Canadian Institute for Advanced Research, Département de Biochimie et de Microbiologie, Université Laval, Québec, Canada
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The Mesostigma cpDNA sequence not only provides important insights into the evolutionary relationships among green plants, but also into the nature of the chloroplast genome in the common ancestor of all green plants (Lemieux, Otis, and Turmel 2000
). Mesostigma cpDNA features numerous ancestral characters and at the gene organizational level more highly resembles its land plant homologs than its chlorophyte homologs, suggesting that the ancestral green algal chloroplast genome has undergone rather limited rearrangements during the long evolutionary period leading to land plants. Also, the gene structure and the gene content of Mesostigma cpDNA predict that this ancestral genome did not have any introns and featured five extra genes in addition to those present in the streptophyte and the chlorophyte cpDNAs examined thus far.
To test the hypothesis that Mesostigma represents the earliest branch of green plant evolution and also to gain insights into the nature of the mitochondrial genome in the common ancestor of chlorophytes and streptophytes, we have undertaken the sequencing of Mesostigma mitochondrial DNA (mtDNA). The complete mtDNA sequences of seven chlorophytes previously reported (see following) and two streptophytes (the liverwort Marchantia polymorpha [Oda et al. 1992
] and the angiosperm Arabidopsis thaliana [Unseld et al. 1997
]) have revealed a great diversity of genome organizations and evolutionary patterns, yielding limited information about the nature of the ancestral green algal mitochondrial genome.
The mtDNAs of the prasinophyte Nephroselmis olivacea (Turmel et al. 1999
) and the nonphotosynthetic trebouxiophyte Prototheca wickerhamii (Wolff et al. 1994
) display an evolutionary pattern termed ancestral (Turmel et al. 1999
), that is characterized by a small genome size (45,223 and 55,328 bp, respectively) and a high density of genes. These chlorophyte mtDNAs and their land plant homologs have retained gene clusters that represent vestiges of prokaryotic operon organization. On the other hand, the mtDNAs of four other chlorophytes (Pedinomonas minor [Turmel et al. 1999
], a green alga of uncertain affiliation, and three members of the Chlorophyceae belonging to the order Chlamydomonadales [Boer and Gray 1991
; Vahrenholz et al. 1993
; Denovan-Wright and Lee 1994
; Kroymann and Zetsche 1998
]) display a reduced derived pattern that is characterized by a severe reduction in size (15,75825,137 bp) and gene number, the presence of only remnants of prokaryotic operons, and the acquisition of several other derived features such as fragmented rRNA genes, an accelerated rate of sequence evolution, a modified genetic code, and a biased codon usage. The 42,919-bp mtDNA of the chlorophycean green alga Scenedesmus obliquus exhibits features of both the ancestral and reduced derived types (Kück, Jekosch, and Holzamer 2000
; Nedelcu et al. 2000
). Unlike the aforementioned green algal mtDNAs, land plant mtDNAs feature an expanded pattern that is marked by an increased size relative to chlorophyte mtDNAs (see table 1
), the tendency to expand through the incorporation of new sequences in intergenic spacers, the loss of a few genes, as well as the appearance of trans-splicing of group II introns and the acquisition of RNA editing in angiosperms. Given the limited sampling of green plant mtDNAs sequenced to date, it is not clear whether the events that led to the large size of land mtDNAs originated during the evolution of charophytes or before the emergence of the Streptophyta and the Chlorophyta. Evidence for the latter hypothesis would indicate that the trend toward a condensed genome in the Chlorophyta was initiated very early after the appearance of this phylum and became even more radical when late-diverging lineages arose within the Chlorophyceae. The origin of the introns present in green plant mtDNAs is also unknown. Although introns have been found in chlorophyte and land plant mtDNAs, their sporadic distribution does not allow one to predict whether some were inherited vertically from the last common ancestor of all green plants.
|
![]() |
Materials and Methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
DNA Isolation, Cloning, and Sequencing
As the chloroplast and the mitochondrial genomes of Mesostigma viride were found to copurify in CsCl-bisbenzimide density gradients, their nucleotide sequences were determined in parallel using a plasmid library prepared from an A + T rich fraction. Isolation of this fraction and preparation of the library from 1,500 to 3,000 bp fragments obtained by nebulization were carried out as described previously (Lemieux, Otis, and Turmel 2000)
. After hybridization of the clones with the original DNA used for cloning, DNA templates from positive clones were prepared with the QIAprep 8 Miniprep kit (Qiagen). All nucleotide sequences were determined with the PRISM dye terminator cycle sequencing kit (Applied Biosystems) on a DNA sequencer (model 343, Applied Biosystems). T3 and T7 primers as well as oligonucleotides complementary to internal regions of plasmid DNA inserts were used to initiate the sequencing reactions. Genomic regions not represented in the clones analyzed were sequenced from PCR-amplified fragments. Sequences were assembled using AUTOASSEMBLER (Version 1.4.0, Applied BioSystems) and analyzed using the Genetics Computer Group (Madison, WI) software (Version 9.1) package. The protein-coding and rRNA genes were identified by BLAST searches (Altschul et al. 1990
) of the nonredundant database at the National Center for Biotechnology Information. The tRNA genes were found using TRNASCAN-SE (Lowe and Eddy 1997
).
The DNA templates sequenced included RT-PCR products that were generated from total cellular RNA with the SuperScript One-Step RT-PCR System from Life Technologies (Burlington, Ontario, Canada). These analyses were carried out to determine whether the introns in nad3 are trans-spliced at the RNA level.
Phylogenetic Analyses
Mitochondrial genome sequences were retrieved from GenBank: Mesostigma viride, AF353999 (this study); Nephroselmis olivacea, AF110138 (Turmel et al. 1999
); Prototheca wickerhamii, U02970 (Wolff et al. 1994
); Marchantia polymorpha, M68929 (Oda et al. 1992
); Arabidopsis thaliana, Y08501 and Y08502 (Unseld et al. 1997
); Chondrus crispus, Z47547 (Leblanc et al. 1995
); Cyanidioschyzon merolae, D89861 (Ohta, Sato, and Kuroiwa 1998
). The data sets were prepared as follows: the deduced amino acid sequences from individual genes were aligned using CLUSTALW 1.74 (Thompson, Higgins, and Gibson 1994
), these protein alignments concatenated, and the ambiguously aligned regions deleted. Symmetric maximum likelihood distances were computed using PUZZLE 4.0.2 (Strimmer and von Haeseler 1996
), whereas Logdet distances were calculated using SPLITSTREE 2.4 (Huson 1998
). Distance and maximum parsimony trees were constructed using NEIGHBOR and PROTPARS, respectively, in PHYLIP 3.573c (Felsenstein 1995
). The JTT and mtREV24 models with either a uniform rate or gamma-distributed rates (over eight categories) of substitutions across sites were used for the distance analyses. The robustness of distance and maximum parsimony trees was assessed by bootstrap percentages after 100 replications. Maximum likelihood analyses with a uniform rate of substitutions across sites were carried out using PROTML in MOLPHY 2.3b3 (Adachi and Hasegawa 1996
), whereas analyses assuming rate heterogeneity (eight gamma categories) were carried out using the AAML program in PAML (Yang 1997
). Local bootstrap probabilities were estimated by resampling of the estimated log likelihood (RELL) after 10,000 replications (Adachi and Hasegawa 1996
).
Comparisons of Amino Acid Substitution Rates in Different Lineages
For this analysis, we used the data set of 4,139 amino acid positions. To compare the rates of substitution in different lineages, we applied the relative rate test as described by Gu and Li (1992)
. The sequences of Porphyra purpurea were used as the outgroup.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
Mesostigma mtDNA contains four group I introns and three group II introns. The presence of both group I and group II introns in a green plant mtDNA is not without precedent as the two classes of introns have been identified in both Marchantia and Scenedesmus mtDNAs.
Conserved Genes
The 65 conserved genes identified in Mesostigma mtDNA encode three rRNA species, 26 tRNAs, 15 ribosomal proteins, 19 components of the respiratory chain and ATP synthase, one component of the Sec-independent protein translocation pathway, and one protein of unknown function (table 2
). Although none of these genes represents a novel coding sequence among green plant mtDNAs, it is noteworthy that four of them (rps1, sdh3, sdh4, and trnL[caa]) have not been reported previously in chlorophyte mtDNAs and that two others (rpl14 and trnI[gau]) have not been identified in the streptophyte mtDNAs analyzed so far. With 69 conserved genes, Marchantia is the only known green plant that has a larger mitochondrial gene repertoire than Mesostigma. Marchantia mtDNA encodes 27 tRNAs instead of 26 as in Mesostigma mtDNA (the extra tRNAIle[cau] and tRNAThr[ggu], but not tRNAIle[gau]), 16 ribosomal proteins instead of 15 (the extra Rpl2 and Rps8, but not Rpl6), and three components involved in cytochrome c biogenesis (YejR, YejU and YejV), the genes for the last products being absent from Mesostigma mtDNA.
|
|
|
Gene Organization
All the genes in the 18,114-bp region of Mesostigma mtDNA which is delimited by K(uuu) and rns, with the exception of two unlinked tRNA genes, are encoded by the same strand, whereas all the genes in the rest of the genome, except again tRNA genes (five individual ones and one pair), are located on the complementary strand (fig. 1
). This gene distribution predicts a minimum of 16 potential transcription units, seven of which are monocistronic and made up of tRNA genes. In Nephroselmis mtDNA, potential transcription units are also numerous, but are predicted to be mainly multicistronic. Genes in Prototheca mtDNA form as few as two potential transcription units.
Comparison of gene orders in Mesostigma mtDNA and other mtDNAs reveals only two conserved gene clusters, rps12-rps7 and rpl6-rps13. Commonly found in protist mtDNAs, these gene pairs are also present in the genomes of the bacterial progenitors of mitochondria in which they are part of the large ribosomal gene cluster corresponding to the str, S10, spc, and operons of E. coli (Lang, Gray, and Burger 1999
). Of the green plant mtDNAs examined so far, that of Nephroselmis has retained the largest fraction of this ancestral gene cluster.
Intron Content
Table 4
summarizes the features of the seven introns found in Mesostigma mtDNA. Two group I introns are located in rnl (Mvrnl·1 and Mvrnl·2), whereas two others lie in cox1 (Mvcox1·1 and Mvcox1·2). We have classified these four group I introns within distinct subdivisions of the group I family (fig. 3
) on the basis of their sequences and secondary structures (Michel and Westhof 1990
). Each of the rnl introns as well as Mvcox1·2 contains an ORF specifying a potential homing endonuclease of the LAGLIDADG family. Experimental evidence for such an enzymatic activity has been demonstrated for the homologous proteins encoded by chloroplast group I introns residing at the same insertion sites as Mvrnl·1 and Mvrnl·2 within the LSU rRNA gene (Dürrenberger and Rochaix 1991
; Turmel et al. 1995
; Lucas et al. 2001
). Apart from the introns in the mtDNA of the lobose amoeba Acanthamoeba castellanii and the bacterium Simkania negevensis, introns occupying the same positions as the Mesostigma mitochondrial rnl introns have been reported only in green algae (table 4
). Introns residing at the same positions as Mvcox1·1 and Mvcox1·2 have also been described previously (table 4
). Of the four group I insertion sites in Mesostigma mtDNA, that occupied by Mvcox1·2 features the broadest phylogenetic distribution; introns at this site have been found in the mtDNA of various yeasts and fungi, the slime mold Dictyostelium discoideum, the green alga Chlamydomonas eugametos, and the liverwort Marchantia. Each of these coxI introns, except that of Allomyces macrogynus, displays an ORF; however, unlike the situation that prevails for the other introns sharing insertion sites with Mesostigma rnl introns, the ORF is found at more than one location within the intron sequences (L1 and L9.1), and unrelated ORFs occupy the different positions.
|
The insertion sites of the three group II introns in Mesostigma mtDNA are unique to this mitochondrial genome. Two introns reside in nad3 (Mvnad3·1 and Mvnad3·2) and the third in cox2 (Mvcox2·1). All three introns belong to the subdivision IIA. As they differ from the majority of group II introns characterized previously (Michel and Ferat 1995
) by their degenerate domain I (fig. 4
), they probably require factors for splicing. Mvnad3·2 also lacks domain II, a region dispensable for intron splicing (Michel and Ferat 1995
) but almost universally present in group II introns (fig. 4
). The two Mesostigma nad3 introns are bipartite: the two pieces constituting each of these introns are far apart on the mitochondrial genome and occur in separate transcription units (fig. 1
). Both introns are trans-spliced at the RNA level in vivo, as demonstrated by sequencing nad3 cDNAs encompassing each or both of the intron insertion sites. The breakpoint of each intron lies within domain IV (fig. 4
), a common feature of trans-spliced group II introns (Michel and Ferat 1995
). The two Mesostigma nad3 introns lack an ORF, whereas Mvcox2·1 encodes a potential protein. Unlike most group II intronencoded proteins identified so far (Michel and Ferat 1995
), this protein does not exhibit a polymerase domain of reverse transcriptases; it shares only very limited sequence identity with other group II intronencoded proteins.
|
|
|
Rates of Amino Acid Substitutions in Different Lineages
The branch lengths in the maximum likelihood tree shown in figure 5 suggest that Mesostigma mtDNA has evolved at a rate similar to those observed for the mtDNAs of Nephroselmis, Prototheca and Arabidopsis. To compare more precisely the rates of amino acid substitution in these green plant lineages, we used the method developed by Gu and Li (1992)
to demonstrate a higher rate of sequence evolution in rodents than in humans. When we compared the rate of amino acid substitution in the lineage leading to Mesostigma with those leading to other green plants (table 6
), only the Mesostigma and Nephroselmis lineages showed a significant difference at P < 0.001, thus providing evidence for an overall faster substitution rate in the lineage leading to Mesostigma relative to the lineage leading to Nephroselmis (table 6
). At P < 0.05, the rate observed for the Mesostigma lineage significantly differed from the rates exhibited by all other lineages examined, except the Prototheca lineage. Comparisons of other pairs of green plant lineages showed that amino acid substitution rate is significantly (P < 0.001) faster in the lineage leading to Arabidopsis than in the Marchantia and Prototheca lineages. Note here that the amino acid differences observed for the pairs of green plants, including Arabidopsis, were overestimated, as the large number of edited sites in mRNA derived from Arabidopsis mitochondrial genes (Giege and Brennicke 1999
) were not taken into account in our analysis.
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Comparison of the gene content and the gene organization of Mesostigma mtDNA with those of other green plant mtDNAs disclosed only a few ancestral features that support the positioning of Mesostigma as the earliest branch of green plant evolution. The most important of these structural features is the presence in Mesostigma mtDNA of two genes that are specific to chlorophytes (rpl14 and trnI[gau]) and of four genes that are specific to streptophytes (rps1, sdh3, sd4, trnL[caa]) (fig. 6
). The high density of genes encoded by Mesostigma mtDNA is also consistent with the notion that this prasinophyte represents the earliest green plant divergence (see following). Both the aforementioned features have been identified in the chloroplast genome of Mesostigma (Lemieux, Otis, and Turmel 2000
). This genome exhibits the highest gene density among the green plant cpDNAs investigated so far. Thirteen of its 135 genes have been found to be specific to chlorophytes and seven to streptophytes.
|
Of the three types of evolutionary patterns that have been attributed to green plant mtDNAs (Turmel et al. 1999
), the ancestral pattern best describes the evolutionary trends displayed by Mesostigma mtDNA. At both the size and gene density levels, Mesostigma mtDNA most closely resembles the two ancestral mtDNAs that have been sequenced to date (Nephroselmis and Prototheca mtDNAs); however, unlike these mtDNAs, it exhibits virtually no vestiges of prokaryotic gene organization. Although Mesostigma mtDNA shows a number of derived organizational features, its evolutionary pattern is distinct from that of Scenedesmus mtDNA and thus cannot be considered as intermediate between the ancestral and reduced derived patterns. Compared with Scenedesmus mtDNA, Mesostigma mtDNA diplays a substantially higher gene density (86.6% vs. 60.6%) and evolves much more slowly at the sequence level. As revealed by our analysis of amino acid substitutions in 19 mtDNA-encoded proteins, the rate of sequence evolution of Mesostigma mtDNA is comparable to that of Prototheca mtDNA but is slightly higher than that of Nephroselmis mtDNA (table 6
).
Given the irregular distribution and poor phylogenetic content of the introns identified to date in green plant mtDNAs (Gray et al. 1998
), inferring the intron makeup of the mitochondrial genome in the common ancestor of all green plants is a highly speculative endeavor. It appears that only two of the seven introns in Mesostigma mtDNA, the introns in the rnl gene, might have been inherited from the common ancestor of all green plants. The three group II introns in Mesostigma mtDNA are unlikely to have been acquired by vertical descent from this common ancestor because their insertion sites are unique to Mesostigma mtDNA. Although their origin remains unclear, they most probably took residence in this mtDNA via lateral transfer. Considering that all three introns belong to the same subgroup and share a degenerate domain I, it seems plausible that they arose following lateral transfer of a group II intron and subsequent transposition of this intron at two other mtDNA loci. In contrast, all four group I introns in Mesostigma mtDNA have a number of close relatives at identical gene locations in other genomes. Because the homologs of the two Mesostigma cox1 introns are prevalent in yeast and fungal mtDNAs and occur sporadically in green plant mtDNAs (table 4 ), both these introns were probably acquired following lateral transfer events between the mitochondria of divergent organisms.
The notion that the mitochondrial rnl introns of Mesostigma were inherited vertically from the common ancestor of all green plants is consistent with the finding that their homologs occupy multiple green plant lineages (including deep branches) and also with their limited occurrence outside this phylum. Their nongreen plant homologs are restricted to Acanthamoeba mtDNA and to the genome of the bacterium Simkania (see Results for a discussion on the possible origin of these introns). Considering that the mobility of the two Mesostigma rnl introns and their homologs is facilitated by intron-encoded homing endonucleases (Lucas et al. 2001
), it is surprising that these introns are not more widespread among eukaryotes. The reason for such a limited phylogenetic distribution is not obvious.
Relatively early during the evolution of green algae, homologs of the Mesostigma mitochondrial rnl introns appear to have been successful in invading the chloroplast genome and establishing a niche at cognate sites in the rnl gene. This transfer of genetic information might have occurred between the mitochondria and chloroplast of the same cell, as DNA exchange between these organelles has been documented (Palmer 1985
). Interorganellar transfer of rnl introns is supported by the finding that homologs of the two Mesostigma rnl introns have been identified not only in mtDNA but also in cpDNA (table 4
). In some green algae such as Monomastix, introns similar to their Mesostigma homologs have been found in both organelle genomes (Lucas et al. 2001
). We favor the view that rnl introns were transferred from mitochondria to the chloroplast, as absence of introns is an ancestral character for the chloroplast genome (both Mesostigma and Nephroselmis harbor introns in their mitochondrial genome but none in their chloroplast genome).
We have shown that the two group II introns in the Mesostigma nad3 gene feature a bipartite structure and are trans-spliced at the RNA level in vivo. Prior to our study, trans-splicing of mitochondrial group II introns had been described only in land plants, more specifically in angiosperms (Michel and Ferat 1995
). It is very unlikely that trans-spliced group II introns were present in the mitochondrial genome of the common ancestor of green plants, as three lines of evidence support the idea that trans-splicing of group II introns originated independently in Mesostigma and streptophyte mtDNAs. First, the mitochondrial genome of the bryophyte Marchantia lacks any trans-spliced introns, suggesting that trans-splicing appeared late during the evolution of streptophytes (after the divergence of bryophytes and vascular plants). Second, no introns have been identified in the nad3 gene of land plants. Third, the trans-spliced introns found in Mesostigma and angiosperm mtDNAs differ remarkably in structure, notably with respect to domain I. Trans-splicing in both the Mesostigma and streptophyte lineages likely arose following genome rearrangements that led to fragmentation of cis-spliced introns and dispersal of the resulting pieces (Michel and Ferat 1995
).
In conclusion, the few structural features that can be regarded as ancestral in Mesostigma mtDNA predict that the common ancestor of all green plants had a compact mtDNA containing at least 75 genes and perhaps two group I introns in the rnl gene. Mesostigma features the most compact mtDNA among the green plants analyzed so far. Considering that land plant mtDNAs are much larger in size and continue to expand in size because of the incorporation of foreign sequences (Palmer 1985
), we infer that mtDNA size began to increase dramatically in the Streptophyta, either during the evolution of charophytes or during the transition of the charophytes to land plants. Complete sequencing of mtDNAs from a number of charophytes and early-diverging land plants will be required to distinguish between these two hypotheses.
![]() |
Supplementary Material |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Acknowledgements |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Footnotes |
---|
Abbreviations: cpDNA, chloroplast DNA; mtDNA, mitochondrial DNA; NIES, National Institute for Environmental Studies; ORF, open reading frame; RELL, resampling of the estimated log likelihood; rRNAs, ribosomal RNAs.
Keywords: green algae
Mesostigma viride
mitochondrial DNA
group I introns
group II introns
trans-splicing
Address for correspondence and reprints: Monique Turmel, Département de Biochimie et de Microbiologie, Pavillon C.-E. Marchand, Université Laval, Québec (QC) G1K 7P4, Canada. monique.turmel{at}rsvs.ulaval.ca
.
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Adachi J., M. Hasegawa, 1996 MOLPHY Version 2.3: programs for molecular phylogenetics based on maximum likelihood method Comput. Sci. Monogr 28:1-150
Altschul S. F., W. Gish, W. Miller, E. W. Myers, D. J. Lipman, 1990 Basic local alignment search tool J. Mol. Biol 215:403-410[ISI][Medline]
Baldauf S. L., A. J. Roger, I. Wenk-Siefert, W. F. Doolittle, 2000 A kingdom-level phylogeny of eukaryotes based on combined protein data Science 290:972-977
Bhattacharya D., K. Weber, S. S. An, 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., M. W. Gray, 1991 Short dispersed repeats localized in spacer regions in Chlamydomonas reinhardtii mitochondrial DNA Curr. Genet 19:309-312[ISI][Medline]
Burger G., D. Saint-Louis, M. W. Gray, B. F. Lang, 1999 Complete sequence of the mitochondrial DNA of the red alga Porphyra purpurea: cyanobacterial introns and shared ancestry of red and green algae Plant Cell 11:1,675-1,694
Burke J. M., M. Belfort, T. R. Cech, R. W. Davies, R. J. Schweyen, D. A. Shub, J. W. Szostak, H. F. Tabak, 1987 Structural conventions for group I introns Nucleic Acids Res 15:7,217-7,221[Abstract]
Cavalier-Smith T., 1981 Eukaryote kingdoms: seven or nine? Biosystems 14:461-481[ISI][Medline]
Chapman R. L., M. A. Buchheim, 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 plant II DNA sequencing. Kluwer Academic Press, Norwell, Mass
Denovan-Wright E. M., R. W. Lee, 1994 Comparative structure and genomic organization of the discontinuous mitochondrial ribosomal RNA genes of Chlamydomonas eugametos and Chlamydomonas reinhardtii J. Mol. Biol 241:298-311[ISI][Medline]
Dürrenberger F., J. D. Rochaix, 1991 Chloroplast ribosomal intron of Chlamydomonas reinhardtii: in vitro self-splicing, DNA endonuclease activity and in vivo mobility EMBO J 10:3495-3501[Abstract]
Everett K. D., R. M. Bush, A. A. Andersen, 1999 Emended description of the order Chlamydiales, proposal of Parachlamydiaceae fam. Nov. and Simkaniaceae fam. Nov., each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms Int. J. Syst. Bacteriol 49:415-440[Abstract]
Felsenstein J., 1988 Phylogenies from molecular sequences: inference and reliability Annu. Rev. Genet 22:521-565[ISI][Medline]
. 1995 PHYLIP (phylogeny inference package). Version 3.5 Distributed by the author, Department of Genetics, University of Washington, Seattle
Friedl T., 1997 The evolution of the green algae Plant Syst. Evol 11:(Suppl.)87-101
Giege P., A. Brennicke, 1999 RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs Proc. Natl. Acad. Sci. USA 96:15324-15329
Gray M. W., B. F. Lang, R. Cedergren, et al. (14 co-authors) 1998 Genome structure and gene content in protist mitochondrial DNAs Nucleic Acids Res 26:865-878
Graybeal A., 1998 Is it better to add taxa or characters to a difficult phylogenetic problem? Syst. Biol 47:9-17[ISI][Medline]
Gu X., W.-H. Li, 1992 Higher rates of amino acid substitution in rodents than in humans Mol. Phylogenet. Evol 1:211-214[Medline]
Huson D. H., 1998 SplitsTree: a program for analyzing and visualizing evolutionary data Bioinformatics 14:68-73[Abstract]
Kroymann J., K. Zetsche, 1998 The mitochondrial genome of Chlorogonium elongatum inferred from the complete sequence J. Mol. Evol 47:431-440[ISI][Medline]
Kück U., K. Jekosch, 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[ISI][Medline]
Lang B. F., L. J. Goff, M. W. Gray, 1996 A 5 S rRNA gene is present in the mitochondrial genome of the protist Reclinomonas americana but is absent from red algal mitochondrial DNA J. Mol. Biol 261:607-613[ISI]
Lang B. F., M. W. Gray, G. Burger, 1999 Mitochondrial genome evolution and the origin of eukaryotes Annu. Rev. Genet 33:351-397[ISI][Medline]
Leblanc C., C. Boyen, O. Richard, G. Bonnard, J.-M. Grienenberger, B. Kloareg, 1995 Complete sequence of the mitochondrial DNA of the rhodophyte Chondrus crispus (Gigartinales): gene content and genome organization J. Mol. Biol 250:484-495[ISI][Medline]
Lemieux C., C. Otis, M. Turmel, 2000 Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution Nature 403:649-652[ISI][Medline]
Lockhart P. J., C. J. Howe, A. C. Barbrook, A. W. D. Larkum, D. Penny, 1999 Spectral analysis, systematic bias, and the evolution of chloroplast Mol. Biol. Evol 16:573-576
Lockhart P. J., A. W. D. Larkum, M. A. Steel, P. J. Waddell, D. Penny, 1996 Evolution of chlorophyll and bacteriochlorophyll: the problem of invariant sites in sequence analysis Proc. Natl. Acad. Sci. USA 93:1930-1934
Lockhart P. J., M. A. Steel, M. D. Hendy, D. Penny, 1994 Recovering evolutionary trees under a more realistic model of sequence evolution Mol. Biol. Evol 11:605-612
Lowe T. M., 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, C. Lemieux, 2001 Rapid evolution of the DNA-binding site in LAGLIDADG homing endonucleases Nucleic Acids Res 29:960-969
Marin B., M. Melkonian, 1999 Mesostigmatophyceae, a new class of streptophyte green algae revealed by SSU rRNA sequence comparisons Protist 150:399-417[ISI][Medline]
Melkonian M., 1989 Flagellar apparatus ultrastructure in Mesostigma viride (Prasinophyceae) Plant Syst. Evol 164:93-122[ISI]
Melkonian M., B. Marin, B. Surek, 1995 Phylogeny and evolution of the algae Pp. 153176 in R. Arai, M. Kato, and Y. Doi, eds. Biodiversity and evolution. The National Science Museum Foundation, Tokyo
Michel F., J.-L. Ferat, 1995 Structure and activities of group II introns Annu. Rev. Biochem 64:435-461[ISI][Medline]
Michel F., K. Umesono, H. Ozeki, 1989 Comparative and functional anatomy of group II catalytic intronsa review Gene 82:5-30[ISI][Medline]
Michel F., 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]
Moore P. B., 1995 The structure and function of 5S ribosomal RNA Pp. 199236 in R. A. Zimmermann and A. E. Dahlberg, eds. Ribosomal RNA: structure, evolution, processing and function in protein biosynthesis. CRC Press, Boca Raton
Nedelcu A. M., R. W. Lee, C. Lemieux, M. W. Gray, 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
Oda K., K. Yamato, E. Ohta, et al. (11 co-authors) 1992 Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA J. Mol. Biol 223:1-7[ISI][Medline]
Ohta N., N. Sato, T. Kuroiwa, 1998 Structure and organization of the mitochondrial genome of the unicellular red alga Cyanidioschyzon merolae deduced from the complete nucleotide sequence Nucleic Acids Res 26:5190-5198
Palmer J. D., 1985 Evolution of chloroplast and mitochondrial DNA in plants and algae Pp. 131240 in R. J. MacIntyre, ed. Monographs in evolutionary biology: molecular evolutionary genetics. Plenum, New York
Pfitzinger H., J. H. Weil, D. T. N. Pillay, P. Guillemaut, 1990 Codon recognition mechanisms in plant chloroplasts Plant Mol. Biol 14:805-814[ISI][Medline]
Qiu Y.-L., J. Lee, 2000 Transition to a land plant flora: a molecular phylogenetic perspective J. Phycol 36:799-802[ISI]
Shimodaira H., M. Hasegawa, 1999 Multiple comparisons of log-likelihoods with applications to phylogenetic inference Mol. Biol. Evol 16:1114-1116
Silberman J. D., C. G. Clark, L. S. Diamond, M. L. Sogin, 1999 Phylogeny of the genera Entamoeba and Endolimax as deduced from small-subunit ribosomal RNA sequences Mol. Biol. Evol 16:1740-1751
Stiller J. W., B. D. Hall, 1999 Long-branch attraction and the rDNA model of early eukaryotic evolution Mol. Biol. Evol 16:1270-1279
Strimmer K., A. von Haeseler, 1996 Quartet puzzling: a quartet maximum-likelihood method for reconstructing tree topologies Mol. Biol. Evol 13:964-969
Thompson J. D., D. G. Higgins, 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]
Turmel M., V. C, C. Otis, J.-P. Mercier, M. W. Gray, K. M. Lonergan, 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., C. Lemieux, G. Burger, B. F. Lang, C. Otis, I. Plante, 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
Unseld M., J. R. Marienfeld, P. Brandt, A. Brennicke, 1997 The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides Nat. Genet 15:57-61[ISI][Medline]
Vahrenholz C., G. Rieman, E. Pratje, B. Dujon, G. Michaelis, 1993 Mitochondrial DNA of Chlamydomonas reinhardtii: the structure of the ends of the linear 15.8-kb genome suggests mechanisms for DNA replication Curr. Genet 24:241-247[ISI][Medline]
Wolff G., I. Plante, B. F. Lang, U. Kück, G. Burger, 1994 Complete sequence of the mitochondrial DNA of the chlorophyte alga Prototheca wickerhamii J. Mol. Biol 237:75-86[ISI][Medline]
Yang Z., 1997 PAML: a program package for phylogenetic analysis by maximum likelihood CABIOS 13:555-556[Medline]