| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1 Department of Biology, Derring Hall, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061-0406
Received for publication December 8, 1998. Accepted for publication April 22, 1999.
ABSTRACT
Insertion/deletion events (indels) and nucleotide substitutions at the extreme 3' end of the chloroplast gene matK have been identified that distinguish certain major lineages of grasses. A 1-bp (base pair) deletion creating a shift in the open reading frame (ORF) and a point mutation support the positions of Streptochaeta and Anomochloa as the two most basal lineages in Poaceae. Another 1-bp deletion resulting in early termination of the ORF is unique to Ehrharta, a member of the taxonomically disputable tribe Ehrharteae. A 6-bp insertion supports monophyly of subfamilies Panicoideae, Arundinoideae, Centothecoideae, and Chloridoideae (PACC). This marker appears useful in defining PACC clade members and may have potential in providing insight into the sister-group relationship between PACC and other lineages. Alignment of deduced amino acid sequences from bryophytes, gymnosperms, and angiosperms shows that this region is relatively conserved, but variation is notably higher in Poaceae. The evolutionary implications of these changes in grasses and other plant families are addressed.
Key Words: grasses • indels • markers • matK • phylogeny • plants • Poaceae
Molecular characters used in systematic studies are basically of three types: nucleotide substitutions, rearrangements, and insertions/deletions (indels). Indels are usually more frequent in noncoding than coding regions and could be useful in circumscribing lineages and defining evolutionary trends. In coding regions, all insertions and deletions translate into nonsynonymous substitutions either at the immediate site of the mutation or further downstream if a frameshift is generated. Because natural selection acts largely at the protein level, these mutations could be subject to greater selective constraints due to their impact on the function and/or structure of the encoded products. Conversely, synonymous substitutions maintain protein composition and are considered effectively neutral (Clegg et al., 1994
; Nielsen, 1997
). In systematic and evolutionary studies, informative indels not only can be combined with other molecular characters, but also can work as qualitative molecular markers depending on their size, position, and influence on the open reading frame (ORF). Such molecular markers are particularly useful in phylogenies where resolution is low or disagreements prevail among data sets. The phylogeny of the Poaceae presents a case where such molecular markers can be useful (Clark, Zhang, and Wendel, 1995
).
Several hypotheses have been proposed concerning the most basal lineages in Poaceae. Subfamily Bambusoideae s.l. (sensu lato) was traditionally considered the most ancestral group based on the presence of presumably primitive reproductive characters (Stebbins, 1956
; Soderstrom and Calderón, 1979
). However, Soderstrom (1981)
indicated that the Bambusoideae should not be regarded as ancestral to other grasses due to certain derived anatomical and vegetative morphological characters. Anomochloa, Streptochaeta, and Pharus, formerly classified as herbaceous bamboos, appear basal or distinct when included in morphological-anatomical and molecular analyses (Hilu and Wright, 1982
; Clark, Zhang, and Wendel, 1995
; Duvall and Morton, 1996
; Soreng and Davis, 1998
; Hilu, Alice, and Liang, in press). When these genera are not included in phylogenies, either oryzoids and woody bambusoids are basal (Cummings, King, and Kellogg, 1994
; Barker, Linder, and Harley, 1995
; Liang and Hilu, 1996
) or there is a basal split in the family into Pooideae and the rest of the Poaceae (Davis and Soreng, 1993
; Nadot, Bajon, and Lejeune, 1994
).
Definitions of major clades in the Poaceae have also been disputed. The appearance of subfamilies Panicoideae, Arundinoideae, Centothecoideae, and Chloridoideae in one major group (named PACC; Davis and Soreng, 1993
) is supported by morphological, anatomical, and molecular data (Hilu and Wright, 1982
; Hilu and Esen, 1988
; Esen and Hilu, 1989
; Davis and Soreng, 1993
; Barker, Linder, and Harley, 1995
; Clark, Zhang, and Wendel, 1995
; Duvall and Morton, 1996
; Liang and Hilu, 1996
; Mathews and Sharrock, 1996
; Soreng and Davis, 1998
). In addition, using ndhF sequences, Clark, Zhang, and Wendel (1995)
recognized a lineage (named BOP) that comprises most bambusoids plus oryzoid and pooid taxa. An alternative relationship identified in Soreng and Davis's (1998)
study includes the Pooideae plus PACC as a major clade.
In a systematic study of the Poaceae using sequences of the plastid gene matK, we detected molecular markers near the 3' end of the coding region that appear phylogenetically informative. In this study, we investigate the use of these markers in evaluating current hypotheses on grass evolution and assess the phylogenetic position of taxonomically disputable taxa. The evolutionary hypotheses to be tested are outlined in the next section. Also addressed are patterns of nucleotide and amino acid substitutions resulting from these mutations and their evolutionary implications in Poaceae and other plant groups.
MATERIALS AND METHODS
We examined matK sequences representing 52 grass genera, 26 tribes, and nine subfamilies (Table 1). In addition, we obtained seven sequences of seed plant taxa and 45 GenBank sequences, bringing the total to 26 bryophyte, gymnosperm, and angiosperm families. Leaf tissue was harvested from either greenhouse-grown or field-collected plants. Total genomic DNA isolation and polymerase chain reaction (PCR) amplification of the entire trnK intron (including matK) followed Liang and Hilu (1996)
. Because the matK region of interest is located at the 3' end of the coding region, two primers (matK7B and/or MG15) were used in direct sequencing of PCR products. Primer matK7B is located ~330 base pairs (bp) upstream from the 3' terminus of matK and primer MG15 is in the trnK 3' exon, ~275 bp from the end of matK. Nucleotide data used in this study were obtained either by manual sequencing (described in Liang and Hilu, 1996
) and/or automated sequencing. For automated sequencing, trnK region PCR products were electrophoresed in 0.8% agarose gels and DNA fragments of appropriate size were excised and purified using a QiaQuick gel extraction kit (QIAGEN, Inc., Valencia, California). Sequencing reactions were carried out using an ABI PrismTM Dye Terminator Cycle Sequencing Ready Reaction Kit with Amplitaq DNA polymerase FS (Perkin Elmer, Norwalk, Connecticut). Samples were sequenced in an ABI 373A automated DNA sequencer with a stretch gel (Applied Biosystems, Inc., Foster City, California). Chromatograms were manually edited using Sequence Navigator 1.0 software (Applied Biosystems, Inc., Foster City, California).
|
) from 26 seed plant and bryophyte families plus three Poaceae genera (Fig. 1). For these taxa, comparisons of the matK 3' region were based only on deduced amino acid sequences (generated by Sequence Navigator) to avoid ambiguity of nucleotide alignment at this taxonomic level. The second included nucleotide sequences and their corresponding deduced amino acids from Poaceae, Joinvilleaceae, and Restionaceae (Fig. 2). Alignments of nucleotide and amino acid sequences were unambiguous and, thus, done visually.
|
|
study using ndhF sequences and shows Anomochloa and Streptochaeta in one clade sister to the remaining grasses, a result consistent with Soreng and Davis' (1998)
cpDNA restriction site analysis. In this phylogeny, the Bambusoideae s.s. (sensu stricto), Oryzoideae, and Pooideae (BOP) clade is sister to the PACC group, a relationship supported by phytochrome sequence data (Mathews and Sharrock, 1996
). The second phylogenetic model is based on Soreng and Davis' (1998)
analysis of 42 structural characters. This diagram depicts Streptochaeta as the most basal lineage followed by Anomochloa (which is unresolved along with Eremitis and Pharus in their study), then Bambusoideae s. s., Oryzoideae, and finally Pooideae plus PACC in one clade. The positions of Streptochaeta and Anomochloa as shown in Fig. 4 are corroborated by analysis of complete matK sequences (Hilu, Alice, and Liang, in press). Thus, the major differences between these phylogenies are whether (1) Anomochloa and Streptochaeta comprise one or two lineages, (2) subfamilies Bambusoideae s. s., Oryzoideae, and Pooideae occur in one or several clades, and (3) the BOP clade or Pooideae is the sister group of PACC.
|
Patterns of variation in the matK 3' end
Length of the targeted ORF region at the 3' end is 13 amino acids in Marchantia, 19 in gymnosperms, and 4–8 in most angiosperms. Although these data do not imply an overall trend in length reduction from bryophytes to flowering plants, the consistency in the gymnosperm families Ginkgoaceae and Pinaceae and, to a certain degree in angiosperms, might have phylogenetic value. All flowering plant species examined (Fig. 1) have ORF endings shorter than most grasses except for Epifagus and Pisum (pea). It is important to note that these two genera have lost large sectors of their chloroplast genomes. Epifagus, with an ORF ending three amino acids shorter than those of most angiosperms, is a parasitic plant that lost ~65% of its chloroplast genes, including the two trnK exons within which matK is nested, and has a large deletion at the 5' end of its matK coding region (Wolfe, Morden, and Palmer, 1992
; Ems et al., 1995
). In pea, the chloroplast genome is 30 kilobase pairs (kbp) shorter than the related mung bean, has only one of the two sets of ribosomal genes, and lacks one of the two inverted repeats (Palmer and Thompson, 1981
). Because the inverted repeat is estimated to be 23 kbp in length, the remaining 7 kbp represents other deletions in the pea chloroplast genome. Thus, the chloroplast genomes and matK of Epifagus and Pisum signify atypical situations.
In Poaceae, the length of the ORF ending in Streptochaeta and Anomochloa is the same as those found in most other angiosperms (Fig. 1). However, in the remaining grasses examined (excluding Ehrharta), a 1-bp deletion (Fig. 2, nucleotide position 11) caused a frameshift, extending the ORF one codon fixed as proline. A 6-bp insertion (nucleotide positions 16–21) found only in members of PACC further extended the ORF by two codons. These two mutations appear to be found only in Poaceae. Unique among Poaceae taxa examined is Ehrharta in which the stop codon is located at nucleotide sites 4–6, resulting in an ending four amino acids shorter than those of Streptochaeta, Anomochloa, and most other flowering plants.
Phylogenetic implications
This study focuses on the 28 aligned characters at the 3' end of the matK coding region because of the concentration of indels in this region and the occurrence of the highly conserved domain X upstream (Ems et al., 1995
; Hilu and Liang, 1997
). Consensus nucleotide sequences and their corresponding amino acids exemplifying variability within the Poaceae and in related families are shown in Fig. 2. With Joinvillea as a reference taxon, the region in Poaceae includes 18 variable sites and three indels; ten of the variable sites and two of the indels are potentially phylogenetically informative. Figures 3–4 summarize the two phylogenetic models for grass evolution (discussed in Materials and Methods) with three of the potentially informative mutations mapped on the branches. These trees indicate that in the Poaceae Streptochaeta and Anomochloa represent the two most basal lineages. This relationship is supported by the 1-bp deletion that unites all grasses except Streptochaeta and Anomochloa and the outgroup Joinvillea (Fig. 2). Mapping of the point mutation at nucleotide site 12 onto Fig. 3 requires two steps, whereas only one step is needed for optimization on the Fig. 4 topology. Thus, this mutation supports Streptochaeta as the most basal grass genus. The phylogeny also resolves the PACC subfamilies as a single lineage distinguished by the 6-bp insertion. This study does not offer support regarding the monophyly of the BOP subfamilies nor does it resolve the sister group to PACC. However, the presence of the 6-bp insertion in species generally classified in non-PACC subfamilies could be construed as evidence of sister-group relationship to the PACC lineage, a hypothesis that can be tested by independent data.
The polyphyly of the Bambusoideae s. l. and positions of Streptochaeta, Anomochloa, and Pharus sister to the other grasses have been demonstrated by Clark, Zhang, and Wendel (1995)
and Soreng and Davis (1998). Support for a basal position of Anomochloa was also cited in the rbcL-based study of Duvall and Morton (1996)
, although Streptochaeta and Pharus were not sampled. Clark and Judziewicz (1996)
resurrected subfamily Anomochlooideae to accommodate the first two genera. In contrast, the point mutation at nucleotide site 12 (Fig. 2) as well as separate analyses of complete matK sequences (Hilu, Alice, and Liang, in press) and structural characters (Soreng and Davis, 1998
) identify Streptochaeta as the most basal lineage in the Poaceae followed by Anomochloa. Although ndhF and cpDNA restriction site data (Clark, Zhang, and Wendel, 1995
; Soreng and Davis, 1998
) support the monophyly of Streptochaeta and Anomochloa, Clark and Judziewicz (1996)
asserted that it is not easy to find anatomical and morphological synapomorphies to define this clade. Clark and Judziewicz (1996)
also erected subfamily Pharoideae to encompass the tribe Phareae. In this study, Pharus shares the apomorphic frameshift indel with most grasses and, therefore, appears phylogenetically distinct from Streptochaeta and Anomochloa.
The strong support for the PACC subfamilies has been documented in numerous studies and is here supported by the 6-bp insertion that appears unique among all plant taxa studied (Figs. 1, 2). The appearance of the Panicoideae, Arundinoideae, Centothecoideae, and Chloridoideae in one major group was first established by Hilu and Wright (1982)
based on a UPGMA (Unweighted Pair Group Method using Arithmatic Averages) cluster analysis of 85 morphological and anatomical characters. Prolamin seed storage protein and immunological studies demonstrated that the PACC group possesses a characteristic size class (20–35 kDa) that is structurally distinct from the other two size groups in grasses as determined by ELISA cross-reactivities (Hilu and Esen, 1988, 1990, 1993
; Esen and Hilu, 1989
). Monophyly of this group has since been substantiated by molecular and structural data. Thus, the PACC clade represents a well-defined lineage supported by different sources of data.
Several other phylogenetic hypotheses have been proposed concerning major lineages in Poaceae. Disregarding the basal positions of Streptochaeta, Anomochloa, and Pharus, this study does not support a split in the family into Pooideae and the remaining grass taxa proposed by Davis and Soreng (1993)
and Nadot, Bajon, and Lejeune (1994)
, nor does it support the division into PACC and the rest of the Poaceae (Mathews and Sharrock, 1996
). Although the PACC clade is well supported here, there is no synapomorphy substantiating the association between remaining bambusoid, oryzoid, and pooid grasses (BOP clade). Support for the BOP clade was low (decay index of 1) based on ndhF sequences but was strong (decay index of 9) using phytochrome gene sequences (Clark, Zhang, and Wendel, 1995
; Mathews and Sharrock, 1996
).
Molecular markers identified in this study provide valuable information on the phylogenetic alliance of some disputable tribes/genera. The Stipeae have been placed in the Arundinoideae (Tateoka, 1957
) and Festucoideae/Pooideae (e.g., Stebbins and Crampton, 1961
; Hilu and Wright, 1982
; Clayton and Renvoize, 1986
; Clark, Zhang, and Wendel, 1995
). Arguments related to the inconsistent taxonomic placement of the Stipeae are discussed in Barkworth and Everett (1987)
. The lack of the 6-bp insertion characterizing the PACC clade suggests that the Stipeae are not closely related to the Arundinoideae. The phylogenetic position of Ehrharta (Ehrharteae) has also been questioned. This genus has been included in the Pooideae, Oryzoideae, and Arundinoideae (discussed in Hilu and Wright, 1982
). Although Ehrharta has an autapomorphic deletion that results in early termination of the matK gene, it should be excluded from the Arundinoideae due to its lack of the 6-bp insertion. Recent molecular studies of the Poaceae support the nonarundinoid position of Ehrharta, placing it sister to the Oryzeae (Clark, Zhang, and Wendel, 1995
; Soreng and Davis, 1998
).
The 3' region also provides some resolution within certain subfamilies (tree not shown). In the Pooideae, the third codon (amino acid site 3; Fig. 2) yields two synapomorphies when compared with Soreng and Davis' (1998)
combined phylogeny: lysine unites the Poeae and Aveneae, and aspartate distinguishes Stipa and Nassella (Stipeae). This is noteworthy because all other grasses and monocots examined have an asparagine at this site. This study, thus, points to higher variability in the matK 3' end of Pooideae compared with other grass subfamilies. Diversity of prolamin polypeptide components in Poaceae also supports increased levels of variation in this subfamily (Hilu and Esen, 1988
; Hilu, in press). In the Chloridoideae, a synapomorphy at nucleotide site 13 (Fig. 2) characterizes members of the Pappophoreae, Uniolinae, and some Eragrostis species. In a comprehensive study of the Chloridoideae using complete matK sequences, these taxa form a strongly supported basal clade (Hilu and Alice, in press).
Evolutionary and functional significance of matK indels
The rate and pattern of variation in matK sequences suggest that this gene is not as functionally constrained as rbcL (Steele and Vilgalys, 1994
; Hilu and Liang, 1997
). Systematic studies using matK sequences within and among families have shown that indels do occur in this gene and some are phylogenetically informative (Johnson and Soltis, 1994, 1995
; Steele and Vilgalys, 1994
; Plunkett, Soltis, and Soltis, 1996, 1997
; Kron, 1997
; Xiang, Soltis, and Soltis, 1998
; Kron et al., in press
). Yet, Plunkett, Soltis, and Soltis (1997)
noted that indels are relatively rare in matK sequences. The indels determined in these studies range in length from 1 to 12 bp, with the majority being a multiple of three. Within the Ericaceae, Kron (1997) and Kron et al. (in press) reported a 5-bp insertion and a 1-bp deletion, although their positions and impact on the ORF were not discussed.
Length mutations that are not in multiples of three theoretically could occur at any point in a coding region. However, the farther upstream a frameshift mutation occurs in a gene, the more nonsynonymous substitutions it will generate unless the ORF is restored by another indel. Frameshift and restoration in single-copy and functionally essential genes require two simultaneous and independent mutational events, usually a low-probability situation. If a restoration indel does not arise, either a truncated product or pseudogene will be produced depending on the distance of the mutation from the stop codon. An individual possessing such a mutation is likely to experience strong negative selection if the region in which it occurs is functionally and structurally important for the gene product. Thus, the likelihood of a frameshift mutation becoming established in a population would decrease as distance from the termination codon increases. This assessment is supported by Ems et al.'s (1995)
observation that among the nine matK sequences they examined from across the plant kingdom, only indels in multiples of three are found in the 5' region. It is, therefore, conceivable that the frameshift mutations observed here in matK of grasses would be confined to the extreme 3' end. Functionally important regions are less likely to accommodate frameshift mutations regardless of their distance from the stop codon as is the case in domain X of maturase genes (Ems et al., 1995
; Hilu and Liang, 1997
).
Indels and nucleotide substitutions at the 3' end of matK provide valuable phylogenetic markers in Poaceae and may yield characters useful in phylogeny reconstruction of other plant taxa. Available data suggest that length of the matK ORF at the 3' end varies among major plant groups. A greater sampling of matK within and among other plant families is, therefore, needed to further assess patterns of variation in and evolutionary significance of this region.
FOOTNOTES
1 The authors thank the U.S. Department of Agriculture-Agricultural Research Service, National Plant Germplasm System for seeds; N. Barker, L. Clark, J. Davis, G. Fleming, S. Jacobs, O. Mistretta, and the Missouri and University of Bonn Botanical Gardens for providing material; T. Borsch and T. Bodo Slotta for unpublished sequences; Patty Singer of the University of Maine DNA sequencing facility; and J. Bond, G. Davidse, and C. Neinhuis for their assistance. This work was supported by NSF grant number DEB 9634231 to KWH. 
LITERATURE CITED
Barker, N. P., H. P. Linder, and E. H. Harley. 1995 Polyphyly of Arundinoideae (Poaceae): evidence from rbcL sequence data. Systematic Botany 20: 423–435. [CrossRef][ISI]
Barkworth, M. E., and J. Everett. 1987 Evolution in the Stipeae: identification and relationships of its monophyletic taxa. In T. R. Soderstrom, K. W. Hilu, C. S. Campbell, and M. A. Barkworkth [eds.], Grass systematics and evolution, 251–264. Smithsonian Institution Press, Washington, DC.
Clark, L. G., and E. J. Judziewicz. 1996 The grass subfamilies Anomochlooideae and Pharoideae (Poaceae). Taxon 45: 641–645. [CrossRef][ISI]
———, W. Zhang, and J. F. Wendel. 1995 A phylogeny of the grass family (Poaceae) based on ndhF sequence data. Systematic Botany 20: 436–460.
Clayton, W. D., and S. A. Renvoize. 1986 Genera Graminum. HMSO Publications, London.
Clegg, M. T., B. S. Gaut, G. H. Learn, and B. R. Morton. 1994 Rates and patterns of chloroplast DNA evolution. Proceeding of the National Academy of Sciences, USA 91: 6795–6801.
Cummings, M. P., L. M. King, and E. A. Kellogg. 1994 Slipped-strand mispairing in a plastid gene: rpoC2 in grasses (Poaceae). Molecular Biology and Evolution 11: 1–8. [Abstract]
Davis, J. I., and R. J. Soreng. 1993 Phylogenetic structure in the grass family (Poaceae) as inferred from chloroplast DNA restriction site variation. American Journal of Botany 80: 1444–1454. [CrossRef][ISI]
Duvall, M. R., and B. R. Morton. 1996 Molecular phylogenetics of Poaceae: an expanded analysis of rbcL sequence data. Molecular Phylogenetics and Evolution 5: 352–358. [CrossRef][ISI][Medline]
Ems, S. C., C. W. Morden, C. K. Dixon, K. H. Wolfe, C. W. Depamphilis, and J. D. Palmer. 1995 Transcription, splicing and editing of plastid RNAs in the nonphotosynthetic plant Epifagus virginiana. Plant Molecular Biology 29: 721–733.
Esen, A., and K. W. Hilu. 1989 Immunological affinities among subfamilies of the Poaceae. American Journal of Botany 76: 196–203. [CrossRef][ISI]
Hilu, K.W. In press. Contributions of prolamin size diversity and structure to the systematics of the Poaceae. In S. W. L. Jacobs and J. Everett [eds.], Grass systematics and evolution, vol. 2, Proceedings of 2nd International Conference on the Comparative Biology of Monocotyledons, 1998, Sydney Australia. CSIRO Press, Melbourne.
———, and L. A. Alice. In press. Phylogenetic relationships in subfamily Chloridoideae (Poaceae) based on matK sequences: A preliminary assessment. In S. W. L. Jacobs and J. Everett [eds.], Grass systematics and evolution, vol. 2, Proceedings of 2nd International Conference on the Comparative Biology of Monocotyledons, 1998, Sydney, Australia. CSIRO Press, Melbourne.
———, ———, and H. Liang. In press. Phylogeny of Poaceae inferred from matK sequences. Annals of the Missouri Botanical Garden.
———, and A. Esen. 1988 Prolamin size diversity in the Poaceae. Biochemical Systematics and Ecology 16: 457–465. [CrossRef]
———, and ———. 1990 Prolamin and immunological studies in Poaceae. I. Subfamily Arundinoideae. Plant Systematics and Evolution 173: 57–70.
———, and ———. 1993 Prolamin and immunological studies in the Poaceae: III. Subfamily Chloridoideae. American Journal of Botany 80: 104–113. [CrossRef][ISI]
———, and H. Liang. 1997 The matK gene: sequence variation and application in plant systematics. American Journal of Botany 84: 830–839. [Abstract]
———, and K. Wright. 1982 Systematics of Gramineae: a cluster analysis study. Taxon 31: 9–36. [CrossRef][ISI]
Johnson, L. A., and D. E. Soltis. 1994 matK DNA sequences and phylogenetic reconstruction in Saxifragaceae s. str. Systematic Botany 19: 143–156.
———, and ———. 1995 Phylogenetic inference in Saxifragaceae sensu stricto and Gilia (Polemoniaceae) using matK sequences. Annals of the Missouri Botanical Garden 82: 149–175. [CrossRef][ISI]
Kron, K. A. 1997 Phylogenetic relationships of Rhododendroideae (Ericaceae). American Journal of Botany 84: 973–980. [Abstract]
———, R. Fuller, D. M. Crayn, P. A. Gadek, and C. J. Quinn. In press. Phylogenetic relationships of epacrids and vaccinioids (Ericaceae s. l.) based on matK sequence data. Plant Systematics and Evolution.
Liang, H., and K. W. Hilu. 1996 Application of the matK gene sequences to grass systematics. Canadian Journal of Botany 74: 125–134. [CrossRef]
Mathews, S., and R. A. Sharrock. 1996 The phytochrome gene family in grasses (Poaceae): a phylogeny and evidence that grasses have a subset of the loci found in dicot angiosperms. Molecular Biology and Evolution 13: 1141–1150. [Abstract]
Nadot, S., R. Bajon, and B. Lejeune. 1994 The chloroplast gene rps4 as a tool for the study of Poaceae phylogeny. Plant Systematics and Evolution 191: 27–38. [CrossRef][ISI]
Nielsen, R. 1997 The ratio of replacement to silent divergence and tests of neutrality. Journal of Evolutionary Biology 10: 217–231. [CrossRef][ISI]
Palmer, J. D., and W. F. Thompson. 1981 Rearrangements in the chloroplast genomes of mung bean and pea. Proceedings of the National Academy of Sciences, USA 78: 5533–5537.
Plunkett, G. M., D. E. Soltis, and P. S. Soltis. 1996 Evolutionary patterns in Apiaceae: inferences based on matK sequence data. Systematic Botany 21: 477–495. [CrossRef][ISI]
———, ———, and ———. 1997 Clarification of the relationship between Apiaceae and Araliaceae based on matK and rbcL sequence data. American Journal of Botany 84: 565–580. [Abstract]
Soderstrom, T. R. 1981 Some evolutionary trends in the Bambusoideae (Poaceae). Annals of the Missouri Botanical Garden 68: 15–47. [CrossRef][ISI]
———, and C. E. Calderón. 1979 A commentary on the bamboos (Poaceae: Bambusoideae). Biotropica 11: 161–172.
Soltis, D. E., C. Hibsch-Jetter, P. S. Soltis, M. W. Chase, and J. S. Farris. 1997 Molecular phylogenetic relationships among angiosperms: An overview based on rbcL and 18S rDNA sequences. In K. Iwatsuki and P. H. Raven [eds.], Evolution and diversification of land plants, 157–178. Springer, Tokyo.
Soreng, R. J., and J. I. Davis. 1998 Phylogenetics and character evolution in the grass family (Poaceae): Simultaneous analysis of morphological and chloroplast DNA restriction site character sets. Botanical Review 64: 1–85.
Stebbins, G. L. 1956 Cytogenetics and evolution of the grass family. American Journal of Botany 43: 890–905. [CrossRef][ISI]
———, and B. Crampton. 1961 A suggested revision of the grass genera of temperate North America. Recent Advances in Botany 1: 133–145.
Steele, K. P., and R. Vilgalys. 1994 Phylogenetic analyses of Polemoniaceae using nucleotide sequences of the plastid gene matK. Systematic Botany 19: 126–142.
Tateoka, T. 1957 Miscellaneous papers on the phylogeny of Poaceae (10): proposition of a new phylogenetic system of Poaceae. Journal of Japanese Botany 32: 275–287.
Wolfe, K. H., C. W. Morden, and J. D. Palmer. 1992 Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plants. Proceedings of the National Academy of Sciences, USA 89: 10648–10652.
Xiang, Q.-Y., D. E. Soltis, and P. S. Soltis. 1998 Phylogenetic relationships of Cornaceae and close relatives inferred from matK and rbcL sequences. American Journal of Botany 85: 285–297. [Abstract]
This article has been cited by other articles:
|
|
 |
|
  J. V. Freudenstein and D. M. Senyo Relationships and evolution of matK in a group of leafless orchids (Corallorhiza and Corallorhizinae; Orchidaceae: Epidendroideae) Am. J. Botany, April 1, 2008; 95(4): 498 - 505. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Dane and P. Lang Sequence variation at cpDNA regions of watermelon and related wild species: implications for the evolution of Citrullus haplotypes Am. J. Botany, November 1, 2004; 91(11): 1922 - 1929. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. W. Hilu, T. Borsch, K. Muller, D. E. Soltis, P. S. Soltis, V. Savolainen, M. W. Chase, M. P. Powell, L. A. Alice, R. Evans, et al. Angiosperm phylogeny based on matK sequence information Am. J. Botany, December 1, 2003; 90(12): 1758 - 1776. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Matsuoka, Y. Yamazaki, Y. Ogihara, and K. Tsunewaki Whole Chloroplast Genome Comparison of Rice, Maize, and Wheat: Implications for Chloroplast Gene Diversification and Phylogeny of Cereals Mol. Biol. Evol., December 1, 2002; 19(12): 2084 - 2091. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. T. Chandler, R. J. Bayer, and M. D. Crisp A molecular phylogeny of the endemic Australian genus Gastrolobium (Fabaceae: Mirbelieae) and allied genera using chloroplast and nuclear markers Am. J. Botany, September 1, 2001; 88(9): 1675 - 1687. [Abstract] [Full Text]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
