Evolution of the mitochondrial genome: protist connections
to animals, fungi and plants
Charles E Bullerwell and Michael W Gray
The past decade has seen the determination of complete
mitochondrial genome sequences from a taxonomically
diverse set of organisms. These data have allowed an
unprecedented understanding of the evolution of the
mitochondrial genome in terms of gene content and order, as
well as genome size and structure. In addition, phylogenetic
reconstructions based on mitochondrial DNA (mtDNA)encoded protein sequences have firmly established the
identities of protistan relatives of the animal, fungal and plant
lineages. Analysis of the mtDNAs of these protists has provided
insight into the structure of the mitochondrial genome at the
origin of these three, mainly multicellular, eukaryotic groups.
Further research into mtDNAs of taxa ancestral and
intermediate to currently characterized organisms will help to
refine pathways and modes of mtDNA evolution, as well as
provide valuable phylogenetic characters to assist in unraveling
the deep branching order of all eukaryotes.
Addresses
Department of Biochemistry and Molecular Biology, Dalhousie
University, Room 8F-2, Sir Charles Tupper Medical Building,
5850 College Street, Halifax, Nova Scotia B3H 1X5, Canada
e-mail: [email protected]
Current Opinion in Microbiology 2004, 7:528–534
This review comes from a themed issue on
Genomics
Edited by Charles Boone and Philippe Glaser
Available online 11th September 2004
1369-5274/$ – see front matter
# 2004 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.mib.2004.08.008
Abbreviations
FMGP
Fungal Mitochondrial Genome Project
mtDNA mitochondrial DNA
OGMP
Organelle Genome Megasequencing Program
Introduction
The first mitochondrial genome to be completely
sequenced (in 1981) was that of Homo sapiens [1]. Over
the following decade, mitochondrial genome sequencing
focused on other members of the metazoan lineage, as
well as on ascomycete fungi (such as the yeast Saccharomyces cerevisiae [2]) and land plants (such as the liverwort
Marchantia polymorpha [3]). Although these data constituted an important starting point in the definition of
mitochondrial genomics, they were not sufficient for
determining the origin and evolution of mitochondrial
Current Opinion in Microbiology 2004, 7:528–534
DNA (mtDNA). For example, the first sequenced mitochondrial genomes of animals, fungi and plants were
found to have very dissimilar genome organizations that
did not immediately suggest common evolutionary origins. To address issues relating to mtDNA structural
diversity in the context of mitochondrial evolution, information was needed about mitochondrial genomes from
representatives spanning the phylogenetic breadth and
depth of eukaryotes (domain Eucarya). Of particular
importance in this regard were the protists, mainly unicellular organisms that encompass most of the evolutionary diversity of this domain.
Sequencing efforts over the past decade, particularly
those of the Organelle Genome Megasequencing Program (OGMP; http://megasun.bch.umontreal.ca/ogmp)
[4,5] and the Fungal Mitochondrial Genome Project
(FMGP; http://megasun.bch.umontreal.ca/People/lang/
FMGP/FMGP.html) [6,7] have greatly increased the
number of complete mtDNA sequences, and also their
phylogenetic diversity. This research has revealed a variety of genome structures, from the several hundred small
linear pieces found in the mitochondrion of the ichthyosporean Amoebidium parasiticum ([8], discussed below),
to the gene-rich eubacteria-like mitochondrial genome of
the jakobid flagellate Reclinomonas americana [9]. These
data, in combination with phylogenies based on mitochondrial protein sequences, have strongly supported a
monophyletic origin for the mitochondrial genome, specifically from within the a-Proteobacteria [5,10,11,12].
Despite enormous variations in genome size, ranging
from the tiny apicomplexan mtDNAs (6 kbp) to the
expansive plant mtDNAs (>150 kbp), the coding function of the mitochondrial genome has remained relatively
stable. In general, mtDNAs code only for genes involved
in the mitochondrial translation apparatus, electron transport and oxidative phosphorylation [12].
A particular goal of the OGMP and the FMGP was to
sequence the mitochondrial genomes of protists diverging basally to the animal, fungal and plant lineages. These
studies aimed to define the evolution of the mitochondrial
genome from the presumed protist ancestors of these
groups by identifying evolutionary intermediates. Candidates for these early diverging groups, based on morphological, ultrastructural and molecular evidence, included
the choanoflagellates (believed to represent early diverging unicellular ancestors of the animals), chytridiomycetes (believed to be related to fungi), and green algae
(believed to be specifically affiliated with the land plant
lineage).
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Evolution of the mitochondrial genome: protist connections to animals, fungi and plants Bullerwell and Gray 529
In this review, we focus on recent advances that have
helped to bridge the gap between the well-established
animal, fungal and plant lineages and their unicellular
protistan ancestors.
Clade Holozoa: choanoflagellates and
ichthyosporeans are specific relatives
of the animals
Choanocytes, the feeding cells of sponges, bear remarkable morphological similarity to members of the choanoflagellate protists. This resemblance, first recognized in
the 19th century, prompted the long-standing view that
sponges represent an early form of multicellular animal,
specifically related to choanoflagellates. However, in
eukaryotic phylogenies based on molecular sequence
data, the branching position of the choanoflagellates
has not been clear-cut (see [13] for discussion). Thus,
it has been argued that choanoflagellates are specific
relatives of either animals or fungi, or that they branch
before the divergence of animals and fungi. The specific
relationship of choanoflagellates to the metazoan lineage
has only recently been firmly established through phylogenetic reconstructions based on mitochondrial protein
sequence data [13] (Figure 1). This analysis also clearly
confirms a sister group of the animal-choanoflagellate
clade: the ichthyosporean protists. Ichthyosporeans, once
referred to as DRIPs (from the first initial of the four
founding members of the group [14]), were similarly
believed to have diverged near the animal-fungal split.
Based on these new data, Metazoa, Choanoflagellata and
Ichthyosporea can be considered a monophyletic group
(Holozoa [13]) that branches as a sister group to Fungi
(Figures 1 and 2).
With the identities of some relatively close protistan
relatives of the animals established, it was possible to
Figure 1
animals (>460)
sponges (0)
Holozoa
choanoflagellates (1)
ichthyosporeans (1)
ascomycetes (16)
basidiomycetes (2)
Fungi
zygomycetes (3)
chytridiomycetes (7)
land plants (6)
charophytes (2)
Viridiplantae
chlorophytes (10)
Current Opinion in Microbiology
Schematic phylogenetic tree illustrating the branching order within
Holozoa (red), Fungi (blue) and Viridiplantae (green). Numbers in
brackets indicate complete mtDNA sequences publicly available.
www.sciencedirect.com
infer the structure of the mitochondrial genome before
the emergence of multicellularity in this lineage. Of
particular interest was the timing of the transition from
the large, gene-rich mtDNAs seen in some protists to
the small, gene-poor mitochondrial genomes seen in
animals. For example, R. americana contains the most
ancestral (eubacteria-like) mtDNA identified to date: a
69 kbp genome that encodes almost 100 genes [9]. By
contrast, animal mitochondrial genomes are much smaller (with sizes ranging from 13 to 22 kbp) and are highly
compact [15], with open reading frames and tRNA
genes often overlapping, and some stop codons created
by the addition of a 30 oligo(A) tail to processed
mRNAs. Metazoan mtDNAs generally encode fewer
than 40 genes, a set that includes no ribosomal protein
genes.
The mitochondrial genome of Monosiga brevicollis, a choanoflagellate, is much larger than metazoan mtDNAs and
encodes many more genes than the latter [8]. M. brevicollis mtDNA is 76 568 bp long, circular mapping, and
encodes 55 different genes, including 11 specifying ribosomal proteins. This mtDNA is much more similar to
those of protists such as R. americana than to those of
multicellular animals. Genome content and organization
indicate that the extreme reduction in mtDNA observed
in metazoans occurred after the divergence of M. brevicollis (and possibly all choanoflagellates) from the line
leading to metazoan animals (Figure 2). The mitochondrial genome sequence from a member of the sponge
lineage, which is likely to have a branching position
between those of other multicellular animals and choanoflagellates (Figure 1), would undoubtedly help to establish more precisely the evolutionary timing of mtDNA
reduction in the animal lineage.
In contrast to the mtDNA of M. brevicollis, the mtDNA
of Amoebidium parasiticum (an ichthyosporean protist)
has possibly the most unusual mitochondrial genome
structure ever found [8]. A. parasiticum mtDNA is over
200 kbp in size and consists of hundreds of short (0.3–
8.3 kbp) linear fragments. Of the 80 ‘chromosomes’ that
have been partially or completely sequenced, three
types have been described: i) small DNA molecules
without identified coding function, ii) medium-sized
DNA species carrying a single gene, and iii) larger
molecules encoding multiple genes. All chromosomes
contain a virtually identical array of short terminal
repeats. Although other instances of linear mtDNAs
and mtDNAs consisting of multiple linear or circular
components have been described (e.g. [16]), no other
example is known with such an extensive collection of
genomic fragments. Despite the unusual appearance of
A. parasiticum mtDNA, the sequences of the proteins it
specifies and the secondary structures of its encoded
rRNAs clearly identify it as a unicellular ancestor of the
animal lineage [8].
Current Opinion in Microbiology 2004, 7:528–534
530 Genomics
Figure 2
choanoflagellates
55
animals
37
H. sapiens
ichthyosporeans
>44
M. brevicollis
A. parasiticum
ascomycetes
35
S. cerevisiae
S. commune
R. americana
44 basidiomycetes
40
R. stolonifer
98
41
A. macrogynus
S. punctatus
24
R. brooksianum
H. curvatum
Harpochytrium105
24
zygomycetes
23
23
Monoblepharella15
Harpochytrium94
24
25
chytridiomycetes
Current Opinion in Microbiology
Branching order of deeply diverging groups within Holozoa (red) and Fungi (blue) based on molecular phylogenetic analyses of mtDNA-encoded
protein sequences [13,21]. Chytridiomycete orders are indicated by color: Blastocladiales (pink), Spizellomycetales (purple), Chytridiales
(orange), Monoblepharidales (brown). The conformation and relative size of the mtDNA in each species is indicated graphically, with the
number of identified genes encoded by the mtDNA (not including introns and unidentified ORFs) indicated. R. americana is included as an
outgroup for comparison. Species shown ([references], NCBI acc. no.): Reclinomonas americana ([9], AF007261), Homo sapiens ([1], V00662,
X93334, J01415, M12548, M58503, M63932, M63933), Monosiga brevicollis ([8], AF538053), Amoebidium parasiticum ([8], AF538042-AF538052),
Saccharomyces cerevisiae ([2], AJ011856), Schizophyllum commune ([20], AF402141), Rhizopus stolonifer ([7], FMGP; unpublished),
Allomyces macrogynus ([22], U41288) Spizellomyces punctatus ([20], AF404303-AF404305), Rhizophydium brooksianum ([20], AF404306),
Hyaloraphidium curvatum ([20], NC003048), Monoblepharella15 ([21], AY182007), Harpochytrium94 ([21], AY182005), Harpochytrium105
([21], AY182006).
Clade Fungi: chytridiomycetes are deeply
diverging members of the fungi
Although the structures of several ascomycete mtDNAs
have been available for some time (for example [2,17–
19]), efforts over the past decade have provided complete
mitochondrial genome sequences from representatives of
two other lineages long accepted as fungi, namely basidiomycetes and zygomycetes ([7,20], NCBI acc. no.
AY376688). A great variety of genome size and structure
exists in the fungi, with mtDNAs ranging from 19 kbp
in Schizosaccharomyces pombe [18] to 100 kbp in Podospora anserina [17]. By contrast, gene content is quite
consistent across fungal classes, although the distribution
of several genes is scattered.
Chytridiomycetes (chytrids) are of particular evolutionary
interest because they have conserved ancestral characters,
such as flagellated spores, that are not present in other
fungi; accordingly, chytrids are believed to represent
deeply diverging members of the fungal kingdom. Molecular data including mitochondrial sequence information
Current Opinion in Microbiology 2004, 7:528–534
have established with high statistical support the specific
association of chytrids with the rest of the fungi, as well
as the branching order of the four fungal divisions (for
example [6,21]). As expected, the chytrids diverge deeply with respect to the other three lineages, with zygomycetes separating next relative to the ascomycete and
basidiomycete lineages (Figures 1 and 2).
Complete mtDNA sequences from seven members
of the chytridiomycete lineage have been determined
[7,20,21,22,23]. These mtDNAs are very similar to
those of other fungi in terms of gene content and genome
size, with the latter ranging from 20 kbp in Harpochytrium94 to 70 kbp in Rhizophydium brooksianum. The
mtDNA of Allomyces macrogynus [22], a deeply branching
chytrid, encodes even more genes, including one specifying a small subunit ribosomal protein, Rps3 (a gene that
has a scattered distribution among fungal mtDNAs), as
well as a full complement of tRNA genes. By contrast,
other examined chytrid mtDNAs have markedly reduced
tRNA gene complements. Thus, we infer that by the time
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Evolution of the mitochondrial genome: protist connections to animals, fungi and plants Bullerwell and Gray 531
chytridiomycetes diverged from the other fungal lineages,
the basic form of fungal mtDNA had been established,
with features such as genetic code changes (observed in
all divisions except zygomycetes), gene loss and tRNA
editing (observed only in chytrid mitochondria [23,24])
emerging later. Because both M. brevicollis and A. parasiticum mtDNAs have gene contents larger than those of
either fungal or animal mtDNAs, and because both fungal
and animal mitochondrial genomes encode basically the
same set of genes, we also conclude that independent
reduction of gene complements has occurred in the fungal
and animal lineages since their divergence from the
protistan ancestor of the fungal-animal clade (opisthokonts) (Figure 2). If non-chytrid protists exist that specifically associate with the fungi in molecular phylogenies
to the exclusion of Holozoa, such organisms will yield
further insights into when in evolution the common
features of fungal mtDNA structure and gene complement took shape.
Clade Viridiplantae: green algae are
specifically related to land plants
Land plants have long been grouped with green algae on
the basis of various biochemical, physiological and ultrastructural data. The organisms in these lineages (comprising Viridiplantae) can be further resolved into two phyla:
Streptophyta, containing land plants (embryophytes) and
their presumed specific green algal relatives, the charophytes (Charophyceae), and Chlorophyta, which contains
most other green algae (Figures 1 and 3). Chlorophyta
consists of three monophyletic classes (Chlorophyceae,
Ulvophyceae and Trebouxiophyceae) plus a probable
paraphyletic assemblage of primitive green algae (Prasinophyceae). Whereas recent phylogenetic analyses based
on molecular data support streptophyte monophyly
[25,26], branching order within the chlorophytes and
the deep relationships of all green plants (e.g. the precise
branching position of the primitive green alga, Mesostigma
viride [25,27,28]) remain unsettled. This uncertainty is
mostly owing to the high rates of sequence divergence
in some green algal lineages. Despite these limitations,
complete sequencing of green plant mtDNAs has considerably deepened our understanding of mitochondrial genome evolution in this group, which displays great plasticity
in terms of genome size and rate of sequence divergence.
For the six land plant mtDNAs completely sequenced to
date ([3,29–32], NCBI acc. No. AY506529) genome size
ranges from 187 kbp in Marchantia polymorpha (liverwort)
to 570 kbp in Zea mays (corn), with sizes up to 2400 kbp
having been reported for some species of cucurbit [33].
Despite their large sizes, land plant mitochondrial genomes do not encode a proportionately greater number of
genes than mtDNAs in other lineages (Figure 3); genome
expansion is accounted for primarily by large intergenic
regions, repeated segments, introns and intron open reading frames, as well as by incorporation of foreign DNA
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Figure 3
charophytes
land plants
68
C. vulgaris
69
67
65
C. globosum
M. polymorpha
M. viride
65
N. olivacea
61
R. americana
98
P. wickerhamii
P. akinetum
57
P. minor
S. obliquus
P. parva
10
C. eugametos
C. reinhardtii
C. elongatum 13
12
12
22
42
chlorophytes
Current Opinion in Microbiology
Branching order of deeply diverging groups within Viridiplantae
(green plants) based on molecular phylogenetic analyses of mtDNAencoded protein sequences [26,44] (the position of P. parva is
based on phylogenetic reconstructions using nuclear [46] and
chloroplast [47] rRNA sequences). The precise branching position
of M. viride remains controversial, although recent analyses of both
mitochondrial [27] and chloroplast [28] gene sequences identify
Mesostigma as the earliest diverging plant lineage, emerging
before the split between Streptophyta and Chlorophyta. Chlorophyte
lineages are indicated by color: Prasinophyceae (pink), Ulvophyceae
(brown), Trebouxiophyceae (blue), Chlorophyceae (orange). The
conformation and relative size of the mtDNA in each species is indicated
graphically, with the number of genes encoded by the mtDNA (not
including introns and unidentified ORFs) indicated. R. americana is
included as an outgroup for comparison. Species shown ([references],
NCBI acc. no.): Reclinomonas americana ([9], AF007261), Marchantia
polymorpha ([3], M68929), Chara vulgaris ([26], AY267353),
Chaetosphaeridium globosum ([36], AF494279), Mesostigma viride
([27], AF353999), Nephroselmis olivacea ([38], AF110138), Prototheca
wickerhamii ([37], U02970), Pseudendoclonium akinetum ([44],
AY359242), Pedinomonas minor ([37], AF116775), Scenedesmus
obliquus ([42,43], AF204057), Polytomella parva ([16], AY062933,
AY062934), Chlamydomonas reinhardtii ([39,40], U03843),
Chlorogonium elongatum ([45], Y07814, Y13643, Y13643),
Chlamydomonas eugametos ([41], AF008237).
(plastid, nuclear and plasmid). Intriguingly, despite this
gross structural variability, plant mitochondrial gene sequences are generally considered to exhibit the slowest
rate of divergence of any genetic system (but see [34]). In
addition, although land plant mitochondrial genomes are
circular mapping, their native physical structure may be
considerably more complex [35].
Recent data from the charophyte algae Chaetosphaeridium
globosum [36] and Chara vulgaris [26] have placed the
Current Opinion in Microbiology 2004, 7:528–534
532 Genomics
time of origin of the unique genome architecture in land
plants subsequent to the embryophyte–charophyte split,
i.e. concurrent with the emergence of land plants
(Figure 3). The mtDNAs of these two algae, although
similar in terms of gene content and rate of sequence
divergence to land plant mtDNAs, are much smaller in
size (both are less than 70 kbp). This size difference is in
marked contrast to the striking resemblance between the
mitochondrial genomes of C. vulgaris and M. polymorpha
in terms of A+T content, codon usage and gene order. A
greater variety of genome architectures in this littleexplored algal lineage is likely, given that ongoing
sequencing of the mtDNA of a basally diverging charophyte, Klebsormidium flaccidum, indicates a genome size
close to that of M. polymorpha (OGMP, unpublished).
Acknowledgements
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In the more deeply branching chlorophyte algae, a wide
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observed in the chlorophycean alga Scenedesmus obliquus
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recently been described in the ulvophycean alga, Pseudendoclonium akinetum [44], although this mtDNA actually encodes a slightly smaller number of genes than
earlier diverging chlorophyte relatives such as P. wickerhamii and N. olivacea. The study of P. akinetum mtDNA
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Conclusions
Comparative genomics has proven to be a fruitful
approach for understanding the evolution of mitochondrial DNAs, including reduction of the gene coding
content from that of the a-proteobacterial ancestor, genome size expansion (e.g. in plants) and genome size
contraction (e.g. in animals). Future work in mitochondrial genomics should focus on determining mtDNA
sequences from taxa intermediate to the major eukaryotic
lineages, as well as additional sequences of ancestral
mtDNAs, to better understand the process of organellar
genome evolution. At the same time, mtDNA-encoded
proteins have proven their value in the resolution of deep
phylogenetic relationships within Eucarya (such as the
protistan links to the animal, fungal and plant lineages
described in this review). Such sequences may well provide a robust dataset for clarifying additional, currently
unresolved phylogenetic connections among other eukaryotic groups.
Current Opinion in Microbiology 2004, 7:528–534
Work in the authors’ laboratory on mitochondrial genome structure
and evolution is supported by an operating grant (MOP-4124) to
M.W.G. from the Canadian Institutes of Health Research. The
authors gratefully acknowledge studentship support from the Nova
Scotia Health Research Foundation and Walter C. Sumner Foundation
(to C.E.B.) and salary support from the Canada Research Chairs Program
and Canadian Institute for Advanced Research (to M.W.G.).
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