrial rpl2 sequences determined in this study have been assigned GenBank accession numbers AF387174AF387188.
EST clones of nuclear 3' rpl2 from Arabidopsis (AW004239) and soybean (BE473673) were purchased from Incyte Genomics and sequenced using M13 forward and reverse primers; maize rpl2 EST AW066220 was purchased from the ZmDB maize ESTsequencing project and completely sequenced using M13 primers and the following internal primers: (5'-AAGCCAAAGCGGATGAAGAAG-3' and 5'-CTTTCTTAGCTTGCGTGTACC-3'). The genomic sequences of nuclear 3' rpl2 from cotton, tomato, and soybean were obtained by PCR amplification and sequencing using the following primers: cotton (5'-GAGGGCGCACAGCGTCTTTGA-3' and 5'-TAARWCTCGAMTTACGGTTTAG-3'), tomato (5'-CTCGAATGGCTTCATCTTTCC-3' and 5'-GGATACTTAATTGTCAATGTTATG-3'), and soybean (5'-GAAATGGCTGTGTCACTGTGG-3' and 5'-CCAACTGCCCTCGGGTGTTA-3'). The genomic sequence of the nuclear 5' rpl2 gene from soybean was PCR-amplified using the primers (5'-GAAGAAAAGAGTGTAAGAGTAG-3') and (5'-TGCTTTGCCACGAAATCGCTG-3'). Nuclear rpl2 sequences determined in this study have been assigned GenBank accession numbers AY044158AY044160.
Accession numbers for additional nuclear EST and Arabidopsis genome sequences utilized in this study are as follows: soybean 5' rpl2 (BG406182, AW706585, BF071707), Medicago 5' rpl2 (BE941643 and BF646066), Lotus 5' rpl2 (AV422504 and AV424117), Arabidopsis 3' rpl2 genomic sequence (AC004005), cotton 3' rpl2 (BE054892 and BF269312), tomato 3' rpl2 (AW626051 and BE460252), and Medicago 3' rpl2 (BF646435 and AL373876).
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Results |
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Truncation of Mitochondrial rpl2 at the Base of Core Eudicots
To determine how and when the 5' rpl2 ORF was formed, a region of exon 2 spanning the sites of the 5' ORF termination codons in Arabidopsis and Oenothera (the stop codons are not in the same position in these two species) and including most of 3' rpl2 (see fig. 1
) was PCR-amplified and sequenced from 12 diverse eudicots. In Dicentra, Platanus, and Trochodendron (three members of the basal eudicot grade), the entire sequenced region was an intact ORF (i.e., the termination codons present in Oenothera and Arabidopsis were absentsee fig. 4
). Thus, the structure of rpl2 in the mitochondrion of Dicentra, Platanus, and Trochodendron appears to be one entire ORF (probably interrupted by an intron), as in rice (see fig. 1
). The same region was also isolated and sequenced from nine core eudicots belonging to groups in which there was hybridization of the DNAs to the 3' rpl2 probe. The sequences from all nine taxathe asterids Lonicera, Viburnum, Diospyros, Hydrangea, Chamaedaphne, and Cornus (fig. 3 , right), the rosids Quercus and Abutilon (fig. 3
, middle), and Corylopsis from the Saxifragales (fig. 3
, middle)contain a stop codon (TAA) at the same position as the 5' ORF termination codon in Oenothera (fig. 4
). Thus, the gene fission event that created the 5' rpl2 ORF/gene seems to have occurred via a C-to-T terminator mutation in the common ancestor of core eudicots, after the divergence of the Trochodendraceae (fig. 3
, large gray arrow). An unlikely alternative is that a rare U-to-C RNA editing event might restore the CAA codon in the mRNA. Very few U-to-C edits (only four out of the hundreds of known edits) have been documented in flowering plants (reviewed in Maier et al. 1996
), and there are no U-to-C edits among the 441 RNA editing sites in the mitochondrial mRNAs of Arabidopsis (Giegé and Brennicke 1999
). Even if the TAA codon were corrected by RNA editing, the rpl2 gene would be truncated in eight of the nine species examined by premature stop codons, and frameshifts would disrupt the reading frame in several species, as discussed later.
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In contrast to the 3' rpl2 pseudogenes in the mitochondrial DNA of several core eudicots, exon 1 of 5' rpl2 (most of the 5' end; fig. 1 ) is intact in the mitochondrion of Arabidopsis, Oenothera, and potato (see literature cited in Introduction). In order to determine if exon 1 of 5' rpl2 is intact in a few other core eudicots to which there was good hybridization on the blots, the genomic sequence of this region was obtained by PCR amplification from Gossypium, Ulmus, and Lonicera. Each sequenced region (ranging from 686812 bp) was uninterrupted by stop codons or frameshifts.
3' rpl2 Has Been Transferred to the Nucleus in Four Angiosperm Families
To determine if 3' rpl2 has been transferred to the nucleus in core eudicots, searches of the NCBI sequence databases were performed. Nuclear 3' rpl2 cDNA sequences were discovered from tomato, cotton, Arabidopsis, soybean, and M. trunculata (see Materials and Methods for accession numbers). EST clones from Arabidopsis and soybean were purchased from Incyte Genomics and sequenced, whereas the available tomato and cotton EST sequences, and a contig of multiple Medicago ESTs, already represented full-length 3' rpl2 ORFs. The genomic sequence of Arabidopsis rpl2 is present on chromosome 2 (Lin et al. 1999
), but it was not annotated as a gene, and rpl2 appears to be single copy in the mostly complete Arabidopsis genome sequence. An unpublished Arabidopsis 3' rpl2 cDNA sequence (X82556) is also available, but this sequence contains errors that caused the extent of the coding region to be incorrectly inferred relative to the data presented in this paper. The complete genomic sequences from cotton, tomato, and soybean were obtained by PCR amplification and sequencing, revealing one intron in each species (see below).
The nuclear 3' RPL2 aa sequences from each species have a well-conserved (relative to each other) region of about 155 aa that begins at a position corresponding to codon 354 in the entire RPL2 aa sequence from rice mitochondria (see fig. 5
). The nuclear 3' RPL2 sequences include all of the carboxy terminal sequence that is well conserved among plants, protists, and bacteria. The mitochondrial rpl2-homologous region in the nuclear 3' rpl2 genes begins 32 codons downstream of the mitochondrial 5' rpl2 stop codon in eudicots (35 codons in rice); thus, a short segment that is not in a highly conserved region of the RPL2 protein seems to have been lost in the core eudicots. Each nuclear sequence contains a 5' extension of the ORF that has no similarity to the rice mitochondrial sequence. For each gene, a portion of this region is predicted by MITOPROT (Claros and Vincens 1996
) and TargetP (Emanuelsson et al. 2000
) to be a mitochondrial targeting presequence, although the predicted lengths vary. (Another mitochondrial protein prediction programPredotar version 0.5 [www.inra.fr/Internet/Produits/Predotar]predicts nuclear 3' rpl2 codes for a mitochondrial protein, but this program does not predict presequence cleavage sites.) The 5' extensions are not as well conserved among the different species as the corresponding mature coding regions, consistent with many other mitochondrially targeted proteins (reviewed in Glaser et al. 1998
). Despite some length variation, the extensions align sufficiently well to be judged homologous (fig. 5
). The genes from cotton and Arabidopsis contain a phase 1 intron that is in the same position; the genomic sequences from tomato and soybean also have an intron that appears to be in the same position, although this inference is partially dependent on sequence alignment (fig. 5
). The evident homology (in both primary sequence and intron location) of the putative presequences of the nuclear 3' rpl2 genes strongly implies that they are the product of the same functional gene transfer event, an event that probably occurred early in eudicot evolution at about the same time as rpl2 truncation within the mitochondrial genome (see Discussion).
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Discussion |
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We infer that 5' rpl2 was created from the entire rpl2 gene by the formation of a stop codon (TAA) in a common ancestor of core eudicots, after divergence of the Trochodendraceae (figs. 3 and 4 ). Three lines of evidence suggest that the 3' rpl2 nuclear genes from cotton, Arabidopsis, tomato, soybean, and Medicago are the result of a single transfer to the nucleus in a common ancestor of rosids and asterids. First, the mitochondrial targeting presequences of the nuclear 3' rpl2 gene from the four rosids and one asterid align relatively well and thus appear to be homologous (fig. 5 ). Second, the nuclear 3' rpl2 genes have an intron that is in the same position within the presequence (fig. 5 ). Third, the 3' rpl2 sequence does not appear ever to have been functional in core eudicots as a stand-alone ORF in the mitochondrial genome. Taken together, the three lines of evidence provide far stronger support for the hypothesis of a single transfer of the 3' region to the nucleus than for the hypothesis of multiple recent transfers. The functional transfer of the 3' region to the nucleus and the creation of the 5' ORF in the mitochondrion appear to have been approximately concurrent, given our current understanding of eudicot relationships (fig. 3 ).
Two models can be envisioned to explain rpl2 fission in the mitochondrion and transfer of the 3' region to the nucleus. In the first model, the entire rpl2 gene split into two functional ORFs, both initially resident in the mitochondrial genome. Soon afterwards, the 3' ORF was transferred to the nucleus. This was our hypothesis during the early stages of this project. However, as discussed earlier, there is no evidence that the 3' region was ever a functional ORF in core eudicot mitochondrial DNA. Thus, we do not favor the above model.
In the second, preferred model, the crucial initiating event was the functional transfer of the 3' region to the nucleus. This relieved selection on the corresponding 3' region of the ancestrally full-length rpl2 gene in the mitochondrion, allowing the mitochondrial 5' ORF to be formed via a point mutation that created a premature stop codon. In other words, rpl2 gene fission seems to be a consequence of partial gene transfer to the nucleus, although the two events were presumably independent. How could transfer and activation of only a portion of a mitochondrial gene in the nucleus occur? One possibility is that the entire gene was transferred to the nucleus, but only the 3' end became activated, perhaps because of a genomic rearrangement during presequence acquisition. Alternatively, the physical transfer event may have included only the 3' end of rpl2, either because of incomplete reverse transcription of mitochondrial rpl2 mRNA or because only a tiny fragment of the mitochondrial genome was transferred. The 3' region of rpl2 has only one RNA editing site in rice mitochondria and contains no introns (Kubo et al. 1996
), raising the possibility of a DNA-mediated transfer of 3' rpl2 to the nucleus.
Under our preferred model, once 3' rpl2 became a functional gene in the nucleus, there was presumably a transition period when both the full-length mitochondrially synthesized RPL2 protein and the 3' RPL2 protein (synthesized in the cytosol) were present in the mitochondrion. Because the carboxy end of the full-length RPL2 protein was probably redundant to the 3' RPL2 protein, it is not clear if and how both proteins were assembled into the ribosome. Questions also arise as to how the mitochondrially synthesized 5' RPL2 protein and the cytosolically synthesized 3' RPL2 protein might assemble and interact in the ribosome. Do they in fact interact with one another in the ribosome (structurally, functionally, or both), and might they possibly even become fused together? Are they part of the same ribosomal protein assembly pathway, or are they assembled separately? Future biochemical experiments could address these questions.
Has there been a single transfer or multiple transfers of 5' rpl2 to the nucleus? The many, mostly recent and phylogenetically isolated losses of 5' rpl2 from core eudicot mitochondrial DNA, taken together with the presence of an intact 5' rpl2 exon 1 in the mitochondrion of all six core eudicots examined, suggest that there may have been many recent functional transfers of 5' rpl2. For one case of 5' rpl2 loss, in legumes, there is a corresponding gene in the nucleus that probably represents a recent transfer.
Mitochondrial Gene Fissions in Other Eukaryotes
Fission of genes in mitochondrial DNA appears to be a relatively rare process. Few examples are known, only one of which involves gene transfer to the nucleus, in addition to rpl2. The cytochrome c biogenesis gene that is homologous to the bacterial gene ccl1 is present as three separate ORFs in the liverwort Marchantia and in the Brassicaceae (with only one of the two fission points being shared), and as two separate ORFs in four other examined angiosperms (see Introduction). It appears that the ccl1 gene split once before the evolution of land plants, with the smaller portion (designated ccb452 in Arabidopsis) then splitting in the Marchantia lineage and the larger portion (ccb577) splitting in the Brassicaceae. Transfer of a cytochrome c biogenesis gene to the nucleus has not been reported in land plants. In another case of mitochondrial gene fission, the NADH dehydrogenase subunit 1 gene (nad1) has been split into two separately transcribed ORFs in Tetrahymena and Paramecium (Edqvist, Burger, and Gray 2000)
.
A particularly intriguing case of gene fissionone that does involve gene transfer to the nucleusinvolves the cox2 gene in green algae. In Chlamydomonas and Polytomella, the cox2 gene is split into two separately expressed ORFs (cox2A and cox2B), and both ORFs are present in the nucleus (Pérez-Martínez et al. 2001
). In another green alga, Prototheca, the entire cox2 gene is present in the mitochondrion as a single ORF (Wolff et al. 1994
). Yet another green alga, Scenedesmus, contains a truncated cox2 gene (cox2A) in the mitochondrion (Kuck, Jekosch, and Holzamer 2000; Nedelcu et al. 2000)
, and it is hypothesized that the 3' end of cox2 (cox2B) is present in the nucleus of Scenedesmus (Pérez-Martínez et al. 2001
). The variable presence of cox2 as one or two ORFs and in the nucleus or mitochondrion of green algae could be explained by two models. Pérez-Martínez et al. (2001)
proposed that there was cox2 fission in the mitochondrion, followed by transfers of each ORF (cox2A and cox2B) to the nucleus in the common ancestor of Polytomella and Chlamydomonas; presumably, the hypothesized nuclear cox2B in Scenedesmus would have been derived from a separate transfer. Alternatively, transfer of cox2B to the nucleus might have occurred first, in a common ancestor of Scenedesmus, Polytomella, and Chlamydomonas, followed by formation of the cox2A ORF in the mitochondrion, similar to what we have proposed for rpl2 in eudicots. In either model, cox2A was transferred to the nucleus in the lineage containing Polytomella and Chlamydomonas, after the divergence from the Scenedesmus lineage.
Perspectives on Gene Retention in the Mitochondrion Following Duplicative Transfer to the Nucleus
If our inference of a single transfer of the 3' end of rpl2 to the nucleus early during core eudicot evolution is correct, then numerous rosids and asterids have retained this region as a pseudogene in the mitochondrion for a relatively long period of time. Pseudogene retention on this scale is surprising, given the potential for deletion or recombination to eliminate the nonfunctional gene, and contrasts dramatically with the survey hybridization results obtained for the genes rps2 and rps11 in eudicots (Adams et al. 2001a). Rps11 and rps2 were probably transferred to the nucleus at about the same time as the 3' end of rpl2, yet the gene probes hybridized strongly to only one or two DNAs from the 179 core eudicots examined.
Why have pseudogenes of 3' rpl2 been so widely retained in eudicot mitochondrial DNAs? One possibility is that because the 3' end of rpl2 is tightly linked to the still-functional 5' rpl2 ORF, elimination by a large deletion is relatively difficult, as such a deletion might disrupt the 5' ORF. Other factors, such as the involvement of the 3' end in the regulation of the 5' ORF or in some other regulatory role, might also be at work. A very different possibility involves stochastic factors relating to the timing of mitochondrial gene loss relative to eudicot diversification. If 3' rpl2 happened to survive as a mitochondrial pseudogene through perhaps a rapid period of early eudicot diversification, then many separate mitochondrial losses, each occurring at the base of each of these early-arising lineages, would be required to produce an rps2/rps11like hybridization pattern, and instead a pattern similar to that observed for 3' rpl2 might be more likely to result. Perhaps both rps2 and rps11 happened to be lost from the mitochondrial genome only once, relatively soon after transfer to the nucleus, before there was diversification into any of the many different descendant lineages of extant eudicots. (According to this model, the one or two deeply nested eudicot mitochondrial DNAs to which rps2 and rps11 probes hybridized strongly would have regained the relevant gene via reverse transfer from the nucleus or lateral transfer from some other taxa. Our preliminary data favor the latter possibility in the one case examined so far.) If so, then for rps2 or rps11, there would be no possibility of long-term retention of mitochondrial pseudogenes (and many separate losses within the eudicot transfer clade). Finally, it should be noted that these various selective and stochastic or phylogenetic possibilities are not mutually exclusive.
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Acknowledgements |
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Footnotes |
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Keywords: plant mitochondria
gene fission
gene transfer
ribosomal protein genes
Abbreviations: aa, amino acids; ORF, open reading frame.
Address for correspondence and reprints: Keith L. Adams, Department of Botany, Iowa State University, Ames, Iowa 50011. kladams{at}iastate.edu
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References |
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