Department of Biology, University of Massachusetts at Amherst;
Institute of Systematic Botany, University of Zurich, Zurich, Switzerland
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Abstract |
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Introduction |
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Several approaches have been explored to deal with the distant-outgroup problem. The first approach is to use genes that duplicated along the branch leading to the ingroup, to reciprocally root the two gene phylogenies with each other and thus to infer the organismal phylogeny (Gogarten et al. 1989
; Iwabe et al. 1989
; Donoghue and Mathews 1998
). This strategy works when the duplication occurred close to the point at which the ingroup diversified and when the duplicated copies did not experience dramatic rate acceleration. Another way to deal with the distant-outgroup problem is to extend the length of sequence analyzed by combining data from multiple genes of all three genomes so that the signal/noise ratio can be increased to allow a reliable rooting of the ingroup topology (Hillis 1996
; Soltis et al. 1998
; Qiu and Palmer 1999
; Graham and Olmstead 2000
). A third way to circumvent the distant-outgroup problem is to use genomic structural features that are conserved in their evolution and have clearly understood evolutionary mechanisms (Manhart and Palmer 1990
; Raubeson and Jansen 1992
; Qiu et al. 1998
). Finally, understanding the homology of morphological characters across the large gap between the outgroup and the ingroup at a deeper level by taking the molecular developmental biology approach represents a major direction for future investigation of diversification patterns at the bases of major clades (Kellogg and Shaffer 1993
; Doyle 1994
; Carroll 1995
; Davidson, Peterson, and Cameron 1995
; Raff 1996
; Frohlich and Meyerowitz 1997
; Shubin, Tabin, and Carroll 1997
; Theissen et al. 2000
).
In reconstructing relationships among basal angiosperms, the first two strategies have been used in several recent studies that identified the first branches of the angiosperm phylogeny (Mathews and Donoghue 1999, 2000
; Parkinson, Adams, and Palmer 1999
; Qiu et al. 1999, 2000
; Soltis, Soltis, and Chase 1999
; Barkman et al. 2000
; Graham and Olmstead 2000
; Soltis et al. 2000
). Despite the mutual corroboration between the studies that employed the duplicated gene rooting strategy and those that adopted the multigene analysis approach in identifying the ANITA lineages as the basalmost extant angiosperms, it is essential to demonstrate that the multigene analysis approach can stand on a solid analytic ground on its own and that sampling multiple genes can indeed enhance the level of phylogenetic signal and thus can overcome the divergence gap problem between gymnosperms and angiosperms. This concern is especially justified by the fact that duplicated gene rooting has been shadowed by the difficulty of placing Ceratophyllum (Mathews and Donoghue 1999, 2000
), which was identified as the first lineage of angiosperms in earlier rbcL analyses (Les, Garvin, and Wimpee 1991
; Chase et al. 1993
; Qiu et al. 1993
).
The key argument used in suggesting that distant outgroups might no longer be appropriate outgroups in molecular phylogenetic analyses is that the outgroup sequences are so divergent that the variation they contain has been randomized due to back-mutations and parallel mutations during the long time span since separation of the ingroup and the outgroup (Miyamoto and Boyle 1989
; Wheeler 1990
; Qiu and Palmer 1999
). Hence, one can test whether or not a particular outgroup still contains phylogenetic signal to root the ingroup by replacing it with a random sequence. If the subsequent analysis reproduces the ingroup topology obtained by the original outgroup, this may be an indication of LBA caused by the randomized outgroup. Alternatively, if the random sequence attracts the longest ingroup branch and yields a different topology, this would suggest that the use of the original outgroup might have been appropriate (Miyamoto and Boyle 1989
; Wheeler 1990
; Maddison, Ruvolo, and Swofford 1992
; Donoghue 1994
; Graham 1997
, pp. 122161; Sullivan and Swofford 1997
).
In this study, we performed a series of analyses on the original data matrix used to identify ANITA as the earliest-diverging lineages of angiosperms (Qiu et al. 1999, 2000
) using several types of artificial (random and nonrandom) sequences, as well as sequences that are more divergent than those of gymnosperms, namely, those of a lycopod and a bryophyte, to test whether our original use of gymnosperms as the outgroup was justified. Together with the ingroup taxon deletion analyses and constraint topology analyses presented earlier (Qiu et al. 2000
), we hope that these analyses provide a rigorous analytic perspective for identifying the ANITA lineages as the earliest branches of the angiosperm phylogeny.
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Materials and Methods |
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To identify the longest ingroup branch and to examine distribution of branch lengths within angiosperms, we performed an unrooted ingroup (i.e., angiosperm only) analysis without using any outgroup. All of the angiosperms in the original matrix (Qiu et al. 2000
) were kept after the eight gymnosperms were deleted. A heuristic search with 1,000 random-taxon-addition replicates and the same tree search procedure described above was conducted.
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Results |
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Discussion |
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The next question to ask is whether the ANITA rooting can still be an artifact caused by some mechanisms that generate similarities in unrelated lineages by chance but do not necessarily produce long branches. One molecular evolutionary phenomenon, RNA editing, so far known to occur only in organellar genomes (Yoshinaga et al. 1996
; Steinhauser et al. 1999
), may be such a mechanism (Bowe and dePamphilis 1996
; Qiu and Palmer 1999
). Nevertheless, individual analyses of three genes from two organellar genomes (mitochondrial atp1 and matR and plastid atpB) have all identified the ANITA clades as the earliest-branching angiosperm lineages (Qiu et al. 1999, 2000
; Barkman et al. 2000
; Savolainen et al. 2000
). It is highly unlikely that the three genes in two genomes would experience extensive RNA editing in both gymnosperms and the ANITA members but not in any other lineages. Furthermore, an analysis of the nuclear 18S rDNA alone with extensive taxon sampling also placed Austrobaileya-Illiciales and Amborella at the base of angiosperm phylogeny (Soltis et al. 1997
). No RNA editing has been reported at this locus to date. Finally, and most importantly, rooting of the angiosperm phylogeny using duplicated nuclear phytochrome genes has produced a similar result (Mathews and Donoghue 1999, 2000
), reinforcing our belief that the ANITA rooting was not caused by RNA editing.
GC content bias is another mechanism that does not necessarily increase branch length dramatically but still can generate analytic artifacts in phylogenetic analysis of DNA sequences (Steel, Lockhart, and Penny 1993
). A brief examination of the GC content in the five genes across all major lineages of basal angiosperms and gymnosperms shows that there is no significant difference among lineages. Thus, it is unlikely that the ANITA rooting was affected by this factor.
A final question to ask is whether the concern that distant outgroups could cause LBA was well placed (Miyamoto and Boyle 1989
; Wheeler 1990
; Qiu et al. 1993
; Donoghue and Mathews 1998
; Qiu and Palmer 1999
). Our analyses using well-aligned lycopod and bryophyte sequences as the outgroup to root the angiosperm phylogeny indicate that exceedingly divergent outgroups can indeed generate a spurious rooting topology. Both analyses identified either Acorus or Alisma-Triglochin-Potamogeton as the first branch of the angiosperm phylogeny and placed the monocots as a basal grade (table 1
). These results suggest that the lycopod and bryophyte sequences are so divergent that they behave like random sequences. The outgroup branch length in the bryophyte rooting analysis was 1,464 steps, and that in the lycopod rooting analysis was 1,181 steps, as opposed to the 354 steps of the gymnosperm branch in Qiu et al. (2000)
. (Note that the alignment used for the bryophyte and lycopod rooting analyses was a slightly different one.) On the other hand, placing aligned gymnosperm sequences back into the matrix produced the ANITA rooting again (data not shown; the gymnosperms formed a monophyletic group, and the Gnetum-Welwitschia clade was sister to Pinus), supporting the earlier suggestion that one can avoid LBA by judiciously increasing taxon sampling to break long branches (Chase et al. 1993
; Hillis 1996
; Graybeal 1998
; Soltis et al. 1998
; Qiu et al. 1999
; Qiu and Palmer 1999
).
The analyses presented here demonstrate that the gymnosperms were an appropriate outgroup with which to root the angiosperm phylogeny in our earlier multigene analyses (Qiu et al. 1999, 2000
) and that the ANITA rooting is likely free of the LBA effect. Several other multigene analyses reached similar conclusions on the identity of the earliest angiosperms (Parkinson, Adams, and Palmer 1999
; Soltis, Soltis, and Chase 1999
; Barkman et al. 2000
; Graham and Olmstead 2000
; Soltis et al. 2000
). It can be extrapolated that their use of gymnosperms as the outgroup did not violate any fundamental rule of choosing an appropriate outgroup. In retrospect, gymnosperms were well-behaved outgroups even in most single-gene analyses. Various members of the ANITA grade were placed at the base of angiosperm trees: Schisandraceae in nuclear rbcS (Martin and Dowd 1991
), Nymphaeales in nuclear rDNAs as well as plastid ITS and rDNA (Hamby and Zimmer 1992
; Goremykin et al. 1996
; Chaw et al. 1997
), and Austrobaileya-Illiciales and Amborella in nuclear 18S rDNA (Soltis et al. 1997
). Insufficient taxon sampling in all of these studies and the use of single genes (which obviously contain less signal than multigene data sets) naturally complicate the effort of building a well-resolved phylogeny and lead to the suspicion that these seemingly different rooting topologies were produced by LBA due to the great divergence between gymnosperms and angiosperms. Ironically, the only single-gene analyses that sampled basal angiosperms extensively produced a rooting that seems to be an analytical artifact, i.e., the Ceratophyllum rooting (Chase et al. 1993
; Qiu et al. 1993
). A reanalysis of the rbcL matrix used in our recent multigene analyses (Qiu et al. 1999, 2000
) shows that even the placement of Ceratophyllum as the sister to all other angiosperms was also largely due to the historical signal contained in the gymnosperm sequences. When the gymnosperm sequences were replaced with the artificial sequences and misaligned gymnosperm sequences used in this study, the angiosperm trees were rooted at various taxa that have branches longer than Ceratophyllum (data not shown). Ceratophyllum is likely an early-diverging lineage of angiosperms, even though its exact relationship to other major clades of basal angiosperms is not well resolved at present (Qiu et al. 1999, 2000
; Soltis, Soltis, and Chase 1999
; Mathews and Donoghue 2000
; Savolainen et al. 2000
; Soltis et al. 2000
). Thus, its placement at the base of angiosperm trees in the rbcL analyses was probably caused by both phylogenetic signal and a few homoplasious changes that happened to be shared with gymnosperms (not necessarily by LBA).
Reconstruction of phylogenetic relationships at the bases of major clades using molecular sequence data routinely generates controversial results (Qiu and Palmer 1999
; Adoutte et al. 2000
; Philippe, Germot, and Moreira 2000
), largely due to use of divergent outgroups and sparse taxon sampling. The LBA problem is frequently invoked to explain results that are otherwise inexplicable. Nevertheless, most claims of LBA have not been substantiated by explicit analyses. Several parsimony- or likelihood-based tests have been developed to examine whether long branches indeed attract each other and to reduce the LBA effect (Huelsenbeck 1997
; Lyons-Weiler and Hoelzer 1997
; Willson 1999
; Sanderson et al. 2000
). The strategy employed here follows the ideas of Miyamoto and Boyle (1989)
, Wheeler (1990)
, Maddison, Ruvolo, and Swofford (1992)
, Graham (1997)
, and Sullivan and Swofford (1997)
in using random sequences to evaluate whether phylogenetic signal in the outgroup has been randomized. We further elaborated this approach by increasing the repertoire of test sequences by using homo- and heteropolymers, misaligned original outgroup sequences, and more distantly related aligned outgroup sequences. In particular, this last category of outgroup sequences showed several increments of divergence levels and helped to define the point beyond which the outgroup was no longer appropriate for rooting the ingroup. As it becomes clear that sampling multiple genes from all two or three genomes of a large number of organisms can lead to reliable reconstruction of complicated organismal phylogenies (Hillis 1996
; Qiu et al. 1999, 2000
; Soltis, Soltis, and Chase 1999
; Savolainen et al. 2000
; Soltis et al. 2000
) and that the LBA problem is tractable thanks to the various strategies that are being developed, phylogenetic analyses of DNA sequences will undoubtedly, along with comparative genomics and evolutionary developmental biology, allow evolutionary biologists to tackle many of the issues in the tree of life.
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Acknowledgements |
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Footnotes |
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1 Abbreviations: ANITA, Amborella, Nymphaeales, and Illiciales-Trimeniaceae-Austrobaileya; LBA, long-branch attraction.
2 Keywords: Amborella
ANITA
basal angiosperms
long-branch attraction
outgroup
random sequences
3 Address for correspondence and reprints: Yin-Long Qiu, Department of Biology, University of Massachusetts, Amherst, Massachusetts 01003-5810. yqiu{at}bio.umass.edu
.
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References |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Adoutte A., G. Balavoine, N. Lartillot, O. Lespinet, B. Prud'homme, R. de Rosa, 2000 The new animal phylogeny: reliability and implications Proc. Natl. Acad. Sci. USA 97:4453-4456
Barkman T. J., G. Chenery, J. R. McNeal, J. Lyons-Weiler, W. J. Ellisens, G. Moore, A. D. Wolfe, C. W. dePamphilis, 2000 Independent and combined analyses of sequences from all three genomic compartments converge on the root of flowering plant phylogeny Proc. Natl. Acad. Sci. USA 97:13166-13171
Bowe L. M., C. W. dePamphilis, 1996 Effects of RNA editing and gene processing on phylogenetic reconstruction Mol. Biol. Evol 13:1159-1166[Abstract]
Carroll S. B., 1995 Homeotic genes and the evolution of arthropods and chordates Nature 376:479-485[ISI][Medline]
Chase M. W., D. E. Soltis, R. G. Olmstead, et al. (39 co-authors) 1993 Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL Ann. Mo. Bot. Gard 80:528-580
Chaw S.-M., A. Zharkikh, H.-M. Sung, T.-C. Lau, W.-H. Lee, 1997 Molecular phylogeny of extant gymnosperms and seed plant evolution: analysis of nuclear 18S rRNA sequences Mol. Biol. Evol 14:56-68[Abstract]
Dahlgren R., K. Bremer, 1985 Major clades of the angiosperms Cladistics 1:349-368
Davidson E. H., K. J. Peterson, R. A. Cameron, 1995 Origin of bilaterian body plans: evolution of developmental regulatory mechanisms Science 270:1319-1325[Abstract]
Donoghue M. J., 1994 Progress and prospects in reconstructing plant phylogeny Ann. Mo. Bot. Gard 81:405-418
Donoghue M. J., J. A. Doyle, 1989 Phylogenetic analysis of angiosperms and the relationships of Hamamelidae Pp. 1745 in P. R. Crane and S. Blackmore, eds. Evolution, systematics, and fossil history of the Hamamelidae. Vol. 1. Clarendon, Oxford, England
Donoghue M. J., S. Mathews, 1998 Duplicated genes and the root of angiosperms, with an example using phytochrome sequences Mol. Phylogenet. Evol 9:489-500[ISI][Medline]
Doyle J. A., M. J. Donoghue, E. A. Zimmer, 1994 Integration of morphological and ribosomal RNA data on the origin of angiosperms Ann. Mo. Bot. Gard 81:419-450
Doyle J. J., 1994 Evolution of a plant homeotic multigene family: toward connecting molecular systematics and molecular developmental genetics Syst. Biol 43:307-328[ISI]
Farris J. S., 1972 Estimating phylogenetic trees from distance matrices Am. Nat 106:645-668[ISI]
Felsenstein J., 1978 Cases in which parsimony and compatibility methods will be positively misleading Syst. Zool 27:401-410[ISI]
Frohlich M. W., E. M. Meyerowitz, 1997 The search for homeotic gene homologs in basal angiosperms and Gnetales: a potential new source of data on the evolutionary origin of flowers Int. J. Plant Sci 158:S131-S142[ISI]
Gogarten J. P., H. Kilbak, P. Dittrich, L. Taiz, E. J. Bowman, B. J. Bowman, M. F. Manolson, R. J. Poole, T. Date, T. Oshima, 1989 Evolution of vacuolar H+-ATPase: implications for the origin of eukaryotes Proc. Natl. Acad. Sci. USA 86:6661-6665[Abstract]
Goremykin V., V. Bobrova, J. Pahnke, A. Troitsky, A. Antonov, 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. Bio. Evol 13:383-396[Abstract]
Graham S. W., 1997 Phylogenetic analysis of breeding system evolution in heterostylous monocotyledons Ph.D. dissertation, University of Toronto, Toronto, Canada
Graham S. W., R. G. Olmstead, 2000 Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms Am. J. Bot 87:1712-1730
Graybeal A., 1998 Is it better to add taxa or characters to a difficult phylogenetic problem? Syst. Biol 47:9-17[ISI][Medline]
Hamby R. K., E. A. Zimmer, 1992 Ribosomal RNA as a phylogenetic tool in plant systematics Pp. 5091 in P. S. Soltis, D. E. Soltis, and J. J. Doyle, eds. Molecular systematics of plants. Chapman and Hall, New York
Hendy M. D., D. Penny, 1989 A framework for the quantitative study of evolutionary trees Syst. Zool 38:297-309[ISI]
Hillis D. M., 1996 Inferring complex phylogenies Nature 383:130-131[ISI][Medline]
Huelsenbeck J. P., 1997 Is the Felsenstein zone a fly trap? Syst. Biol 46:69-74[ISI][Medline]
Iwabe N., K.-I. Kuma, M. Hasegawa, S. Osawa, T. Miyata, 1989 Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes Proc. Natl. Acad. Sci. USA 86:9355-9359[Abstract]
Kellogg E. A., H. B. Shaffer, 1993 Model organisms in evolutionary studies Syst. Biol 42:409-414[ISI]
Les D. H., D. K. Garvin, C. F. Wimpee, 1991 Molecular evolutionary history of ancient aquatic angiosperms Proc. Natl. Acad. Sci. USA 88:10119-10123[Abstract]
Loconte H., D. W. Stevenson, 1991 Cladistics of the Magnoliidae Cladistics 7:267-296[ISI]
Lyons-Weiler J., G. A. Hoelzer, 1997 Escaping from the Felsenstein zone by detecting long branches in phylogenetic data Mol. Phylogenet. Evol 8:375-384[ISI][Medline]
Maddison D. R., M. Ruvolo, D. L. Swofford, 1992 Geographic origins of human mitochondrial DNA: phylogenetic evidence from control region sequences Syst. Biol 41:111-124[ISI]
Maddison W. P., M. J. Donoghue, D. R. Maddison, 1984 Outgroup analysis and parsimony Syst. Zool 33:83-103[ISI]
Manhart J. R., J. D. Palmer, 1990 The gain of two chloroplast tRNA introns marks the green algal ancestors of land plants Nature 345:268-270[ISI][Medline]
Martin P. G., J. M. Dowd, 1991 Studies of angiosperm phylogeny using protein sequences Ann. Mo. Bot. Gard 78:296-337
Mathews S., M. J. Donoghue, 1999 The root of angiosperm phylogeny inferred from duplicate phytochrome genes Science 286:947-950
. 2000 Basal angiosperm phylogeny inferred from duplicated phytochromes A and C Int. J. Plant Sci 161:S41-S55[ISI]
Miyamoto M. M., S. M. Boyle, 1989 The potential importance of mitochondrial DNA sequence data to eutherian mammal phylogeny Pp. 437450 in B. Fernholm, K. Bremer, and H. Joernvall, eds. The hierarchy of life. Elsevier, Amsterdam, the Netherlands
Nixon K. C., J. M. Carpenter, 1993 On outgroups Cladistics 9:413-426[ISI]
Parkinson C. L., K. L. Adams, J. D. Palmer, 1999 Multigene analyses identify the three earliest lineages of extant flowering plants Curr. Biol 9:1485-1488[ISI][Medline]
Philippe H., A. Germot, D. Moreira, 2000 The new phylogeny of eukaryotes Curr. Opin. Genet. Dev 10:596-601[ISI][Medline]
Qiu Y.-L., M. W. Chase, D. H. Les, C. R. Parks, 1993 Molecular phylogenetics of the Magnoliidae: cladistic analyses of nucleotide sequences of the plastid gene rbcL Ann. Mo. Bot. Gard 80:587-606
Qiu Y.-L., Y. Cho, J. C. Cox, J. D. Palmer, 1998 The gain of three mitochondrial introns identifies liverworts as the earliest land plants Nature 394:671-674[ISI][Medline]
Qiu Y.-L., J. Lee, F. Bernasconi-Quadroni, D. E. Soltis, P. S. Soltis, M. Zanis, E. A. Zimmer, Z. Chen, V. Savolainen, M. W. Chase, 1999 The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes Nature 402:404-407[ISI][Medline]
. 2000 Phylogeny of basal angiosperms: Analyses of five genes from three genomes Int. J. Plant Sci 161:S3-S27[ISI]
Qiu Y.-L., J. D. Palmer, 1999 Phylogeny of early land plants: insights from genes and genomes Trends Plant Sci 4:26-30[ISI][Medline]
Raff R. A., 1996 The shape of life University of Chicago Press, Chicago
Raubeson L. A., R. K. Jansen, 1992 Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants Science 255:1697-1699[ISI]
Sanderson M. J., M. F. Wojciechowski, J.-M. Hu, T. Sher Khan, S. G. Brady, 2000 Error, bias, and long-branch attraction in data for two chloroplast photosystem genes in seed plants Mol. Biol. Evol 17:782-797
SAS Institute. 2000 SAS 8.1 SAS Institute, Cary, N.C
Savolainen V., M. W. Chase, S. B. Hoot, C. M. Morton, D. E. Soltis, C. Bayer, M. F. Fay, A. Y. de Bruijn, S. Sullivan, Y.-L. Qiu, 2000 Phylogenetics of flowering plants based upon a combined analysis of plastid atpB and rbcL gene sequences Syst. Biol 49:306-362[ISI][Medline]
Shubin N., C. Tabin, S. Carroll, 1997 Fossils, genes, and the evolution of animal limbs Nature 388:639-648[ISI][Medline]
Sidall M. E., M. F. Whiting, 1999 Long branch abstraction Cladistics 15:9-24[ISI]
Soltis D. E., P. S. Soltis, M. W. Chase, et al. (16 co-authors) 2000 Angiosperm phylogeny inferred from 18S rDNA, rbcL and atpB sequences Bot. J. Linn. Soc 133:381-461[ISI]
Soltis D. E., P. S. Soltis, M. E. Mort, M. W. Chase, V. Savolainen, S. B. Hoot, C. M. Morton, 1998 Inferring complex phylogenies using parsimony: an empirical approach using three large DNA data sets for angiosperms Syst. Biol 47:32-42[ISI][Medline]
Soltis D. E., P. S. Soltis, D. L. Nickrent, et al. (16 co-authors) 1997 Angiosperm phylogeny inferred from 18S ribosomal DNA sequences Ann. Mo. Bot. Gard 84:1-49
Soltis P. S., D. E. Soltis, M. W. Chase, 1999 Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology Nature 402:402-404[ISI][Medline]
Steel M. A., P. J. Lockhart, D. Penny, 1993 Confidence in evolutionary trees from biological sequence data Nature 364:440-442[ISI][Medline]
Steinhauser S., S. Beckert, I. Capesius, O. Malek, V. Knoop, 1999 Plant mitochondrial RNA editing J. Mol. Evol 48:303-312[ISI][Medline]
Stevens P. F., 1980 Evolutionary polarity of character states Annu. Rev. Ecol. Syst 11:333-358[ISI]
Sullivan J., D. L. Swofford, 1997 Are guinea pigs rodents? The importance of adequate models in molecular phylogenetics J. Mamm. Evol 4:77-86
Swofford D. L., 1998 PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0b2 Sinauer, Sunderland, Mass
Taylor D. W., L. J. Hickey, 1992 Phylogenetic evidence for the herbaceous origin of angiosperms Plant Syst. Evol 180:137-156[ISI]
Theissen G., A. Becker, A. Di Rosa, A. Kanno, J. T. Kim, T. Muenster, K.-U. Winter, H. Saedler, 2000 A short history of MADS-box genes in plants Plant Mol. Biol 42:115-149[ISI][Medline]
Thompson J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, D. G. Higgins, 1997 The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res 24:4876-4882
Wheeler W. C., 1990 Nucleic acid sequence phylogeny and random outgroups Cladistics 6:363-367[ISI]
Willson S. J., 1999 A higher order parsimony method to reduce long-branch attraction Mol. Biol. Evol 16:694-705
Yoshinaga K., H. Iinuma, T. Masuzawa, K. Ueda, 1996 Extensive RNA editing of U to C in addition to C to U substitution in the rbcL transcripts of hornwort chloroplasts and the origin of RNA editing in green plants Nucleic Acids Res 24:1008-1014