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Chapter 1 Introduction
1.1 DNA Sequence in Plant Systematics
Although nucleic acid sequencing is a relatively new approach in plant systematics, the
power of the technique and the data generated have made it become one of the most utilized of
the molecular approaches for inferring phylogenetic history. DNA sequence data are the most
informative tool for molecular systematics, and comparative analysis of DNA sequences is
becoming increasingly important in plant systematics. There are two major reasons why
nucleotide sequencing is becoming so valuable in plant systematics: 1) the characters
(nucleotides) are the basic units of information encoded in organisms; 2) the potential sizes of
informative data sets are immense. For example, one in 100 nucleotides is polymorphic in the
human genome so that there will be about 2 × 107 polymorphisms in the human genome as a
whole. Thus, for most studies, systematically informative variation is essentially inexhaustible.
Furthermore, different genes or parts of the genome might evolve at different rates. Therefore,
questions at different taxonomic levels can be addressed using different genes or different
regions of a gene.
Unlike animals, plants have an additional genome, chloroplast genome (cpDNA) in
addition to the nuclear (nDNA) and mitochondrial (mtDNA) genomes.
Because of its
complexity and repetitive properties, the nuclear genome is used in systematic botany less
frequently. The mitochondrial genome is used at the species level due to its rapid changes in its
structure, size, configuration, and gene order. On the other hand, the chloroplast genome is
well suited for evolutionary and phylogenetic studies particularly above the species level,
because cpDNA, 1) is a relatively abundant component of plant total DNA, thus facilitating
extraction and analysis; 2) contains primarily single copy genes; 3) has a conservative rate of
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nucleotide substitution; and 3) extensive background for molecular information on the
chloroplast genome is available.
Therefore, most phylogenetic reconstructions in plant
systematics conducted so far is based on molecular data from the cpDNA genes.
The most common gene used to provide sequence data for plant phylogenetic analyses
is the plastid-encoded rbcL gene (Chase et al., 1993; Donoghue et al., 1993). This single copy
gene is approximately 1430 base pairs in length, is free from length mutations except at the far
3' end, and has a fairly conservative rate of evolution. The function of the rbcL gene is to code
for the large subunit of ribulose 1, 5 bisphosphate carboxylase/oxygenase (RUBISCO or
RuBPCase). The sequence data of the rbcL gene are widely used in the reconstruction of
phylogenies throughout the seed plants. However, it is apparent that the ability of rbcL to
resolve phylogenetic relationships below the family level is often poor (Doebley et al., 1990).
Thus, interest exists in finding other useful DNA regions that evolve faster than does rbcL to
facilitate lower-level phylogenetic reconstruction. The matK gene is a promising gene in this
regard.
1.2 The matK Gene
1.2.1 Overview of the matK Gene
The matK gene was first identified by Sugita et al. (1985) from tobacco (Nicotiana
tabacum) when they sequenced the trnK gene encoding the tRNALys (UUU) of the chloroplast.
They found a 509 codon major open reading frame (ORF) in the intron of the trnK gene; no
function for the ORF509 was assumed. The complete sequence of the liverwort Marchantia
polymorpha (Ohyama et al., 1986) confirmed the existence of this open reading frame in the
non-vascular plant. Later, Neuhaus and Link (1987) found that the anticodon loop of the
tRNALys was interrupted by a 2,574 base pair intron containing a long open reading frame for
524 amino acids in mustard (Sinapis alba). They suggested a possible maturase function of the
matK gene for the first time based upon a homology search result. This open reading frame
was identified in the complete sequence of rice (Oryza sativa) chloroplast genome, as well
(Hiratsuka et al., 1989).
The trnK gene from two pine species (Pinus contorta and P.
thunbergii) also contained the open reading frame (Lidholm and Gustafsson, 1991). This open
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reading frame is flanked by two exons of the trnK gene in all land plants studied so far with
only one exception. In beech drop (Epifagus virginiana), the matK gene appeared as a freestanding gene with neither the trnK exons nor the interrupting introns present (Wolfe et al.,
1992).
1.2.2 Function of the matK gene: maturase MatK
The first putative function of the matK gene came from a sequence homology search
through the GenBank, databases for DNA sequences. Neuhaus and Link (1987) found that a
segment near the carboxyl terminus of the derived Sinapsis alba matK polypeptide was
structurally related to portions of the maturase-like polypeptides of introns of the mitochordrial
cytochrome c oxidase subunit I gene (COXI) of yeast and Podospora anserina. In later
analyses (Ems et al., 1995) it was hypothesized that the putative maturase, MatK, acts to assist
the splicing of group II introns other than the one in which it is normally encoded. Two good
candidates are the single group II intron in rpl2 and the second intron in rps12. The maturase
MatK presumably helps fold the intron RNA into the catalytically-active structure. The 3’ end
of the matK was identified to contain a conserved region of about 100 amino acids and this
region was named domain X (Mohr et al., 1993; Liang and Hilu, 1996). Comparison of group
II introns (Mohr et al., 1993) indicated that three domains (reverse transcriptase, Zn-fingerlike, and X domain) existed in the ancestral open reading frame of all group II introns. During
the evolutionary process, the reverse transcriptase and Zn-finger-like domains were lost in
some cases. The retention of domain X supports the hypothesis that the matK gene plays an
essential function in RNA splicing.
1.2.3 Application of the matK gene to plant systematics
There have been several studies using the matK gene sequence in phylogenetic
reconstruction. These studies involved six families. In Saxifragaceae, matK was found to
evolve approximately three-fold faster than rbcL (Johnson and Soltis, 1994, 1995; Johnson et
al., 1996). The sequences of matK in Polemoniaceae varied at an overall rate twice that of
rbcL sequences (Steele and Vilgalys, 1994; Johnson and Soltis, 1995). Substitutions at the
third codon position predominated in rbcL sequences, while in matK substitutions were more
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evenly distributed across codon positions. Recently, the matK gene sequences have been also
used in Orchidaceae tribe Vandeae (Jarrell and Clegg, 1995), Myrtaceae (Gadek et al.
1996), Poaceae (Liang and Hilu 1996), Apiaceae (Plunkett et al. 1996), and flowering plants
(Hilu and Liang, 1997). According to the detailed analysis of the matK sequence data
available in Gene Bank and preliminary studies (Liang and Hilu, 1996; Hilu and Liang, 1997),
matK has higher variation than any other chloroplast genes. Although the variation is slightly
higher at the 5’ region than at the 3’ region, approximate even distribution was observed
throughout the entire gene. In addition, the high proportion of tranversion of the matK gene
might provide more phylogenetic information. These factors underscore the usefulness of the
matK gene in systematic studies and suggest that comparative sequencing of matK may be
appropriate for phylogenetic reconstruction at subfamily and family levels.
1.3 Grass Family (Poaceae)
1.3.1 Size and Importance
The grass family (Poaceae) is the fourth largest flowering plant family, with 651
genera and about 10,000 species (Clayton and Renvoize, 1986). Included in this family
are many important cereal crops, such as wheat, maize, barley, rice and sorghum, and
economic plants such as sugar cane, bamboo and turf grasses. There are possible energy
sources such as sweet sorghum, sugar cane and maize for alcohol which could be very
valuable in industrial societies. Grasslands are valuable resources for grazing, and are
ecologically important as well.
1.3.2 Poaceae History
Fossil evidence indicates that Poaceae may have first appeared in the Late
Cretaceous, approximately 70 million years ago (Thomasson, 1987). Although there are
many fossil records for the grass family, the ambiguity caused by their similarity to several
related families such as Cyperaceae and Juncaceae greatly reduces their application value.
The extant grass species share many unique characters in their stems, leaves, flowers and
inflorescences, and caryopsis fruits, and are placed in Liliopsida (Monocotyledonae)
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(Stebbins, 1982, 1987). The monogeneric Joinvilleaceae is thought to be the most closely
related family to Poaceae, since Poaceae and Joinvilleaceae are phylogenetically allied and
share a very unique inverted repeat of about 6 kilobases in their chloroplast genomes
(Doyle et al., 1992).
Thus, Joinvillea is the best outgroup for Poaceae in cladistic
analyses.
The grass family was first named by de Jussieu (1789), and the grouping of the 58
genera in his treatment was mainly based on numerical characters, such as number of
styles, stamens and florets. In 1814, the grass family was divided into two “tribes”:
Paniceae with a basal reduction of the spikelets and Poaceae with an apical reduction of
the spikelets (Brown, 1814). Later, with additional evidence from leaf epidermis and
anatomy (Prat, 1936; Brown, 1958), chromosome number and morphology (Avdulov,
1931), embryo structure (Reeder, 1957), and numerical taxonomy (Hilu and Wright,
1982; Watson et al., 1985), a better understanding of grass systematics was achieved and
various subfamily systems were proposed. With the introduction of molecular data such
as from proteins and nucleic acids, more grouping patterns and evolutionary lineages of
the grass family were presented (Hamby and Zimmer, 1988; Hilu and Esen, 1988; Doebley
et al., 1990; Davis and Soreng, 1993; Cummings et al., 1994; Hsiao et al., 1994; Nadot et
al., 1994; Barker et al., 1995; Clark et al., 1995; Duvall and Morton, 1996). Although the
number of subfamilies recognized in these publications varied from 5 to 13, the following
major groups are commonly recognized: Aundinoideae, Bambusoideae, Centothecoideae,
Chloridoideae, Oryzoideae, Panicoideae and Pooideae.
1.3.3 Major Subfamilies
Bambusoideae
Bambusoideae contains both herbaceous and woody species, with 13 tribes and 91
genera (Clayton and Renvoize, 1986). All species of this subfamily are C3 and without
Kranz structure in leaf anatomy. Most species in this subfamily also have elongated,
finger-like microhairs.
Bambusoideae has distinctive anatomy: arm and fusoid cells,
sclerome tissue around the leaf midrib, and vertically oriented silica bodies. However,
most herbaceous bamboos do not show these anatomical characters. Based upon the
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recent ndhF sequence data, two new subfamilies were proposed that include the
herbaceous bamboos: Anomochloa and Pharus (Clark and Judziewcz, 1996).
Bambusoideae has been suggested to be the basal group of the grass family according to
its morphological, anatomical, cytogenetic and molecular characters (Stebbins, 1956; Hilu
and Wright, 1982; Kellogg and Campbell, 1987; Kellogg and Watson, 1993).
Oryzoideae
Oryzoideae has been treated as tribe Oryzeae in the Bambusoideae because it has
arm cells and finger-like microhairs, which are shared with bambusoid species. However,
fusoid cells are not always present. According to numerical and immunological studies,
Oryzeae should be treated as a separate subfamily Oryzoideae (Hilu and Wright, 1982;
Esen and Hilu, 1989). All species of Oryzoideae are C3.
Pooideae
Pooideae has been called Festucoideae and is one of the largest subfamilies of
Poaceae with about 160 genera and 3000 species (Clayton and Renvoize, 1986).
Pooideae is characterized by the absence of microhairs, C3 pathway, and a unique stoma
with parallel-sided subsidiary and overlapped guard cells.
Panicoideae
Most panicoid species have C4 pathway, and a unique intermediate C3-C4 type
exists in this subfamily in some Panicum species (Morgan and Brown, 1979).
Occasionally, a single species such as Alloteropsis semialate has both C3 and C4 pathways
(Ellis, 1974). These species are of particular interest both functionally and taxonomically
and could help to understand the evolution of the C4 photosynthetic pathway. Panicoideae
includes 7 tribes and 207 genera and is mostly characterized by its spikelet characters
(Clayton and Renvoize, 1986). Anatomically, it is a diverse group (Ellis, 1987).
Chloridoideae
Chloridoideae includes about 5 tribes and 145 genera and all are C4 except for one
species of Eragrostis (Clayton and Renvoize, 1986). Chloridoid species are anatomically
distinct with inflated, spherical microhairs and Kranz structure.
This subfamily was
considered to be a homogeneous group but the homogeneity has been questioned by
numerical and molecular studies (Hilu and Wright, 1982; Esen and Hilu, 1989).
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Arundinoideae
Arundinoideae is a diverse assemblage without reliable diagnostic features. Most
arundinoid species are C3 with Kranz structure and rarely C4 without Kranz structure.
There are no arm cells or fusoid cells in this subfamily, but elongated, finger-like
microhairs exist throughout arundinoid species. The subfamily has 4 tribes and 45 genera
and is a taxonomically problematic group (Clayton and Renvoize, 1986).
Centothecoideae
Centothecoideae is a small monotribal subfamily with 10 genera (Clayton and
Renvoize, 1986). The subfamily is mainly characterized by its distinctive embryo and was
previously treated as a tribe Centotheceae in subfamily Arundinoideae (Stebbins, 1956;
Tsvelev, 1983).
1.3.4 Difficulties in Grass Systematics
Compared to other plant families, systematics and evolutionary studeis in Poaceae
have the following particular difficulties: 1) large numbers of taxa to cover; 2) the
simplicity of floral and vegetative morphology; 3) coexistance of advancement and
reduction for their character evolution, or bidirectional character evolution, which makes
it difficult to determine the polarity of a character during phylogenetic analyses (Stebbins,
1987); 4) widespread hybridization and polyploidy. About 80% of the taxa studied for
chromosome numbers have undergone polyploidy sometime during their evolutionary
histories (de Wet, 1987); and 5) frequent parallel evolution caused by adaptation to
similar environments and mosaic evolution of different characters at different rates along
the same line (Stebbins, 1956, 1987; Hilu and Wright, 1982; Pohl, 1987).
Because of these difficulties, the systematics and evolution of the Poaceae has been
studied extensively in the past few decades using morphological, anatomical, cytological,
numerical, physiological, biochemical, and molecular approaches. Among these methods,
DNA sequencing appears to be very promising.
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1.4 Previous Studies on Poaceae Using DNA Sequences
There are only ten publications focusing on phylogenetic reconstruction using
DNA sequence data in the grass family; earliest being that of Hamby and Zimmer (1988).
Three studies utilized the non-coding intergenic transcription region (ITS) and
phytochrome gene (Hamby and Zimmer 1988; Hsiao et al. 1994; Mathews and Sharrock,
1996). Most used the chloroplast genome, especially the rbcL gene (Doebley et al., 1990;
Barker et al., 1995; Duvall and Morton, 1996). The species number included in these
studies ranged from 9 to 45 and the subfamilies involved were 3 to 7. Different lengths of
DNA were used in these studies and the informative sites ranged from 85 of 18S rRNA
and 26S rRNA to 487 of ndhF (Clark et al., 1995). The most common outgroup is
Joinvillea in the Joinvilleaceae, but some studies used very distant outgroups such as
Nicotiana and Spinacia (Doebley et al., 1990; Cummings et al., 1994). Some of the
previous nucleic acid studies were not comprehensive because of their small sample sizes
that did not include the major groups of the grass family, or they had insufficient
information to resolve the major lineages (Hamby and Zimmer, 1988; Doebley et al.,
1990; Hsiao et al., 1994; Nadot et al., 1994).
As to the phylogenies of Poaceae generated from the previous studies using DNA
sequence data, there are some consistencies and disagreements. The following points and
questions remain to be resolved.
1) Which group is the root of the grass family? Bambusoideae appears most
likely to be the most primitive subfamily of Poaceae. The DNA sequence
studies involving bambusoid species done so far supported the primitive
postion of Bambusoideae and it appeared as the basal group of the grass family
phylogeny. The results agree with its trimerous flowering parts and bracteate
indeterminate inflorescence, which are considered to be primitive characters.
However, other subfamilies that were also suggested to be the basal group of
Poaceae are Oryzoideae (Hsiao et al., 1994), Arundinoideae (Cummings et al.,
1994) or Panicoideae (Doebley et al., 1990). While the Clark et al. (1995) study
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indicated a polyphyletic origin of the Bambusoideae, all other studies
supported its monophyletic position.
2) Is Aundinoideae a polyphyletic or monophyletic group? Most nucleic acid
studies supported the polyphyletic origin of Aruninoideae. Among the four
studies including species from Arundinoideae, only one supported the
monophyletic orgin of this group; the study included only two species of the
Arundinoideae (Duvall and Morton, 1996).
These results confirmed that
Arundinoideae might be a diverse assemblage without reliable diagnostic
features in their morphology. The relationships between Arundinoideae and
other groups varied from one study to another. Arundinoideae was grouped
with Pooideae (Cummings et al., 1994), with Panicoideae (Clark et al., 1995),
or with Chloridoideae (Barker et al., 1995).
3) What is the systematic position of oryzoid species? In most cases, it appears as
a clade near to the basal lineage Bambusoideae. However, it was also grouped
with Panicoideae and in one study it appeared as a polyphyletic group
(Cummings et al., 1994).
4) What is the circumscription of Pooideae?
Most studies supported the
monophyly of the Pooideae, with one exception (Cummings et al., 1994). In
the cladogram of that study, Pooideae was separated by a species of
Arundinoideae (Lygenum spartum). This result indicates that Pooideae is a
group of very closely related taxa and agrees with its obvious diagnostic
morphological characters of C3 pathway, a unique stoma and absence of
microhairs throughout the subfamily (Ellis, 1987).
5) Is Panicoideae a monophyletic or polyphyletic group? Based on the rbcL gene
result, Pancoideae is a monophyletic group (Barker et al. 1995). However,
ndhF and rpoC2 data indicated that Panicoideae was a polyphyletic group
(Cummings et al., 1994; Clark et al., 1995). While only one study showed that
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Panicoideae was the basal lineage of the grass family (Doebley et al., 1990), all
other studies placed the Panicodeae near the bases of the cladograms.
6) Chloridoideae is a poorly studied group. Morphologically, Chloridoideae is
not a well defined group despite its large number of species.
The
representatives of Chloridoideae were included in only three studies (Barker et
al., 1995; Clark et al. 1995; Duvall and Morton 1996). The chloridoid species
always were grouped together as a single group and appeared to be related to
Arundinoideae. The monophyletic origin of Chloridoideae based on DNA
sequences is not supported by the previous numerical and immunological
studies (Hilu and Wright, 1982; Hilu and Esen, 1988).
7) Centhothecoideae is a small group with questionable phylogenetic status.
Based on its morphology and anatomy, it was placed within the Arundinoideae.
The current nucleic acid results suggested that it was related either to
Panicoideae or Arundinoideae (Barker et al., 1995; Clark et al., 1995). Thus,
it remains to be seen if this group of grasses deserves a subfamily status and
where it should be in the grass phylogeny.
8) There are some problematic tribes or genera, such as Aristedeae, Stipeae,
Bromus, Brachpodium and Ehrharta.
These tribes or genera often share
morphological and anatomical characters from different groups and their
taxonomic positions are not well resolved.
There are about 40 tribes in the grass family according to common classification
systems. Most studies so far only covered few tribes and used one or two representative
species from each tribe.
Table 1.1 summarizes the sample representatives for these
previous DNA sequence studies.
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Table 1.1 Tribes and genera in the previous studies with DNA sequence
Subfamilies and tribes
Bambusoideae
Anomochloeae
Bambuseae
Brachyelytreae
Diarrheneae
Ehrharteae
Olyreae
Oryzeae
Phaenospermatae
Phareae
Streptochaeteae
Pooideae
Aveneae
Poeae
Stpeae
Triticeae
Centostecoideae
Centotheceae
Arundinoideae
Aristideae
Arundineae
Micrairaeae
Thysanolaeneae
Chloridoideae
Chlorideae
Eragrosteae
Pappophoreae
Zoysieae
Panicoideae
Andropogoneae
Arundinelleae
Paniceae
Species
13 tribes and 91 Genera
Anomochloa
Arundinaria, Bambusa, Cephalostachyum, Chesquea,
Guadua, Phyllostachys
Brachyelytrum
Diarrhena
Ehrharta
Lithachne, Olyra, Raddia
Leersia, Lithachne, Oryza, Zizania
Phaenosperma
Pharus
Streptochaeta,
10 tribes and 152 Genera
Avena
Poa, Puccinellia
Stipa
Aegilops, Hordeum, Triticum
1 tribe and 10 genera
Zeugites, Chasmanthium
4 tribes and 45 genera
Aristida, Stipagrostis
Arundo, Centropodia, Danthonia, Gynerium, Karroochloa,
Merxmuellera, Moliniopsis, Monachather, Rytidosperma,
Plinthanthesis, Molinia, Pharagmites
Micraira
Thysanolaena
5 tribes and 145 genera
Eustachys
Eragrostis, Erioneuron, Muhlenbergia, Sporobolus
Enneapogon
Zoysia
7 tribes and 207 genera
Hyparrhenia, Saccharum, Sorghum, Tripsacum, Zea
Danthoniopsis, tristachya
Neurachne, Panicum, Pennisetum, Setaria
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1.5 Objectives of the Research
There are three major objectives for this research. The first one is to study the utility of
the matK gene in plant evolution. For this goal, the following questions will be answered:
1. How much variation does the matK gene have? What proportion of the variation is
phylogenetically informative? Are there any differences in this variation for different
plant groups?
2. What is the distribution of the variation throughout the different regions of the matK
gene?
Which part of the matK gene is variable and which part is more
conservative?
3. What is the phylogeny of the representative species from various plant groups
generated from the matK gene sequences? Which part of the matK gene provides
more reliable phylogenetic information? And at which taxonomic level could these
regions be used to reconstruct a phylogeny?
4. How many nucleotides of the matK gene are sufficient to generate a robust
phylogeny and from which part of the matK gene?
The second objective is to characterize the matK gene in the grass family. The
following questions will be addressed:
1. What is the rate and pattern of nucleotide variation of the matK gene in Poaceae?
2. What are the transition and transversion ratios (tr/tv) among the major groups of
Poaceae?
Is the (tr/tv) related to G+C content or region specific in the gene?.
Transition and transversion are important characters in phylogenetic reconstruction
since transition tend to be weighted heavily in some studies.
Is there any
relationships between the (tr/tv) and the phylogenetic hierarchy of Poaceae?
3 At which taxonomic levels is the matK gene useful in Poaceae? Which parts of the
matK gene have more phylogenetic signal for the Poaceae?
The last major goal is to address the phylogenetic questions in the Poaceae using the
matK sequences from representatives of different grass groups .
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1. How many subfamilies should the grass family be divided into? What are the
relationships among these subfamilies? Which individual subfamilies are
monophyletic and which are polyphyletic?
2. Are the pooids, bambusoids senso lato, or herbaceous bamboos the most basal
lineages in the family? Is there an early major dichotomy in the Poaceae, such
as the PACC (Panicoideae, Arundinoideae, Centeostheocoideae and Chloridoideae)
and BOP (Bambusoideae, Oryzoideae, and Pooideae) clades?
Do some
herbaceous bamboos represent a distinct phylogenetic entity that deserves a
subfamilial taxonomic treatment?
3. Do the oryzoid and bambusoid grasses represent a single monophyletic taxon?
Should the oryzoids be considered as a separate family?
4. Is the PACC clade a monophyletic group?
5. Where does the Centothecoideae belong in the phylogeny?
6. What are the taxonomic position of some of the problematic tribes or genera:
Stipeae, Aristedeae, Brachpodieae, Ehrharta and Bromus.
This dissertation has six chapters. Chapter 1 (this chapter) introduces the grass
family (Poaceae), the matK gene and the major objectives of the research. Chapter 2 deals
with the general analysis of the matK gene and its application in plant systematics; it has
been published in American Journal of Botany. Chapter 3 addresses the preliminary
applications of the matK gene to the phylogenetic reconstruction of Poaceae; it has been
published in Canadian Journal of Botany. Chapter 4 characterizes the matK genes in the
Poaceae from the 13 grass species and one outgroup (Joinvillea). Chapter 5 examines the
phylogeny of 48 grass species using Joinvillea as a outgroup based on 966 bps sequences
at the 3’ region of the matK gene. Chapter 6 will summarize the results and provide some
suggestions for future work.
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_____, AND G. JUDZIEWCZ.
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