Gualberto14 Plantmitgenomes

Biochimie 100 (2014) 107e120
Contents lists available at ScienceDirect
Biochimie
journal homepage: www.elsevier.com/locate/biochi
Review
The plant mitochondrial genome: Dynamics and maintenance

Jos M. Gualberto, Daria Mileshina, Clmentine Wallet, Adnan Khan Niazi,
Frdrique Weber-Lot, Andr Dietrich*
Institut de Biologie Molculaire des Plantes, CNRS and Universit de Strasbourg, 12 rue du Gnral Zimmer, 67084 Strasbourg, France
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 22 July 2013
Accepted 17 September 2013
Available online 26 September 2013
Plant mitochondria have a complex and peculiar genetic system. They have the largest genomes, as
compared to organelles from other eukaryotic organisms. These can expand tremendously in some
species, reaching the megabase range. Nevertheless, whichever the size, the gene content remains
modest and restricted to a few polypeptides required for the biogenesis of the oxidative phosphorylation
chain complexes, ribosomal proteins, transfer RNAs and ribosomal RNAs. The presence of autonomous
plasmids of essentially unknown function further enhances the level of complexity. The physical organization of the plant mitochondrial DNA includes a set of sub-genomic forms resulting from homologous
recombination between repeats, with a mixture of linear, circular and branched structures. This material
is compacted into membrane-bound nucleoids, which are the inheritance units but also the centers of
genome maintenance and expression. Recombination appears to be an essential characteristic of plant
mitochondrial genetic processes, both in shaping and maintaining the genome. Under nuclear surveillance, recombination is also the basis for the generation of new mitotypes and is involved in the evolution of the mitochondrial DNA. In line with, or as a consequence of its complex physical organization,
replication of the plant mitochondrial DNA is likely to occur through multiple mechanisms, potentially
involving recombination processes. We give here a synthetic view of these aspects.
2013 Elsevier Masson SAS. All rights reserved.
Keywords:
Mitochondria
mtDNA
Replication
Recombination
Repair
1. Introduction
Mitochondria are key players in plant development, tness and
reproduction. Their contribution to energy production, metabolism
and cell homeostasis relies on the performance of their own genetic
system that makes them semi-autonomous. As in other organisms,
the mitochondrial genome in plants encodes a series of essential
polypeptides that build up the complexes of the oxidative phosphorylation chain, together with nuclear-encoded subunits. But
plant mitochondrial DNAs (mtDNAs) have remarkable features that
distinguish them from their animal and fungal counterparts. In
particular, higher plants harbor large mtDNAs that are highly variable in size and structural organization. On top of that, in many
plant species, mitochondria contain various forms of plasmids that
replicate independently from the main chromosome. In most plant
species, the mtDNA gene sequences evolve very slowly, as
compared to animal mtDNA sequences, and point mutations are
rare. It is believed that this is because plant mitochondria contain
* Corresponding author. Tel.: 33 3 67 15 53 73; fax: 33 3 88 61 44 42.

E-mail addresses: jose.gualberto@ibmp-cnrs.unistra.fr (J.M. Gualberto),
Daria.Mileshina@ibmp-cnrs.unistra.fr (D. Mileshina), clementine.wallet@ibmpcnrs.unistra.fr (C. Wallet), Adnan-Khan.Niazi@ibmp-cnrs.unistra.fr (A.K. Niazi),
lotf@unistra.fr (F. Weber-Lot), andre.dietrich@ibmp-cnrs.unistra.fr (A. Dietrich).
0300-9084/$ e see front matter 2013 Elsevier Masson SAS. All rights reserved.
http://dx.doi.org/10.1016/j.biochi.2013.09.016
an active DNA recombination system that allows copy correction of

mutations. Indeed, numerous studies have shown that plant
mitochondrial genomes undergo extensive and high frequency
homologous recombination (HR). Such processes make plant
mtDNA prone to rearrangements. When not lethal, mtDNA mutations/rearrangements can generate severe phenotypes or cause
cytoplasmic male sterility (CMS). Hence the requirement for efcient DNA repair and maintenance pathways in a context where
oxidative pressure, replication defaults or environmental hazard
generate base modications and strand breaks. Finally, mitochondrial genome dynamics generates heteroplasmy, with alternative
mtDNA congurations coexisting with the main mtDNA. Segregation of alternative mitotypes signicantly contributes to the rapid
evolution of the plant mtDNA structure. The present review addresses these issues, with special emphasis on the specicities of
the plant mitochondrial genetic system.
2. Plant mitochondrial DNA structure and organization
2.1. Genome size and content
The structure of higher plant mitochondrial genomes has a
number of unique features. Whereas most animals possess circular
mtDNAs of 15e17 kb in size, the mitochondrial genomes of plants
108
J.M. Gualberto et al. / Biochimie 100 (2014) 107e120
Fig. 1. Circular and linear models of the mtDNA structure in plants. The dynamics of the mtDNA of plants allow several models. a) A circular genome model representing the
different organisations of the mtDNA of A. thaliana ecotype C24. The two pairs of large, frequently recombining repeats (A and B) and their orientations are represented by blue and
red arrows. The different parts of the genome are colored in a range of gray scale. Intramolecular recombination events are represented with dashed lines, and in orange,
recombination leading to subgenomic molecules. Dotted line shows possible intermolecular recombination. b) The mtDNA has been observed as predominantly constituted by a
complex array of linear molecules. Branched forms of the mtDNA could be intermediates of recombination-dependent processes: 30 single-stranded sequences resulting from the
recession of double-strand breaks can invade homologous double-stranded DNA, forming a D-loop and leading to the establishment of replication forks.
are much larger and differ greatly in size, even between very close
species or within species [1,2]. They commonly range between 200
and 750 kb in angiosperms [1], but with a tremendous further
extension in some lineages. As an example, proliferation of
dispersed repeats, expansion of existing introns and acquisition of
sequences (including sequences of nuclear, plastid, viral and bacterial origin) account for the expansion of the cucumber (Cucumis
sativus) mitochondrial genome into a tri-chromosome structure
with components of 1556, 84, and 45 kb in size [3]. Sequencing of
the mtDNA from two Silene species with exceptionally high mutation rate revealed enormous mitochondrial genomes of 6.7 (Silene
noctiora) and 11.3 (Silene conica) megabase-pairs resulting from
massive proliferation of non-coding content [4]. Moreover, these
genomes are distributed into a large number of circular chromosomes: 59 for S. noctiora and over 128 for S. conica. These chromosomes range themselves in size from 44 to 192 kb. As a
comparison, the more typical, slowly evolving mitochondrial
genome of Silene latifolia accounts for a single chromosome of
253 kb [4]. Remarkably, plant mitochondrial genomes are large but
their ploidy appears to be low. Whereas thousands of mtDNA
copies can be present in a mammalian cell, much lower mtDNA
levels were detected in plants. Preuten et al. [5] analyzed the ploidy
of several individual mitochondrial genes in various samples of
Arabidopsis thaliana, Nicotiana tabacum and Hordeum vulgare, using
real time quantitative PCR. The copy numbers of the investigated
genes both differed from each other and varied greatly between
organs or during development, with the highest estimates around
280 copies per cell for the atp1 gene in mature leaves. This was
actually less than the mean number of mitochondria per cell, which
was around 450 in protoplasts derived from mature leaves. Thus,
individual mitochondria in plants may contain only part of the
genome or potentially no DNA [5].
Despite their large sizes, land plant mtDNAs do not contain a
signicantly greater number of genes than mitochondrial genomes
of other lineages. The known genes usually range between 50 and

60, while multiple cis- or trans-spliced introns and large intergenic
regions complete the genomes. Protein genes in plant mtDNAs
encode subunits of the oxidative phosphorylation chain complexes
but also proteins involved in the biogenesis of these complexes, as
well as several ribosomal proteins. First to be entirely sequenced,
the 367 kb A. thaliana mtDNA (ecotype C24) codes for 32 proteins,
3 ribosomal RNAs (5S, 18S and 26S rRNAs) and 22 tRNAs [6], while
the 16.5 kb human mtDNA codes for 13 proteins, 2 rRNAs (12S and
16S) and 22 tRNAs [7]. With a total of 57 genes versus 37, this
makes a 1.5 fold difference in gene content for a 22 fold difference
in size. Identied genes represent a minor part of the plant mtDNA
content (10% in A. thaliana), whereas the major part (60% in
A. thaliana) has no recognizable origin and function [6]. Introns
and duplications expand (8% and 7% in A. thaliana, respectively), as
well as integrated nuclear and plastid sequences (5% as a whole in
A. thaliana). Further putative open reading frames of signicant
length can be detected, which also add up to 10% of the genome in
A. thaliana [6].
Differences in gene content among plant species are also not
linked to genome size. The large cucumber mtDNA carries just 4
more protein genes than the A. thaliana genome within 1.3 megabase of extra sequence [3]. On the other hand, it can be noted that
the cucumber mitochondrial genome has integrated 7 more tRNA
genes of plastid origin, whereas 2 tRNA genes of authentic mitochondrial origin present in other species are missing. Similarly, the
253 kb mtDNA of S. latifolia and the 11.3 megabase mtDNA of
S. conica carry the same reduced set of 25 protein genes and, while
the S. latifolia mtDNA contains 9 tRNA genes, that of S. conica has
only 2 [4]. The intergenic sequences with no recognizable origin or
function thus represent 91.5% (10.3 megabase) of the S. conica
mitochondrial genome. With the emergence of second-generation
sequencing technologies, the number of completed plant mitochondrial genome sequences rapidly increased in the last few years,
with 77 deposited in the GenBank database (http://www.ncbi.nlm.

nih.gov/genomes/) by June 2013.
2.2. Physical organization
The physical structure of plant mitochondrial genomes is usually represented by a circle of double-stranded DNA, called master
chromosome, housing the complete set of mitochondrial genes.
However, such a structure is derived from mapping and sequence
assembly and has not been directly observed. Thus, although it
might exist, the master circle must be rare. On the other hand, the
620 kb mitochondrial insertion characterized in A. thaliana nuclear
chromosome 2 [8] seems to derive from a concatemer of mitochondrial genomes, suggesting that such concatemers may exist
in vivo. Plant mtDNAs usually contain repeated sequences dispersed
throughout the genome, which can be in direct or inverted orientation. They can pair up and recombine, redistributing sequences
and generating sub-genomic circular DNA molecules (Fig. 1a).
Indeed, numerous studies have shown that plant mitochondrial
genomes undergo extensive and high frequency homologous
recombination. Especially, recombination between a few large repeats (several kb in size) is frequent and reciprocal, leading to
multiple, interconverting congurations of the genome. These
recombinationally active long repeats are not homologous between
species, but the process is conserved. In A. thaliana, two large repeats of 6.5 and 4.2 kb were shown to be involved in recombination
[9]. In the N. tabacum mtDNA, there are three pairs of large repeated
sequences, with lengths of 18 kb, 6.9 kb and 4.7 kb [10]. But the
number of recombinogenic repeats can be much larger, as for
example in wheat where there are 10 pairs of large repeats [11]. As
a consequence, the mtDNA of plants cannot be physically represented as a unique, organized structure that could be used to
determine phylogenetic relationships between species. Furthermore, besides sub-genomic circles, early observations highlighted
linear forms [12]. In the case of the maize (Zea mays) CMS-S cytoplasm, it was proposed that the mitochondrial genome would exist
mainly as multiple linear molecules. These would result from
recombination of the mitochondrial chromosome with a linear
plasmid (see Section 4 below) specic to CMS-S. The sequencing
data seemed to be consistent with this premise [2]. Also in early
studies, the morphology of carefully isolated mtDNA was consistent
with a predominance of linear molecules [13]. Altogether, it appears that the entity of a plant mitochondrial genome is an array of
inter-convertible linear and circular DNA molecules that most likely
reect recombination intermediates between repeated sequences,
yielding a mixture of various subgenomic DNA molecules with
different structures and contents (Fig. 1). The concept of a circular
master chromosome remains because the question of how multipartite and branched DNA molecules are properly transmitted to
the next generation is unsolved. Finally, a signicant portion of the
mtDNA (2e8%) was reported to be in a single-stranded form in
Chenopodium album suspension culture or whole plants [14].
Homologous recombination between the numerous intermediate size repeats (ISRs, usually ranging from 50 to 600 bp in size)
also present in the genome is generally infrequent but, when
occurring, leads to further complex rearrangements. It has been
proposed that most of the recombination processes involving ISRs
result from Break-Induced Replication (BIR) pathways [15]. But
other pathways, such as Single-Strand Annealing (SSA), might also
be involved [16]. These low frequency recombination activities are
non-allelic, and the process is asymmetrical, resulting in accumulation of only one of the expected reciprocal recombination products and leading to duplication or deletion of genomic sequences. In
addition, illegitimate recombination processes involving very short
sequence homologies of a few nucleotides (microhomologies) have
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also been described [17], which can lead to gene chimeras. Both low
frequency recombination between ISRs and error-prone repair
processes mediated by microhomologies (see below) yield lowcopy number alternative congurations (or mitotypes) of the
mitochondrial genome that contribute to the natural heteroplasmy
of the plant mtDNA. Finally, additional processes might be at work,
depending on the species. In particular, the large size of the mitochondrial genomes in the genera Cucumis and Silene have been
linked with the accumulation of short (30e53 bp) repeated sequences [3,4,18].
Contrary to a prevailing idea, the mtDNA is not naked but is
packed into nucleoprotein particles called nucleoids [19]. In these
membrane-anchored particles, the DNA is associated with a number of factors involved in its compaction and metabolism. Nucleoids
are considered as the heritable units of mtDNA and their structure
inuences mtDNA segregation and transcriptional regulation [20].
The actual set of nucleoid-associated proteins is still discussed and
seems to vary between the different organisms, suggesting that the
composition of mitochondrial nucleoproteins has been reinvented
several times along with mtDNA evolution [19]. Mitochondrial
nucleoids contain a set of core proteins involved in DNA maintenance and expression, as well as peripheral factors that are components of signaling pathways [21]. Plant mitochondrial nucleoids
were characterized as dynamic entities, with chromatin-like or
bril-like structures, depending on the developmental stage or
tissue [22,23]. Chromatin-like structures were associated with a
vesicle component.
Whereas a nucleoid-enriched proteome has been established
for chloroplasts [24], information on the composition of their
mitochondrial counterparts remains scarce. Plant nucleoids
appeared to share a qualitatively similar phospholipid composition
with the whole organelle and to contain polypeptides of both inner
and outer membrane origin [22]. The association of the identied
proteins with isolated nucleoids was a function of the detergent
concentration in the isolation procedure, so that the structural or
functional signicance has to be further evaluated. Little is known
about the proteins responsible for nucleoid organization in plants
[25]. The presence of nucleosome-like structures was suggested,
depending on the developmental stage [22,26]. It was reported that
histone H3 and histone deacetylase might be targeted to mitochondria in cauliower [27,28]. However, such a view was contradicted by studies in tobacco cells [29]. Actin was persistently
recovered in plant nucleoids, where it seemed to associate with the
mtDNA [22]. Import of actin to the inside of mitochondria was
indeed reported and its potential function in the organelles was
discussed [30]. It would bind to the mtDNA in complexes also
containing porin and the ADP/ATP carrier. Plant mitochondrial
nucleoids likely have a heterogeneous genomic organization. Open
circles, supercoils, complex forms, and linear molecules with
interspersed sigma-shaped structures and/or loops represented
about 70% of the mtDNA molecules present in mung bean nucleoids
[23]. As in fungi or mammals, mitochondrial nucleoids in plants are
not only compaction and segregation units but they support the
entire DNA metabolism. Isolated mung bean nucleoids were reported to run DNA synthesis and were capable of directing regulated RNA synthesis [22]. Membrane-association of the plant
mitochondrial base excision repair (BER) components (see Section
6.2) also supports the assumption that mtDNA maintenance and
repair pathways take place in the membrane-bound nucleoids
[31,32].
3. Mitochondrial DNA replication
Replication of plant mitochondrial genomes is far from being
understood. Several factors involved in organellar genome
110
replication have been identied by sequence homology and from

proteomic data. Among those, plant organellar DNA polymerases
were identied by their similarities to the known mitochondrial
DNA polymerase of animals and yeast. In A. thaliana, there are two
organellar DNA polymerases, Pol1A and Pol1B, which are dualtargeted to both mitochondria and plastids [33e35] and which
are apparently redundant in their functions [36,37]. Individually,
each of them is dispensable, because the mutants show no visible
phenotypes, apart from a small reduction in mtDNA and chloroplast DNA (cpDNA) copy numbers. Conversely, the double mutant is
not viable, showing that the two polymerases are redundant for
organellar genome replication [37]. However, the situation might
not be the same in other species. While single mutants of each of
the A. thaliana organellar DNA polymerases have a very mild effect
on mtDNA and cpDNA copy numbers, in Z. mays, deciency in a
plastid-localized DNA polymerase results in albino plants because
of a drastic reduction in cpDNA copy number [38]. This suggests
that in maize the organellar DNA polymerases are not redundant
and might be specic for each type of organelle.
Additional mtDNA replication factors have been identied,
which are, in most cases, also dual-targeted to chloroplasts and
mitochondria. A helicase similar to the Twinkle helicase of animal
mitochondria is present in all plant genomes sequenced, and is
targeted to both types of organelles in A. thaliana. Like its T7 phage
homolog, it combines helicase and primase activities in a single
protein [35,39]. Genes coding for organellar Type I and Type II
topoisomerases have also been identied [24,35,40] and there are
homologs of bacterial single-stranded DNA-binding (SSB) proteins
in plant mitochondria [41].
Regarding the mechanisms of replication, they are still open to
debate, mainly because the large size and multipartite complexity
of the plant mtDNA render this process difcult to analyze. In a
search for replication origins as they had been described in metazoan mitochondrial genomes, two putative fragments (oriA and
oriB) were identied from the genome of Petunia hybrida. These
fragments were able to initiate DNA synthesis in an in vitro DNA
synthesizing system derived from puried P. hybrida mitochondria
[42]. DNA synthesis performed with both the A and B origins in the
same plasmid, in complementary strands, initiated rst in the Aorigin and proceeded in the direction of the B-origin, after which
replication was also initiated in the B-origin. Based on these observations, the authors proposed a model of mtDNA replication in
plants structurally comparable to the one of mammalian mtDNA
heavy and light strands [43]. Similarly, a search for sequences of
Papaver somniferum (Opium poppy) mtDNA able to promote
autonomous plasmid replication in yeast revealed a 917 bp fragment with high A/T content [44]. However, these experiments
strongly relied on the premises that most of the plant mtDNA exists
as genome-size circles replicating according to a theta model of
circular DNA replication. But, as commented on in Section 2.2,
while data arising from restriction mapping can imply circular
mtDNA genomes, direct observation of plant mtDNA failed to
support that assumption. Early experiments aiming to characterize
the topology of the mtDNA of plants mainly revealed linear and
small circular molecules, and the inability to purify full-size circular
genomes was attributed to artifactual shearing of large molecules
(reviewed in Ref. [12]). Structural analysis of plant mtDNA using
pulsed-eld gel electrophoresis and moving pictures of DNA
migration in agarose revealed that most of the genome is contained
in large linear molecules and complex branched molecular structures larger in size than the predicted genome size [13,45]. Analysis
of the mtDNA of the liverwort Marchantia polymorpha by digestion
with restriction enzymes with one recognition site per genome and
pulsed-eld gel electrophoresis showed that the genome is
constituted of linear and head-to-tail concatemers [46]. These
concatemeric molecules could be generated both by rolling circle

replication and by recombination-mediated replication, as in phage
T4. The latter model could also account for the complex branched
mtDNA molecules (Fig. 1b).
Rolling-circle and recombination-dependent replication have
also been inferred from electron microscopy observation of the
C. album mitochondrial genome and plasmids (see Section 4
below). In these studies, the mtDNA preparations contained
mostly linear molecules of variable size, but also subgenomic circular DNA molecules, circular molecules with tails (sigma-like
structures), as well as more complex rosette-like and catenate-like
molecules [47]. The distribution of single-stranded mtDNA in the
sigma structures and the detection of entirely single-stranded
molecules indicated a rolling-circle type of replication of subgenomic circles [48], while analysis of replicating mtDNA in cell
cultures also revealed characteristic recombination intermediates
compatible with a phage T4-like mechanism of recombinationmediated replication [49]. Dramatic changes in the absolute and
relative amounts of the different replicative structures occurred
during cell growth, unveiling the plasticity of the mtDNA structure.
Taken together, the pulsed-eld gel electrophoresis, movies of
migrating DNA and electron microscope observations suggest the
coexistence of a recombination-dependent mode of replication
initiation with a rolling-circle mode of replication. In the yeast
Candida albicans, a comprehensive topological analysis of the
mtDNA also supported a model of recombination-driven replication initiation [50], and inverted repeats in the genome seem to be
predominantly involved in replication initiation via homologous
recombination. As in C. albicans, replication of plant mtDNA might
initiate by recombination involving the large repeats that are
usually present in plant genomes.
However, the present models of recombination-dependent
replication do not satisfactorily explain how the complex populations of mtDNA molecules are transmitted in a near homoplasmic fashion from cell to cell and from one generation to
another. At present, it cannot be excluded that replication involves
different processes and factors according to the plant tissue and the
developmental stage. These questions have to be addressed in order to understand how the mtDNA is faithfully and completely
transmitted, and how its copy number is regulated, probably in
coordination with the replication of the plastid and nuclear
genomes.
4. Mitochondrial plasmids
In addition to a large and dynamic main genome, mitochondria
of many higher plant species contain a variety of smaller DNA
molecules whose size can range from 0.7 to over 20 kb [51e54].
These can be regarded as extrachromosomal replicons or plasmids
that can be autonomously replicated in mitochondria because they
are usually present at a high stoichiometry relative to the main
genome [54]. Multimeric forms of these mitochondrial plasmids
have been observed that likely result from homologous recombination processes [55]. The pattern of mitochondrial plasmids is
species-specic and can be different among varieties of the same
plant species [56]. In Silene species, plasmids further contribute to
the complexity of mitochondrial genetics [57]. Although remnants
of putative integration into the mtDNA were sometimes reported
[58], most plant mitochondrial plasmid DNAs have essentially no
sequence similarity with the main chromosome and cannot be
considered as subgenomic forms. In that respect, they resemble
mitochondrial plasmids found in several fungus species, such as
Neurospora crassa or Neurospora intermedia. Their presence or
absence has no correlation with species peculiarities but their
amplication changes along the development. Additional plasmid
variants can arise from recombination events [59]. The nuclear

context participates in the control of mitochondrial plasmid
appearance and copy number [59].
Mitochondrial plasmids in plants were studied more extensively
in the 1980s, when they were expected to provide vectors for
mitochondrial transformation. The eld subsequently became less
active. They can in turn be classied into two types, circular and
linear plasmids. Circular plasmids have been found in a diverse
group of plant species. Their size is often in the range of 1e2.5 kb,
although it can extend to 9 kb or more [51e53]. They can share
short regions of homology or contain sequences homologous to the
nuclear genome (reviewed in Ref. [54]). In early studies, replication
of the mtp2 (1.7 kb) and mtp3 (1.5 kb) circular mitochondrial
plasmids of Vicia faba was reported to start at a specic origin, close
to sequences that can fold into hairpin structures, and to proceed in
the same, single direction around the molecules [60]. An asymmetric rolling circle replication mechanism with unique features
was documented for the C. album mp1 circular DNA plasmid
(1.3 kb) [61]. This plasmid would contain a putative replication
origin sharing homology with double-stranded rolling circle origin
(dso) or transfer origin (oriT) nicking motifs of bacterial plasmids
[62]. Typical rolling circle intermediates and concatemers were
characterized [63]. Sigma-like molecules with long doublestranded tails were identied and their structure suggested the
occurrence of strand switching during rolling circle replication, as
for bacterial replicons [62]. A/T-rich regions containing tandem
sequences that resemble the yeast ARS (autonomously replicating
sequence)-type replication origin were highlighted in the Z. mays
1.4 and 1.9 kb circular plasmids [64,65]. Within their limited size,
plant circular mitochondrial plasmids mostly carry open reading
frames of modest length, although some reach 1 kb. Nevertheless,
these orfs are transcribed, as established in a number of species
[64e69]. The function of such transcripts is not understood.
Notably, differences were reported in the set of circular plasmids
and transcripts derived thereof between male fertile and CMS lines
of Beta vulgaris [70].
Linear mitochondrial plasmids have been characterized in Beta,
Brassica, Daucus, Sorghum and Zea species, but they seem to be less
frequent than circular forms [54]. Linear plasmids are generally
larger and commonly range from 2 to 12 kb [54]. They usually
contain terminal inverted repeats (TIRs) and their 50 -termini were
reported to carry specic covalently-bound proteins (reviewed in
Ref. [54]). Such invertron features are shared with different
classes of fungal mitochondrial plasmids, virus or phage DNAs and
transposable elements [71]. The terminal proteins are presumably
involved in the initiation of DNA replication at both 50 termini. Five
linear plant mitochondrial plasmids have been studied more
closely: the Z. mays S1 [72], S2 [73] and 2.3 kb [74] plasmids, the
B. vulgaris 10.4 kb plasmid (GenBank accession Y10854), and the
Brassica napus 11.6 kb plasmid [75]. The terminal inverted repeats
at their ends range from 170 bp (Z. mays 2.3 kb plasmid) to 407 bp
(B. vulgaris 10.4 kb plasmid). TIR sequences are unrelated, except for
the S1 and S2 plasmids, which share identical terminal repeats.
Apart from the Z. mays 2.3 kb plasmid, linear mitochondrial plasmids contain several open reading frames (up to 6 in the 11.6 kb
B. napus plasmid) that are larger than those present in circular
plasmids. Several of these orfs are considered to encode DNA or
RNA polymerases, while the others have no recognizable function.
Like the nuclear-encoded RNA polymerases that transcribe the
main mitochondrial genome, linear plasmid-encoded RNA polymerases are of phage-type. But the two classes of enzymes are
different. Plasmid-encoded DNA polymerases have similarities
with group B DNA polymerases characteristic of phages and viruses.
The presence of DNA and RNA polymerase genes in linear mitochondrial plasmids supports the idea that these plasmids are
111
autonomously replicated and transcribed. It has been proposed that

gene conversion involving the TIRs (considered as palindromic
telomeres) can shape the architecture of mitochondrial linear genetic elements, including plasmids [76]. Transcription and translation of putative genes carried by linear plasmids have been
detected, especially of those coding for RNA or DNA polymerases
likely to be required for expression and replication [77,78].
Expression of orfs with unknown function was established in
particular for the 11.6 kb linear plasmid of B. napus, demonstrating
that these are functional genes [75]. Similarly, the protein encoded
by orf1 of the Z. mays 2.3 kb plasmid could be detected [79]. This
polypeptide is similar to a domain of the putative RNA polymerase
encoded by the Z. mays S2 linear plasmid, but it was hypothesized
that it is rather the protein that covalently binds to the 50 ends of
the 2.3 kb plasmid [79]. Interestingly, transcription appeared to
start inside or just at the end of the TIR sequence in both the 11.6 kb
B. napus plasmid and the 2.3 kb Z. mays plasmid [75,79]. The latter
carries the only functional tRNATrp gene of Z. mays mitochondria
and is therefore the only plant mitochondrial episome with a clear
function, explaining its ubiquitous presence in Z. mays lines [74].
The presence of the S1 and S2 plasmids of Z. mays and their exchanges with the main mtDNA were reported to be involved in CMS
or non-chromosomal stripe (NCS) phenotypes, although a strict
correlation remained difcult to establish (discussed in Ref. [54]).
Conversely, mtDNA rearrangements involving short repeats shared
with the S2 plasmid were reported to be responsible for both CMSS reversion to fertility and NCS mutation [80,81]. However, CMS-S
reversion is not necessarily accompanied by a loss of the S plasmids [82]. Similarly, association of the 11.6 kb linear plasmid with
CMS in Brassica was found not to be exclusive [83]. In Lolium perenne, a linear plasmid-like element carrying the characteristic DNA
and RNA polymerase orfs was found to be integrated into the main
mtDNA in a CMS line, while in fertile lines it is present as a lowcopy number extrachromosomal replicon [84].
Mitochondrial plasmids are transmitted uniparentally from the
maternal plant to the progeny, together with the main genome.
However, deviations from a strict maternal inheritance were
observed for the Beta maritima 10.4 kb linear plasmid [85]. The
possibility of paternal inheritance through the pollen was established and extensively studied for the 11.6 kb Brassica linear
plasmid [86,87].
The origin of mitochondrial plasmids is mostly unknown but
their presence in many plant species indicates that their acquisition
is not a rare event. Short similarities were highlighted between
several circular plasmids from different species, raising the idea of a
common ancestor [88]. Mitochondrial plasmids often contain sequences that have nuclear counterparts, which in turn suggests
intercompartment exchange. Conversely, the invertron structure of
linear plasmids [71] rather points out to a common ancestral
invertron of viral origin [54]. However, the orf sequences and the
structural organization differ among plant mitochondrial linear
plasmids, in agreement with independent origins. Finally, it has
been speculated that horizontal DNA transfer, in particular from
fungi, might have played a role in the acquisition of linear plasmids
by plant mitochondria [54].
5. Recombination control
5.1. Recombination factors
At the core of the organellar homologous recombination (HR)
activities, there are eubacterial-type RecA proteins inherited from
the corresponding prokaryotic endosymbiont ancestors. RecA catalyzes DNA strand-exchange during homologous recombination.
Initially, RecA polymerizes on single-stranded DNA to form a long
112
presynaptic DNA-protein lament. In the presence of homologous

double-stranded DNA, RecA catalyzes strand exchange, forming a
D-loop that is a common intermediate in homologous recombination pathways. The process can be modulated by many factors.
These include SSB proteins, which have very high afnity for singlestranded DNA that they sequester from RecA, and recombination
mediators, which can displace SSBs and promote DNA annealing.
After strand invasion, several outcomes are possible, according to
the recombination pathway that is engaged (reviewed in Ref. [89])
and the available recombination factors. The processes that are
active in plant mitochondria are still not identied.
In A. thaliana and all owering plants, there are two mitochondrial RecA-like proteins, RECA2 and RECA3 (Table 1). While
RECA3 is strictly mitochondrial, RECA2 was described as dualtargeted [90], but loss of RECA2 only affects mitochondrial functions [16]. By heterologous expression in Escherichia coli, it was
shown that RECA2 and RECA3 are functional RecAs, with overlapping but also specic activities [16]. Accordingly, the A. thaliana
recA2 and recA3 mutants displayed different phenotypes: recA2
plants are unable to develop past the seedling stage, while recA3
plants are phenotypically normal [16,90].
The essential functions of RECA2 are still unknown, but they
might be related to C-terminal sequences that it shares with most
known RecA proteins and that are not present in RECA3. The recA2
and recA3 mutants have normal mtDNA copy numbers, indicating
that RecA functions are not essential for replication. But both recA2
and recA3 mutants display molecular phenotypes of increased
recombination between ISRs [16]. The RecA-independent homologous recombination activity is exacerbated in recA2 mutants,
where accumulation of crossover products is an order of magnitude
higher than in recA3 mutants. As discussed below, RECA2 and
RECA3, as well as additional genes, are apparently involved in
surveillance pathways that restrict mtDNA recombination. The
reshufing of the mitochondrial genome by recombination is
probably the cause of the observed recA2 lethal phenotypes.
As RECA2 and RECA3, additional core elements of the plant

mtDNA maintenance machinery were inherited from the bacterial
ancestors of plant organelles. That is the case of the eubacterialtype single-stranded DNA-binding proteins SSB. In bacteria, SSB is
an abundant essential protein that cooperatively binds singlestranded DNA, forming protein laments that saturate long
stretches of the DNA. Binding of SSB protects the exposed singlestranded DNA from nucleases, but also melts secondary structures that inhibit elongation of RecA-single-stranded DNA laments. However, the high-afnity binding of SSB also limits RecA
assembly onto single-stranded DNA [91]. To overcome recombination inhibition by SSB, recombination mediators are required.
Mediators can be other single-stranded DNA-binding proteins that
promote the displacement of SSB and the assembly of RecA [92]. In
A. thaliana and in most owering plants, there are two SSB genes,
SSB1 and SSB2 (Table 1) [33,41]. Both proteins are targeted to
mitochondria ([41] and our unpublished results). SSB1 was shown
to have similar properties as E. coli SSB: it specically binds singlestranded DNA but not double-stranded DNA and stimulates RecAdependent strand invasion [41]. Essential functions for SSB2 were
conrmed in A. thaliana, where ssb2 mutants are unable to develop
past the seedling stage (our unpublished results).
In addition to eubacterial-type SSBs, plant mitochondria have
specic single-stranded DNA-binding proteins. The precise molecular functions of these proteins are not well characterized, but
they might have multiple and possibly redundant roles in mtDNA
replication, recombination and repair. Among them there are the
organellar single-stranded DNA-binding proteins OSB (Table 1),
which in A. thaliana form a small family of four proteins targeted to
either mitochondria or plastids, or dual-targeted to both organelles
[93]. OSB proteins are characterized by the presence of a central
domain similar to the OB-fold domain followed by one, two or three
C-terminal PDF domains. The PDF domain is a well-conserved
domain of 50 amino acids only found in OSB proteins. It is
required for proteineDNA interaction [93]. In A. thaliana, the
Table 1
Nuclear-encoded proteins involved or suspected to be involved in organelle DNA replication, recombination and repair in A. thaliana.
Category
Name
AGI
Targeting
Function
References
DNA polymerase
Pol1A
Pol1B
Twinkle
GyrIIA
GyrIIB1
GyrIIB2
Topo I
RECA2
RECA3
SSB1
SSB2
OSB1
OSB2
OSB3
OSB4
WHY1
WHY2
WHY3
ODB1
ODB2
MSH1
UNG
FPG
OGG1
ARP
APE1L
APE2
LIG1
At1g50840
At3g20540
At1g30680
At3g10690
At3g10270
At5g04130
At4g31210
At2g19490
At3g10140
At4g11060
At3g18580
At3g18580
At4g20010
At5g44785
At1g31010
At1g14410
At1g71260
At2g02740
At1g71310
At5g47870
At3g24320
At3g18630
At1g52500
At1g21710
At2g41460
At3g48425
At4g36050
At1g08130
Mt Cp
Mt Cp
Mt Cp
Mt Cp
Cp
Mt
Mt Cp
Mt Cp
Mt
Mta
Mt
Mt
Cp
Mt Cp
Mt
Cp
Mt
Cp
Mt Nuc?
Cp Nuc?
Mt Cp
Mt
Nuca
Nuc, Cpa
Cp
Nuca Cp
Nuca Mta
Mt Nuc
Replication
Replication, Repair
Replication
Replication?
[34e37,144]
Helicase/primase
Topoisomerase
Recombinase
ssDNA-binding/recombination mediator
MutS
DNA glycosylase
AP endonuclease
DNA ligase
ssDNA: single-stranded DNA; Mt: mitochondrion; Cp: chloroplast; Nuc: nucleus.

a
Predicted (SUBA3, http://suba.plantenergy.uwa.edu.au).
[35,39,145]
[40]
Replication?
Recombination surveillance
Recombination surveillance, Repair
Replication, Repair?
[35]
[16,90]
n.d.
n.d.
Repair
[93]
Repair
Repair
Repair
Replication, repair
[33,41]
Unpublished
[95,146]
[17,146]
[95,146]
[96,97,147]
[96,97]
[106]
[31,148]
[123,124]
[121,122]
[118]
[127]
[130]
molecular phenotype of the mutants for the mitochondriontargeted OSB1 and OSB4 proteins is the same as that of the recA2
and recA3 mutants: mutant plants accumulate aberrant mtDNA
sequences resulting from ectopic recombination between certain
ISRs ([93] and our unpublished results). This suggests that OSB
proteins are also involved in the surveillance of mtDNA recombination. The specic expression of OSB1 in gametophytic cells
further suggests that recombination surveillance by OSB proteins is
required to prevent transmission of aberrant mtDNA congurations
generated by ectopic recombination [93].
Whirly (WHY) proteins are further single-stranded DNA-binding proteins present in plant organelles (reviewed in Refs. [89,94]).
In plastids, WHY proteins have multiple DNA- and RNA-related
roles [89,94]. In A. thaliana mitochondria there is a single WHY
protein (WHY2) (Table 1), whose roles are not yet completely understood. Over-expression of WHY2 affected the transcription of
several mitochondrial genes but this could be a non-specic effect
due to masking of the mtDNA by WHY2. Rather, like chloroplast
WHY1 and WHY3, mitochondrial WHY2 seems to be involved in
the surveillance of illegitimate recombination, preventing errorprone pathways of double-strand break (DSB) repair through
sequence microhomologies [17,95]. It is possible that WHY proteins
function as recombination mediators, promoting RecA-dependent
homologous recombination repair pathways to the detriment of
alternative illegitimate recombination processes.
Proteins with sequence and structural similarities to eukaryotic
RAD52, a recombination mediator, are present in plants [96,97]. The
two RAD52-like genes identied in the A. thaliana genome were
reported to generate four orfs through differential splicing, with the
respective isoforms being distributed between the nucleus, mitochondria and chloroplasts [96]. However, a specic antibody only
detected the mitochondrial and chloroplast isoforms [97]. Like
WHY2, the RAD52-like mitochondrial protein ODB1 (organellar
DNA-binding) is possibly an additional recombination mediator
(Table 1). ODB1 co-puried with WHY2 from cauliower mitochondrial extracts and both proteins were shown to coimmunoprecipitate [97]. ODB1 has a high afnity for singlestranded DNA, with no apparent sequence specicity, but is also
able to bind double-stranded DNA, although with much less afnity. On the other hand, ODB1 is able to promote annealing of
complementary sequences [97]. In this respect, ODB1 seems to be a
functional homolog of yeast mitochondrial Mgm101p. Also
distantly related to RAD52, the latter is involved in mtDNA maintenance and has recombination mediator properties similar to
those of RAD52 [98e100]. In agreement with this assumption,
A. thaliana knockout mutants of ODB1 are impaired in homologous
recombination-dependent repair of mtDNA breaks generated by
genotoxic treatment [97].
An important component of the mitochondrial recombination
machinery is the MSH1 gene, which encodes a MutS-like protein
(Table 1). MSH1 has essential functions in the surveillance of
mtDNA recombination. The gene was identied in A. thaliana as
responsible for the cytoplasmic inherited CHM (chloroplast mutator) phenotype. The msh1 mutants display phenotypes of variegated and distorted leaves that correlated with important
rearrangements of the mtDNA by recombination [15,90,101e103].
In additional species where MSH1 was knocked down by RNA
silencing, mtDNA recombination was also increased, accompanied
by phenotypic defects that included male sterility [104]. In
A. thaliana, MSH1 is targeted to both mitochondria and chloroplasts
[105] and recently it was shown that it is also active in the maintenance of the plastidial genome, explaining the variegation
phenotype of msh1 plants [106]. In bacteria, MutS is a protein that
participates in mismatch repair and in the suppression of ectopic
recombination. Together with MutL, it recruits the endonuclease
113
MutH to mismatches that arise during replication and homologous

recombination [107]. There is no known MutH-like gene in
A. thaliana, but plant mitochondrial MSH1 contains a C-terminal
GIY-YIG-type homing endonuclease domain. It is therefore possible
that MSH1 combines mismatch recognition and endonuclease
functions. In recombination reactions, MSH1 probably recognizes
heteroduplexes in strand-exchange complexes when there is little
sequence homology. MSH1 would then promote their rejection
[105,108].
Additional putative components of the plant mitochondrial
recombination machinery have been identied by their similarity
to known factors from other species, including DNA polymerases.
As discussed in Section 3, in A. thaliana there are two organellar
DNA polymerases, Pol1A and Pol1B (Table 1), which are targeted to
both mitochondria and plastids and have redundant roles in DNA
replication [33e35,37]. However, Pol1B, but not Pol1A, apparently
has specic functions in DNA repair, because pol1B mutants, and
not pol1A mutants, are hypersensitive to genotoxic agents that
specically induce DNA breaks in organellar genomes [37].
Finally, although many factors involved in mtDNA recombination have been identied either by their DNA-binding activities or
from sequence comparisons, many additional ones are predicted to
be required that remain to be identied. These might not be of
eubacterial origin, because corresponding genes could not be found
in the A. thaliana genome. They might be of viral origin or might
have been recruited from the eukaryotic host. For example, an
initial fundamental step in homologous recombination of DSBs is
the recognition of free DNA extremities and their resection by 50 e30
exonucleases, to form long 30 -overhangs that are substrates for
RecA and other mediators. DNA helicases should also have important roles in recombination, for instance during recession, to unwind branched duplex DNA and help to process Holliday-junctions
by catalyzing branch migration. Several candidates can be pinpointed, from genes coding for proteins with corresponding functional motifs and predicted organellar targeting sequences.
However, the putative mitochondrial functions of these proteins
remain to be validated.
5.2. Recombination specicity
Homologous recombination involves the exchange between the
invading single strand of the donor DNA and the double-stranded
recipient DNA. The length of sequence homology required for
efcient strand-exchange is characteristic of the recombinase enzymes that catalyze the reaction, which in plant mitochondria are
eubacterial-type RecAs [16,90,109]. The minimal pairing sequence
of bacterial RecA can be as small as 25 bp, but efciency greatly
increases with sizes of sequence homology greater than 200 bp
[110]. Repeated sequences are the main sites of intramolecular
recombination in plant mtDNAs and repeats of diverse size and
number have been identied in the plant mitochondrial genomes
so far sequenced [3,111]. Accordingly, the efciencies of recombination observed in plant mitochondria correlate with the size and
homology of the repeats. Large repeats of sizes larger than 1 kb
mediate high frequency, reciprocal homologous recombination.
This type of recombination involving large repeats is responsible
for the well described multipartite structure of plant mitochondrial
genomes. On the other hand, ISRs recombine sporadically, and
often the products of their recombination are not detectable by
conventional map-based sequencing approaches. But such products can be visualized on overexposed Southern blots and by PCR.
The infrequent ectopic recombination mediated by these repeats
leads to many possible alternative congurations of the mtDNA and
has been associated with intraspecic variation of the mtDNA
[15,103]. But this type of recombination can also lead to deleterious
114
DSB in mtDNA
RECA3, RECA2
ODB1, WHY2
RECA3, RECA2,
MSH1, OSB1, OSB4
RecA-dependent
D-loop formation
MicroHomology-Mediated
Recombination (MHMR)
POL1B
Break-Induced
Synthesis-Dependent Replication (BIR)
Strand Annealing (SDSA)
Gene conversion
without crossovers
RecA-independent
Recombination
Single-Strand
Annealing (SSA)
Increased recombination
involving ISRs
Fig. 2. Alternative recombination-dependent repair pathways that might exist in plant mitochondria. Double strand breaks (DSBs) of the mtDNA can be repaired by RecAdependent and independent homologous recombination (HR) pathways. RecA-independent repair of mtDNA DSBs that occur in somatic tissues can lead to increased recombination involving intermediate-size repeats (ISRs), probably by single-strand annealing (SSA). These recombination events are under recombination surveillance, and are derepressed in certain mutant backgrounds (mutants decient in RECA3, RECA2, MSH1, OSB1 or OSB4). DSBs that can be induced by genotoxic treatments are repaired by breakinduced replication (BIR), which requires RecA activity for initial D-loop formation. Mutants decient in RecA-dependent mtDNA repair show reduced recombination following
genotoxic treatment and can accumulate products of illegitimate microhomology-mediated recombination (MHMR).
changes in gene expression, and is under tight control. Thus, mutants of several genes that apparently modulate mtDNA recombination can have dramatically higher frequencies of ectopic
recombination between ISRs, correlating with phenotypes of distorted and variegated leaves. Among these, mutants affected in the
expression of MSH1 have been extensively characterized in several
plant species [90,106,108]. In A. thaliana, in addition to MSH1, other
genes have been identied whose mutants have the same molecular phenotypes of increased ectopic recombination across ISRs.
These are the genes coding for the two mitochondrion-targeted
RecA proteins RECA2 and RECA3 [16] and the plant-specic
organellar single-stranded DNA-binding proteins OSB1 and OSB4
([93] and our unpublished results). The mtDNA rearrangements
induced by the loss of any of these surveillance genes concern ISRs
ranging from about 50 bp up to 556 bp in A. thaliana [15,16,103].
These can be identical in sequence or imperfect repeated sequences, and the efciency of sequence exchange appears to
loosely correlate with repeat size and sequence homology. How far
apart the repeats are located in the genome and how they are
oriented might also inuence the recombination efciency and the
differential accumulation of the corresponding crossover products
[15,16].
The similar molecular and visible phenotypes of these mutants
suggest that the corresponding genes are involved in recombination surveillance processes that restrict recombination when
sequence homology between repeats is below a certain size. In the
case of MSH1, like for other MutS factors, when there is little
sequence homology the protein might recognize heteroduplexes in
strand-exchange complexes, and promote their rejection. The Cterminal GIY-YIG-type homing endonuclease domain of MSH1
could be responsible for cleaving the heteroduplexes and starting
over the process of sequence homology scanning [105]. However,
different recombination pathways might be affected in other mutants. In the case of the RECA2 and RECA3 mutants, the observed
increase in ectopic recombination suggests that it is the loss of
RecA-dependent recombination that favors RecA-independent
pathways under more relaxed control. These could involve the
Single-Strand Annealing recombination pathway (SSA) that can
occur when complementary single-stranded DNA sequences are
exposed [16]. The OSB1 and OSB4 proteins might also be involved in
modulating RecA-dependent recombination, for instance by promoting or suppressing binding of RecA to single-stranded DNA.
In addition to ectopic recombination that is suppressed under
normal plant conditions, it was observed that genotoxic treatments
also result in increased ectopic recombination across ISRs. This can
be explained by the mobilization of recombination factors for the
repair of DNA breaks by the BIR pathway. This homologous
recombination-dependent repair pathway depends on RecA-like
activities and accordingly it was found that genotoxin-induced
mtDNA recombination is suppressed in RECA3 mutants [16].
Other genes were also found to be involved in this genotoxininduced repair process: the organellar DNA polymerases Pol1B
[37], the Rad52-like protein ODB1 [97] and the plant-specic single-stranded DNA-binding protein WHY2 [17]. The corresponding
mutants are not affected in recombination surveillance under
normal growth conditions, but under genotoxic treatment they
have reduced recombination, as compared to wild-type plants.
Concomitant with the loss of the RecA-dependent repair activity,
these mutants also display increased illegitimate recombination
involving microhomologies of just a few nucleotides [17,37,97].
Such sequence chimeras are of very low abundance, and can only be
detected by PCR-based approaches. But collectively they likely
constitute a major source of mtDNA heteroplasmy. On an evolutionary time scale, they are probably responsible for the important
changes in the mtDNA structure observed between plant species.
6. Mitochondrial DNA repair
6.1. Recombination-dependent repair
Repair of DSBs is essential for genome stability because they can
lead to collapsed replication forks, gene loss and genome instability. The sequence of plant mtDNAs revealed numerous examples
of gene chimeras or fusions of unrelated sequences likely emerging
from repair by illegitimate recombination, involving none or just a
few nucleotides. Several of these gene chimeras have been associated with CMS phenotypes.
In chloroplasts there is extensive evidence for the participation
of plastid-targeted RecA in DNA repair [112e114]. In Physcomitrella
patens, it was shown that disruption of a mitochondrial RecA results
in reduced recovery of the mtDNA following genotoxic damage

[115]. In the mitochondria of owering plants, it was demonstrated
that RECA3 has specic functions in mtDNA repair [16]. In wildtype A. thaliana plants, treatments that induce DNA repair activities result in the accumulation of specic ISR-derived crossover
products. This induced recombination activity is lost in the recA3
background, showing that RECA3 is part of an HR-dependent repair
activity induced by genotoxic stress [16]. The possible roles of
RECA2 could not be assessed, given the seedling-lethal phenotype
of the recA2 mutant.
The patterns of recombination that are triggered by RECA3dependent repair activities are specic and distinct from RECAindependent ones that spontaneously occur in recA3, recA2 and
the other mutants involved in recombination surveillance (Fig. 2).
In particular, crossover events that result from recombination
based on a repeated sequence spanning the 30 -end of the atp9 gene
and part of the downstream intergenic region towards the cox3
gene are diagnostic of each one of these pathways (i.e. RECAdependent repair induced by genotoxic treatment and RECAindependent recombination relaxed in surveillance mutants). This
could be tested by qPCR analysis of plants grown in the presence
and absence of genotoxic drugs, such as the antibiotic ciprooxacin
that specically inhibits the organellar-targeted gyrase, thus provoking DSBs in the organellar genomes but not in the nuclear DNA.
The studies showed that RECA3 and the RAD52-like protein ODB1
are involved in homologous recombination-dependent repair of
the mtDNA [16,97]. Similar experiments conrmed the specic
involvement in repair of the single-stranded DNA-binding protein
WHY2 and of the organellar DNA polymerase POL1B, but not of
POL1A (our unpublished results).
As a consequence of decient homologous recombinationdependent mtDNA repair, alternative pathways of illegitimate
recombination repair are apparently activated, in particular nonhomologous end joining (NHEJ) and microhomology-mediated
recombination (MHMR) (Fig. 2). This was shown in why2, pol1B
and odb1 mutants. Increased repair by NHEJ and MHMR-dependent
pathways can explain the chimeric sequences often observed in
plant mitochondrial genomes.
Importantly, mutants decient in mitochondrial recombinationdependent repair can be hypersensitive to genotoxic drugs that
induce DNA breaks [16,37], showing that repair of organellar
genome lesions signicantly contributes to the survival of plants
under stress conditions. It is apparent that many studies dealing
with plant responses under stress often overlook the contribution
of the organellar genomes to these processes.
6.2. Base excision repair
A major consequence of mtDNA oxidation caused by respiration
byproducts or environmental conditions is the formation of
abnormal bases. Oxidized bases are preferentially replaced through
base excision repair (BER). The BER pathway [116] is initiated by a
specic DNA glycosylase that cleaves the N-glycosidic bond between the abnormal base and the deoxyribose, thus generating an
abasic (AP) site. Two ways are then possible for the process to
proceed, short-patch BER (spBER) and long-patch BER (lpBER). In
the case of spBER, if the cleavage has been carried out by a monofunctional DNA glycosylase, an AP endonuclease recognizes the AP
site and cleaves the phosphodiester chain on the downstream side,
leaving a 50 -deoxyribose phosphate (dRp) end. DNA polymerase
then extends the upstream 30 -hydroxyl end, adds the missing
nucleotide and eliminates the 50 dRp. Finally, the gap is sealed by a
ligase. When the DNA glycosylase is bi-functional and possesses a
lyase activity, it not only cleaves the N-glycosidic bond but also
makes a single-stranded incision on the 30 side of the AP site. On the
115
Fig. 3. Short-patch base excision repair in plant mitochondria. The rst step involves
either a monofunctional DNA-glycosylase (1) or a bifunctional DNA glycosylase (2).
UNG, uracil-DNA glycosylase; OGG1, 8-oxoguanine-DNA glycosylase; FPG:
formamidopyrimidine-DNA glycosylase; APE2 and APEL1, homologs of AP endonucleases from yeast and bacteria. For enzymes followed by question marks, the
involvement is not established.
other side, the AP endonuclease subsequently generates a 30 -hydroxyl end that is used by DNA polymerase. One nucleotide is
inserted in the case of spBER, while for lpBER 2e6 nucleotides are
added from the 30 -hydroxyl end, thus displacing the nucleotides
downstream of the gap on the same DNA strand. Plant mitochondria possess an spBER pathway (Fig. 3) but did not seem to run
lpBER [31], contrary to mammalian mitochondria [117].
The rst step of the BER pathway involves a DNA glycosylase. In
A. thaliana, DNA glycosylases were found in mitochondria [31] and
in chloroplasts [118]. Several DNA glycosylase activities exist in
plant mitochondria (Table 1). Uracil-DNA glycosylase (UDG) activity
was detected by in vitro assays with mitochondrial fractions from
Z. mays seedlings [119] and by in vitro and in organello assays with
A. thaliana and Solanum tuberosum mitochondria [31]. The enzyme
did not seem to have a lyase activity and was in part membraneassociated. In vivo targeting and in vitro import of GFP fusion proteins showed that the enzyme encoded by the single putative
A. thaliana UDG gene is indeed targeted into mitochondria [31]. For
8-oxoguanine-DNA glycosylase (OGG1) and formamidopyrimidineDNA glycosylase (FPG), which are functional analogs, the situation
is less clear. A DNA glycosylase activity recognizing 8-oxoguanine in
A. thaliana and S. tuberosum mitochondria was characterized, using
in vitro and in organello assays (Boesch P., Paulus F. and Dietrich A.,
unpublished data). Plants are the only organisms where the presence of both OGG1 and FPG has been reported [120]. There are thus
two candidates to account for the 8-oxoguanine-cleaving activity.
A. thaliana OGG1 is a bi-functional enzyme that was shown to
localize to the nucleus by GFP fusion experiments [121]. Based on
bioinformatic analysis, Macovei et al. [122] suggested the presence
of a putative mitochondrial targeting sequence in the N-terminal
part of the Medicago truncatula, A. thaliana, Populus nigra and Oryza
sativa OGG1. However, when considering all relevant bioinformatic
tools, prediction of OGG1 localization in plants is either
116
mitochondrial or plastidic, depending on the program used, with

an overall preference for plastids. FPG, also a bi-functional enzyme,
was found in M. truncatula and A. thaliana [122,123]. In both species, FPG contains a nuclear targeting sequence. Remarkably, in
A. thaliana there is a single copy of the FPG gene that comprises ten
exons and codes potentially for seven FPG forms, due to alternative
splicing of the mRNA [124]. The different forms of FPG could be
specic for different oxidized substrates but it can also be hypothesized that they would be localized in different compartments
of the cell. As a whole, one might still speculate that OGG1 or FPG
would be relocalized to the organelles when the mtDNA or the
cpDNA is oxidized. This was shown to be the case for Saccharomyces
cerevisiae N-glycosylase1 (Ntg1). Ntg1 possesses both a nuclear and
a mitochondrial targeting sequence and is sent to the compartment
where the DNA is oxidized [125,126]. Sumoylation, a posttranslational modication, seems to be involved in Ntg1 nuclear
relocalisation [125].
After base excision, an AP endonuclease is necessary for the BER
pathway to proceed. An AP endonuclease activity was characterized in A. thaliana and S. tuberosum mitochondria [31]. A. thaliana
possesses three genes, named ARP, APE1L and APE2 (Table 1), that
encode homologs of AP endonucleases from human, yeast and
bacteria. Transient expression of GFP fusions established that the
ARP protein is targeted to chloroplasts [118]. APE1L was found in a
plastid proteome [127]. Alternative splicing yields two forms of
APE2, the longest showing organelle targeting predictions. Also in
B. napus, the putative AP endonuclease is predicted to be targeted
to the organelles. Upon elimination of the damaged nucleotide, a
DNA polymerase is needed to ll the gap. As discussed in previous
sections, in A. thaliana, two organellar g-type DNA polymerases,
POL1A and POL1B, are dual-targeted to chloroplasts and mitochondria (Table 1) [33,34,128] and both function in mtDNA replication [36]. Whether one or both of these enzymes are involved in
BER remains to be established. At the nal step, a ligase is needed to
reconnect the two parts of the DNA strand. Cordoba-Canero et al.
[129] showed that DNA ligase1 is required for both short-patch and
long-patch BER in the A. thaliana nucleus. In this species, transcription of the DNA ligase1 gene yields one major and two minor
mRNA variants differing in the length of the 50 leader preceding a
common orf. According to in planta targeting of GFP fusions, the
longer protein resulting from translation starting at the rst in
frame AUG codon is imported into mitochondria (Table 1), whereas
the other forms are not [130]. The mitochondrial isoform actually
possesses both an internal nuclear localization signal and a
mitochondrial-targeting signal. Altogether, a number of factors
involved in plant mitochondrial BER are still to be conrmed or
identied. As in yeast and in animals (reviewed in Ref. [32]), sharing
repair proteins and modulating factors with other compartments
might turn out to be a major characteristic of plant mitochondrial
DNA repair pathways. As mentioned above, it was suggested that in
yeast BER factors re-localize either to the nucleus or to mitochondria upon genotoxic stress in one or the other compartment
[125,126]. One can further speculate about a possible contribution
of such mechanisms to mtDNA maintenance in plants, in that case
with the chloroplast as a third player.
7. Mitochondrial genome segregation and evolution
An important consequence of mtDNA heteroplasmy is that, from
a heteroplasmic parent, individuals can segregate in which certain
substoichiometric mitotypes were amplied and became the predominant mtDNA. This process is called substoichiometric shifting
(SSS) [131,132]. SSS can result in the activation or silencing of
mitochondrial sequences, including the expression of gene chimeras, thus altering mitochondrial gene expression with
potentially deleterious consequences to the plant. But SSS is also

responsible for the rapid evolution of the mtDNA structure and to
cytoplasm-nucleus conicts, which can result in CMS [133]. This
was clearly revealed by intra-specic sequence comparisons
showing that intergenic regions change rapidly through sequence
duplications, inversions, deletions and insertions resulting from
recombination [2]. Through the production of specic stoichiometric changes, the activity of the MSH1 recombination factor
appeared to account for the polymorphisms distinguishing
A. thaliana ecotypes [103]. Mutation or down regulation of genes
coding for key recombination factors like MSH1, OSB1 or RECA3
triggers extensive mitochondrial genome reorganization in
A. thaliana or crop species, leading to marked phenotypes
[90,93,103,104]. In OSB1-mutated lines, subgenomic levels of homologous recombination products accumulate, one of them
becoming predominant in subsequent generations [93]. Remarkably, the mtDNA structural changes triggered by recombination
factor mutation or down regulation are irreversible after SSS, and it
is possible to revert to the wild type nuclear genome by backcrossing, while maintaining the modied mtDNA genome that is
maternally inherited [93,104]. In that way, down regulating MSH1
allowed the production of stable, non-transgenic, male sterile lines
[104].
In the case of non-allelic recombination involving ISRs, a model
based on BIR was proposed that could account for the events
leading to stoichiometric changes [15,90]. However, it is difcult to
reconcile this model with the accumulation of recombined mtDNA
in mutants decient for RecA [16,90,134], which should be required
for the BIR pathway. Most probably, both RecA-dependent BIR and
additional RecA-independent homologous recombination processes co-exist in plant mitochondria and contribute to the pool of
recombined mtDNA sequences [16]. But while BIR and additional
homologous and illegitimate recombination processes can account
for the accumulation of re-shufed mtDNA sequences in somatic
tissues, these pathways cannot explain the maintenance and
segregation of very low copy number sequences that cannot be recreated de novo by recombination [135]. It is therefore possible that
selective replication of alternative mtDNA sequences is also
involved in the SSS process.
How these molecules segregate and can be amplied during SSS
is not well understood. The segregation of alternative mitotypes
likely occurs during gametogenesis, and it is therefore signicant
that several genes described as involved in the suppression of
ectopic recombination involving ISRs are expressed in the female
gamete [16,90,93]. This suggests that their activities are important
to repress the transmission of recombined mtDNA molecules. As it
has been speculated in animals, the segregation of mitotypes could
involve a genetic bottleneck during oogenesis that would reduce
the copy number of transmitted mtDNA molecules. However, there
is no evidence that such a process exists in plants, because the
mtDNA copy number in egg cells seems to be equivalent to the one
in mesophyll cells, at least in A. thaliana [136]. Since the mtDNA
copy numbers in plants are relatively small, as compared to animals
[5], the existence of a bottleneck is probably not necessary.
Models have also been proposed to account for the evolution of
mitochondrial genome structures and explain the combination of
low mutation rates and genome expansion. A mutation burden
hypothesis put forward by Lynch et al. [137] proposes that the
fundamental features of genome evolution are largely dened by
the relative power of random genetic drift and mutation, i.e. primary non-adaptive forces. Especially, high mutation rates would be
a barrier to organelle genome evolution. In this respect, that plant
and animal mitochondrial genomes evolved to opposite architectural complexity would be a consequence of a two order of
magnitude difference in their mutation rates. Such a model would
stand for plant species with low mtDNA mutation rates and high
mitochondrial genome expansion, but it remains difcult to apply
to species like S. noctiora or S. conica, which show both exceptionally high mutation rates in genes and highly expanded genomes. Christensen proposed a model based on DNA repair and
recombination mechanisms [138] that might account both for low
mutation rates in genes combined with high expansion, rearrangement and mutation rates in the rest of the mitochondrial
genome, and for the conundrum posed by species with huge genomes and high mutation rates in genes [4,139,140]. The model
postulates different repair mechanisms in transcribed and nontranscribed regions [138]. Accurate template-directed DSB repair
by synthesis-dependent strand annealing (SDSA) with enhanced
second strand capture, gene conversion and BER would keep mutation rates low in coding regions. Conversely, BIR, NHEJ and
further error-prone repair pathways, such as microhomologymediated BIR, would explain expansion, rearrangements and
rapid divergence in non-coding regions. In species with both high
gene mutation rates and dramatic expansion of non-coding regions, lack of some BER or mismatch repair mechanisms would
promote the accumulation of damaged and unpaired bases in
coding regions, the xation of mutations, the enhancement of DSB
formation and the frequency of BIR [138]. This attractive hypothesis
implies that transcription-directed repair processes exist in plant
mitochondria, although the mechanisms and factors involved
remain to be identied.
8. Conclusion
In many aspects, the genetics of plant mitochondria is more
complex than that of most other organisms. The capacity to integrate and/or expand intergenic non-coding sequences in the
organellar genome is remarkable, especially versus the strictly
compact mammalian mtDNA. One might speculate that gain of
sequences is related to the competence of plant mitochondria for
DNA import [141]. Notably, both the acquisition of plasmids and the
import competence are shared with fungal mitochondria [142].
However, mammalian organelles are competent as well [143] and
their genome size is stable. Also, many years after their discovery,
the signicance of mitochondrial plasmids and their cross-talk with
the main mitochondrial genome are still a mystery. Not only the
sequence content but also the physical organization of the plant
mtDNA is a complex mix that either results from or supports a
variety of replication and maintenance mechanisms. While rare in
mammalian organelles, recombination is a major player in shaping
plant mitochondrial genomes, redistributing sequences, generating
polymorphism, driving evolution and at the same time preserving
the genetic information. In the end, the challenge remains to understand how the high plasticity of the plant mtDNA can combine
with gene conservation, intercompartment genome coordination
and appropriate functional efciency of the organelles. In this
respect, it can be noted that, apart from reported mutants, mtDNA
maps and restriction patterns have been reproduced many times
for many species and generations, which indicates that, although
dynamic, plant mitochondrial genomes remain stable on an
observable time scale.
Acknowledgments
Our projects are funded by the French Centre National de la
Recherche Scientique (CNRS, UPR2357), the Universit de Strasbourg (UdS), the Agence Nationale de la Recherche (ANR-06MRAR-037-02, ANR-09-BLAN-0240-01) and the Ministre de la
Recherche et de lEnseignement Suprieur (Investissements
dAvenir/Laboratoire dExcellence MitoCross).
117
References
[1] T. Kubo, K.J. Newton, Angiosperm mitochondrial genomes and mutations,
Mitochondrion 8 (2008) 5e14.
[2] J.O. Allen, C.M. Fauron, P. Minx, L. Roark, S. Oddiraju, G.N. Lin, L. Meyer,
H. Sun, K. Kim, C. Wang, F. Du, D. Xu, M. Gibson, J. Cifrese, S.W. Clifton,
K.J. Newton, Comparisons among two fertile and three male-sterile mitochondrial genomes of maize, Genetics 177 (2007) 1173e1192.
[3] A.J. Alverson, D.W. Rice, S. Dickinson, K. Barry, J.D. Palmer, Origins and
recombination of the bacterial-sized multichromosomal mitochondrial
genome of cucumber, Plant Cell 23 (2011) 2499e2513.
[4] D.B. Sloan, A.J. Alverson, J.P. Chuckalovcak, M. Wu, D.E. McCauley, J.D. Palmer,
D.R. Taylor, Rapid evolution of enormous, multichromosomal genomes in
owering plant mitochondria with exceptionally high mutation rates, PLoS
Biol. 10 (2012) e1001241.
[5] T. Preuten, E. Cincu, J. Fuchs, R. Zoschke, K. Liere, T. Borner, Fewer genes than
organelles: extremely low and variable gene copy numbers in mitochondria
of somatic plant cells, Plant J. 64 (2010) 948e959.
[6] M. Unseld, J.R. Marienfeld, P. Brandt, A. Brennicke, The mitochondrial
genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides,
Nat. Genet. 15 (1997) 57e61.
[7] S. Anderson, A.T. Bankier, B.G. Barrell, M.H. de Bruijn, A.R. Coulson, J. Drouin,
I.C. Eperon, D.P. Nierlich, B.A. Roe, F. Sanger, P.H. Schreier, A.J. Smith,
R. Staden, I.G. Young, Sequence and organization of the human mitochondrial genome, Nature 290 (1981) 457e465.
[8] R.M. Stupar, J.W. Lilly, C.D. Town, Z. Cheng, S. Kaul, C.R. Buell, J. Jiang,
Complex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis
thaliana chromosome 2: implication of potential sequencing errors caused by
large-unit repeats, Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 5099e5103.
[9] M. Klein, U. Eckert-Ossenkopp, I. Schmiedeberg, P. Brandt, M. Unseld,
A. Brennicke, W. Schuster, Physical mapping of the mitochondrial genome of
Arabidopsis thaliana by cosmid and YAC clones, Plant J. 6 (1994) 447e455.
[10] Y. Sugiyama, Y. Watase, M. Nagase, N. Makita, S. Yagura, A. Hirai, M. Sugiura,
The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants, Mol. Genet. Genom. 272 (2005) 603e615.
[11] Y. Ogihara, Y. Yamazaki, K. Murai, A. Kanno, T. Terachi, T. Shiina, N. Miyashita,
S. Nasuda, C. Nakamura, N. Mori, S. Takumi, M. Murata, S. Futo, K. Tsunewaki,
Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome, Nucleic
Acids Res. 33 (2005) 6235e6250.
[12] A.J. Bendich, Reaching for the ring: the study of mitochondrial genome
structure, Curr. Genet. 24 (1993) 564e588.
[13] D.J. Oldenburg, A.J. Bendich, Size and structure of replicating mitochondrial
DNA in cultured tobacco cells, Plant Cell 8 (1996) 447e461.
[14] S. Backert, R. Lurz, O.A. Oyarzabal, T. Borner, High content, size and distribution of single-stranded DNA in the mitochondria of Chenopodium album
(L.), Plant Mol. Biol. 33 (1997) 1037e1050.
[15] J.I. Davila, M.P. Arrieta-Montiel, Y. Wamboldt, J. Cao, J. Hagmann, V. Shedge,
Y.Z. Xu, D. Weigel, S.A. Mackenzie, Double-strand break repair processes
drive evolution of the mitochondrial genome in Arabidopsis, BMC Biol. 9
(2011) 64.
[16] M. Miller-Messmer, K. Kuhn, M. Bichara, M. Le Ret, P. Imbault, J.M. Gualberto,
RecA-dependent DNA repair results in increased heteroplasmy of the Arabidopsis mitochondrial genome, Plant Physiol. 159 (2012) 211e226.
[17] L. Cappadocia, A. Marechal, J.S. Parent, E. Lepage, J. Sygusch, N. Brisson,
Crystal structures of DNAeWhirly complexes and their role in Arabidopsis
organelle genome repair, Plant Cell 22 (2010) 1849e1867.
[18] J.W. Lilly, M.J. Havey, Small, repetitive DNAs contribute signicantly to the
expanded mitochondrial genome of cucumber, Genetics 159 (2001) 317e
328.
[19] M. Kucej, R.A. Butow, Evolutionary tinkering with mitochondrial nucleoids,
Trends Cell Biol. 17 (2007) 586e592.
[20] A.P. Rebelo, L.M. Dillon, C.T. Moraes, Mitochondrial DNA transcription
regulation and nucleoid organization, J. Inherit. Metab. Dis. 34 (2011) 941e
951.
[21] R. Gilkerson, L. Bravo, I. Garcia, N. Gaytan, A. Herrera, A. Maldonado,
B. Quintanilla, The mitochondrial nucleoid: integrating mitochondrial DNA
into cellular homeostasis, Cold Spring Harb. Perspect. Biol. 5 (2013) a011080.
[22] H. Dai, Y.S. Lo, A. Litvinchuk, Y.T. Wang, W.N. Jane, L.J. Hsiao, K.S. Chiang,
Structural and functional characterizations of mung bean mitochondrial
nucleoids, Nucleic Acids Res. 33 (2005) 4725e4739.
[23] Y.-S. Lo, L.-J. Hsiao, N. Cheng, A. Litvinchuk, H. Dai, Characterization of the
structure and DNA complexity of mung bean mitochondrial nucleoids, Mol.
Cells 31 (2011) 217e224.
[24] W. Majeran, G. Friso, Y. Asakura, X. Qu, M. Huang, L. Ponnala, K.P. Watkins,
A. Barkan, K.J. van Wijk, Nucleoid-enriched proteomes in developing plastids
and chloroplasts from maize leaves: a new conceptual framework for
nucleoid functions, Plant Physiol. 158 (2012) 156e189.
[25] A. Sakai, H. Takano, T. Kuroiwa, Organelle nuclei in higher plants: structure,
composition, function, and evolution, Int. Rev. Cytol. 238 (2004) 59e118.
[26] M. Takusagawa, T. Hayashi, H. Takano, A. Sakai, Organization of
mitochondrial-nucleoids in BY-2 cultured tobacco cells, Cytologia 74 (2009)
329e341.
118
[27] B.Z.M. Katherine, J.M. Donohue, B.A. Everitt, Evidence that core histone H3 is
targeted to the mitochondria in Brassica oleracea, Cell Biol. Int. 34 (2010)
997e1003.
[28] M.B. Scher, A. Vaquero, D. Reinberg, SirT3 is a nuclear NAD-dependent
histone deacetylase that translocates to the mitochondria upon cellular
stress, Genes Dev. 21 (2007) 920e928.
[29] M. Takusagawa, S. Tamotsu, A. Sakai, Histone H3 is absent from organelle
nucleoids in BY-2 cultured tobacco cells, Cell Biol. Int. 37 (2013) 748e754.
[30] Y.S. Lo, N. Cheng, L.J. Hsiao, A. Annamalai, G.Y. Jauh, T.N. Wen, H. Dai,
K.S. Chiang, Actin in mung bean mitochondria and implications for its
function, Plant Cell 23 (2011) 3727e3744.
[31] P. Boesch, N. Ibrahim, F. Paulus, A. Cosset, V. Tarasenko, A. Dietrich, Plant
mitochondria possess a short-patch base excision DNA repair pathway,
Nucleic Acids Res. 37 (2009) 5690e5700.
[32] P. Boesch, F. Weber-Lot, N. Ibrahim, V. Tarasenko, A. Cosset, F. Paulus,
R.N. Lightowlers, A. Dietrich, DNA repair in organelles: pathways, organization, regulation, relevance in disease and aging, Biochim. Biophys. Acta 1813
(2011) 186e200.
[33] A. Elo, A. Lyznik, D.O. Gonzalez, S.D. Kachman, S.A. Mackenzie, Nuclear genes
that encode mitochondrial proteins for DNA and RNA metabolism are clustered in the Arabidopsis genome, Plant Cell 15 (2003) 1619e1631.
[34] A.C. Christensen, A. Lyznik, S. Mohammed, C.G. Elowsky, A. Elo, R. Yule,
S.A. Mackenzie, Dual-domain, dual-targeting organellar protein presequences in Arabidopsis can use non-AUG start codons, Plant Cell 17 (2005)
2805e2816.
[35] C. Carrie, K. Kuhn, M.W. Murcha, O. Duncan, I.D. Small, N. OToole, J. Whelan,
Approaches to dening dual-targeted proteins in Arabidopsis, Plant J. 57
(2009) 1128e1139.
[36] J.D. Cupp, B.L. Nielsen, Arabidopsis thaliana organellar DNA polymerase IB
mutants exhibit reduced mtDNA levels with a decrease in mitochondrial
area density, Physiol. Plant. 149 (2013) 91e103.
[37] J.S. Parent, E. Lepage, N. Brisson, Divergent roles for the two PolI-like
organelle DNA polymerases of Arabidopsis, Plant Physiol. 156 (2011) 254e
262.
[38] D.B. Udy, S. Belcher, R. Williams-Carrier, J.M. Gualberto, A. Barkan, Effects of
reduced chloroplast gene copy number on chloroplast gene expression in
maize, Plant Physiol. 160 (2012) 1420e1431.
[39] J. Diray-Arce, B. Liu, J.D. Cupp, T. Hunt, B.L. Nielsen, The Arabidopsis
At1g30680 gene encodes a homologue to the phage T7 gp4 protein that has
both DNA primase and DNA helicase activities, BMC Plant Biol. 13 (2013) 36.
[40] M.K. Wall, L.A. Mitchenall, A. Maxwell, Arabidopsis thaliana DNA gyrase is
targeted to chloroplasts and mitochondria, Proc. Natl. Acad. Sci. U. S. A. 101
(2004) 7821e7826.
[41] A.C. Edmondson, D. Song, L.A. Alvarez, M.K. Wall, D. Almond, D.A. McClellan,
A. Maxwell, B.L. Nielsen, Characterization of a mitochondrially targeted
single-stranded DNA-binding protein in Arabidopsis thaliana, Mol. Genet.
Genom. 273 (2005) 115e122.
[42] J.M. de Haas, J. Hille, F. Kors, B. van der Meer, A.J. Kool, O. Folkerts,
H.J. Nijkamp, Two potential Petunia hybrida mitochondrial DNA replication
origins show structural and in vitro functional homology with the animal
mitochondrial DNA heavy and light strand replication origins, Curr. Genet.
20 (1991) 503e513.
[43] D.L. Robberson, D.A. Clayton, Replication of mitochondrial DNA in mouse L
cells and their thymidine kinase e derivatives: displacement replication on a
covalently-closed circular template, Proc. Natl. Acad. Sci. U. S. A. 69 (1972)
3810e3814.
[44] J. Farkasovska, Sequence analysis of a Papaver somniferum L. mitochondrial
DNA fragment promoting autonomous plasmid replication in Saccharomyces
cerevisiae and Kluyveromyces lactis, Curr. Genet. 24 (1993) 366e367.
[45] S. Backert, P. Dorfel, T. Borner, Investigation of plant organellar DNAs by
pulsed-eld gel electrophoresis, Curr. Genet. 28 (1995) 390e399.
[46] D.J. Oldenburg, A.J. Bendich, Mitochondrial DNA from the liverwort Marchantia polymorpha: circularly permuted linear molecules, head-to-tail concatemers, and a 50 protein, J. Mol. Biol. 310 (2001) 549e562.
[47] S. Backert, R. Lurz, T. Borner, Electron microscopic investigation of mitochondrial DNA from Chenopodium album (L.), Curr. Genet. 29 (1996) 427e
436.
[48] S. Backert, P. Dorfel, R. Lurz, T. Borner, Rolling-circle replication of mitochondrial DNA in the higher plant Chenopodium album (L.), Mol. Cell. Biol. 16
(1996) 6285e6294.
[49] S. Backert, T. Borner, Phage T4-like intermediates of DNA replication and
recombination in the mitochondria of the higher plant Chenopodium album
(L.), Curr. Genet. 37 (2000) 304e314.
[50] J.M. Gerhold, A. Aun, T. Sedman, P. Joers, J. Sedman, Strand invasion structures in the inverted repeat of Candida albicans mitochondrial DNA reveal a
role for homologous recombination in replication, Mol. Cell 39 (2010) 851e
861.
[51] D.M. Lonsdale, J.M. Grienenberger, The mitochondrial genome of plants, in:
R.G. Hermann (Ed.), Cell Organelles, Springer-Verlag, New York, 1992, pp.
181e218.
[52] R.H. Brown, M. Zhang, Mitochondrial plasmids: DNA and RNA, in:
C.S. Levings III, K. VasiI (Eds.), The Molecular Biology of Plant Mitochondria,
Kluver Academic Publishers, Dordrecht, The Netherlands, 1995, pp. 61e91.
[53] B.O. Bengtsson, H. Andersson, The population genetics of plant mitochondrial
plasmids, J. Theor. Biol. 188 (1997) 163e176.
[54] H. Handa, Linear plasmids in plant mitochondria: peaceful coexistences or

malicious invasions? Mitochondrion 8 (2008) 15e25.
[55] C. Hallden, C. Lind, T. Bryngelsson, Minicircle variation in Beta mitochondrial
DNA, Theor. Appl. Genet. 77 (1989) 337e342.
[56] M.R. Hanson, M.F. Conde, Functioning and variation of cytoplasmic genomes:
lesson from cytoplasmic-nuclear interactions affecting male fertility in
plants, Intern. Rev. Cytol. 94 (1985) 213e267.
[57] H. Andersson-Ceplitis, Evolutionary dynamics of mitochondrial plasmids in
natural populations of Silene vulgaris, Evolution 56 (2002) 1592e1598.
[58] M.M. Robison, D.J. Wolyn, A mitochondrial plasmid and plasmid-like RNA
and DNA polymerases encoded within the mitochondrial genome of carrot
(Daucus carota L.), Curr. Genet. 47 (2005) 57e66.
[59] M.C. Flamand, G. Duc, J.P. Goblet, L. Hong, O. Louis, M. Briquet, M. Boutry,
Variant mitochondrial plasmids of broad bean arose by recombination and
are controlled by the nuclear genome, Nucleic Acids Res. 21 (1993) 5468e
5473.
[60] J.A. Wahleithner, D.R. Wolstenholme, Origin and direction of replication in
mitochondrial plasmid DNAs of broad bean, Vicia faba, Curr. Genet. 14 (1988)
163e170.
[61] S. Backert, K. Meissner, T. Borner, Unique features of the mitochondrial
rolling circle-plasmid mp1 from the higher plant Chenopodium album (L.),
[62] S. Backert, M. Kunnimalaiyaan, T. Borner, B.L. Nielsen, In vitro replication of
mitochondrial plasmid mp1 from the higher plant Chenopodium album (L.): a
remnant of bacterial rolling circle and conjugative plasmids? J. Mol. Biol. 284
(1998) 1005e1015.
[63] S. Backert, Strand switching during rolling circle replication of plasmid-like
DNA circles in the mitochondria of the higher plant Chenopodium album
(L.), Plasmid 43 (2000) 166e170.
[64] S.R. Ludwig, R.F. Pohlman, J. Vieira, A.G. Smith, J. Messing, The nucleotide
sequence of a mitochondrial replicon from maize, Gene 38 (1985) 131e138.
[65] A.G. Smith, D.R. Pring, Nucleotide sequence and molecular characterization
of a maize mitochondrial plasmid-like DNA, Curr. Genet. 12 (1987) 617e623.
[66] J.A. Wahleithner, D.R. Wolstenholme, Mitochondrial plasmid DNAs of broad
bean: nucleotide sequences, complex secondary structures, and transcription, Curr. Genet. 12 (1987) 55e67.
[67] L. de la Canal, D. Crouzillat, M.C. Flamand, A. Perrault, M. Boutry, G. Ledoigt,
Nucleotide sequence and transcriptional analysis of a mitochondrial plasmid
from a cytoplasmic male-sterile line of sunower, Theor. Appl. Genet. 81
(1991) 812e818.
[68] M.C. Flamand, J.P. Goblet, G. Duc, M. Briquet, M. Boutry, Sequence and
transcription analysis of mitochondrial plasmids isolated from cytoplasmic
male-sterile lines of Vicia faba, Plant Mol. Biol. 19 (1992) 913e923.
[69] C.M. Thomas, Sugarbeet minicircular mitochondrial DNAs: high-resolution
transcript mapping, transcript abundance and copy number determination,
Mol. Gen. Genet. 234 (1992) 457e465.
[70] C.M. Thomas, The nucleotide sequence and transcription of minicircular
mitochondrial DNAs associated with male-fertile and cytoplasmic malesterile lines of sugarbeet, Nucleic Acids Res. 14 (1986) 9353e9370.
[71] K. Sakaguchi, Invertrons, a class of structurally and functionally related genetic elements that includes linear DNA plasmids, transposable elements,
and genomes of adeno-type viruses, Microbiol. Rev. 54 (1990) 66e74.
[72] M. Paillard, R.R. Sederoff, C.S. Levings, Nucleotide sequence of the S-1
mitochondrial DNA from the S cytoplasm of maize, EMBO J. 4 (1985) 1125e
1128.
[73] C.S. Levings, R.R. Sederoff, Nucleotide sequence of the S-2 mitochondrial DNA
from the S cytoplasm of maize, Proc. Natl. Acad. Sci. U. S. A. 80 (1983) 4055e
4059.
[74] P. Leon, V. Walbot, P. Bedinger, Molecular analysis of the linear 2.3 kb
plasmid of maize mitochondria: apparent capture of tRNA genes, Nucleic
Acids Res. 17 (1989) 4089e4099.
[75] H. Handa, K. Itani, H. Sato, Structural features and expression analysis of a
linear mitochondrial plasmid in rapeseed (Brassica napus L.), Mol. Genet.
Genom. 267 (2002) 797e805.
[76] D.R. Smith, P.J. Keeling, Gene conversion shapes linear mitochondrial
genome architecture, Genome Biol. Evol. 5 (2013) 905e912.
[77] C. OBrien, G. Zabala, V. Walbot, Integrated R2 sequence in mitochondria of
fertile B37N maize encodes and expresses a 130 kD polypeptide similar to
that encoded by the S2 episome of S-type male sterile plants, Nucleic Acids
Res. 17 (1989) 405e422.
[78] G. Zabala, V. Walbot, An S1 episomal gene of maize mitochondria is
expressed in male sterile and fertile plants of the S-type cytoplasm, Mol. Gen.
Genet. 211 (1988) 386e392.
[79] P. Leon, C. OBrien-Vedder, V. Walbot, Expression of ORF1 of the linear 2.3 kb
plasmid of maize mitochondria: product localization and similarities to the
130 kDa protein encoded by the S2 episome, Curr. Genet. 22 (1992) 61e67.
[80] C.L. Schardl, D.R. Pring, D.M. Lonsdale, Mitochondrial DNA rearrangements
associated with fertile revertants of S-type male-sterile maize, Cell 43 (1985)
361e368.
[81] K.J. Newton, J.M. Mariano, C.M. Gibson, E. Kuzmin, S. Gabay-Laughnan,
Involvement of S2 episomal sequences in the generation of NCS4 deletion
mutation in maize mitochondria, Dev. Genet. 19 (1996) 277e286.
[82] J.T. Matera, J. Monroe, W. Smelser, S. Gabay-Laughnan, K.J. Newton, Unique
changes in mitochondrial genomes associated with reversions of S-type
cytoplasmic male sterility in maizemar, PLoS One 6 (2011) e23405.

[83] R.J. Kemble, J.E. Carlson, L.R. Erickson, J.L. Sernyk, D.J. Thompson, The Brassica
mitochondrial DNA plasmid and large RNAs are not exclusively associated
with cytoplasmic male sterility, Mol. Gen. Genet. 205 (1986) 183e185.
[84] P. McDermott, V. Connolly, T.A. Kavanagh, The mitochondrial genome of a
cytoplasmic male sterile line of perennial ryegrass (Lolium perenne L.) contains an integrated linear plasmid-like element, Theor. Appl. Genet. 117
(2008) 459e470.
[85] P. Saumitou-Laprade, G. Pannebecker, F. Maggouta, R. Jean, G. Michaelis,
A linear 10.4 kb plasmid in the mitochondria of Beta maritima, Curr. Genet.
16 (1989) 181e186.
[86] L. Erickson, R. Kemble, E. Swanson, The Brassica mitochondrial plasmid can
be sexually transmitted. Pollen transfer of a cytoplasmic genetic element,
Mol. Gen. Genet. 218 (1989) 419e422.
[87] M. Oshima, H. Handa, The identication of quantitative trait loci that control
the paternal inheritance of a mitochondrial plasmid in rapeseed (Brassica
napus L.), Genes Genet. Syst. 87 (2012) 19e27.
[88] T. Shikanai, Z.Q. Yang, Y. Yamada, Nucleotide sequence and molecular
characterization of plasmid-like DNAs from mitochondria of cytoplasmic
male-sterile rice, Curr. Genet. 15 (1989) 349e354.
[89] A. Marchal, N. Brisson, Recombination and the maintenance of plant
organelle genome stability, New Phytol. 186 (2010) 299e317.
[90] V. Shedge, M. Arrieta-Montiel, A.C. Christensen, S.A. Mackenzie, Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs, Plant Cell 19 (2007) 1251e1264.
[91] R.D. Shereda, A.G. Kozlov, T.M. Lohman, M.M. Cox, J.L. Keck, SSB as an
organizer/mobilizer of genome maintenance complexes, Crit. Rev. Biochem.
Mol. Biol. 43 (2008) 289e318.
[92] S.L. Gasior, H. Olivares, U. Ear, D.M. Hari, R. Weichselbaum, D.K. Bishop,
Assembly of RecA-like recombinases: distinct roles for mediator proteins in
mitosis and meiosis, Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 8411e8418.
[93] V. Zaegel, B. Guermann, M. Le Ret, C. Andres, D. Meyer, M. Erhardt,
J. Canaday, J.M. Gualberto, P. Imbault, The plant-specic ssDNA binding
protein OSB1 is involved in the stoichiometric transmission of mitochondrial
DNA in Arabidopsis, Plant Cell 18 (2006) 3548e3563.
[94] D. Desveaux, A. Marechal, N. Brisson, Whirly transcription factors: defense
gene regulation and beyond, Trends Plant Sci. 10 (2005) 95e102.
[95] A. Marechal, J.S. Parent, F. Veronneau-Lafortune, A. Joyeux, B.F. Lang,
N. Brisson, Whirly proteins maintain plastid genome stability in Arabidopsis,
Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 14693e14698.
[96] A. Samach, C. Melamed-Bessudo, N. Avivi-Ragolski, S. Pietrokovski, A.A. Levy,
Identication of plant RAD52 homologs and characterization of the Arabidopsis thaliana RAD52-like genes, Plant Cell 23 (2011) 4266e4279.
[97] S. Janicka, K. Kuhn, M. Le Ret, G. Bonnard, P. Imbault, H. Augustyniak,
J.M. Gualberto, A RAD52-like single-stranded DNA binding protein affects
mitochondrial DNA repair by recombination, Plant J. 72 (2012) 423e435.
[98] X.J. Chen, M.X. Guan, G.D. Clark-Walker, MGM101, a nuclear gene involved in
maintenance of the mitochondrial genome in Saccharomyces cerevisiae,
[99] S. Meeusen, Q. Tieu, E. Wong, E. Weiss, D. Schieltz, J.R. Yates, J. Nunnari,
Mgm101p is a novel component of the mitochondrial nucleoid that binds
DNA and is required for the repair of oxidatively damaged mitochondrial
DNA, J. Cell Biol. 145 (1999) 291e304.
[100] M. Mbantenkhu, X. Wang, J.D. Nardozzi, S. Wilkens, E. Hoffman, A. Patel,
M.S. Cosgrove, X.J. Chen, Mgm101 is a Rad52-related protein required for
mitochondrial DNA recombination, J. Biol. Chem. 286 (2011) 42360e42370.
[101] J.M. Martinez-Zapater, P. Gil, J. Capel, C.R. Somerville, Mutations at the
Arabidopsis CHM locus promote rearrangements of the mitochondrial
genome, Plant Cell 4 (1992) 889e899.
[102] W. Sakamoto, H. Kondo, M. Murata, F. Motoyoshi, Altered mitochondrial
gene expression in a maternal distorted leaf mutant of Arabidopsis induced
by chloroplast mutator, Plant Cell 8 (1996) 1377e1390.
[103] M.P. Arrieta-Montiel, V. Shedge, J. Davila, A.C. Christensen, S.A. Mackenzie,
Diversity of the Arabidopsis mitochondrial genome occurs via nuclearcontrolled recombination activity, Genetics 183 (2009) 1261e1268.
[104] A.P. Sandhu, R.V. Abdelnoor, S.A. Mackenzie, Transgenic induction of mitochondrial rearrangements for cytoplasmic male sterility in crop plants, Proc.
Natl. Acad. Sci. U. S. A. 104 (2007) 1766e1770.
[105] R.V. Abdelnoor, A.C. Christensen, S. Mohammed, B. Munoz-Castillo,
H. Moriyama, S.A. Mackenzie, Mitochondrial genome dynamics in plants and
animals: convergent gene fusions of a MutS homologue, J. Mol. Evol. 63
(2006) 165e173.
[106] Y.Z. Xu, M.P. Arrieta-Montiel, K.S. Virdi, W.B. de Paula, J.R. Widhalm,
G.J. Basset, J.I. Davila, T.E. Elthon, C.G. Elowsky, S.J. Sato, T.E. Clemente,
S.A. Mackenzie, MutS HOMOLOG1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light, Plant Cell
23 (2011) 3428e3441.
[107] M.J. Schoeld, P. Hsieh, DNA mismatch repair: molecular mechanisms and
biological function, Annu. Rev. Microbiol. 57 (2003) 579e608.
[108] R.V. Abdelnoor, R. Yule, A. Elo, A.C. Christensen, G. Meyer-Gauen,
S.A. Mackenzie, Substoichiometric shifting in the plant mitochondrial
genome is inuenced by a gene homologous to MutS, Proc. Natl. Acad. Sci. U.
S. A. 100 (2003) 5968e5973.
[109] Z. Lin, H. Kong, M. Nei, H. Ma, Origins and evolution of the recA/RAD51 gene
family: evidence for ancient gene duplication and endosymbiotic gene
transfer, Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 10328e10333.
119
[110] S.T. Lovett, R.L. Hurley, V.A. Sutera Jr., R.H. Aubuchon, M.A. Lebedeva,
Crossing over between regions of limited homology in Escherichia coli. RecAdependent and RecA-independent pathways, Genetics 160 (2002) 851e859.
[111] A.J. Alverson, S. Zhuo, D.W. Rice, D.B. Sloan, J.D. Palmer, The mitochondrial
genome of the legume Vigna radiata and the analysis of recombination
across short mitochondrial repeats, PLoS One 6 (2011) e16404.
[112] H. Cerutti, A.M. Johnson, J.E. Boynton, N.W. Gillham, Inhibition of chloroplast
DNA recombination and repair by dominant negative mutants of Escherichia
coli RecA, Mol. Cell. Biol. 15 (1995) 3003e3011.
[113] T. Kwon, E. Huq, D.L. Herrin, Microhomology-mediated and nonhomologous
repair of a double-strand break in the chloroplast genome of Arabidopsis,
Proc. Natl. Acad. Sci. U. S. A. 107 (2010) 13954e13959.
[114] B.A. Rowan, D.J. Oldenburg, A.J. Bendich, RecA maintains the integrity of
chloroplast DNA molecules in Arabidopsis, J. Exp. Bot. 61 (2010) 2575e2588.
[115] M. Odahara, T. Inouye, T. Fujita, M. Hasebe, Y. Sekine, Involvement of
mitochondrial-targeted RecA in the repair of mitochondrial DNA in the moss,
Physcomitrella patens, Genes Genet. Syst. 82 (2007) 43e51.
[116] J.S. Sung, B. Demple, Roles of base excision repair subpathways in correcting
oxidized abasic sites in DNA, FEBS J. 273 (2006) 1620e1629.
[117] P. Boesch, N. Ibrahim, A. Dietrich, R.N. Lightowlers, Membrane association of
mitochondrial DNA facilitates base excision repair in mammalian mitochondria, Nucleic Acids Res. 38 (2010) 1478e1488.
[118] B.L. Gutman, K.K. Niyogi, Evidence for base excision repair of oxidative DNA
damage in chloroplasts of Arabidopsis thaliana, J. Biol. Chem. 284 (2009)
17006e17012.
[119] R.J. Bensen, H.R. Warner, The partial purication and characterization of
nuclear and mitochondrial uracil-DNA glycosylase activities from Zea mays
seedlings, Plant Physiol. 83 (1987) 149e154.
[120] T. Morales-Ruiz, M. Birincioglu, P. Jaruga, H. Rodriguez, T. Roldan-Arjona,
M. Dizdaroglu, Arabidopsis thaliana Ogg1 protein excises 8-hydroxyguanine
and 2,6-diamino-4-hydroxy-5-formamidopyrimidine from oxidatively
damaged DNA containing multiple lesions, Biochemistry 42 (2003) 3089e3095.
[121] H. Chen, P. Chu, Y. Zhou, Y. Li, J. Liu, Y. Ding, E.W. Tsang, L. Jiang, K. Wu,
S. Huang, Overexpression of AtOGG1, a DNA glycosylase/AP lyase, enhances
seed longevity and abiotic stress tolerance in Arabidopsis, J. Exp. Bot. 63
(2012) 4107e4121.
[122] A. Macovei, A. Balestrazzi, M. Confalonieri, M. Fae, D. Carbonera, New insights on the barrel medic MtOGG1 and MtFPG functions in relation to
oxidative stress response in planta and during seed imbibition, Plant Physiol.
Biochem. 49 (2011) 1040e1050.
[123] T. Ohtsubo, O. Matsuda, K. Iba, I. Terashima, M. Sekiguchi, Y. Nakabeppu,
Molecular cloning of AtMMH, an Arabidopsis thaliana ortholog of the
Escherichia coli mutM gene, and analysis of functional domains of its product,
Mol. Gen. Genet. 259 (1998) 577e590.
[124] T.M. Murphy, M.J. Gao, Multiple forms of formamidopyrimidine-DNA glycosylase produced by alternative splicing in Arabidopsis thaliana,
J. Photochem. Photobiol. B 61 (2001) 87e93.
[125] L.M. Grifths, D. Swartzlander, K.L. Meadows, K.D. Wilkinson, A.H. Corbett,
P.W. Doetsch, Dynamic compartmentalization of base excision repair proteins in response to nuclear and mitochondrial oxidative stress, Mol. Cell.
Biol. 29 (2009) 794e807.
[126] D.B. Swartzlander, L.M. Grifths, J. Lee, N.P. Degtyareva, P.W. Doetsch,
A.H. Corbett, Regulation of base excision repair: Ntg1 nuclear and mitochondrial dynamic localization in response to genotoxic stress, Nucleic Acids
Res. 38 (2010) 3963e3974.
[127] T. Kleffmann, D. Russenberger, A. von Zychlinski, W. Christopher,
K. Sjolander, W. Gruissem, S. Baginsky, The Arabidopsis thaliana chloroplast
proteome reveals pathway abundance and novel protein functions, Curr.
Biol. 14 (2004) 354e362.
[128] Y. Mori, S. Kimura, A. Saotome, N. Kasai, N. Sakaguchi, Y. Uchiyama,
T. Ishibashi, T. Yamamoto, H. Chiku, K. Sakaguchi, Plastid DNA polymerases
from higher plants, Arabidopsis thaliana, Biochem. Biophys. Res. Commun.
334 (2005) 43e50.
[129] D. Cordoba-Canero, T. Roldan-Arjona, R.R. Ariza, Arabidopsis ARP endonuclease functions in a branched base excision DNA repair pathway completed
by LIG1, Plant J. 68 (2011) 693e702.
[130] P.A. Sunderland, C.E. West, W.M. Waterworth, C.M. Bray, An evolutionarily
conserved translation initiation mechanism regulates nuclear or mitochondrial targeting of DNA ligase 1 in Arabidopsis thaliana, Plant J. 47 (2006) 356e
367.
[131] I. Small, R. Suffolk, C.J. Leaver, Evolution of plant mitochondrial genomes via
substoichiometric intermediates, Cell 58 (1989) 69e76.
[132] O.A. Kajander, A.T. Rovio, K. Majamaa, J. Poulton, J.N. Spelbrink, I.J. Holt,
P.J. Karhunen, H.T. Jacobs, Human mtDNA sublimons resemble rearranged
mitochondrial genomes found in pathological states, Hum. Mol. Genet. 9
(2000) 2821e2835.
[133] F. Budar, P. Touzet, R. De Paepe, The nucleo-mitochondrial conict in cytoplasmic male sterilities revisited, Genetica 117 (2003) 3e16.
[134] M. Odahara, H. Kuroiwa, T. Kuroiwa, Y. Sekine, Suppression of repeatmediated gross mitochondrial genome rearrangements by RecA in the
moss Physcomitrella patens, Plant Cell 21 (2009) 1182e1194.
[135] M. Woloszynska, D. Trojanowski, Counting mtDNA molecules in Phaseolus
vulgaris: sublimons are constantly produced by recombination via short
repeats and undergo rigorous selection during substoichiometric shifting,
Plant Mol. Biol. 70 (2009) 511e521.
120
[136] D.Y. Wang, Q. Zhang, Y. Liu, Z.F. Lin, S.X. Zhang, M.X. Sun, Sodmergen, The
levels of male gametic mitochondrial DNA are highly regulated in angiosperms with regard to mitochondrial inheritance, Plant Cell 22 (2010) 2402e
2416.
[137] M. Lynch, B. Koskella, S. Schaack, Mutation pressure and the evolution of
organelle genomic architecture, Science 311 (2006) 1727e1730.
[138] A.C. Christensen, Plant mitochondrial genome evolution can be explained by
DNA repair mechanisms, Genome Biol. Evol. 5 (2013) 1079e1086.
[139] C.L. Parkinson, J.P. Mower, Y.L. Qiu, A.J. Shirk, K. Song, N.D. Young,
C.W. dePamphilis, J.D. Palmer, Multiple major increases and decreases in
mitochondrial substitution rates in the plant family Geraniaceae, BMC Evol.
Biol. 5 (2005) 73.
[140] J.P. Mower, P. Touzet, J.S. Gummow, L.F. Delph, J.D. Palmer, Extensive variation in synonymous substitution rates in mitochondrial genes of seed
plants, BMC Evol. Biol. 7 (2007) 135.
[141] M. Koulintchenko, Y. Konstantinov, A. Dietrich, Plant mitochondria actively
import DNA via the permeability transition pore complex, EMBO J. 22 (2003)
1245e1254.
[142] F. Weber-Lot, N. Ibrahim, P. Boesch, A. Cosset, Y. Konstantinov,
R.N. Lightowlers, A. Dietrich, Developing a genetic approach to investigate
the mechanism of mitochondrial competence for DNA import, Biochim.
Biophys. Acta 1787 (2009) 320e327.
[143] M. Koulintchenko, R.J. Temperley, P.A. Mason, A. Dietrich, R.N. Lightowlers,

Natural competence of mammalian mitochondria allows the molecular
investigation of mitochondrial gene expression, Hum. Mol. Genet. 15 (2006)
143e154.
[144] Y. Ono, A. Sakai, K. Takechi, S. Takio, M. Takusagawa, H. Takano, NtPolI-like1
and NtPolI-like2, bacterial DNA polymerase I homologs isolated from BY-2
cultured tobacco cells, encode DNA polymerases engaged in DNA replication in both plastids and mitochondria, Plant Cell Physiol. 48 (2007) 1679e
1692.
[145] T.E. Shutt, M.W. Gray, Twinkle, the mitochondrial replicative DNA helicase, is
widespread in the eukaryotic radiation and may also be the mitochondrial
DNA primase in most eukaryotes, J. Mol. Evol. 62 (2006) 588e599.
[146] K. Krause, I. Kilbienski, M. Mulisch, A. Rodiger, A. Schafer, K. Krupinska, DNAbinding proteins of the Whirly family in Arabidopsis thaliana are targeted to
the organelles, FEBS Lett. 579 (2005) 3707e3712.
[147] M. Vermel, B. Guermann, L. Delage, J.M. Grienenberger, L. Marchal-Drouard,
J.M. Gualberto, A family of RRM-type RNA-binding proteins specic to plant
mitochondria, Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 5866e5871.
[148] D. Cordoba-Canero, E. Dubois, R.R. Ariza, M.P. Doutriaux, T. Roldan-Arjona,
Arabidopsis uracil DNA glycosylase (UNG) is required for base excision repair
of uracil and increases plant sensitivity to 5-uorouracil, J. Biol. Chem. 285
(2010) 7475e7483.

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Biochimie 100 (2014) 107e120

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The plant mitochondrial genome: Dynamics and maintenance

* Corresponding author. Tel.: 33 3 67 15 53 73; fax: 33 3 88 61 44 42.

an active DNA recombination system that allows copy correction of

J.M. Gualberto et al. / Biochimie 100 (2014) 107e120

of other lineages. The known genes usually range between 50 and

J.M. Gualberto et al. / Biochimie 100 (2014) 107e120

with 77 deposited in the GenBank database (http://www.ncbi.nlm.

J.M. Gualberto et al. / Biochimie 100 (2014) 107e120

replication have been identied by sequence homology and from

concatemeric molecules could be generated both by rolling circle

J.M. Gualberto et al. / Biochimie 100 (2014) 107e120

variants can arise from recombination events [59]. The nuclear

autonomously replicated and transcribed. It has been proposed that

J.M. Gualberto et al. / Biochimie 100 (2014) 107e120

presynaptic DNA-protein lament. In the presence of homologous

As RECA2 and RECA3, additional core elements of the plant

ssDNA: single-stranded DNA; Mt: mitochondrion; Cp: chloroplast; Nuc: nucleus.

J.M. Gualberto et al. / Biochimie 100 (2014) 107e120

MutH to mismatches that arise during replication and homologous

J.M. Gualberto et al. / Biochimie 100 (2014) 107e120

J.M. Gualberto et al. / Biochimie 100 (2014) 107e120

in reduced recovery of the mtDNA following genotoxic damage

J.M. Gualberto et al. / Biochimie 100 (2014) 107e120

mitochondrial or plastidic, depending on the program used, with

potentially deleterious consequences to the plant. But SSS is also

J.M. Gualberto et al. / Biochimie 100 (2014) 107e120

J.M. Gualberto et al. / Biochimie 100 (2014) 107e120

[54] H. Handa, Linear plasmids in plant mitochondria: peaceful coexistences or

J.M. Gualberto et al. / Biochimie 100 (2014) 107e120

J.M. Gualberto et al. / Biochimie 100 (2014) 107e120

[143] M. Koulintchenko, R.J. Temperley, P.A. Mason, A. Dietrich, R.N. Lightowlers,

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