Département de Biochimie et de Microbiologie, Université Laval, Québec, Québec, Canada
Correspondence: E-mail: Monique.Turmel{at}rsvs.ulaval.ca.
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Abstract |
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Key Words: Green algae Ulvophyceae Pseudendoclonium akinetum mitochondrial DNA group I introns repeated sequences
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Introduction |
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Because of their large size and their tendency to incorporate foreign DNA (from the nucleus and the chloroplast), land-plant mitochondrial genomes have been reported to feature an "expanded" pattern of evolution (Turmel et al. 1999). These mitochondrial genomes are the largest (187 kb in Marchantia to 2,000 kb in muskmelon) among green plants, and they also show the greatest structural complexity. Most of the increased size of land-plant mtDNAs relative to their green-algal homologs is accounted for by noncoding sequences that reside either in intergenic regions or introns (Oda et al. 1992; Unseld et al. 1997; Kubo et al. 2000; Notsu et al. 2002). Sixty-nine mitochondrial genes have been identified in Marchantia (Oda et al. 1992; Gray et al. 1998), whereas about 50 have been found in angiosperms (Unseld et al. 1997; Kubo et al. 2000; Notsu et al. 2002). This substantial difference in coding capacity is attributed to gene transfer to the nucleus, a widespread and ongoing phenomenon (Schuster and Brennicke 1994; Palmer et al. 2000; Adams et al. 2002). In embryophyte mitochondria, unicircular genome-sized molecules coexist in a dynamic equilibrium with subgenomic circles (Palmer and Shields 1984; Mackenzie, He, and Lyznik 1994). In Marchantia mitochondria, unicircular-genome sized molecules apparently coexist with linear molecules and complex branched structures of multigenomic sizes (Oldenburg and Bendich 2001). In contrast to their fluid structure, land-plant mitochondrial genomes evolve extremely slowly at the sequence level; in angiosperm mitochondria, point mutations can occur at a frequency up to 100 times lower than in vertebrate mitochondria (Wolfe, Li, and Sharp 1987; Palmer and Herbon 1988).
The more compact green-algal mitochondrial genomes display distinctive evolutionary patterns. They range in size from 16 kb (in C. reinhardtii) to 67.8 kb (in Mesostigma) and encode 12 (in C. reinhardtii, C. eugametos, and Chlorogonium) to 67 (in Chaetosphaeridium) genes. An "ancestral" (minimally derived) evolutionary pattern (Turmel et al. 1999) has been ascribed to the circular-mapping mtDNAs of Mesostigma, Chaetosphaeridium, Nephroselmis, and Prototheca, because of their large number of conserved genes (>60), their high gene density, and their important sequence conservation. Not only fewer genes but also a greater variability in gene content (12 to 42 genes) and structural organization (linear or circular-mapping molecules, or even multimeric molecules, as reported for Polytomella [Fan and Lee 2002]) have been found in chlorophycean green-algal mtDNAs. The coding sequences of these genomes are highly divergent from those of other green plants and feature numerous deletions/additions; moreover, the rRNA gene-coding regions are fragmented into pieces that are dispersed throughout the genomes. As a consequence of this high sequence divergence, chlorophycean taxa exhibit very long branches in mitochondrial trees, and, most probably because of long-branch attraction artifacts, usually lie outside the green-plant clade when other green plants and nongreen-plant taxa are included in the analyses. A "reduced-derived pattern" (Turmel et al. 1999) of evolution has been assigned to the three smallest and gene-poorest chlorophycean mtDNAs (i.e., to C. reinhardtii, C. eugametos, and Chlorogonium mtDNAs). Because of its less-derived characters, the Scenedesmus mtDNA sequence has been considered to display an "intermediate" pattern of evolution (Nedelcu et al. 2000).
The present study was undertaken to gather information about the evolutionary trends of the mitochondrial genome in the Ulvophyceae and also to gain insights into the phylogenetic relationships between ulvophytes and other chlorophytes. Various hypotheses have been proposed concerning the phylogenetic position of the Ulvophyceae within the Chlorophyta, but none is strongly supported by statistical analyses. On the basis of ultrastructural studies (Mattox and Stewart 1984; O'Kelly and Floyd 1984) and some phylogenetic analyses of nuclear small subunit (SSU) rDNA sequences (Friedl 1995; Bhattacharya, Friedl, and Damberger 1996; Nakayama, Watanabe, and Inouye 1996; Chapman et al. 1998; Watanabe et al. 2000; Wolf et al. 2002), it has been proposed that the Ulvophyceae are a monophyletic assemblage that emerged before the divergence of the Trebouxiophyceae and Chlorophyceae. Independent inferences from nuclear SSU rDNA sequences (Friedl 1997; Marin and Melkonian 1999) and from concatenated chloroplast SSU and large subunit (LSU) (Turmel et al. 2002) rDNA sequences suggest a possible sister-group relationship between the Ulvophyceae and Chlorophyceae, with the Trebouxiophyceae occupying a basal position. On the other hand, separate nuclear SSU rDNA trees (Bhattacharya and Medlin 1998) favor the hypothesis that the Chlorophyceae appeared before the divergence of the Ulvophyceae and Trebouxiophyceae, whereas recent trees, including a wider diversity of ulvophytes (Friedl and O'Kelly 2002) failed to revolve the branching order of the Trebouxiophyceae, Chlorophyceae, and Ulvophyceae. Moreover, other nuclear SSU rDNA trees, including several ulvophytes (Watanabe, Kuroda, and Maiwa 2001) are in agreement with an earlier report (Zechman et al. 1990) and with the concept of the Ulvophyceae sensu Sluiman (1989) in supporting the notion that the ulvophytes are nonmonophyletic. In the Ulvophyceae sensu Sluiman, ulvophytes and trebouxiophytes are merged to form a green-algal group with a counterclockwise arrangement of kinetid components. The analyses supporting the monophyly of ulvophytes suffer from a relatively poor and/or biased taxon sampling (all five orders recognized in this class were not represented), whereas those supporting their nonmonophyly may be plagued with long-branch attraction artifacts.
In this study, we report the complete mtDNA sequence of Pseudendoclonium akinetum, a unicellular member of the Ulvophyceae that belongs to a putatively deep-branching lineage (Floyd and O'Kelly 1990). At 95,880 bp, this ulvophyte mtDNA is the largest green-algal mtDNA analyzed thus far. Our phylogenetic analyses provide support for a sister-group relationship between the Ulvophyceae and Chlorophyceae.
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Materials and Methods |
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Isolation and Sequencing of mtDNA
A+T-rich organellar DNA was separated from nuclear DNA by CsCl-bisbenzimide isopycnic centrifugation (Turmel et al. 1999). After nebulization of this A+T-rich fraction, a plasmid library of DNA fragments (1200 to 2500 bp) was prepared (Lemieux, Otis, and Turmel 2000). Plasmid DNA templates and PCR fragments spanning uncloned regions of Pseudendoclonium mtDNA were sequenced using ABI Prism 373XL and 377 (Applied Biosystems, Foster City, Calif.) DNA sequencers and the ABI Prism Big Dye terminator sequencing kit (Applied Biosystems) as described previously (Lemieux, Otis, and Turmel 2000). Templates that yielded poor sequences under these conditions were subjected to sequencing using the DYEnamic ET (Amersham Pharmacia Biotech, Baie d'Urfé, Canada) and/or the ABI Prism dGTP Big Dye (Applied Biosystems) dye terminator sequencing kits. Sequences were edited and assembled with AUTOASSEMBLER version 2.1.1 (Applied Biosystems).
Genome Analyses
Gene content was determined by Blast homology searches (Altschul et al. 1990) against the nonredundant database of NCBI. Protein-coding genes and open reading frames (ORFs) were localized precisely using ORFFINDER at NCBI and various programs of the GCG Wisconsin version 10.2 package (Accelrys, Burlington, Mass.), whereas sequences coding for tRNAs were identified with tRNAscan-SE 1.23 (Lowe and Eddy 1997). Patterns of codon usage for protein-coding genes and ORFs were compared using CORRESPOND and CODONPREFERENCE from the Wisconsin package and CAI from the EMBOSS version 2.6.0 package (http://www.hgmp.mrc.ac.uk/Software/EMBOSS/). Repeated sequence elements were identified with PIPMAKER (Schwartz et al. 2000) and REPUTER version 2.74 (Kurtz et al. 2001) and classified with REPEATFINDER (Volfovsky, Haas, and Salzberg 2001).
Phylogenetic Analyses
Mitochondrial genome sequences were retrieved from GenBank: Pseudendoclonium akinetum (accession number AY359242 [this study]), Mesostigma viride (accession number AF353999), Nephroselmis olivacea (accession number AF110138), Prototheca wickerhamii (accession number NC_001613), Pedinomonas minor (accession number NC_000892), Scenedesmus obliquus (accession number AF204057), Chlamydomonas eugametos (accession number NC_001872), Chlamydomonas reinhardtii (accession number NC_001638), Chlorogonium elongatum (accession numbers Y13643 and Y13644), Chaetosphaeridium globosum (accession number NC_004118), Marchantia polymorpha (accession number NC_001660), Arabidopsis thaliana (accession number NC_001284), Beta vulgaris (accession number NC_002511), Chondrus crispus (accession number NC_001677), and Porphyra purpurea (accession number NC_002007). Deduced amino acid sequences from individual genes were aligned using ClustalW version 1.81 (Thompson, Higgins, and Gibson 1994). Data sets were prepared by concatenating the alignments of individual proteins and removing the ambiguously aligned regions with GBLOCKS version 0.73b (Castresana 2000). Phylogenetic trees were inferred using maximum-likelihood (ML) and ML-distance methods. ML trees were computed with PROTML in MOLPHY version 2.3b3 (Adachi and Hasegawa 1996) and CODEML in PAML version 3.11 (Yang 1997) using the amino acid substitution models JTT-F, mtREV24-F, and WAG-F (Whelan and Goldman 2001). -distributed rates of substitutions across sites (eight categories) and/or multiple gene (Mgene option) corrections were applied in some CODEML analyses. Local bootstrap probabilities were estimated by resampling of the estimated log-likelihood (RELL) (Adachi and Hasegawa 1996). Confidence assessments (P-values) of tree selections were evaluated by the Approximately Unbiased, Kishino-Hasegawa, and Shimodaira-Hasegawa tests as implemented in CONSEL version 0.1d (Shimodaira and Hasegawa 2001). The effect of invariable sites on topologies was determined by analysis of a trimmed data set of 1,555 positions containing only the variable sites.
-corrected ML distances were calculated with TREE-PUZZLE version 5.0.2 (Strimmer and von Haeseler 1996) under the WAG-F model, and distance trees were computed by weighted neighbor-joining as implemented in WEIGHBOR version 1.2 (Bruno, Socci, and Halpern 2000). Support for ML-distance trees was obtained by bootstrapping (100 replications) with PUZZLEBOOT version 1.03 (A. Roger and M. Holder, http://www.tree-puzzle.de).
Comparisons of Amino Acid Substitution Rates in Different Lineages
We used the data set of 2,107 amino acid positions that was employed for the ML and ML-distance analyses. Differences in the rates of amino acid substitutions among lineages were assessed using the binomial test of Gu and Li (1992).
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Results |
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Introns
All seven introns in Pseudendoclonium mtDNA belong to the group I family (table 3). All of these introns, with the exception of Paatp1.1, show similarities with group I introns inserted at equivalent positions in other green-plant and/or fungal mtDNAs (table 4). The latter green-plant mtDNAs include those of the streptophyte Marchantia and of various chlorophytes exhibiting an "ancestral" or a "reduced-derived" pattern of mtDNA evolution. Sequence conservation between the core structures of four Pseudendoclonium introns (Pacox1.1, Pacox1.2, Pacox1.4, and Parnl.1) and their green-algal homologs is substantial (fig. 2).
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Repeated Sequence Elements
A comparison of the Pseudendoclonium mtDNA sequence against itself using PIPMAKER (Schwartz et al. 2000) revealed the presence of many degenerated repeated elements within intergenic regions and introns (fig. 3). We identified these repeated sequences using the program REPUTER and found that they are up to 350 nt in size and do not differ substantially from the rest of the Pseudendoclonium genome in terms of nucleotide composition. The repeats that were 50 nt or more were classified using REPEATFINDER (Volfovsky, Haas, and Salzberg 2001); they represent about 10 kb of the genome and form four distinct classes, designated C1 to C4 (fig. 3 and table 5). The members of a given class share no sequence similarity with those of other classes. The first class of repeats (C1) is the largest. Its members map to at least 16 different loci (fig. 3) and can be further classified into 14 subclasses, designated C1R1 through C1R14. The longest repeat within each subclass, defined as the prototype, is made up of repeated units (subrepeats) that also constitute the shorter repeated elements found in the same subclass. Distinct subclasses feature different arrangements of repeated units. The coordinates of the prototypes and number of repeated elements within each subclass are given in table 5. The abundance of subclasses in class 1 suggests that numerous recombination and shuffling events between repeated units took place during the evolution of the mitochondrial genome. On the other hand, classes 2, 3, and 4 are much less complex than class 1. Each exhibits only one subclass of repeats, with two identical copies of the prototype sequence that are far apart from one another. It is likely that these elements arose from single duplication events. In addition to the repeats described above, Pseudendoclonium mtDNA features numerous repeated elements less than 50 nt that span about 4 kb of this genome (fig. 3).
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Rates of Amino Acid Substitutions
Considering the branch lengths of the best ML tree (fig. 4), it appears that Pseudendoclonium mtDNA evolves at a slower rate than the mtDNAs of taxa from the "reduced-derived" clade. To determine whether this interpretation is correct, we assessed the relative rates of amino acid substitutions of mtDNA-encoded proteins among the different lineages using the binomial test of Gu and Li (1992) (table 7). The substitution rates of Pseudendoclonium proteins were found to be significantly smaller (P < 0.001) than those observed for Scenedesmus and other green algae from the "reduced-derived" clade. Pseudendoclonium mtDNAencoded proteins, however, evolve significantly faster (P < 0.001) than their Nephroselmis and Prototheca counterparts.
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Discussion |
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On one hand, the gene content (a relatively complex gene repertoire) and gene structure (lack of fragmented and scrambled rRNA genes) of Pseudendoclonium mtDNA are characteristic of "ancestral" mtDNAs. On the other hand, its low gene density, abundant repeats, and the absence of certain genes (nad9, rpl6, rps7, and rrn5) are typical of Scenedesmus and Pedinomonas mtDNAs. The finding of genomic features that are typical of the "reduced-derived" pattern of mtDNA evolution, together with the presence of ancestral features, suggests that Pseudendoclonium belongs to a lineage that appeared after the emergence of the Trebouxiophyceae but before the divergence of the Chlorophyceae. Further supporting this notion are three independent observations. First, ML and ML-distance trees inferred from mtDNA-encoded proteins always cluster Pseudendoclonium with chlorophycean green algae and consistently place the trebouxiophyte Prototheca at the base of this clade (see next section). Second, the overall rate of sequence evolution appears to be accelerated to an intermediary level in Pseudendoclonium mtDNA as compared with the slow rates observed in "ancestral" mtDNAs and the very fast rates detected in Pedinomonas, Scenedesmus and chlorophycean green-algal mtDNAs (fig. 4). Third, close relatives of the Pacox1.2, Pacox1.4, and Parnl.1 introns are present in mtDNAs displaying both the "ancestral" and "reduced-derived" patterns of evolution.
Phylogenetic Niche of the Ulvophyceae
Our phylogenetic analyses of concatenated mtDNA-encoded protein sequences reveal a close relationship between Pseudendoclonium and chlorophycean green algae, with the trebouxiophyte Prototheca occupying a basal position (fig. 4). These analyses included all the green-algal mtDNA sequences available in public databases to minimize possible undesirable effects of small taxon sampling and used Mesostigma viride as outgroup to maximize the amount of phylogenetic information. The position of Pseudendoclonium relative to the Chlorophyceae and Trebouxiophyceae may be the result of genuine phylogenetic signal because it is consistent with our finding that Pseudendoclonium mtDNA shares derived structural features with its homologs in chlorophycean green algae. However, the branching order of the Chlorophyceae/Ulvophyceae/Trebouxiophyceae remains an unresolved issue. The tree recovered in our analyses may reflect variations in the evolutionary rates of mtDNA sequences rather than the underlying phylogenetic signal, and although we have included all currently available green-algal mtDNAs in our analyses, taxon sampling is still very low, with only one representative of the Ulvophyceae and of the Trebouxiophyceae.
Pseudendoclonium appears to be closely related to Pedinomonas, a green alga of uncertain affiliation. In mitochondrial trees, Pedinomonas branches immediately after the emergence of the Pseudendoclonium lineage. Given the very long branch displayed by Pedinomonas, the phylogenetic position of this chlorophyte might be attributed to long-branch artifacts. However, the existence of a close relationship between Pedinomonas and ulvophytes is supported by the observation that the basal bodies of Pedinomonas and ulvophytes display an absolute counterclockwise orientation that contrasts with the directly opposed or clockwise orientation found in chlorophycean green algae (Melkonian 1990). Considering that the 25-kb mtDNA of Pedinomonas is highly reduced in size and gene content relative to its Pseudendoclonium and Scenedesmus relatives and also considering the much longer branch displayed by Pedinomonas mtDNA, it appears that the mitochondrial genome evolved at a more accelerated rate in the lineage leading to Pedinomonas than in the Pseudendoclonium and Scenedesmus lineages.
Repeated Sequence Elements As an Evolutionary Force in the Chlorophyta
Small repeats have been previously identified in chlorophyte mtDNAs. The few that are found in Prototheca mtDNA vary from 30 to 200 nt, are mostly arranged in tandem, and the recurring motifs are rich in A+T (Wolff et al. 1994). Repeats in Scenedesmus mtDNA range from 16 to 118 nt, and, like their Pseudendoclonium counterparts, account for at least 15% of the genome, flank many individual genes, are composed of various subrepeats, and show a low bias in base composition (Nedelcu et al. 2000). The repeats harbored by chlamydomonad mtDNAs are shorter (9 to 14 nt) and richer in G+C (Boer and Gray 1991; Nedelcu and Lee 1998). Unlike all their known chlorophyte counterparts, the numerous repeated sequences found in Pedinomonas mtDNA are densely packed within a discrete, noncoding region of the genome (Turmel et al. 1999). The low abundance of repeats in Nephroselmis and Prototheca mtDNAs, together with the increased occurrence of these elements in the more derived lineages leading to Pseudendoclonium and Scenedesmus, raise the question on their origin. Repeats might have been present in the mitochondrial genome of the last common ancestor of the ulvophytes and chlorophycean green algae, and have diverged after the split of these lineages. Alternatively, they might have arisen independently in the Ulvophyceae and Chlorophyceae.
Considering that recombination between dispersed repeats can lead to genome rearrangements (gene losses or inversions) and that gene content became reduced as families of dispersed repeats emerged and grew in size during the evolution of chlorophyte mtDNAs (at least in derived lineages), we speculate that repeated elements have played an important role in generating the great diversity of size and gene arrangement seen in these mtDNAs. In chlamydomonad mtDNAs, where gene content is the poorest of the Chlorophyta lineage, excision of coding regions via recombination between flanking short repeats has been invoked to explain their reduced gene content (Nedelcu 1997; Nedelcu 1998). Dispersed repeats are also thought to act as hot spots for recombination in land-plant (Palmer and Herbon 1988; Mackenzie, He, and Lyznik 1994), fungal (Jamet-Vierny, Boulay, and Briand 1997), and animal (Lunt and Hyman 1997) mtDNAs. Aside from dispersed repeats, other factors most probably determine the tempo of gene loss. For angiosperms, it has been shown that the tempo of mitochondrial gene loss (and probably gene transfer to the nucleus) is remarkably punctuated. Certain lineages have rapidly lost most or all of their 16 ribosomal protein and sdh genes, whereas other lineages, mostly ancient lineages, have maintained a constant set of mitochondrial genes for hundreds of millions of years (Adams et al. 2002). This punctuated pattern appears to be driven by major episodic rises in the rate of functional gene transfer.
Interestingly, short, dispersed repeats have been observed in the chloroplast DNAs of Chlamydomonas taxa (Boudreau and Turmel 1996; Maul et al. 2002) and of the trebouxiophyte Chlorella vulgaris (Maul et al. 2002) but not in Nephroselmis chloroplast DNA (Maul et al. 2002). The phylogenetic distribution of small, repeated elements within chlorophyte chloroplast DNAs thus parallels that observed for the mitochondrial genome. Given the evidence for lateral transfers of introns (genetic elements often associated with short repeats) between the mitochondrial and chloroplast compartments (Turmel et al. 1995; Turmel et al. 1999; Lucas et al. 2001; Turmel, Otis, and Lemieux 2002a), it is possible that such events contribute to the dispersal of short repeats and account for the presence of these elements in both organelle genomes of the same cell. In this context, it will be interesting to see if short, repeated elements are found in ulvophyte chloroplast DNAs.
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Conclusion |
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Supplementary Material |
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Acknowledgements |
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Footnotes |
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Literature Cited |
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Adachi, J., and M. Hasegawa. 1996. MOLPHY Version 2.3: programs for molecular phylogenetics based on maximum likelihood method. Comput. Sci. Monogr. 28:1-150.
Adams, K. L., D. O. Daley, J. Whelan, and J. D. Palmer. 2002. Genes for two mitochondrial ribosomal proteins in flowering plants are derived from their chloroplast or cytosolic counterparts. Plant Cell 14:931-943.
Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.[CrossRef][ISI][Medline]
Bhattacharya, D., T. Friedl, and S. Damberger. 1996. Nuclear-encoded rDNA group I introns: origin and phylogenetic relationships of insertion site lineages in the green algae. Mol. Biol. Evol. 13:978-989.
Bhattacharya, D., and L. Medlin. 1998. Algal phylogeny and the origin of land plants. Plant Physiol. 116:9-15.
Bhattacharya, D., K. Weber, S. S. An, and W. Berning-Koch. 1998. Actin phylogeny identifies Mesostigma viride as a flagellate ancestor of the land plants. J. Mol. Evol. 47:544-550.[ISI][Medline]
Boer, P. H., and M. W. Gray. 1991. Short dispersed repeats localized in spacer regions of Chlamydomonas reinhardtii mitochondrial DNA. Curr. Genet. 19:309-312.[ISI][Medline]
Boudreau, E., and M. Turmel. 1996. Extensive gene rearrangements in the chloroplast DNAs of Chlamydomonas species featuring multiple dispersed repeats. Mol. Biol. Evol. 13:233-243.[Abstract]
Bremer, K. 1985. Summary of green plant phylogeny and classification. Cladistics 1:369-385.
Bruno, W. J., N. D. Socci, and A. L. Halpern. 2000. Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol. Biol. Evol. 17:189-197.
Burger, G., B. F. Lang, H.-P. Braun, and S. Marx. 2003. The enigmatic mitochondrial ORF ymf39 codes for ATP synthase chain b. Nucleic Acids Res. 31:2353-2360.
Burke, J. M., M. Belfort, T. R. Cech, R. W. Davies, R. J. Schweyen, D. A. Shub, J. W. Szostak, and H. F. Tabak. 1987. Structural conventions for group I introns. Nucleic Acids Res. 15:7217-7221.[Abstract]
Castresana, J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17:540-552.
Chapman, R. L., M. A. Buchheim, and C. F. Delwiche, et al. (11 co-authors). 1998. Molecular systematics of the green algae. Pp. 508540 in D. E. Soltis, P. S. Soltis, and J. J. Doyle, eds. Molecular systematics of plants II DNA sequencing. Kluwer Academic Press, Norwell, Mass.
Côté, V., J.-P. Mercier, C. Lemieux, and M. Turmel. 1993. The single group-I intron in the chloroplast rrnL gene of Chlamydomonas humicola encodes a site-specific DNA endonuclease (I-ChuI). Gene 129:69-76.[CrossRef][ISI][Medline]
Denovan-Wright, E. M., A. M. Nedelcu, and R. W. Lee. 1998. Complete sequence of the mitochondrial DNA of Chlamydomonas eugametos. Plant Mol. Biol. 36:285-295.[CrossRef][ISI][Medline]
Fan, J., and R. W. Lee. 2002. Mitochondrial genome of the colorless green alga Polytomella parva: two linear DNA molecules with homologous inverted repeat termini. Mol. Biol. Evol. 19:999-1007.
Floyd, G. L., and C. J. O'Kelly. 1990. Phylum Chlorophyta: class Ulvophyceae. Pp. 617635 in L. Margulis, J. O. Corliss, M. Melkonian, and D. J. Chapman, eds. Handbook of Protoctista. Jones and Bartlett Publishers, Boston.
Friedl, T. 1995. Inferring taxonomic positions and testing genus level assignments in coccoid green lichen algae: a phylogenetic analysis of 18S ribosomal RNA sequences from Dictyochloropsis reticulata and from members of the genus Myrmecia (Chlorophyta, Trebouxiophyceae Cl. Nov.). J. Phycol. 31:632-639.[ISI]
Friedl, T. 1997. The evolution of the green algae. Plant Syst. Evol. 11:(suppl.): 87-101.
Friedl, T., and C. J. O'Kelly. 2002. Phylogenetic relationships of green algae assigned to the genus Planophila (Chlorophyta): evidence from 18S rDNA sequence data and ultrastructure. Eur. J. Phycol. 37:373-384.[CrossRef][ISI]
Gray, M. W., B. F. Lang, and R. Cedergren, et al. (15 co-authors). 1998. Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Res. 26:865-878.
Gu, X., and W.-H. Li. 1992. Higher rates of amino acid substitution in rodents than in humans. Mol. Phylogenet. Evol. 1:211-214.[Medline]
Jamet-Vierny, C., J. Boulay, and J.-F. Briand. 1997. Intramolecular cross-overs generate deleted mitochondrial DNA molecules in Podospora anserina. Curr. Genet. 31:162-170.[CrossRef][ISI][Medline]
Karol, K. G., R. M. McCourt, M. T. Cimino, and C. F. Delwiche. 2001. The closest living relatives of land plants. Science 294:2351-2353.
Kroymann, J., and K. Zetsche. 1998. The mitochondrial genome of Chlorogonium elongatum inferred from the complete sequence. J. Mol. Evol. 47:431-440.[ISI][Medline]
Kubo, T., S. Nishizawa, A. Sugawara, N. Itchoda, A. Estiati, and T. Mikami. 2000. The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNACys(GCA). Nucleic Acids Res. 28:2571-2576.
Kück, U., K. Jekosch, and P. Holzamer. 2000. DNA sequence analysis of the complete mitochondrial genome of the green alga Scenedesmus obliquus: evidence for UAG being a leucine and UCA being a non-sense codon. Gene 253:13-18.[CrossRef][ISI][Medline]
Kurtz, S., J. V. Choudhuri, E. Ohlebusch, C. Schleiermacher, J. Stoye, and R. Giegerich. 2001. REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 29:4633-4642.
Lang, B. F., M. W. Gray, and G. Burger. 1999. Mitochondrial genome evolution and the origin of eukaryotes. Annu. Rev. Genet. 33:351-397.[CrossRef][ISI][Medline]
Lemieux, C., C. Otis, and M. Turmel. 2000. Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution. Nature 403:649-652.[CrossRef][ISI][Medline]
Lowe, T. M., and S. R. Eddy. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25:955-964.
Lucas, P., C. Otis, J.-P. Mercier, M. Turmel, and C. Lemieux. 2001. Rapid evolution of the DNA-binding site in LAGLIDADG homing endonucleases. Nucleic Acids Res. 29:960-969.
Lunt, D. H., and B. C. Hyman. 1997. Animal mitochondrial DNA recombination. Nature 387:247.[CrossRef][ISI][Medline]
Mackenzie, S., S. He, and A. Lyznik. 1994. The elusive plant mitochondrion as a genetic system. Plant Physiol. 105:775-780.
Marienfeld, J., M. Unseld, and A. Brennicke. 1999. The mitochondrial genome of Arabidopsis is composed of both native and immigrant information. Trends Plant Sci. 4:495-502.[CrossRef][ISI][Medline]
Marin, B., and M. Melkonian. 1999. Mesostigmatophyceae, a new class of streptophyte green algae revealed by SSU rRNA sequence comparisons. Protist 150:399-417.[ISI][Medline]
Mattox, K. R., and K. D. Stewart. 1984. Classification of the green algae: a concept based on comparative cytology. Pp. 2972 in D. E. G. Irvine and D. M. John, eds. The systematics of the green algae. Academic Press, London.
Maul, J. E., J. W. Lilly, L. Cui, C. W. dePamphilis, W. Miller, E. H. Harris, and D. B. Stern. 2002. The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14:2659-2679.
McCracken, D. A., M. J. Nadakavukaren, and J. R. Cain. 1980. A biochemical and ultrastructural evaluation of the taxonomic position of Glaucosphaera vacuolata. Korsch. New Phytol. 86:39-44.
Melkonian, M. 1990. Chlorophyte orders of uncertain affinities: Order Pedinomonales. Pp. 649651 in L. Margulis, J. O. Corliss, M. Melkonian, and D. J. Chapman, eds. Handbook of Protoctista. Jones and Bartlett Publishers, Boston.
Michaelis, G., C. Vahrenholz, and E. Pratje. 1990. Mitochondrial DNA of Chlamydomonas reinhardtii: the gene for apocytochrome b and the complete functional map of the 15.8 kb DNA. Mol. Gen. Genet. 223:211-216.[ISI][Medline]
Michel, F., and E. Westhof. 1990. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J. Mol. Biol. 216:585-610.[ISI][Medline]
Nakayama, T., S. Watanabe, and I. Inouye. 1996. Phylogeny of wall-less green flagellates inferred from 18S rDNA sequence data. Phycol. Res. 44:151-161.
Nedelcu, A. M. 1997. Fragmented and scrambled mitochondrial ribosomal RNA coding regions among green algae: a model for their origin and evolution. Mol. Biol. Evol. 14:506-517.[Abstract]
Nedelcu, A. M. 1998. Contrasting mitochondrial genome organizations and sequence affiliations among green algae: potential factors, mechanisms, and evolutionary scenarios. J. Phycol. 34:16-28.[CrossRef][ISI]
Nedelcu, A. M., and R. W. Lee. 1998. Short repetitive sequences in green algal mitochondrial genomes: potential roles in mitochondrial genome evolution. Mol. Biol. Evol. 15:690-701.[Abstract]
Nedelcu, A. M., R. W. Lee, C. Lemieux, M. W. Gray, and G. Burger. 2000. The complete mitochondrial DNA sequence of Scenedesmus obliquus reflects an intermediate stage in the evolution of the green algal mitochondrial genome. Genome Res. 10:819-831.
Notsu, Y., S. Masood, T. Nishikawa, N. Kubo, G. Akiduki, M. Nakazono, A. Hirai, and K. Kadowaki. 2002. 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 268:434-445.[CrossRef][ISI][Medline]
Oda, K., K. Yamato, and E. Ohta, et al. (11 co-authors). 1992. Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant mitochondrial genome. J. Mol. Biol. 223:1-7.[ISI][Medline]
O'Kelly, C. J., and G. L. Floyd. 1984. Flagellar apparatus absolute orientations and the phylogeny of the green algae. BioSystems 16:227-251.[CrossRef][ISI]
Oldenburg, D. J., and A. J. Bendich. 2001. Mitochondrial DNA from the liverwort Marchantia polymorpha: circularly permuted linear molecules, head-to-tail concatemers, and a 5' protein. J. Mol. Biol. 310:549-562.[CrossRef][ISI][Medline]
Palmer, J. D., K. L. Adams, Y. Cho, C. L. Parkinson, Y.-L. Qiu, and K. Song. 2000. Dynamic evolution of plant mitochondrial genomes: mobile genes and introns and highly variable mutation rates. Proc. Natl. Acad. Sci. USA 97:6960-6966.
Palmer, J. D., and L. A. Herbon. 1988. Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J. Mol. Evol. 28:87-97.[ISI][Medline]
Palmer, J. D., and C. R. Shields. 1984. Tripartite structure of the Brassica campestris mitochondrial genome. Nature 307:437-440.[ISI]
Schuster, W., and A. Brennicke. 1994. The plant mitochondrial genome: physical structure, information content, RNA editing, and gene migration to the nucleus. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45:61-78.[CrossRef][ISI]
Schwartz, S., Z. Zhang, K. A. Frazer, A. Smit, C. Riemer, J. Bouck, R. Gibbs, R. Hardison, and W. Miller. 2000. PipMakera web server for aligning two genomic DNA sequences. Genome Res. 10:577-586.
Shimodaira, H., and M. Hasegawa. 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246-1247.
Sluiman, H. J. 1985. A cladistic evaluation of the lower and higher green plants (Viridiplantae). Plant Syst. Evol. 149:217-232.[ISI]
Sluiman, H. J. 1989. The green algal class Ulvophyceae: an ultrastructural survey and classification. Crypt. Bot. 1:83-94.
Strimmer, K., and A. von Haeseler. 1996. Quartet puzzling: a quartet maximum-likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 16:964-969.
Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.[Abstract]
Tupa, D. D. 1974. An investigation of certain chaetophoralean algae. Beihefte zur Nova Hedwigia 46:(suppl.): 64-67.
Turmel, M., V. Côté, C. Otis, J.-P. Mercier, M. W. Gray, K. M. Lonergan, and C. Lemieux. 1995. Evolutionary transfer of ORF-containing group I introns between different subcellular compartments (chloroplast and mitochondrion). Mol. Biol. Evol. 12:533-545.[Abstract]
Turmel, M., M. Ehara, C. Otis, and C. Lemieux. 2002. Phylogenetic relationships among Streptophytes as inferred from chloroplast small and large subunit rRNA gene sequences. J. Phycol. 38:364-375.[CrossRef][ISI]
Turmel, M., R. R. Gutell, J.-P. Mercier, C. Otis, and C. Lemieux. 1993. Analysis of the chloroplast large subunit ribosomal RNA gene from 17 Chlamydomonas taxa: three internal transcribed spacers and 12 group I intron insertion sites. J. Mol. Biol. 232:446-467.[CrossRef][ISI][Medline]
Turmel, M., C. Lemieux, G. Burger, B. F. Lang, C. Otis, I. Plante, and M. W. Gray. 1999. The complete mitochondrial DNA sequences of Nephroselmis olivacea and Pedinomonas minor. Two radically different evolutionary patterns within green algae. Plant Cell 11:1717-1729.
Turmel, M., C. Otis, and C. Lemieux. 1999. The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: insights into the architecture of ancestral chloroplast genomes. Proc. Natl. Acad. Sci. USA 96:10248-10253.
Turmel, M., C. Otis, and C. Lemieux. 2002a. The complete mitochondrial DNA sequence of Mesostigma viride identifies this green alga as the earliest green plant divergence and predicts a highly compact mitochondrial genome in the ancestor of all green plants. Mol. Biol. Evol. 19:24-38.
Turmel, M., C. Otis, and C. Lemieux. 2002b. 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 99:11275-11280.
Unseld, M., J. R. Marienfeld, P. Brandt, and A. Brennicke. 1997. The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat. Genet. 15:57-61.[ISI][Medline]
Volfovsky, N., B. J. Haas, and S. L. Salzberg. 2001. A clustering method for repeat analysis in DNA sequences. Genome Biol. 2:0027.0021-0027.0011.
Watanabe, S., A. Himizu, L. A. Lewis, G. L. Floyd, and P. A. Fuerst. 2000. Pseudoneochloris marina (Chlorophyta), a new coccoid ulvophycean alga, and its phylogenetic position inferred from morphological and molecular data. J. Phycol. 36:596-604.[CrossRef][ISI]
Watanabe, S., N. Kuroda, and F. Maiwa. 2001. Phylogenetic status of Helicodictyon planctonicum and Desmochloris halophila gen. et comb. nov. and the definition of the class Ulvophyceae (Chlorophyta). Phycologia 40:421-434.[ISI]
Whelan, S., and N. Goldman. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18:691-699.
Wolf, M., M. Buchheim, E. Hegewald, L. Krienitz, and D. Hepperle. 2002. Phylogenetic position of the Sphaeropleaceae (Chlorophyta). Plant Syst. Evol. 230:161-171.[CrossRef][ISI]
Wolfe, K. H., W.-H. Li, and P. M. Sharp. 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl. Acad. Sci. USA 84:9054-9058.[Abstract]
Wolff, G., I. Plante, B. F. Lang, U. Kück, and G. Burger. 1994. Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii. J. Mol. Biol. 237:75-86.[CrossRef][ISI][Medline]
Yang, Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. CABIOS 13:555-556.[Medline]
Zechman, F. W., E. C. Theriot, E. A. Zimmer, and R. L. Chapman. 1990. Phylogeny of the Ulvophyceae (Chlorophyta): cladistic analysis of nuclear-encoded rRNA sequence data. J. Phycol. 26:700-710.[ISI]