- Research article
- Open Access
Ribosomal protein L10 is encoded in the mitochondrial genome of many land plants and green algae
© Mower and Bonen; licensee BioMed Central Ltd. 2009
- Received: 3 August 2009
- Accepted: 16 November 2009
- Published: 16 November 2009
The mitochondrial genomes of plants generally encode 30-40 identified protein-coding genes and a large number of lineage-specific ORFs. The lack of wide conservation for most ORFs suggests they are unlikely to be functional. However, an ORF, termed orf-bryo1, was recently found to be conserved among bryophytes suggesting that it might indeed encode a functional mitochondrial protein.
From a broad survey of land plants, we have found that the orf-bryo1 gene is also conserved in the mitochondria of vascular plants and charophycean green algae. This gene is actively transcribed and RNA edited in many flowering plants. Comparative sequence analysis and distribution of editing suggests that it encodes ribosomal protein L10 of the large subunit of the ribosome. In several lineages, such as crucifers and grasses, where the rpl10 gene has been lost from the mitochondrion, we suggest that a copy of the nucleus-encoded chloroplast-derived rpl10 gene may serve as a functional replacement.
Despite the fact that there are now over 20 mitochondrial genome sequences for land plants and green algae, this gene has remained unidentified and largely undetected until now because of the unlikely coincidence that most of the earlier sequences were from the few lineages that lack the intact gene. These results illustrate the power of comparative sequencing to identify novel genomic features.
- Mitochondrial Genome
- Edit Site
- Complete Mitochondrial Genome
- Rpl10 Gene
- Plant Mitochondrial Genome
The mitochondrial proteome consists of at least 1000 different proteins. The genes encoding many of these proteins were initially encoded within the original respiring endosymbiont but have undergone intracellular transfer to the nucleus over evolutionary time, so that the proteins must be targeted back to the mitochondrion to perform their function. The number of retained mitochondrial protein-coding genes varies widely among eukaryotes, from 67 in the jakobid Reclinomonas americana  to only 3 in apicomplexans such as Plasmodium falciparum . Genes retained in the mitochondrion encode proteins involved in fundamental mitochondrial processes such as electron transport, ATP synthesis, gene expression, and protein maturation/import. In Reclinomonas mitochondria, genes for the translational machinery comprise the largest single category, with 27 ribosomal protein genes .
In streptophytes (vascular plants, bryophytes, and charophycean green algae), the mitochondrial genome typically contains about 30 to 40 protein-coding genes of identified function. Approximately 20 of these genes are universally present, whereas the others (or a subset thereof) have been lost from various plant groups . Genes encoding ribosomal proteins and subunits of the succinate dehydrogenase complex are most commonly absent , although loss or pseudogenization of other genes, such as cox2 [4, 5], nad7 [6, 7], atp8 , and cytochrome c biogenesis subunits [7, 8] has occurred as well. Typically, a gene is deleted from the plant mitochondrial genome only after successful transfer of a copy to the nucleus, although examples exist where loss is correlated with functional replacement of a "native" mitochondrial ribosomal protein by a nucleus-encoded plastid or cytosolic homolog [9, 10]. The timing of migration of mitochondrial ribosomal protein genes to the nucleus during eukaryotic evolution can be followed by comparative analysis [11, 12].
The mitochondrial genomes of seed plants are particularly large and recombinogenic. They contain many potential unknown open reading frames (ORFs) which have often been annotated as such in genomic sequencing projects when longer than 100 codons. However, most of these ORFs are not broadly conserved, which has brought into question their potential functionality. Moreover, it is not uncommon for plant mitochondrial DNA rearrangements to give rise to novel chimeric ORFs in specific lineages, and in certain instances such ORFs are correlated with mitochondrial dysfunction in the form of cytoplasmic male sterility . On the other hand, a few ORFs have shown conservation among plants, and over recent years these have been upgraded to known mitochondrial genes. This list includes atp4 [14, 15], atp8 [15–17] and mttB (or tatC) [18, 19], which previously were denoted as orf25, orfB, and orfX, respectively. Within the three complete non-vascular plant mitochondrial genomes, there is another unidentified conserved ORF, named orf-bryo1 in the hornwort Megaceros aenigmaticus , orf187 in the moss Physcomitrella patens , and orf168 in the liverwort Marchantia polymorpha , suggesting that it may in fact code for a functional mitochondrial product in plants.
Mitochondrial orf-bryo1is conserved across streptophytes
To determine whether this bryophyte mitochondrial ORF might be more widespread among plants, blastp searches were performed using these three protein sequences to query the NCBI protein database. A homolog was found in the completely sequenced mitochondrial genomes of the angiosperms Nicotiana tabacum (orf159b)  and Vitis vinifera (orf159)  and, albeit with low sequence similarity, in the charophytes Chaetosphaeridium globosum (orf126)  and Chlorokybus atmophyticus (orf295) . An unnamed predicted protein from cDNA analysis (XP_002332837) was also identified from Populus trichocarpa. Interestingly, the moss orf187 shows weak similarity to ribosomal protein L10 from several bacteria, including Rickettsia prowazekii and other members of the alpha-proteobacteria, the lineage from which mitochondria originated , as well as to mitochondrial L10 from the jakobid Reclinomonas americana, a protist that possesses the most "primitive" and gene-rich of all mitochondrial genomes . These observations suggested that the moss orf187 (and its homologs) might encode mitochondrial L10 in plants. Indeed, annotated L10 domains can be found in the GenPept records for Physcomitrella orf187 (BAE93086) and Chlorokybus orf295 (ABO15139).
To determine how widely this mitochondrial rpl10-like gene is represented in seed plants and to gain more insight into the prevalence and timing of apparent pseudogenization in certain lineages, a PCR survey was undertaken using primers designed from the angiosperm and gymnosperm sequences identified above. Sequencing revealed the presence of this gene in another 24 seed plants, of which 5 were pseudogenes (Figure 1). Overall, these results show that homologs to the orf-bryo1 gene can be found across virtually all major streptophyte lineages, although it should be noted that lycophytes are not represented in this data set and no homologous sequences were detected in the mitochondrial data recently presented for Isoetes engelmannii . Notably, the rpl10-like gene appears to have been independently lost at least five times during angiosperm history: from the asterid Pentas, from the caryophyllid Beta, from the crucifers Arabidopsis and Brassica, from monocots, and from the conifer Podocarpus.
Angiosperm orf-bryo1homologs are transcribed, edited and likely encode a functional mitochondrial L10
Pairwise ω (dN/dS) for plant rpl10 sequences
The effect of RNA editing on amino acid sequence
Confirmed Nonsilent Editing Positionsa
In Figure 2, the amino acid alignment of plant and charophycean green algal mitochondrial orf-bryo1 homologs also includes the Reclinomonas americana mitochondrion-encoded L10 protein and homologs from the eubacteria Escherichia coli, Rickettsia prowazekii, and Thermotoga maritima. The L10 ribosomal protein is universally present in the ribosomes of eubacteria, archaea, and eukaryotes, and the crystal structure of L10-L7/L12 stalk has been determined . It is worth noting that the amino-terminal domain is more highly conserved than the carboxy-terminal half. For example, the Rickettsia prowazekii and E. coli L10 proteins share only about 26% amino acid identity over their full length, whereas the beta-1 to alpha-5 region (of 85 amino acids) within the amino-terminal half shows ~35% identity. It is the amino-terminal domain of L10 (or more specifically, the alpha-1 to alpha-3 region) that binds directly to the large subunit ribosomal RNA, whereas the carboxy-terminal domain of L10 (and alpha-8 in particular) interacts with the L7/L12 stalk; together with L11, this complex plays a key role in recruiting translation factors to the ribosome and stimulating GTP hydrolysis [34, 35]. The flowering plant mitochondrial L10 proteins share about 23% amino acid identity with the Rickettsia L10 homolog over the amino-terminal beta-1 to alpha-5 region of 85 amino acids, compared to 27-28% identity seen between Rickettsia L10 and the comparable region of the Physcomitrella or Reclinomonas mitochondrial counterparts. Of particular note are several highly conserved blocks that are believed to be important for protein structure . They contain Gly (and Pro) residues for beta-turns between beta1-alpha2 and alpha4-beta3 in L10 proteins of eubacteria and archaea. Interestingly, 7 of 8 positions of RNA editing lie within conserved blocks, consistent with their functional importance, a hallmark of RNA editing in plant mitochondria .
Status of mitochondrial L10 in grasses and crucifers
For the reasons discussed above, one might expect that all seed plants would possess a mitochondrial-type rpl10 gene either within the mitochondrion or alternatively within the nucleus since the simplest explanation for cases of gene loss from the mitochondrion (see Figure 1) is that successful gene transfer to the nucleus has occurred. Curiously, no mitochondrial-type L10 protein sequences were detected in tblastn searches of the completely sequenced nuclear genomes of Arabidopsis  or rice [38, 39]. However, both these genomes do contain duplicated copies of the chloroplast-derived rpl10 gene (data not shown). In land plants, the chloroplast rpl10 gene is located in the nucleus, and proteomic analysis of spinach chloroplast ribosomes has established its precise protein content . The chloroplast L10 orthologs in Arabidopsis (NP_196855) and rice (NP_001049761) share about 70% amino acid identity (excluding the acquired N-terminal targeting extensions). In contrast, the second chloroplast-type L10-related copy shows only ~41% amino acid identity between the Arabidopsis (NP_187843) and rice (NP_001054498) counterparts, and these proteins are predicted to be localized in the mitochondrion based on targeting programs such as TargetP , PSort , and Predotar  Interestingly, the two Arabidopsis chloroplast-derived L10 paralogs are more closely related to each other (~58% identity) than are two rice ones (~46% identity), suggesting a more recent duplication event in the crucifer lineage. This would also be consistent with their independent recruitment as functional substitutes for the mitochondrial L10 protein at different times during angiosperm evolution, although it cannot be formally excluded that gene conversion events in the Arabidopsis lineage contribute to the higher sequence similarity.
Although the duplicated chloroplast-type L10-related gene is an attractive candidate to serve as a replacement in the mitochondrial ribosome for those plants which lack the "native" mitochondrial rpl10 gene, these proteins in Arabidopsis and rice lack a number of the expected conserved residues, ones that are observed in the plant mitochondrion-encoded genes. Alternative possibilities are that the chloroplast L10 might be dual targeted to both the plastid and the mitochondrion or that the cytosolic ribosomal protein L10 counterpart (called L10e or P0) has been recruited. It is perhaps even possible that plants such as rice and Brassica, which possess what appear to be remnant pseudogene fragments in the mitochondrion, actually have several short genes (mitochondrial or nuclear) that generate a discontinuous L10 protein structure, a phenomenon observed for the mitochondrial rpl2 gene in certain flowering plants . Finally, it is worth noting that non-homologous proteins have been known to perform molecular mimicry in the evolution of the large ribosomal subunit among eubacteria and archaea .
In summary, these observations provide strong evidence that a functional rpl10 gene exists in the mitochondrion of many streptophytes. Despite the fact that there are now over 20 streptophytes with complete mitochondrial genome sequences, this gene has been missed until now due to the unlikely coincidence that most of the plant mitochondrial genomes that were first completely sequenced - the crucifers Arabidopsis thaliana  and Brassica napus ; the grasses Oryza sativa , Zea mays  and Triticum aestivum ; and the sugar beet Beta vulgaris  - are from lineages where this gene has been lost or pseudogenized. Only with the more recent sequence data from diverse streptophytes such as Cycas taitungensis , Physcomitrella patens  and Megaceros aenigmaticus  does the general pattern emerge that this gene is in fact widely present. Indeed, the bryophyte orf-bryo1 sequences were particularly informative in bridging the evolutionary distance between mitochondrial L10 gene homologs in seed plants and those of charophycean green algae/protists, which nicely illustrates the power of obtaining sequence information from diverse organisms in order to reconstruct events related to gene and genome history.
Total genomic DNAs and RNAs were isolated using the DNeasy and RNeasy Plant Mini Kits (QIAGEN) from leaf tissue available in the living collection of the Beadle Center Greenhouse (University of Nebraska). To prepare first-strand cDNA, RNAs were treated with DNase I (Fermentas) to remove contaminating DNA and then reverse transcribed using M-MuLV Reverse Transcriptase (Fermentas) and random hexamers (Fermentas) according to the manufacturer's instructions.
Taxonomy and GenBank accession numbers for rpl10 sequences in this study
Sequences were aligned using Muscle 3.7  and manually adjusted in BioEdit 7.0.9 . Edit sites were identified by comparison of DNA sequences with cDNA and/or EST sequences. To examine levels of functional constraint, poorly-aligned regions were first identified and removed using Gblocks 0.91b , then pairwise dN and dS were computed in MEGA 4.0.2  using the Nei-Gojobori Model with a Jukes-Cantor correction for multiple hits.
Another group has independently discovered the rpl10 gene in the mitochondrial genome of plants . Similar to our study, Kubo and Arimura find that the mitochondrial gene is widely distributed among plants, is transcribed and RNA edited in multiple species, and has been lost from several lineages, including Arabidopsis and rice. These authors suggest, as we do, that a duplicated copy of the nucleus-encoded chloroplast rpl10 gene has functionally replaced the lost mitochondrial rpl10 gene independently in Arabidopsis and rice. For both species, they experimentally show that these putative mitochondrially-functioning L10 proteins have targeting signals that indeed induce localization to the mitochondrion, and also the chloroplast.
We thank Dana Ahmed, Sidra Jawaid, and Derek Schmidt for assistance with DNA and RNA isolations. This work was supported by start-up funds from the University of Nebraska Lincoln (JPM) and by the Natural Sciences and Engineering Research Council of Canada (LB).
- Lang BF, Burger G, O'Kelly CJ, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Gray MW: An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature. 1997, 387: 493-497. 10.1038/387493a0.View ArticlePubMedGoogle Scholar
- Wilson RJM, Williamson DH: Extrachromosomal DNA in the Apicomplexa. Microbiol Mol Biol Rev. 1997, 61: 1-16.PubMed CentralPubMedGoogle Scholar
- Adams KL, Palmer JD: Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol. 2003, 29: 380-395. 10.1016/S1055-7903(03)00194-5.View ArticlePubMedGoogle Scholar
- Nugent JM, Palmer JD: RNA-mediated transfer of the gene coxII from the mitochondrion to the nucleus during flowering plant evolution. Cell. 1991, 66: 473-81. 10.1016/0092-8674(81)90011-8.View ArticlePubMedGoogle Scholar
- Covello PS, Gray MW: Silent mitochondrial and active nuclear genes for subunit 2 of cytochrome c oxidase (cox2) in soybean: evidence for RNA-mediated gene transfer. EMBO J. 1992, 11: 3815-3820.PubMed CentralPubMedGoogle Scholar
- Kobayashi Y, Knoop V, Fukuzawa H, Brennicke A, Ohyama K: Interorganellar gene transfer in bryophytes: the functional nad7 gene is nuclear encoded in Marchantia polymorpha. Mol Gen Genet. 1997, 256: 589-592.PubMedGoogle Scholar
- Li L, Wang B, Liu Y, Qiu YL: The complete mitochondrial genome sequence of the hornwort Megaceros aenigmaticus shows a mixed mode of conservative yet dynamic evolution in early land plant mitochondrial genomes. J Mol Evol. 2009, 68: 665-678. 10.1007/s00239-009-9240-7.View ArticlePubMedGoogle Scholar
- Turmel M, Otis C, Lemieux C: The chloroplast and mitochondrial genome sequences of the charophyte Chaetosphaeridium globosum: insights into the timing of the events that restructured organelle DNAs within the green algal lineage that led to land plants. Proc Natl Acad Sci USA. 2002, 99: 11275-11280. 10.1073/pnas.162203299.PubMed CentralView ArticlePubMedGoogle Scholar
- Adams KL, Daley DO, Whelan J, Palmer JD: Genes for two mitochondrial ribosomal proteins in flowering plants are derived from their chloroplast or cytosolic counterparts. Plant Cell. 2002, 14: 931-943. 10.1105/tpc.010483.PubMed CentralView ArticlePubMedGoogle Scholar
- Mollier P, Hoffmann B, Debast C, Small I: The gene encoding Arabidopsis thaliana mitochondrial ribosomal protein S13 is a recent duplication of the gene encoding plastid S13. Curr Genet. 2002, 40: 405-409. 10.1007/s00294-002-0271-5.View ArticlePubMedGoogle Scholar
- Bonen L, Calixte S: Comparative analysis of bacterial-origin genes for plant mitochondrial ribosomal proteins. Mol Biol Evol. 2006, 23: 701-712. 10.1093/molbev/msj080.View ArticlePubMedGoogle Scholar
- Smits P, Smeitink JAM, Heuvel van den LP, Huynen MA, Ettema TJG: Reconstructing the evolution of the mitochondrial ribosomal proteome. Nucleic Acids Res. 2007, 35: 4686-4703. 10.1093/nar/gkm441.PubMed CentralView ArticlePubMedGoogle Scholar
- Chase CD: Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet. 2007, 23: 81-90. 10.1016/j.tig.2006.12.004.View ArticlePubMedGoogle Scholar
- Burger G, Lang BF, Braun HP, Marx S: The enigmatic mitochondrial ORF ymf39 codes for ATP synthase chain b. Nucleic Acids Res. 2003, 31: 2353-2360. 10.1093/nar/gkg326.PubMed CentralView ArticlePubMedGoogle Scholar
- Heazlewood JL, Whelan J, Millar AH: The products of the mitochondrial orf25 and orfB genes are Fo components in the plant F1Fo ATP synthase. FEBS Lett. 2003, 540: 201-205. 10.1016/S0014-5793(03)00264-3.View ArticlePubMedGoogle Scholar
- Gray MW, Lang BF, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Brossard N, Delage E, Littlejohn TG, Plante I, Rioux P, Saint-Louis D, Zhu Y, Burger G: Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Res. 1998, 26: 865-878. 10.1093/nar/26.4.865.PubMed CentralView ArticlePubMedGoogle Scholar
- Sabar M, Gagliardi D, Balk J, Leaver CJ: ORFB is a subunit of F1F(O)-ATP synthase: insight into the basis of cytoplasmic male sterility in sunflower. EMBO Rep. 2003, 4: 381-386. 10.1038/sj.embor.embor800.PubMed CentralView ArticlePubMedGoogle Scholar
- Bogsch EG, Sargent F, Stanley NR, Berks BC, Robinson C, Palmer T: An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J Biol Chem. 1998, 273: 18003-18006. 10.1074/jbc.273.29.18003.View ArticlePubMedGoogle Scholar
- Weiner JH, Bilous PT, Shaw GM, Lubitz SP, Frost L, Thomas GH, Cole JA, Turner RJ: A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell. 1998, 93: 93-101. 10.1016/S0092-8674(00)81149-6.View ArticlePubMedGoogle Scholar
- Terasawa K, Odahara M, Kabeya Y, Kikugawa T, Sekine Y, Fujiwara M, Sato N: The mitochondrial genome of the moss Physcomitrella patens sheds new light on mitochondrial evolution in land plants. Mol Biol Evol. 2007, 24: 699-709. 10.1093/molbev/msl198.View ArticlePubMedGoogle Scholar
- Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T, Ohyama K: Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA - a primitive form of plant mitochondrial genome. J Mol Biol. 1992, 223: 1-7. 10.1016/0022-2836(92)90708-R.View ArticlePubMedGoogle Scholar
- Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S, Hirai A, Sugiura M: The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol Genet Genomics. 2005, 272: 603-615. 10.1007/s00438-004-1075-8.View ArticlePubMedGoogle Scholar
- Goremykin VV, Salamini F, Velasco R, Viola R: Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Mol Biol Evol. 2009, 26: 99-110. 10.1093/molbev/msn226.View ArticlePubMedGoogle Scholar
- Turmel M, Otis C, Lemieux C: An unexpectedly large and loosely packed mitochondrial genome in the charophycean green alga Chlorokybus atmophyticus. BMC Genomics. 2007, 8: 137-10.1186/1471-2164-8-137.PubMed CentralView ArticlePubMedGoogle Scholar
- Andersson SG, Zomorodipour A, Andersson JO, Sicheritz-Ponten T, Alsmark UC, Podowski RM, Naslund AK, Eriksson AS, Winkler HH, Kurland CG: The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature. 1998, 396: 133-140. 10.1038/24094.View ArticlePubMedGoogle Scholar
- Turmel M, Otis C, Lemieux C: The mitochondrial genome of Chara vulgaris: insights into the mitochondrial DNA architecture of the last common ancestor of green algae and land plants. Plant Cell. 2003, 15: 1888-1903. 10.1105/tpc.013169.PubMed CentralView ArticlePubMedGoogle Scholar
- Chaw SM, Shih ACC, Wang D, Wu YW, Liu SM, Chou TY: The mitochondrial genome of the gymnosperm Cycas taitungensis contains a novel family of short interspersed elements, Bpu sequences, and abundant RNA editing sites. Mol Biol Evol. 2008, 25: 603-615. 10.1093/molbev/msn009.View ArticlePubMedGoogle Scholar
- Grewe F, Viehoever P, Weisshaar B, Knoop V: A trans-splicing group I intron and tRNA-hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii. Nucleic Acids Res. 2009, 37: 5093-5104. 10.1093/nar/gkp532.PubMed CentralView ArticlePubMedGoogle Scholar
- Rüdinger M, Funk HT, Rensing SA, Maier UG, Knoop V: RNA editing: only eleven sites are present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal. Mol Genet Genomics. 2009, 281: 473-481. 10.1007/s00438-009-0424-z.View ArticlePubMedGoogle Scholar
- Mower JP, Palmer JD: Patterns of partial RNA editing in mitochondrial genes of Beta vulgaris. Mol Genet Genomics. 2006, 276: 285-293. 10.1007/s00438-006-0139-3.View ArticlePubMedGoogle Scholar
- Giegé P, Brennicke A: RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc Natl Acad Sci USA. 1999, 96: 15324-15329. 10.1073/pnas.96.26.15324.PubMed CentralView ArticlePubMedGoogle Scholar
- Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K: The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics. 2002, 268: 434-445. 10.1007/s00438-002-0767-1.View ArticlePubMedGoogle Scholar
- Handa H: The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res. 2003, 31: 5907-5916. 10.1093/nar/gkg795.PubMed CentralView ArticlePubMedGoogle Scholar
- Diaconu M, Kothe U, Schlünzen F, Fischer N, Harms JM, Tonevitsky AG, Stark H, Rodnina MV, Wahl MC: Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTPase activation. Cell. 2005, 121: 991-1004. 10.1016/j.cell.2005.04.015.View ArticlePubMedGoogle Scholar
- Shcherbakov D, Dontsova M, Tribus M, Garber M, Piendl W: Stability of the 'L12 stalk' in ribosomes from mesophilic and (hyper)thermophilic archaea and bacteria. Nucleic Acids Res. 2006, 34: 5800-5814. 10.1093/nar/gkl751.PubMed CentralView ArticlePubMedGoogle Scholar
- Gray MW, Covello PS: RNA editing in plant mitochondria and chloroplasts. FASEB J. 1993, 7: 64-71.PubMedGoogle Scholar
- Arabidopsis Genome Initiative: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000, 408: 796-815. 10.1038/35048692.View ArticleGoogle Scholar
- Goff SA, (55 co-authors), et al: A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science. 2002, 296: 92-100. 10.1126/science.1068275.View ArticlePubMedGoogle Scholar
- Yu J, (100 co-authors), et al: A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science. 2002, 296: 79-92. 10.1126/science.1068037.View ArticlePubMedGoogle Scholar
- Yamaguchi K, Subramanian AR: The plastid ribosomal proteins: identification of all the proteins in the 50S subunit of an organelle ribosome (chloroplast). J Biol Chem. 2000, 275: 28466-28482. 10.1074/jbc.M005012200.View ArticlePubMedGoogle Scholar
- Emanuelsson O, Nielsen H, Brunak S, von Heijne G: Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol. 2000, 300: 1005-1016. 10.1006/jmbi.2000.3903.View ArticlePubMedGoogle Scholar
- Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S: Extensive feature detection of N-terminal protein sorting signals. Bioinformatics. 2002, 18: 298-305. 10.1093/bioinformatics/18.2.298.View ArticlePubMedGoogle Scholar
- Small I, Peeters N, Legeai F, Lurin C: Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics. 2004, 4: 1581-1590. 10.1002/pmic.200300776.View ArticlePubMedGoogle Scholar
- Adams KL, Ong HC, Palmer JD: Mitochondrial gene transfer in pieces: fission of the ribosomal protein gene rpl2 and partial or complete gene transfer to the nucleus. Mol Biol Evol. 2001, 18: 2289-2297.View ArticlePubMedGoogle Scholar
- Klein DJ, Moore PB, Steitz TA: The roles of ribosomal proteins in the structure, assembly, and evolution of the large ribosomal subunit. J Mol Biol. 2004, 340: 141-177. 10.1016/j.jmb.2004.03.076.View ArticlePubMedGoogle Scholar
- Unseld M, Marienfeld JR, Brandt P, Brennicke A: The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet. 1997, 15: 57-61. 10.1038/ng0197-57.View ArticlePubMedGoogle Scholar
- Clifton SW, Minx P, Fauron CM, Gibson M, Allen JO, Sun H, Thompson M, Barbazuk WB, Kanuganti S, Tayloe C, Meyer L, Wilson RK, Newton KJ: Sequence and comparative analysis of the maize NB mitochondrial genome. Plant Physiol. 2004, 136: 3486-3503. 10.1104/pp.104.044602.PubMed CentralView ArticlePubMedGoogle Scholar
- Ogihara Y, Yamazaki Y, Murai K, Kanno A, Terachi T, Shiina T, Miyashita N, Nasuda S, Nakamura C, Mori N, Takumi S, Murata M, Futo S, Tsunewaki K: Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome. Nucleic Acids Res. 2005, 33: 6235-6250. 10.1093/nar/gki925.PubMed CentralView ArticlePubMedGoogle Scholar
- Kubo T, Nishizawa S, Sugawara A, Itchoda N, Estiati A, Mikami T: The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNA-Cys (GCA). Nucleic Acids Res. 2000, 28: 2571-2576. 10.1093/nar/28.13.2571.PubMed CentralView ArticlePubMedGoogle Scholar
- Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32: 1792-97. 10.1093/nar/gkh340.PubMed CentralView ArticlePubMedGoogle Scholar
- Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999, 41: 95-98.Google Scholar
- Talavera G, Castresana J: Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007, 56: 564-577. 10.1080/10635150701472164.View ArticlePubMedGoogle Scholar
- Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007, 24: 1596-1599. 10.1093/molbev/msm092.View ArticlePubMedGoogle Scholar
- Kubo N, Arimura S: Discovery of the rpl10gene in diverse plant mitochondrial genomes and its probable replacement by the nuclear gene for chloroplast RPL10 in two lineages of angiosperms. DNA Research. Google Scholar
- The Angiosperm Phylogeny Website. [http://www.mobot.org/mobot/research/apweb/welcome.html]
- Spencer DF, Schnare MN, Coulthart MB, Gray MW: Sequence and organization of a 7.2 kb region of wheat mitochondrial DNA containing the large subunit (26S) rRNA gene. Plant Mol Biol. 1992, 20: 347-352. 10.1007/BF00014506.View ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.