* Institut für Zelluläre und Molekulare Botanik, Abt. Molekulare Evolution, Universität Bonn, Bonn, Germany; Abt. Molekulare Botanik, Universität Ulm, Ulm, Germany
Correspondence: E-mail: volker.knoop{at}uni-bonn.de.
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key Words: Bryophytes evolution phylogeny group I and group II introns RNA editing
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Besides the increased proportion of noncoding DNA, recombinational activity in angiosperm chondriomes is a complicating factor that results in genomic complexity, sometimes as coexisting alternative genomic arrangements of the mtDNA. A peculiar outcome of recombination events on evolutionary timescales is the disruption of the three mitochondrial genes nad1, nad2, and nad5 in a total of five group II intron sequences, which have led to trans-splicing arrangements in angiosperms. The nad genes encode subunits of complex I of the respiratory chain, the NADH-ubiquinone-oxidoreductase. The origins of those trans-splicing introns in land-plant evolution have been traced and have led to the identification of cis-arranged ancestors in early branching plant lineages: moniliformopses, lycophytes, and, in one case, a hornwort (Malek, Brennicke, and Knoop 1997; Malek and Knoop 1998). Additionally, the terminal intron in nad1 has been subject to independent cis-to-trans transition among angiosperms later in evolution (Qiu and Palmer 2004).
The nad5 gene structure of angiosperms is particularly unique: two trans-splicing introns frame a small exon of only 22 nt (Knoop et al. 1991). The large upstream exon has been introduced as a phylogenetically informative locus, and new introns in nad5 have shown up in the analysis of pteridophytes (Vangerow, Teerkorn, and Knoop 1999) and in a hornwort (Beckert et al. 1999). Subsequent studies have integrated this internal region of nad5 into multigene analyses that have identified Charales instead of Coleochaetales as the immediate extant sister group to embryophytes (Karol et al. 2001).
Because the phylogenetic screenings so far excluded the four angiosperm introns in nad5, we have reasoned that a more complete analysis of the large nad5 gene may reveal further valuable cladistic information. We here report the results in the bryophyte classes and find further support for a deep liverwort versus nonliverwort dichotomy in land plants. Two of the angiosperm-type group II introns are shared with mosses, one of which (nad5i1455) is the first cis-arranged moss homolog to a trans-splicing intron of angiosperms. A tracheophyte-hornwort clade finds support in the loss of a group I intron invariably present in mosses and liverworts (nad5i753) and gain of another group II intron (nad5i1477) that later evolves into a trans-splicing status in spermatophytes.
![]() |
Materials and Methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
With the present study, we have tried to maximize the phylogenetic analysis of nad5 by designing PCR primers matching terminally conserved sequences. Intron sizes made the design of further internal primers to amplify the gene region necessary (see Materials and Methods). In Charales algae, none of the eight introns shown in figure 1 is present, as is evident from the full Chara vulgaris chondriome sequence now available (Turmel, Otis, and Lemieux. 2003), and as we can confirm with the sequences of the closely related Charales genera Lamprothamnium and Nitella.
Among mosses, we have chosen to include both the basal branching genus Sphagnum and two (basal) members each from the derived clusters Hypnanae (Ulota and Rhacocarpus) and Dicrananae (Encalypta and Timmia) in our taxon sampling (table 1). Among liverworts, we have analyzed marchantiid liverworts (complex thalloids), considered to be closely and less closely related to Marchantia polymorpha (Corsinia and Monoclea, respectively), the simple thalloid and leafy liverworts from the classically defined orders Metzgeriales (Noteroclada) and Jungermanniales (Bazzania), and the isolated order of as yet unclear affiliation, Calobryales (Haplomitrium). PCR amplification from DNAs of hornwort and fern genera proved to be notoriously difficult, possibly because of the high degree of RNA editing in nad5 (see below), which makes primer design a guesswork. Even multiple rounds of primer redesigning did not allow for successful amplification of the nad5 region covering intron i1455 in hornworts. However, we have been able to identify a 4.7-kb genomic clone from a random BamHI library of Anthoceros agrestis DNA by hybridization that overlaps flanking PCR-derived Anthoceros sequences.
|
|
Group II intron nad5i1455 is trans-disrupted in angiosperms (fig. 1). A cis-arranged ortholog of this intron (1,825 nt long), the presumable ancestral state, has already been identified in the fern Asplenium nidus in a screening for cis-arranged counterparts (Malek and Knoop 1998). At this position, the nad5 reading frame is continuous in Marchantia polymorpha and this is confirmed for all other liverworts we have investigated now. However, we find intron nad5i1455 to be present in cis-arranged form and to be of significant size in all mosses. Sizes of intron nad5i1455 in mosses range from 2,623 nt in Encalypta to 2,676 nt in Sphagnum. Absence of an intron in mosses at this position was erroneously deduced from approximately cDNA-sized products obtained in PCR amplifications, in hindsight probably because of mispriming in the long intron sequence when the short downstream exon of 22 nt precluded design of alternative primers in that screening strategy (Malek and Knoop 1998). In fact, PCR amplification of this gene region still failed in hornworts, but we have been able to identify a genomic clone from a random library of Anthoceros agrestis DNA, encompassing nad5i1455, which is 2,274 nt long in this species. Again, a highly atypical sequence deviating from the group II consensus with the NAY 3' end being replaced by ACC is conserved between mosses, the hornwort, the fern, and angiosperms (fig. 2B).
Group II intron nad5i1477 is likewise trans-disrupted in angiosperms (fig. 1). An ortholog of this intron in cis-arranged form (2,391 nt in size) has been identified in Anthoceros crispulus (Malek and Knoop 1998). Again, the short exon between nad5i1455 and nad5i1477 had precluded alternative upstream primer design. Nevertheless, correct priming in the upstream exon combined with downstream mispriming in the intron clearly determines its presence also in the hornwort genera Phaeoceros and Notothylas, as we found in partial PCR products. Hence, nad5i1477 is a common denominator of this bryophyte class and shared with angiosperms (fig. 2C). As in Marchantia, intron nad5i1477 is absent in all liverworts and all mosses we have investigated now.
Group II intron nad5i1872 is present in all angiosperm nad5 genes investigated and is in the size range of 914 (Vicia faba) to 1,108 nt (Oenothera berteriana). Some partial sequences deposited in the database clearly demonstrate that intron nad5i1872 is also present in gymnosperms (Liepelt, Bialozyt, and Ziegenhagen 2002). We found it absent in all bryophytes we have investigated. However, we have now identified this intron in Asplenium nidus. Therefore, nad5i1872 is obviously a gain in the tracheophyte lineage. Strikingly, the Asplenium intron is only 556 nt long. As in the other group II introns, there is significant sequence conservation of 5' region and domains V and VI (fig. 2D), again making a vertical mode of transmission very likely.
The Coding Region and RNA Editing
The now analyzed nad5 region extends over 601 codons (600 in Charales algae). As previously found, the mitochondrial sequences are highly conserved in the marchantiid liverworts and without any requirement for the C to U type of RNA editing typically observed in other land-plant groups (Steinhauser et al. 1999). In fact, the encoded polypeptides are identical in Marchantia and Corsinia. Four codon changes cannot be corrected by RNA editing in Monoclea. Typical plant organellar RNA editing by C-U pyrimidine exchanges is required in all other plants to reconstitute conserved codon identities (fig. 3). A total of 173 such positions are identified in the alignment, 95 of which are unique to a single species; the remaining 78 are shared between at least two taxa, mostly between Anthoceros and Asplenium. Only moderate levels of RNA editing are expectedly observed for the mosses and the jungermanniid liverworts. However, in stark contrast, we find that the now analyzed mitochondrial sequences of the isolated liverwort genus Haplomitrium present a surprise: overall 65 sites in the nad5 sequence require C to U RNA editing to re-establish conserved codon identities (fig. 3). Both the fern Asplenium and the hornwort Anthoceros show the usual requirement of highly frequent RNA editing in both directions of pyrmidine exchange (fig. 3). Most importantly, many of these sites are shared between the hornwort and the fern and bear the obvious danger of homoplasies in phylogenetic analyses.
|
We have performed maximum-parsimony (MP) analyses and Bayesian-likelihood analyses in parallel. Because of extreme sequence conservation in the marchantiid liverworts, the phylogenetic analyses of the exons alone completely lacks resolution in this subclade. When intron sequences were included (4,687 sites, 1,304 parsimony informative), we obtained a single most-parsimonious tree (3,777 steps) with good bootstrap support for most nodes (fig. 4). However, the lack of introns conserved across all three bryophyte classes and their general absence in the algae restricts a reasonable sequence-based analyzes for out-group rooting to the coding region (1,726 sites, 570 parsimony informative). Topological differences between the eight MP trees obtained for the coding-only region (1,721 steps) are restricted to arrangements within the liverworts and mosses, whereas bootstrap analysis supports the nodes of the phylogenetic backbone. Somewhat expectedly, exclusion of the intron sequences from the phylogenetic analyses decreases bootstrap support for internal nodes within the mosses and liverworts. The posterior probabilities for nodes obtained in a Bayesian analysis conducted in parallel largely coincide with MP bootstrap support (fig. 4). Exceptions are Haplomitrium, which is placed basal to the Bazzania-Noteroclada clade, and Timmia, which is placed basal to the Rhacocarpus-Ulota clade, in the Bayesian analysis.
|
Most importantly, the phylogenetic analysis results in a topology that places hornworts as a sister group to the vascular plants and mosses as the sister clade to the hornwort-tracheophyte group. This topology indeed explains nad5 intron gains and losses parsimoniously (fig. 4). Gain of intron nad5i1477 and loss of group I intron nad5i753 can be interpreted as a synapomorphy of the joint hornwort-tracheophyte clade. The presence of introns nad5i230 and nad5i1455 exclusively shared between mosses, vascular plants, and hornworts to the exclusion of liverworts strongly adds characters to the suggested dichotomy of liverworts and nonliverwort embryophytes and makes other topologies less likely. For example, a hornwort-basal topology with a moss-liverwort clade sister to tracheophytes (Nickrent et al. 2000) would require eight events of nad5 intron gains and losses instead of six, as shown in figure 4.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Trans-splicing group II introns are not exclusively restricted to embryophytes. Recently two trans-splicing group II introns have been reported in the nad3 gene of Mesostigma viride (Turmel, Otis, and Lemieux 2002b). However, no orthologs of these introns are known in other species, and, consequently, their occurrence is, as yet, not of cladistic value for a phylogenetic placement of this alga. Earlier, trans-splicing had already been reported for the chloroplast psaA gene of the alga Chlamydomonas reinhardtii (Choquet et al. 1988), an organism that is clearly yet much more distantly related to land plants. However, as in the Mesostigma example, the lack of orthologs in related clades precludes its use in cladistic analyses. Mechanistically, however, one of the Chlamydomonas psaA introns is particularly interesting, as it is broken twice, thus, requiring three independent RNAs for splicing (Goldschmidt-Clermont et al. 1991). A similar case of tripartite intron reassembly has later been reported for nad5i1477 in the evening primrose (Knoop, Altwasser, and Brennicke 1997).
Trans-splicing in the mitochondrial lineage of land plants affects five group II introns (nad1i394, nad1i669, nad2i542, nad5i1455, and nad5i1477) that are disrupted in all angiosperms. Interest in the evolution of trans-splicing has led us to identify cis-arranged precursor introns in early branches of land-plant evolution (Malek, Brennicke, and Knoop 1997; Malek and Knoop 1998). In summary, the picture has emerged that these introns have entered new genomic loci early in the evolution of tracheophytes or, as is now clearly demonstrated, even in the bryophyte lineages. None of these introns is present in Marchantia or other liverworts.
In contrast to the nad5 introns investigated here, no homologs of the trans-splicing introns in nad1 (Dombrovska and Qiu 2004) and nad2 (Pruchner et al. 2002) mentioned above are present in mosses or hornworts. However, one additional group II intron in nad1, nad1i728, which is subject to independent transitions into trans arrangements now shown to occur frequently and independently among angiosperms (Qiu and Palmer 2004), is conserved as a cis-spliced intron in mosses and hornworts.
Lacking sufficient characters for cladistic analyses, nearly all possible phylogenetic tree topologies for the three bryophyte classes liverworts, hornworts, and mosses have been suggested in the literature. A topology in which hornworts are the basal-most embryophytes and in which a liverwort-moss clade is sister to tracheophytes was obtained through analyses of the nuclear small rRNA (Hedderson et al. 1996) and of a four-gene data set assembled from small rRNA sequences of all three genomes and the chloroplast rbcL gene (Nickrent et al. 2000).
Our study, however, adds arguments to the alternative view that liverworts are the sister group to all other embryophytes (Qiu et al. 1998). Any phylogenetic topology in which liverworts would not be placed as the basal-most embryophytes now need to postulate (1) numerous losses of mitochondrial introns conserved in tracheophytes and shared by mosses and/or hornworts (nad5i230, nad5i1455, and nad5i1477 [this contribution], nad2i156 and nad2i1282 [Pruchner et al. 2002], nad4i461, nad7i140, and nad7i209 [Pruchner et al. 2001], cox2i373, cox2i691, and nad1i728 [Qiu et al. 1998]) and (2) gain of liverwort-type introns that are not observed in the other clades. The positional stability of the mitochondrial introns argues against this option. On the other hand, some intron losses along the phylogenetic backbone affecting entire land-plant clades do obviously exist. For example, the topology now suggested by analysis of nad5 would, on the one hand, nicely explain intron nad2i1282 as a further synapomorphy of the hornwort-tracheophyte clade. However, on the other hand, secondary nad2 intron losses need to be postulated in any tree topology. For the tree shown in figure 4, this would be the loss of nad2i156 in hornworts (present in mosses but absent in liverworts) and the loss of nad2i709 in mosses (present in all other land-plant clades). An intron serendipitously identified in the nad1 gene of a moss (Malek and Knoop 1998), nad1i27, has now been characterized as universally conserved between mosses and hornworts (Dombrovska and Qiu 2004). Presence of this intron can be interpreted as a gain in the nonliverwort lineage and subsequent loss in the common ancestor of tracheophytes in the phylogeny presented here.
Similar larger-scale genomic features of cladistic value are rare in the chloroplast genome, as revealed by the recently completed sequence of the Anthoceros formosae plastome (Kugita et al. 2003). However, loss of the ycf66 gene adds to synapomorphies of the joint hornwort-tracheophyte clade.
The phylogeny presented here is compatible with the "close relationship" of hornworts and tracheophytes that has been observed in the analysis of chloroplast rDNA and ITS sequences (Samigullin et al. 2002). The discrepancies to the phylogenetic studies based on rRNA sequences mentioned above, however, remain to be explained. Nuclear 18S rRNA studies have resulted in phylogenies in which jungermanniid liverworts have been linked to mosses (Capesius and Bopp 1997)a phylogeny that has remained unsupported by all subsequent phylogenetic studies. The small rRNA gene even has been labeled as "positively misleading" for an unrelated issue of plant phylogeny (Duvall and Bricker 2004). A recent study has found bryophytes monophyletic with strong support when concatenated amino acid sequences of 51 chloroplast-encoded genes were used for phylogenetic analysis (Nishiyama et al. 2004). It should be kept in mind that in that study, (1) taxon sampling was somewhat biased towards angiosperms, whereas only one species of each bryophyte class was included, (2) that different weakly supported topologies were obtained when nucleotide instead of amino acid sequences were used, and (3) that node confidence was affected by selective inclusion of outgroup algae.
As in other difficult issues of phylogenetic analysis, an extension of taxon sampling to maximize the inclusion of independent characters from all three plant genomes will provide an ultimate answer in the near future. The present study adds to the view that mitochondrial exons and introns in particular are a valuable resource in that regard. Contrasting modes of intron evolution in the two plant organelle genomes are obvious. Whereas most plastome introns apparently have been gained at an algal level of organization, mitochondrial introns seem to have been gained after establishment of the embryophyte lineage on land. Mycorrhizal and other endophytic fungal symbionts that can interact with bryophytes and that had been present at the time of establishment of land plants (Ligrone, Pocock, and Duckett 1993; Read et al. 2000; Redecker, Kodner, and Graham 2000) allow for speculations on differential gains of mitochondrial introns in the liverwort and nonliverwort lineages, potentially originating form distinct fungal donors.
![]() |
Acknowledgements |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Footnotes |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Beckert, S., S. Steinhauser, H. Muhle, and V. Knoop. 1999. A molecular phylogeny of bryophytes based on nucleotide sequences of the mitochondrial nad5 gene. Plant Syst. Evol. 218:179192.[ISI]
Capesius, I., and M. Bopp. 1997. New classification of liverworts based on molecular and morphological data. Plant Syst. Evol. 207:8797.[ISI]
Choquet, Y., M. Goldschmidt-Clermont, J. Girard-Bascou, U. Kück, P. Bennoun, and J. D. Rochaix. 1988. Mutant phenotypes support a trans-splicing mechanism for the expression of the tripartite psaA gene in the C. reinhardtii chloroplast. Cell 52:903913.[ISI][Medline]
Dombrovska, O., and Y. L. Qiu. 2004. Distribution of introns in the mitochondrial gene nad1 in land plants: phylogenetic and molecular evolutionary implications. Mol. Phylogenet. Evol. 32:246263.[CrossRef][ISI][Medline]
Duvall, M. R., and E. A. Bricker. 2004. 18S gene trees are positively misleading for monocot/dicot phylogenetics. Mol. Phylogenet. Evol. 30:97106.[CrossRef][ISI][Medline]
Goldschmidt-Clermont, M., Y. Choquet, J. Girard-Bascou, F. Michel, M. Schirmer-Rahire, and J. D. Rochaix. 1991. A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell 65:135143.[ISI][Medline]
Handa, H. 2003. 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. 31:59075916.
Hedderson, T. A., R. L. Chapman, and W. L. Rootes. 1996. Phylogenetic relationships of bryophytes inferred from nuclear-encoded rRNA gene sequences. Plant Syst. Evol. 200:213224.[ISI]
Huelsenbeck, J. P., and F. Ronquist. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754755.
Karol, K. G., R. M. McCourt, M. T. Cimino, and C. F. Delwiche. 2001. The closest living relatives of land plants. Science 294:23512353.
Knoop, V., M. Altwasser, and A. Brennicke. 1997. A tripartite group II intron in mitochondria of an angiosperm plant. Mol. Gen. Genet. 255:269276.[CrossRef][ISI][Medline]
Knoop, V., W. Schuster, B. Wissinger, and A. Brennicke. 1991. Trans splicing integrates an exon of 22 nucleotides into the nad5 mRNA in higher plant mitochondria. EMBO J. 10:34833493.[Abstract]
Kohchi, T., K. Umesono, Y. Ogura, Y. Komine, K. Nakahigashi, T. Komano, Y. Yamada, H. Ozeki, and K. Ohyama. 1988. A nicked group II intron and trans-splicing in liverwort, Marchantia polymorpha, chloroplasts. Nucleic Acids Res. 16:1002510036.[Abstract]
Koller, B., H. Fromm, E. Galun, and M. Edelman. 1987. Evidence for in vivo trans splicing of pre-mRNAs in tobacco chloroplasts. Cell 48:111119.[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 tRNA(Cys)(GCA). Nucleic Acids Res. 28:25712576.
Kugita, M., A. Kaneko, Y. Yamamoto, Y. Takeya, T. Matsumoto, and K. Yoshinaga. 2003. The complete nucleotide sequence of the hornwort (Anthoceros formosae) chloroplast genome: insight into the earliest land plants. Nucleic Acids Res. 31:716721.
Liepelt, S., R. Bialozyt, and B. Ziegenhagen. 2002. Wind-dispersed pollen mediates postglacial gene flow among refugia. Proc. Natl. Acad. Sci. USA 99:1459014594.
Ligrone, R., K. Pocock, and J. G. Duckett. 1993. A comparative ultrastructural-study of endophytic basidiomycetes in the parasitic achlorophyllous hepatic Cryptothallus-Mirabilis and the closely allied photosynthetic species Aneura-Pinguis (Metzgeriales). Can. J. Bot. 71:666679.[ISI]
Malek, O., A. Brennicke, and V. Knoop. 1997. Evolution of trans-splicing plant mitochondrial introns in pre-Permian times. Proc. Natl. Acad. Sci. USA 94:553558.
Malek, O. and V. Knoop. 1998. Trans-splicing group II introns in plant mitochondria: the complete set of cis-arranged homologs in ferns, fern allies, and a hornwort. RNA 4:15991609.
Nickrent, D. L., C. L. Parkinson, J. D. Palmer, and R. J. Duff. 2000. Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Mol. Biol. Evol. 17:18851895.
Nishiyama, T., P. G. Wolf, M. Kugita et al. (12 co-authors). 2004. Chloroplast phylogeny indicates that bryophytes are monophyletic. Mol. Biol. Evol. 21:18131819.
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. Genom. 268:434445.[CrossRef][ISI][Medline]
Oda, K., K. Yamato, E. Ohta, Y. Nakamura, M. Takemura, N. Nozato, K. Akashi, T. Kanegae, Y. Ogura, Kohchi, T., and K. Ohyama. 1992. Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA: a primitive form of plant mitochondrial genome. J. Mol. Biol. 223:17.[ISI][Medline]
Pereira de Souta, A., M.-F. Jubier, E. Delcher, D. Lancelin, and B. Lejeune. 1991. A trans-splicing model for the expression of the tripartite nad5 gene in wheat and maize mitochondria. Plant Cell 3:13631378.
Pruchner, D., S. Beckert, H. Muhle, and V. Knoop. 2002. Divergent intron conservation in the mitochondrial nad2 gene: signatures for the three bryophyte classes (mosses, liverworts, and hornworts) and the lycophytes. J. Mol. Evol. 55:265271.[CrossRef][ISI][Medline]
Pruchner, D., B. Nassal, M. Schindler, and V. Knoop. 2001. Mosses share mitochondrial group II introns with flowering plants, not with liverworts. Mol. Genet. Genom. 266:608613.[CrossRef][ISI][Medline]
Qiu, Y. L., Y. R. Cho, J. C. Cox, and J. D. Palmer. 1998. The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394:671674.[CrossRef][ISI][Medline]
Qiu, Y. L., and J. D. Palmer. 2004. Many independent origins of trans-splicing of a plant mitochondrial group II intron. J. Mol. Evol. 59:8089.[ISI][Medline]
Read, D. J., J. G. Duckett, R. Francis, R. Ligrone, and A. Russell. 2000. Symbiotic fungal associations in lower land plants. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355:815830.[CrossRef][ISI][Medline]
Redecker, D., R. Kodner, and L. E. Graham. 2000. Glomalean fungi from the Ordovician. Science 289:19201921.
Samigullin, T. K., S. P. Yacentyuk, G. V. Degtyaryeva, K. M. Valiejo-Roman, V. K. Bobrova, I. Capesius, W. F. Martin, A. V. Troitsky, V. R. Filin, and A. S. Antonov. 2002. Paraphyly of bryophytes and close relationship of hornworts and vascular plants inferred from analysis of chloroplast rDNA ITS (cpITS) sequences. Arctoa 11:3143.
Steinhauser, S., S. Beckert, I. Capesius, O. Malek, and V. Knoop. 1999. Plant mitochondrial RNA editing. J. Mol. Evol. 48:303312.[ISI][Medline]
Swofford, D. L. 2002. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Mass.
Turmel, M., C. Otis, and C. Lemieux. 2002a. 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 99:1127511280.
. 2002b. 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. 19:2438.
. 2003. 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 15:18881903.
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. 15:5761.[ISI][Medline]
Vangerow, S., T. Teerkorn, and V. Knoop. 1999. Phylogenetic information in the mitochondrial nad5 gene of pteridophytes: RNA editing and intron sequences. Plant Biol. 1:235243.[ISI]
Wang, X. Q., D. C. Tank, and T. Sang. 2000. Phylogeny and divergence times in Pinaceae: evidence from three genomes. Mol. Biol. Evol. 17:773781.
|