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Systematics |
2Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California 90095-1737 USA; 3Cell Biology and Molecular Genetics/Plant Biology, 2106 H. J. Patterson Hall, Building 073, University of Maryland, College Park, Maryland 20742-5815 USA; 4Department of Botany, Academy of Natural Sciences, 1900 Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103 USA
Received for publication July 16, 2002. Accepted for publication September 5, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2.5 kilobases [kb]) and matK ORF (1.5 kb) are comparable in size to the intron and ORF of land plants, in which they are similarly found inserted in the trnK exon. Domain X, a sequence of conserved amino acid residues within matK, occurs in the Characeae. Phylogenetic analysis using maximum likelihood (GTR + I + gamma likelihood model) and parsimony (branch and bound search) yielded one tree with high bootstrap support for all branches. The matK tree was congruent with the rbcL tree for the same taxa. The number and proportion of informative sites was higher in matK (501, 31% of matK sequence) compared to rbcL (122, 10%). Characeae branch lengths were on average more than five times longer for matK compared to rbcL and provided better resolution within the Characeae. These findings along with recent genomic analyses demonstrate that the intron and matK invaded the chloroplast genome of green algae prior to the evolution of land plants.
Key Words: Characeae • charophyte green algae • matK • maturase • rbcL • trnK
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Pickett-Heaps, 1975
). These algae have been classified in a separate division, the Charophyta, by some authors (Bold and Wynne, 1985
). Recent molecular studies have confirmed the monophyly of the group (McCourt et al., 1996a
) and strongly support the Characeae as the closest living sister taxon to land plants, or embryophytes (Karol et al., 2001
). Though cosmopolitan in fresh and brackish water, extant charophytes are much less diverse today (one family with six genera) than in the geological record (12 extinct families comprising nearly 80 genera) (Grambast, 1974
; Soulie-Märsche, 1989
; Feist and Grambast-Fessard, 1991
; Taylor et al., 1992
; Martin-Closas and Diéguez, 1998
). Extant Characeae therefore represent a dwindling clade of green algae that is nonetheless sister to one of the most diverse and successful groups of terrestrial organisms. As such, molecular phylogenetic studies of the group take on particular significance in terms of their function as an outgroup to the embryophytes.
Historically, the Characeae and related fossil taxa have been called "charophytes" (Peck, 1953
; Grambast, 1974
), although Karol et al. (2001)
used the term more broadly, including land plants. Several other green algal groups are also closely related to and monophyletic with the Characeae-land plant clade, and we refer to these algae collectively as charophyte green algae. The Characeae are relatively large (up to a meter or more in height) and morphologically complex (Wood and Imahori, 1965
; Feist and Grambast-Fessard, 1991
). Six extant genera of Characeae are recognized: Chara, Lamprothamnium, Nitellopsis, Lychnothamnus, Nitella, and Tolypella. Molecular systematic studies of the Characeae have generally employed one of two genes: the plastid-encoded large subunit of Rubisco (rbcL) or the nuclear-encoded small subunit of ribosomal DNA (SSU rDNA) (Chapman et al., 1998
). Although the two genes differ in the degree of sequence divergence, with that of rDNA typically being much lower than rbcL, both have been used to independently infer the relationships of the Characeae to land plants (Graham, 1993
; Wilcox et al., 1993
; Kranz et al., 1995
, 1997
; McCourt, 1995
; Kranz and Huss, 1996
; Chapman et al., 1998
; Cimino et al., 2000
; Karol et al., 2001
) and to decipher relationships among the six extant genera (McCourt et al., 1996a
, b
, 1999
; Meiers et al., 1997
, 1999
). Despite the utility of these two genes at elucidating phylogenetic relationships among and between the charophyte green algae, the two genes yield conflicting signals regarding the relationships among genera within the Characeae (McCourt et al., 1996a
, b
, 1999
; Meiers et al., 1997
, 1999
). Such ambiguity has led to the search for other genes or genomic characters (e.g., introns and gene arrangements) that might be used to address these questions.
In this study we report on the occurrence of a protein-coding gene, matK, in characean green algae. Although this gene has been shown to reside within a group II intron of the plastid-encoded transfer RNA gene for lysine (trnK) in all embryophytes studied (Ems et al., 1995
), the intron and matK are absent from most other green algae (Lemieux et al., 2000
; Turmel et al., 2002
). Phylogenetic studies of angiosperms have found matK to be more divergent in sequence than either rbcL or the SSU rDNA cistron, which fortuitously predisposes matK for use as a plausible gene for resolving relationships among genera and species of angiosperms (Mohr et al., 1993
; Johnson and Soltis, 1994
, 1995
; Steele and Vilgalys, 1994
; Liere and Link, 1995
; Ooi et al., 1995
; Gadek et al., 1996
; Soltis et al., 1996
; Kelchner, 2002
). We hypothesized that matK, if present in the Characeae, would be useful for lower-level phylogenetic analysis.
The present study is the first to report that the intron containing matK occurs in the Characeae. Moreover, matK sequences in the Characeae contain sufficient phylogenetic signal for reconstructing relationships among genera and species within this algal family and are congruent with phylogeny for the group inferred from rbcL data.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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using 6% CTAB as described by McCourt et al. (1996a
, 1999
). Assuming that matK and the group II intron would be located within the trnK exon in Characeae as in land plants, we initially amplified this region using primers that annealed to the 5' and 3' exons of angiosperm trnK (Johnson and Soltis, 1994
). These primers were later modified slightly based on a few preliminary Characeae sequences and the trnK sequence of Marchantia (5' primer "2B": gggttgctaactcaatgg; 3' (reverse) primer "12B": aactcgtcggatgaagta). Polymerase chain reaction (PCR) fragments were purified using Geneclean II kits (Q-Bio, Carlsbad, California, USA) or, in the case of fragments less than 1.5 kilobases (kb) in length, Wizard Prep kits (Promega, Madison, Wisconsin, USA). In preliminary stages of this study, only manual sequencing was accessible and was performed directly on purified double-stranded PCR products using a modified Sanger dideoxy sequencing method (McCourt et al., 1996a
) and commercial Sequenase (Version 2.0) enzyme kits (U.S. Biochemical, Cleveland, Ohio, USA). Later, automated sequencing of these manually generated sequences was confirmed and further sequencing was performed using an ABI 373 (Applied Biosystems, Foster City, California, USA). Using a single amplicon (to avoid possible chimera assembly of amplicons; Cimino et al., 2000
), sequencing was accomplished by primer walking from both ends. Eventually, forward and reverse sequences overlapped, and sequencing continued for both DNA strands across the entire matK reading frame. These new sequencing primers were also used to obtain PCR products in particular taxa in which the entire region was difficult to amplify in a single amplicon, after which overlapping fragments were matched to the entire region using Sequencher (see below) to ascertain that no chimera sequences were obtained.
Sequence analysis
Sequences of the amplified fragments were translated to amino acids in each of three reading frames to locate start and stop codons of the matK ORF. Sequence contigs were assembled using Sequencher 3.1.1 (GeneCodes, Ann Arbor, Michigan, USA) and alignments adjusted by eye. Alignment of highly divergent regions flanking the group II intron were not possible across all genera. Maximum likelihood (ML) and maximum parsimony (MP) analyses of the matK-encoding region were performed using PAUP* (version 4.0b8 PPC, Swofford, 1998
). Branch and bound MP searches were performed to find the globally most parsimonious trees. Estimates of maximum-likelihood parameters based upon the optimal MP tree were calculated using a series of models in PAUP*, and pairwise likelihood ratio tests were used to determine the best model invoking the fewest estimated parameters (Swofford et al., 1996
). This model, with fixed parameters, was used in a branch and bound search to derive an optimal ML tree.
Both ML and MP bootstrapping were performed with 1000 replicates for each method. For ML, the best model (GTR + I + gamma), with parameters fixed as described earlier, was used. For MP, the heuristic search procedure using tree bisection-reconnection (TBR), save multiple trees (MULTREES), accelerated transformation (ACCTRA), and steepest descent options was used. Parsimony branch lengths were generated using these options to compare relative rates of matK and rbcL divergence.
Maximum likelihood and MP analyses of rbcL sequences from the same DNA samples (from McCourt et al., 1999
and new sequences noted in Table 1) were also performed. Sequences of matK and rbcL for each species were combined in a concatenated data set for the two genes, tested for homogeneity of signal (Farris et al., 1995
as implemented in Swofford, 1998
), and analyzed as described earlier, except that an ML bootstrap was not performed for the rbcL data set.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2.4–2.8 kb in the 10 characean taxa (Table 1), a length approximating that of the 2.5 kb reported for the corresponding region in angiosperms (Steele and Vilgalys, 1994
). The insertion point of the intron is between base pairs 37 and 38 of the trnK 5' exon, making the fragment a phase 1 intron (Graur and Li, 2000
). The trnK regions were sequenced in their entirety in Chara connivens and Nitella opaca and nearly to completion (>90% complete) in eight species representing all of the five remaining genera. Nucleotide sequence variability within the group II intron and matK regions was such that an additional two dozen custom primers were required to sequence all taxa.
matK in the Characeae
The matK ORF within the Characeae trnK intron was identified as a stretch of 1.5 kb uninterrupted by stop codons. This ORF was sequenced for all taxa listed in Table 1 from the six characean genera. The matK region of these algae was approximately the same size as matK in angiosperms (Johnson and Soltis, 1994
, 1995
; Steele and Vilgalys, 1994
; Soltis et al., 1996
).
Phylogeny of the Characeae based on matK
The inferred phylogenetic relationships of the characean taxa based on matK sequences are shown in Fig. 1. A branch-and-bound ML search recovered a single optimal tree (–ln = 7721.244 39), which was identical in topology to the branch-and-bound MP tree (tree length = 1335; consistency index [CI] = 0.8569; 0.7887 excluding uninformative characters) found. Using this taxon set, approximately one-third of the matK sequence (501 base pairs [bp] out of 1626 or 31% of total length) was parsimony informative.
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, 1999
) and four-gene analyses (Karol et al., 2001
). Bootstrap support was 100% for all branches on the matK tree (Fig. 1). An ML heuristic search using rbcL sequence data for these species (same DNA samples) was performed using the same model and yielded a tree identical in topology to that derived from the matK data. Bootstrap support for the MP rbcL tree topology was generally high, but less than that for the matK analysis (Fig. 1). Parsimony lengths for internal branches on the matK tree averaged 5.6 (range 4.25–6.75) times that of corresponding branches for rbcL. Combining the matK and rbcL sequences revealed no heterogeneity of signal and the MP tree for the combined data set was identical to the tree in Fig. 1.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The trnK intron and matK are absent from other green algae reported to date (Turmel et al., 1999
; Lemieux et al., 2000
), with exceptions noted below. Complete plastid genomes for the chlorophytes Chlorella (NC001865), Nephroselmis (NC000927, Turmel et al., 1999
), and the putative charophyte green alga Mesostigma (NC002186, Lemieux et al., 2000
) contain the uninterrupted trnK exon (approximately 75 bp) with no intron. Recently, Turmel et al. (2002
, personal communication) also reported that the plastid genome of Chlorokybus lacks an intron in trnK. Mesostigma and Chlorokybus are usually grouped with the charophyte green algae (Bhattacharya et al., 1998
; Karol et al., 2001
), though Lemieux et al. (2000
, personal communication) concluded, based on analysis of proteins derived from the complete plastid genome, that these genera are sister taxa in a clade basal to all green algae.
Turmel et al. (2002)
also examined the small and large subunits of chloroplast rDNA in charophyte green algae and land plants and found a similar basal phylogenetic placement of Mesostigma, although an alternative placement of this genus within the charophyte green algae plus land plant lineage could not be rejected based on a comparison of log likelihoods. A recent analysis of four gene sequences from nuclear, mitochondrial, and plastid genomes supports the inclusion of Mesostigma with charophyte green algae and land plants (Karol et al., 2001
). If Mesostigma and Chlorokybus are early diverging descendants of the line leading to the Charales and land plants, then the trnK group II intron and matK ORF were absent when this group diverged from other green algae.
Currently under investigation is whether other algae in the more basal orders of charophyte green algae, such as Coleochaetales, Zygnematales, and Klebsormidiales, possess the trnK-matK region. Turmel et al. (2002)
sequenced the entire plastid genome of Chaetosphaeridium globosum, a member of the Coleochaetales, sister group to the Charales/land-plant clade, and found that this species contains the matK ORF. C. Lemieux and M. Turmel (Université Laval, Quebec, Canada, personal communication) also found the matK ORF in the plastid genome of the zygnematalean genus Staurastrum, and we have amplified the gene from Coleochaete (K. G. Karol and R. M. McCourt, unpublished data). Identifying the group II intron and matK in the Coleocaetales, Charales, and other green algae related to land plants supports the hypothesis that these features of the plastid genome constitute a derived character for charophyte green algae that diverged after Mesostigma. Moreover, these studies show that the group II intron and matK ORF invaded the plastid genome at some time prior to the divergence of land plant ancestors from their aquatic algal relatives and thus before the transition from an aquatic to a terrestrial habitat.
The protein encoded by matK (MatK) has maturase, reverse transcriptase (RT), and DNA endonuclease activities in eubacteria and fungal mitochondria (Tsudzuki et al., 1992
; Mohr et al., 1993
; Ems et al., 1995
; Liere and Link, 1995
; Michel and Ferat, 1995
; Matsuura et al., 1997
). The latter two functions likely contribute to the mobility of the intron (Ferat et al., 1994
; Michel and Ferat, 1995
; Matsuura et al., 1997
). However, in land plant MatK, the RT and endonuclease regions of the protein are truncated, a deletion that may interfere with the reverse transcriptase activity of MatK, which would consequently account for the relatively stable location of group II introns in trnK from lower to higher plants (i.e., bryophytes to angiosperms) (Michel and Ferat, 1995
). The data reported here suggest that matK and its intron invaded the chloroplast genome, then were truncated and achieved this stable position long before the divergence of embryophytes.
The nucleotide sequence composition of the 1.5-kb characean matK ORF is more variable in genera and species of Characeae than in land plants. This variability is not surprising given the antiquity of characean genera and species relative to land plant species (Feist and Grambast-Fessard, 1991
). Characean matK nucleotide sequences were not readily alignable to those of angiosperms except for small regions involving approximately three dozen amino acids. This portion of domain X near the 3' end of the matK ORF, although clearly homologous to domain X in land plants, contained insufficient signal to obtain a resolved tree for Characeae and land plants. However, a BLAST (basic local alignment search tool) search of the translated amino acid sequences matched most closely to numerous land plant MatK polypeptide sequences in GenBank. Previous studies of group II intron-encoded proteins have shown that the only highly conserved region among all identified or proposed maturases is domain X, which consists of approximately 100 amino acids and has been proposed to function in RNA binding (Mohr et al., 1993
; Vogel et al., 1997
). Approximately three dozen derived amino acid residues for characean matK within domain X were easily aligned to those inferred from the cDNA sequence of matK for barley (an angiosperm, Hordeum vulgare) and a liverwort (Marchantia polymorpha) (Fig. 2). For the characean taxa, domain X begins near position 1400 in the matK sequence (there is some variability from indels in various taxa). The amino acid sequence similarity is highest for the first 39 amino acid residues (50%), after which the similarity between the characean and two land plant sequences is low (<10%) (Fig. 2).
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) and a consensus sequence SX3–6TLAXKXK that was first described by Mohr et al. (1993)
(Fig. 2). The conservation of domain X may signify that the characean matK gene encodes a functional maturase that plays an essential role in splicing the trnK intron, as has been implicated for MatK from barley (Vogel et al., 1997
). Moreover, RNA editing in at least some angiosperms appears to conserve this YY motif. Vogel et al. (1997)
reported that the genomic DNA sequence for barley encodes a histidine (H) residue instead of tyrosine at the second position (Fig. 2). However, an RNA editing event restores the YY motif in the derived protein sequence. Specifically, a C-to-U edit converts the codon specifying histidine (CAT) in the barley DNA sequence to the codon specifying tyrosine (UAU) in the mRNA transcript. In contrast, genomic nucleotide sequences of lower land plants (e.g., Marchantia) and green algae (e.g., Characeae) exhibit a thymine (T) at the first position of this codon and consequently are not subject to RNA editing. At the nucleotide level, it should be noted that the Characeae and Marchantia differ in the codon used for the second Y in this motif. That is, the YY motif in the Characeae is encoded from nucleotide sequence TAT-TAC, whereas the YY motif in Marchantia is encoded by TAT-TAT. The maintenance of the YY motif effected through synonymous substitution or RNA editing in higher plants lends support to the functional significance of matK in plastids in general and suggests that greater variability in characean nucleotide sequences is not due to lack of functional importance of matK.
Sequence data for matK have been used extensively in phylogenetic studies of families, genera, and species of plants (Johnson and Soltis, 1994
, 1995
; Soltis et al., 1996
). In embryophytes, matK has greater levels of divergence than rbcL. This pattern holds true for the Characeae as well. Parsimony branch lengths for matK are on average more than five times longer than respective rbcL branches, which suggests that the gene will prove useful for studies within the Characeae (and in other charophyte green algae in which it may be found).
The congruence of tree topology for rbcL and matK support the conclusions of McCourt et al. (1996a)
and Karol et al. (2001)
regarding genus-level relationships within the Characeae. The matK data also support the suggestion of McCourt et al. (1999)
that C. connivens and C. globularis form a closely related, perhaps conspecific cluster of taxa. The matK tree, while unrooted, is congruent with the monophyly of the tribes Chareae and Nitelleae recognized by conventional taxonomy (Wood and Imahori, 1965
). McCourt et al. (1999b)
noted longer rbcL branch lengths in the Nitelleae compared to those within the Chareae, a pattern that also holds for the matK tree (Fig. 1). This finding for both genes suggests the branch asymmetry within the Characeae is not restricted to rbcL and may represent a different evolutionary rate or time of origin in the two main clades of the Characeae.
The data show that matK data provide better resolution within the Characeae than rbcL, but rooting the tree remains a problem. The matK ORF and its intron may provide other types of data to address fundamental issues of "deep green" research (see website http://ucjeps.berkeley.edu/bryolab/greenplantpage.html). Additional sampling of the trnK region in other charophyte green algae, combined with studies of the secondary structure of the intron, may provide additional characters or help align sequences and provide better estimates of the root of the tree and of the phylogeny of charophyte algae and land plants.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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