*Department of Plant Biology and Center for Systematic Biology, Southern Illinois University at Carbondale;
and
Department of Biology, Indiana University at Bloomington
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Despite its wide acceptance, the LBT has been challenged by data derived from spermatozoid ultrastructure and spermatogenesis (Renzaglia and Duckett 1991
) and, more recently (Garbary and Renzaglia 1998
), by an extensive cladistic analysis of morphological and ultrastructural data that yielded a monophyletic moss-liverwort clade, with hornworts sister to all land plants. This "hornworts-basal" topology (HBT) was also obtained in analyses of nuclear small-subunit (nuSSU) rDNA (Hedderson, Chapman, and Rootes 1996
), combined analysis of five chloroplast genes (Nishiyama and Kato 1999
), and analyses of mitochondrial cox3 (Malek et al. 1996
), nad5 (Beckert et al. 1999
), and mitochondrial small-subunit (mtSSU) rDNA (Duff and Nickrent 1999
). In an effort to distinguish between the LBT and the HBT and to provide an improved understanding of land plant phylogeny, we generated additional sequence data to allow the construction of a multigene data set representing all three plant genomes and the same suite of exemplar taxa.
![]() |
Materials and Methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Alignments
Separate gene and multigene alignments were conducted manually using SeqApp (Gilbert 1993
). Alignment of rbcL and cpSSU rDNA sequences was trivial, given essentially no length variation, whereas for nuclear and mitochondrial SSU rDNA sequences, alignments were guided by reference to published higher-order structures (Nickrent and Soltis 1995
; Duff and Nickrent 1999
). Terminal priming regions were excluded from all sequences, as were regions where alignment was ambiguous or where extensive length variation occurred (e.g., introns in mtSSU rDNA; see Duff and Nickrent 1999
). There were (with reference to Glycine sequences) 51 such sites for rbcL, 63 for cpSSU rDNA, 133 for nuSSU rDNA, and 633 for mtSSU rDNA, for a total of 909 sites excluded from the multigene data set. The key to excluded regions and the final alignment (6,095 positions: rbcL = 1,351, cpSSU rDNA = 1,480, nuSSU rDNA = 1,720, and mtSSU rDNA = 1,544) can be found at http://www.science.siu.edu/landplants/Alignments/Alignments.html.
Parsimony and Likelihood Analyses
There currently exists conflicting information in the literature as to whether rbcL third codon positions are saturated, or, more specifically, whether the process of substitution has become so randomized as to preclude the use of this position for ascertaining deep phylogenetic relationships. Evidence that third-codon-position transitions are effectively saturated has been presented by Goremykin et al. (1996)
and Chaw et al. (2000)
. Conversely, Lewis, Mishler, and Vilgalys (1997)
showed that trees generated from only third positions are nearly identical to trees produced from all sites and that these trees agree with independent evidence. Hence, they concluded that, despite being highly variable, third positions retain phylogenetic signal across all land plants. A similar conclusion was reached by Källersjö et al. (1998)
. To test for saturation, we plotted uncorrected p-distances from first-, second-, and third-position transitions and transversions against corrected F84 distances (Felsenstein 1984
).
Four versions of the multigene data set were constructed and analyzed with either maximum parsimony (MP) or maximum likelihood (ML). In the first version, all positions, including rbcL third codon positions, were included and were weighted equally. Analyses of this version were called MP+3Ti and ML-rates. The second version also included all positions, but differential weighting (ranging from 0.5 to 1.0) was applied to third codon positions. Analyses of this version were dubbed MP+weights. The third version excluded rbcL third-codon-position transitions, which was accomplished by recoding all third-position nucleotides as either R (A or G) or Y (C or T). Analyses of this version were called MP-3Ti and ML-3Ti. In the fourth version, all positions were included, and site-to-site rate variation was accounted for using the program DNArates (S. Pract, R. Overbeek, and G. Olsen, personal communication; available at the Ribosomal Database Project website). Analysis of this version was called ML+rates.
All MP analyses were conducted using PAUP* (Swofford 1998
). For these analyses, the separate and combined gene matrices were analyzed either with all characters equally weighted or with unequal weighting (see above). Heuristic search strategies with random taxon addition (100 replicates), MULPARS on, and tree bisection-reconnection (TBR) branch swapping was employed. MP bootstrap (BS) support was assessed using PAUP*, employing a heuristic search strategy with 100 replications (1,000 for the multigene data set).
ML analyses employed fastDNAml, version 1.06, rewritten to run in parallel, on 816 nodes of the STARRS/SP cluster (IBM RS/6000 computer platform, located at Indiana University). The F84 model (Felsenstein 1984
) as implemented in PHYLIP (Felsenstein 1993
) was used, with the initial transition/transversion (ti/tv) ratio estimated using PUZZLE, version 4.02, under the Tamura-Nei model of evolution with parameter estimation set to "approximate" (Strimmer and von Haeseler 1996
). Ten initial ML trees were inferred for each individual and the combined data set by randomizing "input" order with jumble and using "global" swapping across all nodes (equivalent to subtree-pruning-regrafting of PAUP*). The optimal tree (best log likelihood score) was then input into PAUP* to reoptimize the ti/tv ratio using a model that incorporated variability in rates of change. We used the F84 evolutionary model assuming a discrete gamma distribution with four categories of site-to-site rate variability. The resulting ti/tv ratio was used to infer a new tree as above, further optimizing branch lengths. This tree and the optimized ti/tv ratio were then used to estimate evolutionary rates of change for each sequence position by partitioning the sites into 35 "rate" categories using DNArates. A new ML tree, incorporating the rate categories and the reoptimized ti/tv ratio, was then inferred. This new optimal tree was then used for a second round of rate estimation and tree inference. This process was iterated until a stable topology was achieved.
ML bootstrapping with and without rates used SEQBOOT (PHYLIP) to generate 100 pseudoreplicate data sets that were analyzed using fastDNAml, and the resulting bootstrap numbers were generated using CONSENSE (PHYLIP). The individual trees from the 100 pseudoreplicates were analyzed as above using fastDNAml, randomizing the input order, and allowing swapping across all nodes. Each initial "no-rates" topology was then used to infer rate categories incorporating the optimized ti/tv ratio. A second round of rate category generation and tree inference was performed, and the final 100 trees were imported into CONSENSE to generate bootstrap node values.
Alternative topologies, evaluated under ML and MP, were determined using the parametric K-H test (Kishino and Hasegawa 1989) and the nonparametric Templeton (1983)
ranked-sums test as implemented in PAUP*. Decay analyses (Bremer 1994) were performed with MP using PAUP* and AUTODECAY (Eriksson 1998).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
|
|
The most striking differences between the MP+3Ti and MP-3Ti analyses involved bryophyte relationships. The single shortest tree recovered from the multigene data set using MP+3Ti (fig. 2 ) showed the liverworts Marchantia and Calypogeia as sister to all other land plants (the LBT), with paraphyletic mosses and the hornworts Megaceros and Phaeoceros sister to the tracheophytes. None of these bryophyte relationships received BS support >50%. Mosses were not supported as monophyletic using any of the nonmitochondrial partitions separately (table 2 ), but only achieved monophyly in the multigene data sets in which rbcL third position transitions were excluded or downweighted (MP+weights). A similar result was obtained for the sister group relationship between mosses and liverworts. One topological difference occurred within the moss clade when using ML-rates as opposed to ML+rates and MP-3Ti. The former method placed Polytrichum as sister to a Takakia/Sphagnum clade (tree not shown), whereas the latter methods placed Takakia as sister to Sphagnum/Polytrichum (fig. 3 ). For the MP+weights analysis, the HBT was obtained using all weights up to 0.93, whereas the LBT was retrieved with weights above this threshold.
In general, BS support for most clades was equivalent or higher for ML+rates than for ML-rates; this was true for the multigene data set and, to a lesser extent, for analyses of individual genes (table 2
). Such an increase in BS support can be seen for the HBT, where the ML+rates and ML-rates BS values were 62% and 78%, respectively. Three clades in the multigene analysis showed marked differences in BS values between ML+rates and MP: gymnosperms, lycophytes, and HBT (table 2
). For the HBT, the lower BS values obtained when using ML-rates (62%) or ML+rates (78%) as compared with MP (95%) may be attributed to the influence of the rbcL partition. Of the four partitions, only mtSSU and cpSSU rDNA analyzed separately retrieved the HBT (but with low to moderate BS support). Using ML and MP methods, combining the three SSU rDNA partitions gave BS values of 96%97% for the HBT. That combined analyses can result in increased resolution and BS support for particular clades that were not well supported following individual analyses has been documented (Kluge 1989
; Mishler et al. 1994
; Soltis et al. 1998
; Soltis, Soltis, and Chase 1999
). Moreover, clades that were not present following analyses of individual genes can appear and gain significant BS support upon combined analyses. Examples here include the euphyllophyte, fern, and gymnosperm clades using rbcL, cpSSU, and nuSSU rDNA separately and in combination.
Decay Analyses and Hypothesis Testing
Decay analysis showed that 12 additional steps were required to collapse the hornworts-basal node (fig. 3
). Five alternative topologies were tested with the multigene data set using the K-H test with ML and MP (fig. 4AF
). Two frequently cited LBTs depict either hornworts (fig. 4C
) or mosses (fig. 4D
) as sister to tracheophytes, but both were rejected as statistically worse (P < 0.05 level) than the ML tree. Similarly, the paraphyletic moss topology (fig. 4F
) was significantly worse than the MP and ML trees. An alternative HBT (fig. 4B
), in which liverworts and mosses were not sister taxa, added six steps to the most-parsimonious MP tree and could not be rejected relative to the ML tree. Finally, a monophyletic-bryophytes topology, although 14 steps longer than the MP tree, also could not be rejected relative to the ML tree. The K-H and Templeton tests conducted using MP as the criterion showed that all alternative trees (BF) were significantly worse than tree A (P < 0.05).
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Lower homoplasy in mitochondrial genes may derive from generally lower mutation rates as compared with nuclear or chloroplast genes (Wolfe, Li, and Sharp 1987
; Palmer 1990
; Wolfe 1996
) and further highlights their utility in addressing ancient land plant relationships. Chloroplast SSU rDNA had the second lowest amount of homoplasy. Although this gene alone contains insufficient phylogenetic signal to resolve many clades, it did recover the liverwort clade and the HBT, two relationships that were not obtained using the longer and more variable nuSSU rDNA alone (table 2
). The poor overall performance of nuSSU rDNA in resolving land plant relationships cannot be attributed to insufficient taxon sampling in this study, as similarly poor results were obtained in a recent study that utilized 93 ingroup sequences (Soltis et al. 1999
).
Influence of the rbcL Partition on Resulting Trees
Chloroplast rbcL alone recovered a number of land plant clades but contained the highest level of homoplasy among the four gene partitions (table 2
). When rbcL was analyzed alone using MP with all positions equally weighted, three trees were obtained that supported the LBT (62% BS support; results not shown). Removal of all third positions resulted in extensive loss of resolution across the entire tree, in agreement with Lewis, Mishler, and Vilgalys (1997)
and Källersjö et al. (1998)
. Removal of third-position transitions resulted in a tree with no BS support for any of the major land plant clades. These exercises demonstrated that most of the phylogenetic signal in rbcL resides in third codon positions, specifically, third-position transitions. When the rbcL partition was included in the multigene data set and third codon positions were weighted 0.94 or less, the HBT was obtained, thus demonstrating how these competing topologies are sensitive to the degree of influence imparted by third-position differences.
Evolutionary Rates
Qiu and Palmer (1999)
list several factors that might potentially confound the problem of determining the basalmost land plant lineage: (1) a wide "evolutionary gap" (both with morphological and molecular characters) between charophyte outgroups and land plants that eliminates synapomorphies; (2) long-branch attraction problems between ingroup and outgroup; (3) ancient and rapid radiation of bryophyte lineages at the base of the land plant tree, leaving little phylogenetic signal; and (4) extinction. As discussed above, the sequence divergence between Chara and a hornwort is equivalent to that between a hornwort and a flowering plant, thus demonstrating that the "evolutionary gap" between ingroup and outgroup is not disproportionate, at least for slowly evolving genes such as mtSSU rDNA. As shown in figures 2 and 3 , both the gnetophyte and the Selaginella clades have increased substitution rates, as indicated by their branch lengths, but in neither case can this be attributed to low taxon sampling. The fast evolutionary rate of gnetophytes has been well documented; however, we do not feel the position of the gnetophyte clade as sister to conifers is artifactual given that this result is in agreement with several recent molecular phylogenetic studies (Bowe, Coat, and dePamphilis 2000
; Chaw et al. 2000
; Sanderson et al. 2000
). Similarly, despite the long branch leading to Selaginella, its position as sister to Isoëtes when ML+rates was employed is fully in line with molecular and morphological analyses. Long-branch effects can be demonstrated with the nuSSU rDNA partition when analyzed alone with MP. Here, Selaginella migrates to the base of the tree, near liverworts. Among bryophytes, there is some evidence of lineage-specific and gene-specific substitution rate heterogeneity. For example, transition rates in complex thalloid liverwort rbcL are about half those seen in leafy and simple thalloid liverworts (Lewis, Mishler, and Vilgalys 1997
), whereas the opposite is true for nuSSU rDNA (Capesius and Bopp 1997
). There is no indication in the present analysis, however, that relationships within and among hornworts, liverworts, and mosses are being influenced by long-branch attraction artifacts.
Mitochondrial Introns
The presence/absence of three mitochondrial introns (Qiu et al. 1998
) has been interpreted as supporting the LBT, as all three introns "are present, with occasional losses, in mosses, hornworts and all major lineages of vascular plants, but are entirely absent from liverworts, green algae and all other eukaryotes." How can this result be reconciled with the findings reported here? If the HBT is correct, these introns must have been acquired in the common ancestor of all land plants and then lost in the common ancestor of liverworts. This scenario is more likely if liverworts are monophyletic, as supported by our analyses (fig. 1
), than if they are paraphyletic, as suggested by some previous studies that sampled more broadly within liverworts (Capesius and Bopp 1997
; Lewis, Mishler, and Vilgalys 1997
). Postulating a single additional loss of each intron is not unreasonable given that all three introns are already known to have been lost in two different lineages (Isoëtes and Ephedra) and that two of the three introns have been lost many times in land plant evolution (Qiu et al. 1998
; Qiu and Palmer, personal communication). Addition of the three intron characters to the multigene matrix does not change the MP-3Ti tree topology, and BS support for the HBT remains high (92%; data not shown).
Reinterpretation of Morphological Features
Given the strong support for the HBT, reinterpretation of key morphological and anatomical innovations is now required. Several ultrastructural features shared between hornworts and charophycean algae (such as Coleochaete) support the concept that hornworts are the earliest land plant lineage. Unique among land plants, hornwort chloroplasts contain pyrenoids (localized groupings of RUBISCO) that are essentially identical to those in green algae (Vaughn et al. 1992
) and also share with algae channel thylakoids. The HBT thus requires that these chloroplast structures have been lost in other land plants. Conversely, hornworts lack chloroplast granal end membranes and staggered spermatozoid flagella, which presumably evolved subsequent to the divergence of hornworts and other land plants (Garbary and Renzaglia 1998
). If the HBT and the sister group status of liverworts and mosses are correct, the presence of stomates in some hornworts and mosses and all vascular plants may indicate that these structures are not homologous (Renzaglia et al. 2000
). If moss and vascular plant stomates are homologous, then stomates were lost in the ancestor of liverworts. Similarly, a loss in liverworts is invoked for the perine layer in spores, a feature shared by mosses and vascular plants (Garbary and Renzaglia 1998
).
As in most analyses to date, the paraphyly of bryophytes is demonstrated in this multigene analysis. The sister group relationship between mosses and liverworts has received support from data derived from spermatogenesis (Garbary, Renzaglia, and Duckett 1993
), sperm ultrastructure (Maden et al. 1997
), and overall morphology (Garbary and Renzaglia 1998
), as well as molecular characters such as nuclear SSU rDNA (Hedderson, Chapman, and Cox 1998
) and mitochondrial SSU rDNA (Duff and Nickrent 1999
) and an analysis of five chloroplast genes (Nishiyama and Kato 1999
). The morphological and ultrastructural synapomorphies that support a moss/liverwort clade are (1) the presence of gametophytic slime papillae, (2) superficial archegonia, (3) dimorphic basal bodies on spermatozoa, and (4) apertures associated with the spline on spermatozoa (Garbary and Renzaglia 1998
). Takakia was first described as a liverwort; however, substantial morphological (Renzaglia, McFarland, and Smith 1997
) and molecular (Hedderson, Chapman, and Rootes 1996
; Duff and Nickrent 1999
) evidence now places the genus within the mosses, a result supported by this multigene analysis. Additional sequencing to allow inclusion of putatively basal liverworts such as Haplomitrium and Monoclea in future multigene analyses is required to test the robustness of the moss-liverwort clade.
![]() |
Conclusions and Future Work |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
As stated in the Introduction, a goal of this study was to determine whether molecular and morphological data better support the LBT or the HBT. It appears that most support for the former hypothesis derives from the chloroplast gene rbcL, specifically, third-codon-position transitions of this gene. In contrast, the HBT is supported by the present study, as well as combined analyses of rbcL and other chloroplast genes (Nishiyama and Kato 1999
), mitochondrial genes (Malek et al. 1996
; Beckert et al. 1999
; Duff and Nickrent 1999
), nuclear SSU rDNA (Hedderson, Chapman, and Cox 1998
), and morphology (Garbary and Renzaglia 1998
). Decay analyses indicate that all the alternative topologies tested using MP result in longer trees, and K-H tests show that these alternatives, including the LBT, are statistically different from the HBT. Thus, we conclude that the HBT hypothesis is most consistent with all of the available evidence (morphological and molecular), is not in conflict with presence/absence data on mitochondrial introns, and therefore provides the best explanation of early land plant evolution. Further refinement and resolution of this tree will provide a firm phylogenetic foundation to help interpret the evolution of plant morphology, ultrastructure, development, and biochemistry.
![]() |
Acknowledgements |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Footnotes |
---|
1 Present address: Department of Biology, University of Central Florida.
2 Present address: Department of Biology, University of Akron.
3 Abbreviations: HBT, hornwort basal topology; LBT, liverwort basal topology.
4 Keywords: land plant phylogeny
embryophyte
hornwort
liverwort
moss
rbcL,
small-subunit ribosomal DNA
5 Address for correspondence and reprints: Daniel L. Nickrent, Department of Plant Biology and Center for Systematic Biology, Southern Illinois University, Carbondale, Illinois 62901-6509. E-mail: nickrent{at}plant.siu.edu
![]() |
literature cited |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
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]
Bowe, L. M., G. Coat, and C. W. dePamphilis. 2000. Phylogeny of seed plants based on all three plant genomic compartments: extant gymnosperms are monophyletic and Gnetales derived conifers. Proc. Natl. Acad. Sci. USA 97:40924097
Bremer, K. 1994. Branch support and tree stability. Cladistics 10:295304
Capesius, I., and M. Bopp. 1997. New classification of liverworts based on molecular and morphological data. Plant Syst. Evol. 207:8797[ISI]
Chaw, S.-M., C. L. Parkinson, Y. Cheng, T. M. Vincent, and J. D. Palmer. 2000. Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. Proc. Natl. Acad. Sci. USA 97:40864091
Duff, R. J., and D. L. Nickrent. 1999. Phylogenetic relationships of land plants using mitochondrial small-subunit rDNA sequences. Am. J. Bot. 86:372386
Eriksson, T. 1998. AutoDecay, version 4.0. Bergius Foundation, Royal Swedish Academy of Sciences, Stockholm
Felsenstein, J. 1978. Cases in which parsimony or compatibility will be positively misleading. Syst. Zool. 27:401410[ISI]
. 1984. Distance methods for inferring phylogenies: a justification. Evolution 38:1624
. 1993. PHYLIP (phylogeny inference package). Version 3.5. Distributed by the author, Department of Genetics, University of Washington, Seattle
Garbary, D. J., and K. S. Renzaglia. 1998. Bryophyte phylogeny and the evolution of land plants: evidence from development and ultrastructure. Pp. 4563 in J. W. Bates, N. W. Ashton, and J. G. Duckett, eds. Bryology for the twenty-first century. Maney and the British Bryological Society, Leeds, England
Garbary, D. J., K. S. Renzaglia, and J. G. Duckett. 1993. The phylogeny of land plants: a cladistic analysis based on male gametogenesis. Plant Syst. Evol. 188:237269[ISI]
Gilbert, D. G. 1993. SeqApp. Version 1.9a157. Biocomputing Office, Biology Department, Indiana University, Bloomington
Goremykin, V., V. Bobrova, J. Pahnke, A. Troitsky, A. Antonov, and W. Martin. 1996. Noncoding sequences from the slowly evolving chloroplast inverted repeat in addition to rbcL data do not support Gnetalean affinities of angiosperms. Mol. Biol. Evol. 13:383396[Abstract]
Gray, J. 1993. Major Paleozoic land plant evolutionary bio-events. Palaeogeogr. Palaeoclimatol. Palaeoecol. 104:153169[ISI]
Hedderson, T. A., R. Chapman, and C. J. Cox. 1998. Bryophytes and the origins and diversification of land plants: new evidence from molecules. Pp. 6577 in J. W. Bates, N. W. Ashton, and J. G. Duckett, eds, Bryology for the twenty-first century. Maney and the British Bryological Society, Leeds, England
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]
Hillis, D. M., and J. J. Bull. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42:182191[ISI]
Hueber, F. M. 1961. Hepaticites devonicus, a new fossil liverwort from the Devonian of New York. Ann. Mo. Bot. Gard. 48:125132
Källersjö, M., J. S. Farris, M. W. Chase, B. Bremer, M. F. Fay, C. J. Humphries, G. Petersen, O. Seberg, and K. Bremer. 1998. Simultaneous parsimony jackknife analysis of 2538 rbcL DNA sequences reveals support for major clades of green plants, seed plants and flowering plants. Plant Syst. Evol. 213:259287[ISI]
Kenrick, P., and P. R. Crane. 1997. The origin and early diversification of land plants: a cladistic study. Smithsonian Institute Press, Washington, D.C
Kishino, H., and M. Hasegawa. 1989. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order of Hominoidea. J. Mol. Evol. 29:170179[ISI][Medline]
Kluge, A. G. 1989. A concern for evidence and a phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Syst. Zool. 38:725[ISI]
Lewis, L. A., B. D. Mishler, and R. Vilgalys. 1997. Phylogenetic relationships of the liverworts (Hepaticae), a basal embryophyte lineage, inferred from nucleotide sequence data of the chloroplast gene rbcL. Mol. Phylogenet. Evol. 7:377393
Maden, A. R., D. P. Whittier, D. J. Garbary, and K. S. Renzaglia. 1997. Ultrastructure of the spermatozoid of Lycopodiella lateralis (Lycopodiaceae). Can. J. Bot. 75:17281738[ISI]
Malek, O., K. Lättig, R. Hiesel, A. Brennicke, and V. Knoop. 1996. RNA editing in bryophytes and a molecular phylogeny of land plants. EMBO J. 15:14031411[Abstract]
Manhart, J. R. 1994. Phylogenetic analysis of green plant rbcL sequences. Mol. Phylogenet. Evol. 3:114127[Medline]
Mishler, B. D., and S. P. Churchill. 1984. A cladistic approach to the phylogeny of the bryophytes. Brittonia 36:406424
Mishler, B. D., L. A. Lewis, M. A. Buchheim, K. S. Renzaglia, D. J. Garbary, C. F. Delwiche, F. W. Zechman, T. S. Kantz, and R. L. Chapman. 1994. Phylogenetic relationships of the "green algae" and "bryophytes." Ann. Mo. Bot. Gard. 81:451483
Mishler, B. D., P. H. Thrall, J. S. J. Hopple, E. De Luna, and R. Vilgalys. 1992. A molecular approach to the phylogeny of bryophytes: cladistic analysis of chloroplast-encoded 16S and 23S ribosomal RNA genes. Bryologist 95:172180
Nemejc, F., and B. Pacltova. 1974. Hepaticae in the Senonian of South Bohemia. Paleobotanist 21:2326
Nickrent, D. L. 1994. From field to film: rapid sequencing methods for field collected plant species. BioTechniques 16:470475
Nickrent, D. L., R. J. Duff, and D. A. M. Konings. 1997. Structural analyses of plastid-derived 16S rRNAs in holoparasitic angiosperms. Plant Mol. Biol. 34:731743[ISI][Medline]
Nickrent, D. L., and D. E. Soltis. 1995. A comparison of angiosperm phylogenies based upon complete 18S rDNA and rbcL sequences. Ann. Mo. Bot. Gard. 82:208234
Nickrent, D. L., and E. M. Starr. 1994. High rates of nucleotide substitution in nuclear small-subunit (18S) rDNA from holoparasitic flowering plants. J. Mol. Evol. 39:6270[ISI][Medline]
Nishiyama, T., and M. Kato. 1999. Molecular phylogenetic analysis among bryophytes and tracheophytes based on combined data of plastid coded genes and the 18S rRNA gene. Mol. Biol. Evol. 16:10271036[Abstract]
Palmer, J. D. 1990. Contrasting modes and tempos of genome evolution in land plant organelles. Trends Genet. 6:115120[ISI][Medline]
Parkinson, C. L., K. L. Adams, and J. D. Palmer. 1999. Multigene analyses identify the three earliest lineages of extant flowering plants. Curr. Biol. 9:14851488[ISI][Medline]
Pryer, K. M., A. R. Smith, and J. E. Skog. 1995. Phylogenetic relationships of extant ferns based on evidence from morphology and rbcL sequences. Am. Fern J. 85:205282[ISI]
Qiu, Y., Y. Lee, F. Bernasconi-Quadroni, D. E. Soltis, P. S. Soltis, M. Zanis, E. A. Zimmer, Z. Chen, V. Savolainen, and M. W. Chase. 1999. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402:404409
Qiu, Y.-L., Y. 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
Qiu, Y.-L., and J. D. Palmer. 1999. Phylogeny of early land plants: insights from genes and genomes. Trends Plant Sci. 4:2630[ISI][Medline]
Raubeson, L. A., and R. K. Jansen. 1992. Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255:16971699
Renzaglia, K. S., and J. G. Duckett. 1991. Towards an understanding of the differences between the blepharoplast of mosses and liverworts, comparisons with hornworts, biflagellated lycopods and charophytes: a numerical analysis. New Phytol. 117:187208[ISI]
Renzaglia, K. S., R. J. Duff, D. L. Nickrent, and D. J. Garbary. 2000. Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355:769793[ISI][Medline]
Renzaglia, K. S., K. D. McFarland, and D. K. Smith. 1997. Anatomy and ultrastructure of the sporophyte of Takakia ceratophylla (Bryophyta). Am. J. Bot. 84:13371350[Abstract]
Richardson, J. B. 1985. Lower Palaeozoic sporomorphs: their stratigraphical distribution and possible affinities. Philos. Trans. R. Soc. Lond. B Biol. Sci. 309:201205[ISI]
Sanderson, M. J., M. F. Wojciechowski, J.-M. Hu, T. S. Khan, and S. G. Brady. 2000. Error, bias, and long-branch attraction in data for two chloroplast photosystem genes in seed plants. Mol. Biol. Evol. 17:782797
Soltis, D. E., and P. S. Soltis. 1998. Choosing an approach and an appropriate gene for phylogenetic analysis. Pp. 142 in D. E. Soltis, P. S. Soltis, and J. J. Doyle, eds. Molecular systematics of plants II. DNA sequencing. Kluwer Academic Publishers, Boston
Soltis, D. E., P. S. Soltis, M. W. Chase et al. (13 co-authors). 2000. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot. J. Linn. Soc. 133:381461[ISI]
Soltis, D. E., P. S. Soltis, M. E. Mort, M. W. Chase, V. Savolainen, S. B. Hoot, and C. M. Morton. 1998. Inferring complex phylogenies using parsimony: an empirical approach using three large DNA data sets for angiosperms. Syst. Biol. 47:3242[ISI][Medline]
Soltis, P. S., D. E. Soltis, and M. W. Chase. 1999. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402:402407
Soltis, P. S., D. E. Soltis, P. G. Wolf, D. L. Nickrent, S.-M. Chaw, and R. L. Chapman. 1999. The phylogeny of land plants inferred from 18S rDNA sequences: pushing the limits of rDNA signal? Mol. Biol. Evol. 16:17741784
Strimmer, K., and A. von Haeseler. 1996. Quartet puzzling: a quartet maximum-likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13:964969
Swofford, D. L. 1998. PAUP*: phylogenetic analysis using parsimony. Version 4.0 b2a. Sinauer, Sunderland, Mass
Taylor, W. A. 1995. Spores in earliest land plants. Nature 373:393392
Templeton, A. R. 1983. Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37:221244
Vaughn, K. C., R. Ligrone, H. A. Owens, J. Hasegawa, E. O. Campbell, K. S. Renzaglia, and J. Monge-Najera. 1992. The Anthocerote chloroplast: a review. New Phytol. 120:169190[ISI]
Wolf, P. G. 1997. Evaluation of atpB nucleotide sequences for phylogenetic studies of ferns and other pteridophytes. Am. J. Bot. 84:14291440[Abstract]
Wolfe, K., W.-H. Li, and P. Sharp. 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc. Natl. Acad. Sci. USA 84:90549058
Wolfe, K. H. 1996. Molecular evolution of plants: more genomes, less generalities. Pp. 4557 in B. Andersson, A. H. Salter, and J. Barber, eds. Molecular genetics of photosynthesis. IRL Press, Oxford, England