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Systematics |
2Department of Biology, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061 USA; 3Botanisches Institut, Friedrich-Wilhelms-Universität Bonn, Meckenheimer Allee 170, 53115 Bonn, Germany; 4School of Biological Sciences, Washington State University, Pullman, Washington 99164 USA; 5Florida Museum of Natural History and the Genetics Institute, University of Florida, Gainesville, Florida 32611 USA; 6Molecular Systematics Section, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK; 7Department of Biology, Western Kentucky University, Bowling Green, Kentucky 42101 USA; 8Biology Department, Acadia University, 24 University Avenue, Wolfville, Nova Scotia, Box 1X0, Canada; 9Muséum National d'Histoire Naturelle, 16, rue Buffon, 75005 Paris, France; 10Institut für Botanik, Zellescher Weg 22, 01062 Dresden, Germany; 11Institut für Allgemeine Botanik, Universität Hamburg, Ohnhorststr. 18, 22609 Hamburg, Germany; 12Department of Biological Sciences, University of Maine, Orono, Maine 04469-5722 USA;and 13National Herbarium of the Netherlands, Utrecht University Branch, Heidelberglaan 2, 3584 CS Utrecht, Netherlands
Received for publication March 27, 2003. Accepted for publication July 3, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPROSPECTS OF USING MATK...LITERATURE CITED |
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Key Words: angiosperms • Bayesian inference • matK • phylogeny • systematics
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPROSPECTS OF USING MATK...LITERATURE CITED |
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; Takhtajan, 1987
; Cronquist, 1988
; Thorne, 1992
). Consequently, the overall phylogeny of angiosperms has been radically revised at all levels. Some subclasses, such as Dilleniidae and Hamamelidae, have been shown to be polyphyletic with their constituent families now placed (APG, 1998
; APG II, 2003
) in several distantly related clades. The composition of other groups has also been altered to varying degrees, e.g., Rosidae, Asteridae, Ericales, Cornales, and Saxifragales. Contributions toward this reassessment of angiosperm phylogeny have come primarily from large data sets of individual genes or combined analyses of these data sets (e.g., Chase et al., 1993
; Qiu et al., 1998
, 1999
, 2000
; Hoot et al., 1999
; Soltis et al., 1999
, 2000
, 2003
; Olmstead et al., 2000
; Savolainen et al., 2000a
, b
; Zanis et al., 2002
). In addition, extensive analyses of morphological, anatomical, and phytochemical characters from across angiosperm families (Nandi et al., 1998
) have also contributed to modern views of angiosperm relationships. Consequently, a new concept for the overall phylogeny of flowering plants has emerged, depicting a basal grade of Amborellaceae, Nymphaeaceae (sensu APG II, 2003
), and Austrobaileyales, followed by eumagnoliids (sensu APG II, 2003
, to include Canellales, Laurales, Magnoliales, and Piperales), monocots, Ceratophyllales, Chloranthaceae, and eudicots. However, a number of questions remain unanswered due to variable or unresolved positions and weak support for various lineages. This situation is particularly true for the eudicots, which constitute about 75% of angiosperm species diversity (Drinnan et al., 1994
). Among eudicots, the basal grade lacks convincing bootstrap (BS)/jackknife (JK) support (Qiu et al., 1998
; Hoot et al., 1999
; Savolainen et al., 2000a
, b
; Soltis et al., 2000
, 2003
). Moreover, relationships among the major clades of core eudicots (i.e., Berberidopsidaceae/Aextoxicaceae, Saxifragales, Caryophyllales, rosids, asterids, and Santalales) remain uncertain (Hoot et al., 1999
; Savolainen et al., 2000a
, b
; Soltis et al., 2000
, 2003
). Phylogenetic relationships among rosids also remain unclear (Savolainen et al., 2000a
; Soltis et al., 2000
, 2003
). For basal angiosperms, there are still questions concerning the position of eumagnoliids, monocots, Ceratophyllaceae, and Chloranthaceae. In addition, alternative hypotheses, albeit with weak support, for the position of Amborella as sister to all other angiosperms have emerged, depicting waterlilies alone or along with Amborella in that position (Parkinson et al., 1999
; Barkman et al., 2000
; Graham and Olmstead, 2000
; Mathews and Donoghue, 2000
; Zanis et al., 2002
). Resolving relationships among these groups is not only essential for a comprehensive systematic treatment of angiosperms, but also for understanding patterns of species diversification and character evolution.
Angiosperm phylogenetic studies based on individual genes have faced two difficulties: limited resolution and low internal support for major clades and topological incongruence (Olmstead and Sweere, 1994
; Soltis et al., 1997
, 2000
, 2003
; Mathews and Donoghue, 1999
, 2000
; Savolainen et al., 2000a
). Combining data sets in multigene analyses improved resolution and internal support (Soltis et al., 2000
, 2003
; Parkinson et al., 1999
; Graham and Olmstead, 2000
; Qiu et al., 2000
; Savolainen et al., 2000a
, b
; Zanis et al., 2002
; Sauquet et al., 2003
). Combined analyses of genes from different subcellular compartments are considered to be a good method to estimate organismal phylogeny (e.g., Donoghue and Sanderson, 1992
; Hillis, 1996
, 1998
; Kim, 1998
), a view supported by empirical studies (Qiu et al., 1999
, 2000
; Soltis et al., 2000,
2003
; Zanis et al., 2002
). Consequently, the consensus tree based on combined rbcL, atpB, and 18S rDNA sequences of Soltis et al. (2000
; henceforth referred to as the three-gene analysis) may be considered the most reliable overall angiosperm phylogeny so far available.
In the majority of broad angiosperm phylogenetic studies, authors have emphasized using sequence information from slowly evolving genes based on the notion that the number of multiple hits and levels of homoplasy are expected to be relatively low (Farris, 1977
; Swofford et al., 1996
; Olmstead et al., 1998
; Graham et al., 2000
). However, use of slowly evolving genomic regions can result in severe limitations in taxon sampling due to need for sequencing a large number of nucleotides per species to obtain sufficient number of variable characters. Consequently, it restricts the number of taxa that can reasonably be sequenced and analyzed cladistically, introducing a new set of phylogenetic problems as pointed out in several recent studies (e.g., Graybeal, 1998
; Rannala et al., 1998
; Pollock et al., 2002
). For example, Graham and Olmstead (2000)
sequenced 13.4 kilobases (kb) of slowly evolving cpDNA genes, but as a result could only include 19 taxa in a study of basal angiosperms. This raises the problem of taxon density, an issue addressed by several authors (e.g., Graybeal, 1998
; Hillis, 1998
; Bremer et al., 1999
; Zwickl and Hillis, 2002
). Therefore, genomic regions that can provide sufficient signal in deep level phylogeny reconstruction without compromising taxon representation are essential for accurate assessment of evolutionary histories. The rapidly evolving matK gene satisfies these prerequisites.
The matK gene is 
1600 base pairs (bp) in most angiosperms, located within the trnK intron, and functionally may be involved in splicing group II introns coding for tRNALys (UUU; Neuhaus and Link, 1987
; Ems et al., 1995
). Believed to code for a maturase based on structural similarities to other such genes (Neuhaus and Link, 1987
; Mohr et al., 1993
), matK is the only maturase of higher plant plastids (Vogel et al., 1997
). The trnK intron, including the matK exon, is transcribed in one piece (Chiba et al., 1996
) and is expressed at the protein level in Solanum (Du Jardin et al., 1994
). The matK open reading frame (ORF) is maintained intact except at the 3' end where frameshift substitutions slightly alter the length with apparently minimal impact on function (Hilu and Alice, 1999
). These data and the analysis of the RNA-binding activity of a trnK-encoded polypeptide from Sinapis (Liere and Link, 1995
) further support a matK function in splicing group II introns. The presence of matK as a free-standing ORF in the plastid genome of the parasitic Epifagus virginiana (Ems et al., 1995
), which has lost 65% of its genes (Wolfe et al., 1992
), also points to the functional significance of matK.
The matK gene stands out among genes used in angiosperm systematics in its substantially greater number of: (1) nucleotide substitutions, (2) nonsynonymous mutations, and (3) insertion/deletion events or indels (Johnson and Soltis, 1994
, 1995
; Olmstead and Palmer, 1994
; Hilu and Liang, 1997
; Soltis and Soltis, 1998
; K. W. Hilu, K. Müller, and T. Borsch, unpublished data). The gene also exhibits a relatively high proportion of transversions, with the transition/transversion ratio (ti/tv) approaching unity (Olmstead and Palmer, 1994
; Hilu and Liang, 1997
). The percentage amino acid substitution for matK between the monocot rice and the eudicot tobacco is up to sixfold higher than for rbcL and atpB (41% vs. 7–8%; Olmstead and Palmer, 1994
). Among-site rate variability for the three codon positions shows that matK is not skewed toward the third position as is the case in most protein-coding genes used in angiosperm systematics. Substitution rates in the first and second codon positions in matK approach those of the third position (Johnson and Soltis, 1994
, 1995
; Hilu and Liang, 1997
; Hilu et al., 1999
), a situation that elevates the rate of nonsynonymous changes. These data point to either a low correlation between structure and function with a rather small core being functionally important (e.g., domain X; Mohr et al., 1993
; Hilu and Liang, 1997
), or that the enzyme's function as a maturase might require a particular stereochemistry in which the actual amino acid sequence is of reduced importance. Therefore, matK has evolutionary patterns and tempo that distinguish it from most genes used in angiosperm phylogeny reconstruction (Olmstead and Palmer, 1994
; Hilu and Liang, 1997
).
Some of these attributes of matK may have discouraged researchers from using matK sequences in broad studies such as overall angiosperm relationships. Another reason for infrequent use of matK at broad levels may be that taxon-specific primers are usually required. The location of matK within the trnK intron and its close proximity to psbA provide nearly universal primers for its amplification, and the need to design primers for sequencing is counterbalanced by the quality of the data provided. Effective sequencing strategies for matK are discussed in Materials and Methods.
This analysis provides an angiosperm tree based on the largest data set so far compiled for matK. We compare the topology obtained with this gene to previously published topologies based on single gene and multigene data sets. We also examine patterns of variability in matK. A parsimony approach has been chosen for data analysis to allow for direct comparison with the three-gene analysis of Soltis et al. (2000)
. We evaluated the effect of including Gnetales as an outgroup on the topology; the angiosperms and Gnetales represent the two most divergent groups of seed plants (e.g., Bowe et al., 2000
). In addition, a Bayesian analysis (Huelsenbeck and Ronquist, 2001
; Huelsenbeck et al., 2002
) was performed.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPROSPECTS OF USING MATK...LITERATURE CITED |
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and 12 gymnosperm genera (Appendix 1; see Supplemental Data accompanying the online version of this article). Large families are represented wherever possible by more than one genus. A large proportion of the matK sequences was generated specifically for this study, and additional sequences were taken from GenBank (Appendix 1).
DNA isolation, polymerase chain reaction (PCR) amplification, and sequencing
Total cellular DNA was isolated from fresh, silica-dried, or herbarium specimens using the hexadecyltrimethylammonium bromide (CTAB) procedure of Doyle and Doyle (1987)
or its modification (Borsch et al., 2003
). Because a large number of the sequences available cover a region from around position 400 through the stop codon of matK, this region (1200 bp) became the focus of this study to avoid potential problems associated with large amounts of missing data. For gene amplification, either the entire trnK intron was amplified using primers trnK3914F and trnK2R (Johnson and Soltis, 1995
) or, in most cases, the 3'-two-thirds of the trnK intron was amplified with a forward primer located approximately 480 bp into the coding region and trnK2R (for information on primers see Appendix 2 in Supplemental Data accompanying the online version of this article). By amplifying this region, the PCR primers could also be used for sequencing because primer annealing was guaranteed within the otherwise rather variable coding region of matK. Primer NYmatK480F (Borsch et al., 2003
), originally designed for Nymphaea, turned out to be useful for many angiosperms. For highly divergent taxa, such as Gnetum and Welwitschia, the whole trnK intron was amplified and sequenced first with the amplification primers; specific internal sequencing primers were subsequently designed by "walking" into the region. For some taxa, internal primers 390F and 1326R were used (Johnson and Soltis, 1994
, 1995
). Cycle sequencing was performed using a Big Dye Terminator Cycle Sequencing Ready Reaction Kit (Applied Biosystems, Foster City, California, USA), and extension products were electrophoresed on ABI 310, 373, and 377 automated sequencers (Applied Biosystems).
Sequence alignment and phylogenetic analysis
Sequences were aligned using QuickAlign (Müller, 2003
) or ClustalX (Thompson et al., 1997
) followed by manual adjustments. All sequences were translated into amino acids and their ORFs checked. Several in-frame gaps were inserted to align the sequences. Frame-shift mutations near the stop codon formed a mutational hot spot 15 bp upstream of the stop codon; this section was excluded from the analysis. Due to differences in amplification procedures used by the collaborators, the sequences of some taxa lack ca. 200 bp at the 3' end of the matK gene.
All aligned positions were given equal weight, and gaps were treated as missing data. Parsimony analyses were conducted using PAUP* 4.0b6 (Swofford, 2001
) and PRAT (Müller, 2002
). PRAT is a program written for this study; it generates command files that execute parsimony ratchet searches (Nixon, 1999
) using PAUP*. Program options include random addition cycles of the ratchet and parsimony jackknifing, applying the ratchet in each replicate. In this study, 10 random addition cycles of 150 ratchet iterations each were used. Each iteration is comprised of two rounds of tree-bisection-reconnection (TBR) swapping, one on a randomly reweighted data set and the other on the original matrix, saving one minimum-length tree. Random upweighting affected 25% of the positions. Because each random addition cycle soon converged on the same tree score, cycles were not extended beyond 150 iterations and further cycles were not added. Shortest trees collected from the different tree islands were subjected to a final TBR swapping with 5000 saved trees, from which a strict consensus tree was computed. To estimate internal support, parsimony jackknifing with 500 cycles was carried out according to the approach and parameters suggested by Farris et al. (1996)
for large data sets, with TBR swapping on five saved trees per cycle. The deleted fraction of characters was e–1, which means that bootstrap frequencies agree with jackknife frequencies (Farris et al., 1996
). This allows us to compare jackknife support values obtained here with bootstrap values reported in other studies. We also compare jackknife values from studies that used the same deletion percentage, e.g., by employing the program JAC (J. S. Farris, unpublished program). Two searches were performed on the matK data set; one on a matrix that included Gnetales among the outgroup taxa (matrix A) and the other on a matrix that excluded this order (matrix B). The second analysis was performed to evaluate the potential effects of Gnetales on the analysis.
Bayesian inference used the program MrBayes (Huelsenbeck and Ronquist, 2001
). Calculations of likelihood were based on a general time reversible model of nucleotide substitution, assuming different stationary nucleotide frequencies and site-specific rate categories for each codon position. The posterior probability (PP) was estimated by sampling trees from the PP distribution, using Metropolis-coupled Markov chain Monte Carlo simulations. Four chains were run for 500 000 generations, starting with one of the shortest trees found with the parsimony ratchet, and the temperature of heated chains was set to 0.2. Chains were sampled every 10 generations. Likelihood scores converged on a stable value after generation 100 000 (the "burn in" of the chain), and calculations of PP were based upon the trees sampled after this generation.
Number of steps and consistency, retention, and rescaled consistency indices (CI, RI, and RC, respectively;) (Kluge and Farris, 1969
; Farris, 1989
) for the three codon positions of matK were calculated with PAUP*. Lists of steps for each codon position were subjected to the nonparametric Mann-Whitney U test to evaluate differences in nucleotide substitutions at these positions. Because the underlying sample distribution is largely unknown, no parametric test was applied.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPROSPECTS OF USING MATK...LITERATURE CITED |
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1200-bp sequenced region of matK resulted in 1749 aligned characters due to the insertion of gaps. Except for the 15-bp region upstream of the stop codon, all indels occurred in multiples of three nucleotides (up to 9 bp in length). Three genera in Caryophyllales (Anredera-Basellaceae, Halophytum-Halophytaceae, and Rhipsalis-Cactaceae) had an inversion 6–24 bp in length. Due to its location in a palindromic region, the actual size of the inversion could not be determined. Inversions are often associated with such palindromic motifs (see Graham et al., 2000
; Kelchner, 2000
). Of the aligned characters, 1221 (70%) are variable and 1083 (62%) are potentially parsimony-informative (based on matrix A). The distribution of variable sites among codon positions is 414, 386, and 421 for the first, second, and third codon positions, respectively. The overall nucleotide p distance is 0.216 and translates into an amino acid p distance of 0.339 using MEGA (Kumar et al., 2001
). Thus, amino acid variation in matK is higher than nucleotide variability. The p distance at synonymous sites is 0.351, which is twice as high as the p distance at nonsynonymous sites (0.176). Based on unambiguous transitions and transversions traced on a single tree from matrix A, the ti/tv ratio in matK is 1.275. According to Holmquist (1983)
, a ratio of 0.4 and below is an indication of highly saturated sequences, a ratio that is certainly not reached here. However, saturation is a complex issue, and its magnitude may differ depending on nucleotide and codon positions along a genomic region; a more complete analysis will be presented elsewhere. Nevertheless, the ratio obtained in this analysis does not point towards a high level of saturation in matK. Base substitutions are fairly evenly distributed across the length of matK (Fig. 1). The low nucleotide variability depicted for the end of the sequenced region corresponds in part to the conserved domain X (Mohr et al., 1993
; Hilu and Liang, 1997
). However, this decrease in variability may be accentuated by the amount of missing data at the end (see Material and Methods).
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reported a CI of 0.12 for their combined three-gene data set (567 taxa) compared to a CI of 0.14 here (374 taxa).
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, Källersjö et al. (1999)
, Savolainen et al. (2000a)
, and others and are correlated with the number of informative sites at the different positions (66% in third vs. 62% and 57% in first and second positions). In addition, levels of homoplasy (CI, Table 1) are not on average higher in 3rd codon positions than in first and second positions. Therefore, differences in numbers of steps, variable sites, and phylogenetic structure are not as high among codon positions in matK as they are in more conserved genes such as rbcL (Källersjö et al., 1999
; K. W. Hilu, K. Müller, and T. Borsch, unpublished data).
Analyses of matrices A and B result in consensus trees with identical topologies, although jackknife support for the basal nodes increases when Gnetales are excluded (Fig. 2). The Bayesian analysis produced a tree that is similar in topology to the MP tree (Fig. 3). Noteworthy differences in the Bayesian tree compared to the parsimony tree are the sister group relationship of Amborella + Nymphaeaceae to the remaining angiosperms in the former, though support is low (0.42 PP), and the positions of Canellales/Piperales and Saxifragales (Figs. 2, 3). The discussion is based on the MP matrix A; results from both matrix B and Bayesian analysis will be contrasted only when relevant. Bootstrap and/or jackknife support of 50–74% is considered low, 75–84% moderate, and >85% high (Chase et al., 2000
). Posterior probabilities for nodes in the Bayesian tree are interpreted as reliable when above 0.95. In cases for which considerable differences exist in JK percentages between matrices A and B, both percentages are reported as A/B.
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. Monocots are (85/99%) sister to Chloranthus (74/81%). A weakly supported eumagnoliid clade (58/56%) consists of Piperales + Canellales (56/61%) and Laurales + Magnoliales (58%). Ceratophyllum is sister to eudicots (71%). The eumagnoliids, monocots + Chloranthaceae, and Ceratophyllum + eudicots diverge after the Austrobaileyales and their relationships are unresolved in the strict consensus tree. Eudicots are strongly supported (96%) and include a basal grade of Ranunculales, Sabiaceae, Proteales, Trochodendraceae, and Buxaceae (including Didymelaceae; APG II, 2003
) that are subsequent sister to the core eudicots. The sister group relationship of Ranunculales to the remaining eudicots and Buxaceae to the core eudicots receive the highest support yet (82% and 91%, respectively). Within the core eudicots, Gunnerales are sister to a trichotomy of Saxifragales, rosids, and a clade comprising Dilleniaceae + Vitaceae, Berberidopsidaceae + Aextoxicaceae, Santalales, and Caryophyllales + asterids. Internal support is low for many core eudicot lineages. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPROSPECTS OF USING MATK...LITERATURE CITED |
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; Qiu et al., 1999
, 2000
; Mathews and Donoghue, 2000
; Zanis et al., 2002
; Borsch et al., 2003
). Most recent phylogenetic analyses of angiosperms, including this study, have converged on a basal assemblage of lineages characterized by monosulcate or monosulcate-derived pollen. This is in contrast to the eudicots, a group that comprises the remaining angiosperms defined by their triaperturate or triaperturate-derived pollen. Amborellaceae, Nymphaeaceae, and Austrobaileyales have emerged with strong support as successive sisters to other angiosperms (Figs. 2–3). In contrast, relationships among eumagnoliids, monocots, Chloranthaceae, and Ceratophyllaceae remain uncertain.
The position of Ceratophyllum has varied in previous analyses from sister to all angiosperms, monocots, Chloranthaceae, eudicots, or in an unresolved position (Chase et al., 1993
; Qiu et al., 2000
; Savolainen et al., 2000a
; Zanis et al., 2002
). Similarly, Chloranthaceae has appeared as sister to either monocots or eudicots or in an unresolved position with other lineages (Chase et al., 1993
; Mathews and Donoghue, 1999
; Graham and Olmstead, 2000
; Savolainen et al., 2000a
; Soltis et al., 2000
; Zanis et al., 2002
). Increased number of characters has not enhanced our understanding of relationships among these lineages. The eumagnoliids, monocots, Ceratophyllum, and Chloranthaceae were unresolved in the five-gene study of Qiu et al. (2000)
. The combined 11-gene data set (Zanis et al., 2002
) showed Ceratophyllum + monocots diverging after Illiciales (= Austrobaileyales), followed by Chloranthaceae, but with only 52% BS as sister to a clade comprising eumagnoliids + eudicots. A recent analysis of combined sequence data for basal angiosperms from the relatively fast-evolving noncoding trnT-trnF plus matK (K. W. Hilu, K. Müller, and T. Borsch, unpublished data) shows 99–100% JK support for the Amborellaceae, Nymphaeaceae, and Austrobaileyales grade, but weak support for the relationships among the rest. Therefore, resolving the relationships among these enigmatic lineages remains one of the major challenges in angiosperm phylogenetics.
Amborellaceae, Nymphaeaceae, and Austrobaileyales
A general consensus exists on the branching pattern of these three most basal nodes (Parkinson et al., 1999
; Qiu et al., 1999
, 2000
; Soltis et al., 1999
, 2000
; Mathews and Donoghue, 2000
; Zanis et al., 2002
; Borsch et al., 2003
). Nevertheless, alternative relationships depicting Nymphaeaceae alone or Amborella + Nymphaeaceae as sister to the rest have been recovered by some methods of analysis (Parkinson et al., 1999
; Barkman et al., 2000
; Graham and Olmstead, 2000
; Qiu et al., 2000
; Zanis et al., 2002
). The position of Amborella as the first branching angiosperm is supported here with 69% JK value in MP (matrix A, Fig. 4). Exclusion of Gnetales from the outgroup (matrix B) increases support for this node to 86%, comparable to analyses based on five genes (Qiu et al., 1999
, 2000
) and 11 genes (Zanis et al., 2002
). Similar JK results were obtained for the Nymphaeaceae as successive sister to the rest (Fig. 2). The three-gene analysis of Soltis et al. (2000)
provided only moderate jackknife support for the same topology. The jackknife support achieved by matK is substantial considering that the number of variable characters in this matK data set is less than one quarter of those analyzed in the three-gene matrix. Among other individual genes, only 18S rDNA (Soltis et al., 2000
; <50% JK), atpB (Savolainen et al., 2000a
; <50% BS), and trnT-trnF (Borsch et al., 2003
; 94–100% JK) identify Amborella and Nymphaeaceae in these positions.
In contrast with the MP topology, BI places Amborella + Nymphaeaceae as sister to all other angiosperms, although support for this clade is very low (0.42 PP, Fig. 3). The meaning of such a low posterior probability is particularly dubious given the recent simulations of Suzuki et al. (2002)
. Kishino-Hasegawa tests (Kishino and Hasegawa, 1989
) carried out by Parkinson et al. (1999)
and Qiu et al. (2000)
on other matrices of combined genes could not reject this position for Amborella + Nymphaeaceae. Neighbor-joining analyses of the six- and nine-gene matrices (Barkman et al., 2000
) in which "noisy" positions were removed with relative apparent synapomorphy analysis (RASA; Lyons-Weiler et al., 1996
) provided high bootstrap support value for an Amborella + Nymphaeaceae clade. However, recent studies suggest that RASA introduces errors when used in removing noisy sites (Farris, 2002
; Simmons et al., 2002
). Analyses of an expanded 11-gene data set (Zanis et al., 2002
) showed high bootstrap and posterior probabilities for Amborella as sister to all other angiosperms, whereas Amborella + Nymphaeaceae as sister to all other angiosperms could be rejected in two of the three tests. The matK data favor the hypothesis that Amborella is sister to all other angiosperms.
Eumagnoliids
As recognized by APG II (2003)
, eumagnoliids include Canellales, Laurales, Magnoliales, and Piperales. Evidence from matK is in line with combined multigene analyses (Graham and Olmstead, 2000
; Qiu et al., 2000
; Zanis et al., 2002
), the strict consensus trees based on analyses of phyA + phyC (Mathews and Donoghue, 2000
), and trnT-trnF sequences (Borsch et al., 2003
) in supporting this definition of eumagnoliids.
Savolainen et al. (2000a)
and Soltis et al. (2000)
recognized the magnoliids to include Chloranthaceae and monocots in addition to these four orders but with low support; we will refer to this clade here as eumagnoliids sensu lato (s.l.). Although the MP analysis of matK shows monocots + Chloranthaceae as an unresolved lineage with eumagnoliids and Ceratophyllum + eudicots (Fig. 4), the Bayesian analysis (Fig. 3) recovers eumagnoliids s.l. with low probability (0.73), encompassing monocots + Chloranthaceae (<0.5 PP) and eumagnoliids (1.0 PP). Eumagnoliids s.l. was also recovered with similar topology in a combined matK + trnT-trnF data analysis, but with <50% JK support (K. W. Hilu, K. Müller, and T. Borsch, unpublished data). Whereas stronger evidence points to the composition of eumagnoliids to include only the Laurales-Magnoliales-Canellales-Piperales, the hypothesis of an expanded eumagnoliids to include monocots and Chloranthaceae cannot be disregarded. Accepting the hypothesis of a eumagnoliid s.l. clade implies that carpel evolution in Chloranthaceae is secondarily ascidiate as pointed out by Doyle and Endress (2000)
and Endress and Igersheim (2000)
.
Although MP support for the Magnoliales and Laurales sister group relationship was weak (58/56% JK), the Bayesian approach infers the same node but with 0.96 PP. This relationship has been inferred from a number of molecular data sets (Mathews and Donoghue, 1999
, 2000
; Qiu et al., 1999
, 2000
; Barkman et al., 2000
; Graham and Olmstead, 2000
; Graham et al., 2000
; Zanis et al., 2002
; Borsch et al., 2003
). In addition, Sauquet et al. (2003)
found particularly good support for this relationship from parsimony analysis of molecular and combined molecular and morphological data (decay index 14 and 17, BS 99%) based on unrooted trees in which all four orders were represented. However, support for this relationship from morphological data alone has been either lacking (Doyle and Endress, 2000
) or weak (Sauquet et al., 2003
). The internal structure of Magnoliales inferred from matK differs from the multigene-based results of Sauquet et al. (2003)
in the arrangement of the five families above Myristicaceae; however, this inconsistency is not well supported (JK 
51%) and may be explained by extremely short branches. The internal structure of Laurales based on matK is congruent with the minimum evolution tree in Renner and Chanderbali (2000)
, but not with the trees retrieved using MP in the same study or in Renner (1999)
.
The MP analysis shows a Piperales + Canellales relationship, but with low support. However, Bayesian analysis (Fig. 3) depicts Piperales as sister to Canellales (74% PP) and Laurales + Magnoliales. The sister group relationship of Piperales to Canellales is consistent with other molecular analyses (Graham and Olmstead, 2000
; Mathews and Donoghue, 2000
; Qiu et al., 2000
; Zanis et al., 2002
; Borsch et al., 2003
). The internal structure of Piperales in the matK tree shows Aristolochiaceae paraphyletic to Lactoridaceae and Saururaceae-Piperaceae in both parsimony (Fig. 4) and Bayesian approaches (tree not shown). A similar situation also occurred in analysis of atpB (Savolainen et al., 2000a
). Phylogeny reconstruction in Piperales is complicated by the presence of several long branches. Results of higher sampling density using sequences of the complete trnK intron and other genomic regions are congruent with those of matK in showing a Piperaceae + Saururaceae clade sister to an Aristolochiaceae + Lactoridaceae clade (S. Wanke, University of Bonn, personal communication).
Monocots
The matK sequences provide good support (85% JK, Fig. 5) for the monophyly of monocots, with Acorus followed by Alismatales as sisters to other monocots. Individual gene analyses, such as rbcL and atpB (Chase et al., 1993
, 1995
; Savolainen et al., 2000a
) and 18S (Soltis et al., 1997
), have indicated such a topology but with low or <50% support. Support for these relationships with matK is comparable to data sets that combined three or more genes (Table 2; Chase et al., 2000
; Soltis et al., 2000
; Zanis et al., 2002
). The circumscription and internal structure of most monocot orders, particularly Liliales and Dioscoreales, revealed by matK is congruent with those suggested by the three-gene analysis, with similar or higher JK/PP support (Figs. 5–6).
|
|
|
, b
, with atpB alone), sister to remaining monocots (Soltis et al., 2000
), or placed within Alismatales (Qiu et al., 2000
); monocot sampling was sparse in both studies and support in both cases was weak or lacking. Compared to three-gene analyses (Chase et al., 2000
; Soltis et al., 2000
), matK provides better support for the Alismatales as sister to the commelinoid/lilioid clades (88% vs. 78% JK) and for the monophyly of the Alismatales (92% vs. 75% JK).
Following Alismatales, the matK consensus tree depicts (53% JK; Fig. 5) Dioscoreales and Pandanales (lilioids) in a clade sister to remaining monocots that appear in a polytomy of two commelinoid lineages (Arecales + Zingiberales and Poales) and the two remaining lilioid clades (Liliales and Asparagales). Clarification of the phylogenetic relationships among the lilioid orders Asparagales, Dioscoreales, Liliales, and Pandanales, as well as within the commelinoids (Poales, Commelinales, Zingiberales, and Arecales), has been a major problem because previous molecular studies, including the detailed three-gene analysis of monocots (Chase et al., 2000
), did not yield topologies with high internal support. The emergence in the MP analysis of a Dioscoreales + Pandanales clade (53% JK; Fig. 5) as sister to the remaining lilioid and commelinoid lineages is supported by 1.0 PP in the BI analysis (Fig. 6). Therefore, matK data also indicate paraphyly of the lilioids to the commelinoids, a hypothesis that requires further evaluation. Significantly, Liliales and most Asparagales uniquely share a particular type of epicuticular wax (parallel platelets; Barthlott et al., 2003
). The commelinoids do not form a clade in the MP analysis of the matK data. In contrast, this lineage was resolved with 1.0 PP in the Bayesian tree (Fig. 6), in line with the three-gene analyses of Chase et al. (2000)
and Soltis et al. (2000)
that resolved this group with weak support. The sister group relationship between Commelinales and Zingiberales as inferred earlier by the three-gene studies with moderate support is well supported with matK sequences (89% JK, 1.0 PP). Moreover, matK places Arecales as sister group to the Commelinales-Zingiberales clade (Figs. 5, 6; <50% MP, 0.88 BI).
Chase et al. (1995
, 2000)
defined Asparagales in a broad sense to include the astelioids, Boryaceae and Orchidaceae. However, the combined rbcL, atpB, and 18S rDNA analyses of Soltis et al. (2000)
and Chase et al. (2000)
only recovered the core Asparagales (sensu Chase et al., 1995
) as a monophyletic group with high support. Hypoxidaceae, Asteliaceae, Boryaceae, Blandfordiaceae, and Orchidaceae appeared in their strict consensus tree as unresolved at the base of the Asparagales s.l. clade. The matK study recovers core Asparagales (Ixoliriaceae to Convallariaceae, Figs. 5, 6) with better support (99% JK, 1.0 PP). At the base of Asparagales, two clades, Boryaceae + Orchidaceae and Blandfordiaceae + Asteliaceae + Lanariaceae + Hypoxidaceae (the latter group was termed the astelioid clade by Fay et al., 2000
; Fig. 5) were found successive sisters to the rest in MP but with <50% JK support (annotated as lower Asparagales in Fig. 5). This topology is identical to the one inferred from the second search of the three-gene data set by Chase et al. (2000)
, although none of the relevant nodes received good support. The matK places Boryaceae as sister to Orchidaceae in the MP tree with <50% JK and shows it nested within the astelioid clade in the Bayesian tree with high PP (the sucessive branching order is Blandfordia, Borya, Astelia, and Rhodohypoxis plus Lanaria; all nodes receive 1.0 PP; details are not shown in Fig. 6). The orchids appear as sister to the commelinoids in the Bayesian tree (Fig. 6). A recent combined rbcL + atpB + trnL-F parsimony analysis of Asparagales (Fay et al., 2000
) showed Boryaceae sister to the astelioid clade, which are in turn sister to the core Asparagales. Orchidaceae appear basal in the latter analysis, but none of these basal nodes within lower Asparagales are well supported. As a result, the order of the first branches within the Asparagales and their broader circumscription to include the orchids are still in need of further testing.
Eudicots
The eudicots include over 200 000 species and comprise about 75% of all angiosperm species (Drinnan et al., 1994
). This clade has consistently been recovered in all recent single-gene and multiple-gene phylogenetic analyses of angiosperms (e.g., Chase et al., 1993
; Hoot et al., 1999
; Barkman et al., 2000
; Graham and Olmstead, 2000
; Mathews and Donoghue, 2000
; Qiu et al., 2000
; Savolainen et al., 2000a
, b
; Borsch et al., 2003
; Soltis et al., 2003
) and in nonmolecular phylogenetic analyses (Drinnan et al., 1994
; Nandi et al., 1998
). The strong support (100%) for eudicot monophyly achieved by combining genes from several genomes is corroborated by matK (Figs. 2, 3). The eudicot clade encompasses a basal grade and a strongly supported core clade that includes the large rosid and asterid clades and the smaller Gunnerales, Caryophyllales, Santalales, Berberidopsidaceae/Aextoxicaceae, and Saxifragales clades. Eudicots have tricolpate or tricolpate-derived pollen (e.g., tricolporate, pantoporate; e.g., Nandi et al., 1998
). Morphologically similar pollen having three apertures in Austrobaileyales have been identified as trisyncolpate (Takahashi, 1994
), but these are apparently convergent.
Early-diverging eudicots
The same lineages of early-diverging eudicots (Ranunculales, Proteales, Sabiaceae, Trochodendraceae including Tetracentron, and Buxaceae including Didymelaceae) have been consistently recovered (e.g., Chase et al., 1993
; Soltis et al., 1997
, 2000
, 2003
; Hoot et al., 1999
; Savolainen et al., 2000a
), although relationships among them are unclear. In addition, support for the nodes is low in several cases (Table 2). Both MP and BI analyses of our matK data yield identical topologies with good support for a grade of Ranunculales/Sabiaceae/Proteales/Trochodendraceae (Fig. 7). The matK tree is for the most part in agreement with those obtained from the combined three- and four-gene analyses (Soltis et al., 2000
, 2003
). However, matK data provide considerably higher support for relationships in this group than in previous studies (Hoot et al., 1999
; Savolainen et al., 2000a
; Soltis et al., 2000
), particularly for the position of Ranunculales as sister to all other eudicots (82/76% JK, 1.0 PP). Within Ranunculales, the exact position of Eupteleaceae and Papaveraceae at the base is method dependent in matK. Euptelea is sister to all other Ranuncuales though without support in MP, whereas Papaveraceae were basal in MB, excluded with 75% PP from the rest of Ranunculales. Family relationships among remaining Ranunculales are identical in both approaches (Bayesian not shown) and in agreement with the results from the multigene analyses of Hoot et al. (1999)
and Soltis et al. (2000
, 2003)
.
|
; Qiu et al., 2000
; Savolainen et al., 2000a
; Soltis et al., 2000
, 2003
), but with weak or no support. Although matK presents a potential position for Sabiaceae branching after Ranunculales, the hypothesis of a Sabiaceae + Proteales clade (see Soltis et al., 2000
) cannot be excluded.
In line with previous studies (Hoot et al., 1999
; Savolainen et al., 2000a
; Soltis et al., 2000
), the matK tree places Nelumbo as the sister to the rest of Proteales. Also evident is the high support for a sister group relationship of Proteaceae and Platanaceae (94% JK, 1.0 PP). Several anatomical and morphological synapomorphies have been identified for Proteales (see Nandi et al., 1998
; Savolainen et al., 2000a
).
Buxaceae and Trochodendraceae exchanged positions in the basal eudicot grade in previous studies; these nodes always received low support (Table 2). This matK study shows for the first time good support for a Trochodendraceae/Buxaceae/core eudicot including Gunnerales (Figs. 2, 3, 7) successive branching. The support is particularly strong for Buxaceae being sister to core eudicots (91% JK, 1.0 PP).
Core eudicots
Core eudicots, composed of Gunnerales, Caryophyllales, Berberidopsidales, Saxifragales, Santalales, Vitaceae, Dilleniaceae, asterids, and rosids, received 100% JK and 1.0 PP support with matK. The core eudicots were recovered with high support in the combined rbcL/atpB analysis, and 100% support was achieved with the addition of 18S and 26S rDNA sequences (Hoot et al., 1999
; Soltis et al., 2000
, 2003
). Thus, the core eudicots stand now as one of the best-supported major clades of angiosperms (Figs. 2, 3). Soltis et al. (2003)
discussed the implications for character evolution of Gunnerales sister to the rest of the core eudicots.
The matK data provide more structure for the major branches within core eudicots than previous single or combined gene analyses (Figs. 8, 9; Table 2). A crown group comprising Berberidopsidales/Santalales/Caryophyllales/asterids is inferred here (65% JK and 1.0 PP; Figs. 2, 3, 8). The sister group relationship of asterids and Caryophyllales is weakly supported (62% JK, 0.79 PP). The study based on 18S rDNA sequences (Soltis et al., 1997
) showed Caryophyllales nested within asterids (BS < 50%), but combined analysis of 18S rDNA and rbcL sequences placed the order within rosids (Soltis and Soltis, 1997
); sparse sampling in the latter study might have affected Caryophyllales placement. All previous analyses have indicated affinities of Caryophyllales to Dilleniaceae (see discussion under Dilleniaceae/Vitaceae), but never with high support. Santalales and Berberidopsidaceae/Aextoxicaceae change positions depending on method of analysis. This unstable position is reflected by the low posterior probability (0.55) for the node uniting Berberidopsidaceae/Aextoxicaceae and asterids/Caryophyllales.
|
|
). The matK analysis provides strong support (99/100% JK and 1.0 PP) for the inclusion of Gunnerales in core eudicots (Figs. 2, 8). However, Gunnerales being sister to the remaining core eudicots receives <50% JK support in MP, yet is highly probable (1.0 PP) in the Bayesian analysis. This position for Gunnerales in the core eudicot clade is in agreement with studies based on individual and combined sequence data analyses (Chase et al., 1993
; Hoot et al., 1999
; Savolainen et al., 2000a
; Soltis et al., 2000
). The solidified relationship of the Gunnera + Myrothamnus clade is important for future analyses of the remarkable evolutionary diversification of these two genera. Myrothamnus comprises two species of small, poikilohydric shrubs on African inselbergs, whereas Gunnera (40 species) includes hemicryptophytes, living in symbiosis with the cyanobacterium Nostoc for nitrogen fixation and inhabiting more or less wet habitats, mostly in the Southern Hemisphere.
Saxifragales
In Saxifragales, four well-supported clades of interest are resolved with matK. One (97%) includes Iteaceae as sister to Grossulariaceae/Saxifragaceae (95%). These three families were part of a large polytomy in trees based on individual and combined analyses of rbcL, atpB, and 18S rDNA (Savolainen et al., 2000a
; Soltis et al., 2000
). The inclusion of the 26S rDNA sequence data improved resolution for Saxifragales with the sister group relationship of Iteaceae (plus Pterostemonaceae) and Saxifragaceae receiving 100% JK. A clade with similar topology and support was recovered in a combined analysis of data from five nuclear and plastid genes (Fishbein et al., 2001
). A second clade resolved here includes Cercidiphyllaceae and Daphniphyllaceae (78% JK), which were unresolved in previous large-scale analyses. A third clade includes Haloragaceae, Tetracarpaeaceae, and Aphanopetalum (formerly included in Cunoniaceae; 95%). A similar clade was recovered in the five-gene study of Fishbein et al. (2001)
. A fourth, weakly supported clade (61% JK) encompasses Altingiaceae (Rhodoleia and Altingia). Rhodoleia has been placed in Rhodeliaceae, Hamamelidaceae, or Altingiaceae.
Vitaceae/Dilleniaceae
Dilleniaceae is sister here to Vitaceae, although support for this relationship varies with the method applied (weak using MP, but 1.0 PP in BI). The phylogenetic positions of these families among core eudicots have been difficult to assess and differ in each analysis. Floral and endosperm characters were proposed as potential synapomorphies for the relationship of Dilleniaceae to Caryophyllales and Vitaceae to rosids (Savolainen et al., 2000a
). In contrast, several features are shared by Dilleniaceae and Vitaceae, such as calcium oxalate raphides (Metcalfe and Chalk, 1950
), an endotesta containing radially elongate cells and a tracheidal endotegmen (Corner, 1976
). Similarities of Dilleniaceae to Vitaceae have also been pointed out by Nandi et al. (1998)
.
Berberidopsidales
The sister group relationship of Berberidopsidaceae and Aextoxicaceae is another case in which matK provides the greatest support (100% JK; Fig. 8) among single-gene analyses. The results are in close agreement with trees inferred from multigene data sets (e.g., Savolainen et al., 2000a
; Soltis et al., 2000
, 2003
).
Santalales
The strong support (99% JK; Fig. 8) for the monophyly of Santalales and internal relationships are in agreement with previous molecular studies. This analysis provides the highest support (66/71% JK and 1.0 PP) for the sister group relationship of Santalales to Caryophyllales + asterids. The position of Santalales has varied considerably in previous molecular studies. Soltis et al. (2000)
noted that Santalales and Caryophyllales may be related and in turn be sister to the asterids; both relationships receive weak support in this study.
Caryophyllales
The matK sequence data strongly support the broadly circumscribed Caryophyllales (99% JK, 1.0 PP) as first indicated by analyses of rbcL alone (Savolainen et al., 2000b
) and in later studies (Savolainen et al., 2000a
; Soltis et al., 2000
, 2003
; Cuénoud et al., 2002
). Two Caryophyllales clades, here named Caryophyllales I and II, are recognized with matK (Fig. 8).
In Caryophyllales I, Rhabdodendron (Rhabdodendraceae) and Simmondsia (Simmondsiaceae) emerge in a polytomy with a clade containing the rest of Caryophyllales I (Fig. 8), which is in agreement with Cuénoud et al. (2002)
. Core Caryophyllales (83% BS, 1.0 PP) sensu Cuénoud et al. (2002)
includes Asteropeia (Asteropeiaceae) as sister to a polytomy comprising Caryophyllaceae, an Amaranthaceae-Chenopodiaceae-Achatocarpaceae clade that was also resolved in Kadereit et al. (in press)
, and a higher core Caryophyllales clade (Fig. 8). The latter group in turn consists of two major clades, higher core Caryophyllales I and II. Caryophyllaceae appears unresolved in MP, but emerges sister to the rest in BI (0.59 PP), a position also reflected by the matK-MP analysis of Cuénoud et al. (2002)
and rbcL + atpB analysis of Savolainen et al. (2000a
). Relationships revealed here for Caryophyllales are in general agreement with Cuénoud et al. (2002)
.
In Caryophyllales II, two subclades are recovered. One encompasses the carnivorous families Ancistrocladaceae, Drosophyllaceae, Droseraceae, and Nepenthaceae in a subclade (96% JK, 1.0 PP) and the Polygonaceae (including Coccolobaceae), Plumbaginaceae, Frankeniaceae, and Tamaricaceae in another (90% JK, 1.0 PP).
Rosids
The rosid clade (not including Vitaceae) corresponds to "eurosids" of Soltis et al. (2000)
. The strong support for rosids with matK (95% JK and 1.0 PP) is only comparable to that obtained from the combined atpB, rbcL, and 18S rDNA sequence data (99% JK; Soltis et al., 2000
). However, the addition of 26S rDNA data to the three-gene data set (Soltis et al., 2003
) decreased the JK value for rosids to 79%. Among single data sets, only rbcL (Chase et al., 1993
; Savolainen et al., 2000a
, b
) and 18S rDNA (Soltis et al., 1997
) demonstrated a rosid clade of similar circumscription but with <50% support. In this circumscription, the rosids include eurosids I and II plus Myrtales, Crossosomatales, and Geraniales (Fig. 9).
Relationships among eurosid I, eurosid II, Crossosomatales, Geraniales, and Myrtales varied among all previous single gene (Chase et al., 1993
; Soltis et al., 1997
; Savolainen et al., 2000a
, b
) and multigene (Soltis et al., 2000
, 2003
) analyses. In this study, topological differences are evident between the MP and Bayesian trees (Figs. 9, 10), reflecting low levels of internal support. The Geraniales/Myrtales plus eurosid II/Crossosomatales/eurosid I grade found in the MP analysis is contrasted with the BI tree that resolves Crossosomatales as sister to the remaining rosids (0.75 PP), followed by eurosid II (excluded from the rest by 0.99 PP), Geraniales, with Myrtales and eurosid I forming the terminal clade (0.54 PP). Low support for such relationships was also evident in previous molecular studies. In contrast to the ambiguous relationships among the major rosid lineages, the rosid orders are generally well supported by matK data. All orders receive 1.0 PP (Fig. 10) and 96–100% JK except for Malpighiales (71%). For most orders, this level of confidence was achieved only by two or more genes (Savolainen et al., 2000a
; Soltis et al., 2000
, 2003
).
|
). However, support declined to <50% when 26S rDNA sequences were added. Within eurosids I, matK reveals two major clades. The first comprises Celastrales, Oxalidales, and Malpighiales, which are weakly supported by MP (60%, Fig. 9) but with 1.0 PP. The other eurosid I clade includes Rosales, Fagales, Fabales, and Cucurbitales (the nitrogen-fixing clade; Soltis et al., 1995
) as well as Zygophyllales. This clade recently received some support in the three-gene analysis (68% JK; Soltis et al., 2000
). The Bayesian tree shows 1.0 PP support for this clade (Fig. 10). The MP topology differs from that of the corresponding Bayesian tree by depicting Zygophyllales as sister to Fabales, albeit with <50% JK support. Anthroquinones are a potential synapomorphy for Zygophyllaceae and the nitrogen-fixing clade (Sheahan and Chase, 2000
). Because none of the previous topologies demonstrated good internal support, the position of Zygophyllales remains questionable.
Malpighiales is currently recognized to include at least 30 families, among which relationships have been difficult to establish. The two analyses of matK (Figs. 9, 10) agree upon the arrangement at the basal nodes, with Rhizophoraceae and Balanopaceae as successive sisters to the rest (0.60 and 0.87 PP, respectively; <50% JK). In the most extensive sampling of the order thus far (Savolainen et al., 2000b
; rbcL only), Rhizophoraceae were sister to Erythroxylaceae (not included here) and the pair sister to the rest. No resolution, however, was provided for such relationships with three genes (Soltis et al., 2000
). For other clades in Malpighiales, support is only achieved for Passifloraceae + Salicaceae in the BI tree (1.0 PP).
Eurosid II
A eurosid II clade is not recovered in the matK MP tree, but instead its components appear in two well-supported clades that form a polytomy with Myrtales (Figs. 9, 10). The three- and four-gene analyses (Soltis et al., 2000
, 2003
) recovered eurosids II, but relationships among its members lacked internal support. The eurosid II taxa resolved with matK appear in two subclades, Sapindales (100% JK) and Brassicales + Malvales (89% JK). In contrast, the Bayesian analysis inferred the three orders in a clade with 1.0 PP support (Fig. 1). The matK data provide high internal support for a sister group relationship of Brassicales and Malvales (89% JK, 1.0 PP); such a relationship was obtained in the atpB and rbcL/atpB analyses, although support in those cases was <50% and 62%, respectively (Savolainen et al., 2000a
). In contrast, the three- and four-gene analyses (Soltis et al., 2000
, 2003
) weakly or moderately depicted Sapindales and Malvales in a clade. No clear morphological synapomorphies for this clade are evident (Judd et al., 1994
; Gadek et al., 1996
).
Asterids
This study reveals a strongly supported (98% JK, 1.0 PP) asterid clade sensu Olmstead et al. (1992
, 1993)
that includes four major lineages: Cornales, Ericales, and euasterid I and II (Figs. 2, 11). Bremer et al. (2002)
referred to euasterid I and II as Lamids and Campanulids, respectively. Internal support within asterids using matK is surpassed only by the analysis of six-genomic region by Bremer et al. (2002)
and is similar to what was obtained in the combined three- and four-gene analyses (Soltis et al., 2000
, 2003
; Albach et al., 2001
). Our matK data alone show Ericales as sister to remaining asterids (79% JK; Fig. 11). In contrast, most other studies depict Cornales (Albach et al., 2001
, ndhF tree; Bremer et al., 2002
; Soltis et al., 2003
) or Cornales + Ericales (Savolainen et al., 2000a
; Soltis et al., 2000
) in this position.
|
and Anderberg et al. (2002)
. In Cornales, Nyssaceae and Cornaceae are successive sisters to other members of the order, which is in agreement with Xiang et al. (1998)
, Soltis et al. (2000)
, and Albach et al. (2001)
.
Euasterid I (Lamids)
The euasterid I clade (consisting of Garryales, Oncothecaceae, Boraginales, Gentianales, Solanales, and Lamiales including Plocospermataceae) has a 1.0 PP but <50% JK support with MP (Fig. 12). Lack of support in MP is in line with other studies, including multigene data sets (e.g., Soltis et al., 2000
, 2003
; Albach et al., 2001
; Bremer et al., 2002
). The matK data provide moderate support for a sister position of Aquifoliales to euasterids I in both MP and BI. The sister group relationship of Garryales and Oncothecaceae to remaining euasterid I in the matK tree (Fig. 12) is in agreement with Bremer et al. (2002)
; however, BI shows 1.0 PP support compared to the low MP support (56–>50% JK) in both studies. Support for relationships among the remaining orders of euasterid I (Boraginaceae, Gentianales, Lamiales, and Solanales) is weak, a situation that has been encountered in all previous studies (Olmstead et al., 1992
, 1993
, 2000
; Chase et al., 1993
; Cosner et al., 1994
; Savolainen et al., 2000a
; Soltis et al., 2000
, 2003
; Albach et al., 2001
; Bremer et al., 2002
).
Gentianales are well resolved and strongly supported as monophyletic (mostly 100% JK, 1.0 PP) with Rubiaceae being sister to the rest. Support within Gentianales has been either very weak or moderate, except for the ndhF study of Olmstead et al. (2000)
and the six-gene-region study of Bremer et al. (2002)
. A sister-group relationship between Lamiales and Solanales is inferred by matK (Fig. 12), receiving 0.8 PP (tree not shown), but only 50% JK.
Monophyly of Lamiales is supported by 99% JK, and the first branching position of Plocospermataceae in the Lamiales receives strong support here (81% JK, 1.0 PP) and in Bremer et al. (2002)
. This position for Plocospermataceae was suggested by a broad sampling of rbcL (Savolainen et al., 2000a
), but with only 56% BS. Plocospermataceae is a small family (one genus, three species) from Central America. The sister group relationship of Paulownia to a clade comprising parasitic and hemi-parasitic tribes of the former Scrophulariaceae, as well as the holoparasitic former family Orobanchaceae sensu stricto (s.s.), is congruent with the topology found by Olmstead et al. (2001)
using ndhF, rbcL, and rps2. The Bayesian approach provides more resolution in Lamiales (see Müller et al., in press
).
Euasterid II (Campanulids)
Within euasterids II, the Apiales, Asterales, and Dipsacales form a strongly supported clade (91% JK, 1.0 PP; Fig. 12) that basically corresponds to euasterids II excluding Aquifoliales. This alliance of Aquifoliales with euasterids II based on matK data is not well supported (76% JK, 0.81 PP; Fig. 12). Aquifoliales appeared as the first branching lineage in euasterids II in most previous studies with highest support achieved in combined analyses of 3–6 genomic regions (Soltis et al., 2000
, 2003
; Bremer et al., 2002
). The relationships among the three euasterids II orders remain unclear.
|
PROSPECTS OF USING MATK IN ANGIOSPERM PHYLOGENETICS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPROSPECTS OF USING MATK...LITERATURE CITED |
|---|
; Savolainen et al., 2000a
, b
; Soltis et al., 2000
, 2003
; Zanis et al., 2002
). The analyses of Qiu et al. (1999)
and Zanis et al. (2002)
were based on 8733 (five genes) and over 15 000 (11 genes) nucleotides, respectively, and thus represent approximately eight and 13 times the number of characters used here. Congruence between our matK phylogenies and the various multigene/multigenome phylogenies of angiosperms underscores the utility of matK in angiosperm phylogenetics.
When clades from the backbone phylogeny of angiosperms are compared in various molecular phylogenetic studies (Table 2), 83% received jackknife support >50% with matK compared with 7–24% for individual analyses of rbcL, atpB, and 18S rDNA. Relationships revealed by matK data are more robust than those derived from combining rbcL and atpB sequences (Savolainen et al., 2000a
). The number of nodes receiving >50% support with matK is in the same range as the combined analyses of 3–4 genes from two genomic compartments (also see Table 2). Examples where matK stands out in terms of support are the backbone of the angiosperms, basal eudicots, core eudicots, asterids, eurosid II, and Cornales.
The topology of the angiosperm tree was not influenced by the exclusion of the Gnetales from the outgroup taxa (matrix B), but JK support generally increased at various nodes, implying a higher level of homoplasy introduced by Gnetales relative to other outgroup taxa. In contrast, the Bayesian approach, although it yields results largely congruent with the most parsimonious trees, provides alternative hypotheses for some relationships. However, alternative topologies were confined to areas of the tree at which internal support (JK or BS) has always been low.
Patterns of molecular evolution in matK that make it notable among other genes used in studying plant phylogenetics are quantity of information (number of parsimony-informative sites/rate of change at variable positions) and quality of characters (signal vs. noise). The matK gene differs from coding genes used in phylogenetic reconstruction in the nearly equitable rates of nucleotide substitution among its three codon positions and the high relative rate of nonsynonymous substitution. This evolutionary mode was previously demonstrated in smaller-scale analyses (Olmstead and Palmer, 1994
; Johnson and Soltis, 1995
; Hilu and Liang, 1997
; Soltis and Soltis, 1998
; Cuénoud et al., 2002
). Such a pattern would imply relatively relaxed selection on amino acid composition in relation to function as determined by physiochemical and structural properties. In an initial analysis comparing different plastid regions in basal angiosperms, K. W. Hilu et al. (unpublished manuscript) demonstrated that purifying selection was determined to be less significant in matK than in other protein coding genes, whereas phylogenetic signal at informative positions was found to be highest.
Although progress has been achieved in understanding angiosperm relationships in this study, several parts of the tree remain unresolved or unsupported. Outstanding among these are the positions of monocots, Chloranthaceae, eudicots, and Ceratophyllum among basal angiosperms. Within eudicots, relationships among the major lineages of the core eudicots remain for the most part unclear. Combining matK sequences with other gene sequences has strong potential to provide more information for inference of angiosperm phylogeny. Using additional rapidly evolving genomic regions is desirable to provide insight needed to improve our understanding of angiosperm evolution.
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FOOTNOTES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONPROSPECTS OF USING MATK...LITERATURE CITED |
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S. Saura-Mas and F. Lloret Leaf and Shoot Water Content and Leaf Dry Matter Content of Mediterranean Woody Species with Different Post-fire Regenerative Strategies Ann. Bot., March 1, 2007; 99(3): 545 - 554. [Abstract] [Full Text] [PDF]
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R. Nyffeler The closest relatives of cacti: insights from phylogenetic analyses of chloroplast and mitochondrial sequences with special emphasis on relationships in the tribe Anacampseroteae Am. J. Botany, January 1, 2007; 94(1): 89 - 101. [Abstract] [Full Text] [PDF]
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R. Samuel, W. Gutermann, T. F. Stuessy, C. F. Ruas, H.-W. Lack, K. Tremetsberger, S. Talavera, B. Hermanowski, and F. Ehrendorfer Molecular phylogenetics reveals Leontodon (Asteraceae, Lactuceae) to be diphyletic Am. J. Botany, August 1, 2006; 93(8): 1193 - 1205. [Abstract] [Full Text] [PDF]
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 H. Won and S. S. Renner Dating Dispersal and Radiation in the Gymnosperm Gnetum (Gnetales)--Clock Calibration When Outgroup Relationships Are Uncertain Syst Biol, August 1, 2006; 55(4): 610 - 622. [Abstract] [Full Text] [PDF]
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 L. Cui, P. K. Wall, J. H. Leebens-Mack, B. G. Lindsay, D. E. Soltis, J. J. Doyle, P. S. Soltis, J. E. Carlson, K. Arumuganathan, A. Barakat, et al. Widespread genome duplications throughout the history of flowering plants Genome Res., June 1, 2006; 16(6): 738 - 749. [Abstract] [Full Text] [PDF]
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K. J. Carpenter Specialized structures in the leaf epidermis of basal angiosperms: morphology, distribution, and homology Am. J. Botany, May 1, 2006; 93(5): 665 - 681. [Abstract] [Full Text] [PDF]
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M. L Taylor and J. M Osborn Pollen ontogeny in Brasenia (Cabombaceae, Nymphaeales) Am. J. Botany, March 1, 2006; 93(3): 344 - 356. [Abstract] [Full Text] [PDF]
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T. Cieslak, J. S. Polepalli, A. White, K. Muller, T. Borsch, W. Barthlott, J. Steiger, A. Marchant, and L. Legendre Phylogenetic analysis of Pinguicula (Lentibulariaceae): chloroplast DNA sequences and morphology support several geographically distinct radiations Am. J. Botany, October 1, 2005; 92(10): 1723 - 1736. [Abstract] [Full Text] [PDF]
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C. L. Anderson, K. Bremer, and E. M. Friis Dating phylogenetically basal eudicots using rbcL sequences and multiple fossil reference points Am. J. Botany, October 1, 2005; 92(10): 1737 - 1748. [Abstract] [Full Text] [PDF]
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J. Leebens-Mack, L. A. Raubeson, L. Cui, J. V. Kuehl, M. H. Fourcade, T. W. Chumley, J. L. Boore, R. K. Jansen, and C. W. dePamphilis Identifying the Basal Angiosperm Node in Chloroplast Genome Phylogenies: Sampling One's Way Out of the Felsenstein Zone Mol. Biol. Evol., October 1, 2005; 22(10): 1948 - 1963. [Abstract] [Full Text] [PDF]
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K. J. Wurdack, P. Hoffmann, and M. W. Chase Molecular phylogenetic analysis of uniovulate Euphorbiaceae (Euphorbiaceae sensu stricto) using plastid RBCL and TRNL-F DNA sequences Am. J. Botany, August 1, 2005; 92(8): 1397 - 1420. [Abstract] [Full Text] [PDF]
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M. Lavin, P. S. Herendeen, and M. F. Wojciechowski Evolutionary Rates Analysis of Leguminosae Implicates a Rapid Diversification of Lineages during the Tertiary Syst Biol, August 1, 2005; 54(4): 575 - 594. [Abstract] [Full Text] [PDF]
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M. H. J. Barfuss, R. Samuel, W. Till, and T. F. Stuessy Phylogenetic relationships in subfamily Tillandsioideae (Bromeliaceae) based on DNA sequence data from seven plastid regions Am. J. Botany, February 1, 2005; 92(2): 337 - 351. [Abstract] [Full Text] [PDF]
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C. Lohne and T. Borsch Molecular Evolution and Phylogenetic Utility of the petD Group II Intron: A Case Study in Basal Angiosperms Mol. Biol. Evol., February 1, 2005; 22(2): 317 - 332. [Abstract] [Full Text] [PDF]
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R. Samuel, H. Kathriarachchi, P. Hoffmann, M. H. J. Barfuss, K. J. Wurdack, C. C. Davis, and M. W. Chase Molecular phylogenetics of Phyllanthaceae: evidence from plastid MATK and nuclear PHYC sequences Am. J. Botany, January 1, 2005; 92(1): 132 - 141. [Abstract] [Full Text] [PDF]
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J. Shaw, E. B. Lickey, J. T. Beck, S. B. Farmer, W. Liu, J. Miller, K. C. Siripun, C. T. Winder, E. E. Schilling, and R. L. Small The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis Am. J. Botany, January 1, 2005; 92(1): 142 - 166. [Abstract] [Full Text] [PDF]
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S. Kim, M.-J. Yoo, V. A. Albert, J. S. Farris, P. S. Soltis, and D. E. Soltis Phylogeny and diversification of B-function MADS-box genes in angiosperms: evolutionary and functional implications of a 260-million-year-old duplication Am. J. Botany, December 1, 2004; 91(12): 2102 - 2118. [Abstract] [Full Text] [PDF]
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L. P. RONSE DE CRAENE Floral Development of Berberidopsis corallina: a Crucial Link in the Evolution of Flowers in the Core Eudicots Ann. Bot., November 1, 2004; 94(5): 741 - 751. [Abstract] [Full Text] [PDF]
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P. S. Soltis and D. E. Soltis The origin and diversification of angiosperms Am. J. Botany, October 1, 2004; 91(10): 1614 - 1626. [Abstract] [Full Text] [PDF]
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M. W. Chase Monocot relationships: an overview Am. J. Botany, October 1, 2004; 91(10): 1645 - 1655. [Abstract] [Full Text] [PDF]
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W. L. Crepet, K. C. Nixon, and M. A. Gandolfo Fossil evidence and phylogeny: the age of major angiosperm clades based on mesofossil and macrofossil evidence from Cretaceous deposits Am. J. Botany, October 1, 2004; 91(10): 1666 - 1682. [Abstract] [Full Text] [PDF]
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W. E. Friedman, R. C. Moore, and M. D. Purugganan The evolution of plant development Am. J. Botany, October 1, 2004; 91(10): 1726 - 1741. [Abstract] [Full Text] [PDF]
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W. S. Judd and R. G. Olmstead A survey of tricolpate (eudicot) phylogenetic relationships Am. J. Botany, September 1, 2004; 91(10): 1627 - 1644. [Abstract] [Full Text] [PDF]
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D. E. Soltis and P. S. Soltis Amborella not a "basal angiosperm"? Not so fast Am. J. Botany, June 1, 2004; 91(6): 997 - 1001. [Abstract] [Full Text] [PDF]
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