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Genetics. Dec 2009; 183(4): 1261–1268.
PMCID: PMC2787419

Diversity of the Arabidopsis Mitochondrial Genome Occurs via Nuclear-Controlled Recombination Activity


The plant mitochondrial genome is recombinogenic, with DNA exchange activity controlled to a large extent by nuclear gene products. One nuclear gene, MSH1, appears to participate in suppressing recombination in Arabidopsis at every repeated sequence ranging in size from 108 to 556 bp. Present in a wide range of plant species, these mitochondrial repeats display evidence of successful asymmetric DNA exchange in Arabidopsis when MSH1 is disrupted. Recombination frequency appears to be influenced by repeat sequence homology and size, with larger size repeats corresponding to increased DNA exchange activity. The extensive mitochondrial genomic reorganization of the msh1 mutant produced altered mitochondrial transcription patterns. Comparison of mitochondrial genomes from the Arabidopsis ecotypes C24, Col-0, and Ler suggests that MSH1 activity accounts for most or all of the polymorphisms distinguishing these genomes, producing ecotype-specific stoichiometric changes in each line. Our observations suggest that MSH1 participates in mitochondrial genome evolution by influencing the lineage-specific pattern of mitochondrial genetic variation in higher plants.

THE plant mitochondrial genome is characterized by several unusual features in its organization and structure. These features include the presence of sequence chimeras (Schnable and Wise 1998), foreign DNA insertions (Xiong et al. 2008), and unusually high levels of recombination (Mackenzie 2007). Recombination in the mitochondrial genome can involve large-size (>1 kb) repeats that undergo high-frequency reciprocal DNA exchange to subdivide the genome, as well as intermediate-size repeats that mediate low-frequency, asymmetric DNA exchange to produce only one of the predicted recombination products. This low-frequency recombination activity is associated with rapid stoichiometric changes in genome configuration (Shedge et al. 2007), referred to as substoichiometric shifting (Small et al. 1987).

Three nuclear genes have been shown to influence recombination within the plant mitochondrial genome: MSH1 (Abdelnoor et al. 2003), RECA3 (Shedge et al. 2007), and OSB1 (Zaegel et al. 2006). Of these, MSH1 appears to have the most profound and immediate effect on the genome and on plant phenotype (Sandhu et al. 2007; Shedge et al. 2007). To better understand the influence of MSH1-regulated recombination on genome structure, we investigated mitochondrial sites in Arabidopsis at which MSH1 appears to function. We show that at least 33 sites within the genome simultaneously become active with MSH1 disruption. Repeat-mediated DNA exchange activity results in extensive changes in mitochondrial genome organization and gene expression patterns by permitting differential modulation of transcription. The pattern of genomic reorganization is highly reproducible, and Arabidopsis cross-ecotype comparisons suggest that these rearrangement processes participate directly in higher plant mitochondrial genome evolution.


Arabidopsis thaliana growth and mutants:

Arabidopsis plants were grown by cold treating (4°) and then sowing seeds directly in potting mix (Metro Mix 360). Plants were grown at an 8-hr-day length at 24° for 8 weeks and then transferred to a 16-hr-day length. Two MSH1 mutants were used for the study: msh1-1(Abdelnoor et al. 2003) and Salk_041951. The RECA3 mutant line Sail_252_C06 was also used for genetic analyses (The Arabidopsis Information Resource, http://www.Arabidopsis.org).

DNA gel blot and PCR assays:

Total genomic DNA was extracted from above-ground tissues of flowering plants using the DNeasy plant mini kit (Qiagen). Total RNA was isolated using TRIzol reagent (Invitrogen) according to the manufacturer's instructions and purified using the RNeasy mini kit (Qiagen). DNA gel blot and hybridizations were as described previously (Janska and Mackenzie 1993). Primers used to PCR amplify repeats are listed in the supporting information (Table S1).

Quantitative PCR:

Equal amounts of DNA were used for quantitative PCR using the SYBR GreenER kit for iCycler (Invitrogen). Quantitative PCR data collection and analysis were conducted using iCycler iQ software (version 3.1; Bio-Rad). Experiments were repeated, each sample was run in triplicate, and the results were averaged. Primers used for real-time analysis of regions present in molecules B and D and molecules A and C, respectively, were RealBDF (5′-ATTCCATCCACTCCGGCTTAGCTT-3′) and RealBDR (5′-TCGCTGTGAAAGG TGGAATCCGTT-3′) and RealACF (5′-ATGTAGAGCCAACTGGAGAGCA-3′) and RealACR (5′-CGGAAAGCCCAAATTCTCCTGCAT-3′).

Bioinformatics analyses:

BLAST and blast2seq (http://www.ncbi.nlm.nih.gov/blast/bl2seq/wblast2.cgi) were used to identify repeated sequences within the C24 mitochondrial genome with a word size of 50 nucleotides. This process identified 104 different repeats, repeats A–Z and AA–ZZ, in descending order of BLAST score. Each repeat copy was numbered (e.g., repeat A-1 and repeat A-2) and distinguished by the flanking sequences. The 33 largest of the intermediate class of repeats, from 108 to 556 bp, are indicated in Figure 1A and Table S2. Most repeats were present in two copies only, with the exceptions of H, V, FF, NN, OO, and RR, present in three copies and BB present in four copies.

Figure 1.
Sites of recombination in the Arabidopsis mitochondrial genome. (A) Computer-generated map of the 33 identified small mitochondrial repeats active in Arabidopsis msh1. Colored repeats represent those tested by gel blot hybridization, with corresponding ...

To identify repeats in the mitochondrial sequences of sorghum, tobacco, and maize, the software REPuter (Kurtz et al. 2001) was used and its results were processed with a Perl script designed to filter close appearances of the repeats. To map ecotype mitochondrial genomes, a script written in Perl generated a network whose nodes are the regions between the repeats and whose arcs indicate evidence of linkages on the same molecule using information gathered from DNA gel blot analysis from the repeated regions for each ecotype. A circuit in this network corresponds to a map of the mitochondrial genome, and circular maps of these circuits were generated for each ecotype. Arabidopsis Genome Initiative locus identifiers are MSH1 (At3g24320) and RECA3 (At3g10140).


Mitochondrial recombination is prolific in the absence of MSH1:

In Arabidopsis msh1 mutants, successful DNA exchange activity increased markedly at repeats ranging in size from 108 bp to 556 bp (Figure 1A, Table S2) relative to wild- type Columbia-0 (Col-0). There exist 33 near-perfect (>90% sequence identity) repeats within this size range in Arabidopsis, named in alphabetical order by BLAST score, and 23 were confirmed to be active in msh1 mutants (Figure 1B; Figure S1). The remaining 10 are assumed to be active, but definitive confirmation was precluded either by their proximity to other active repeats or by their relative product sizes. No repeats are detected in the size range between 556 bp, the upper limit for intermediate repeats, and 4.3 kbp, the lower limit of high-frequency large repeats in the genome.

A selected imperfect (80% sequence identity) repeat (IR-1/IR-2) within the intermediate-size range (342 bp) did not show evidence of recombination (Figure 1C, Table S2), suggesting that a near-perfect sequence homology of a given size range may be essential for successful DNA exchange. This observation appears consistent with what has been reported in yeast mitochondria (Phadnis et al. 2005). Similarly, two repeats below the indicated size range tested negative for recombination activity (Table S2). As reported previously (Shedge et al. 2007), msh1-regulated recombination at each repeat was asymmetric, with only one product retained in the genome. Similar intermediate-size repeated sequences could be identified in the mitochondrial genomes of other plant species, although size range varied slightly, with no evidence of sequence conservation among repeats from different species (Table 1). We postulate that these repeats are activated with the disruption of MSH1 as well (Sandhu et al. 2007).

Sample plant species containing intermediate-size mitochondrial repeats

The extent of the observed mitochondrial rearrangement in the msh1 mutant (formerly designated chm1) is surprising in light of previous reports suggesting a limited, localized point of mitochondrial rearrangement (Sakamoto et al. 1996; Shedge et al. 2007). The seeming disparity in results derives from differing experimental approaches. Evidence of recombination is considerably more difficult to detect when probing with large, cosmid-size genomic segments than with probes designed to specifically target the repeats due to the complex hybridization patterns from multiple fragments and because most recombinant products are present in low stoichiometry in the first generation following MSH1 disruption.

Behavior of msh1 mutants:

Comparison can be made of “early” vs. “advanced” msh1 mutants by comparing lines derived from Col-0 × msh1 for F2 msh1/msh1 progeny (early) with the original chm1-1 mutant reported by Redei (1973) and maintained by recurrent self-pollination (advanced). Differences exist between these two genomes in relative DNA stoichiometries (Figure 2), suggesting that mitochondrial rearrangement continues at some level indefinitely in the absence of MSH1. Analysis of early generation msh1 mutants indicates that all repeats are active in recombination simultaneously, with differences in rate appearing to correspond to repeat size (Figure 3A). The seemingly continuous recombination activity may be a consequence of recombination products serving as substrate for additional DNA exchange activity (Figure 3B), but the process does not appear to be stochastic on the basis of comparisons of the advanced msh1 mutants. Plant-to-plant comparisons of advanced msh1 mutants show very similar mitochondrial genome configuration, with minor differences accounted for largely by secondary recombinations. However, in association with active recombination, a process of cytoplasmic sorting occurs, giving rise to mitochondrial genome variation among individual F3 progeny (Col-0 × msh1) (Figure 3C).

Figure 2.
Early (first-generation) and advanced-generation msh1 mutants differ in mitochondrial genome configuration. Evaluations were made with three different repeats—B, D, and F—to demonstrate recombination (A and B, parental molecules; C, recombinant ...
Figure 3.
Features of msh1-regulated recombination. (A) A gradient of recombination based on repeat size may exist. For example, molecules A and B recombine at repeat G (335 bp) to give product C, and molecules B and D (which do not hybridize with this probe) recombine ...

The msh1 recA3 double mutant (Shedge et al. 2007) undergoes more extensive rearrangement of the mitochondrial genome than is observed in the advanced msh1 (chm1-1) mutants. The nature of recombination is altered in the double mutant, so that reciprocal recombination products accumulate for some of the repeats (Figure 4). The extensive degree of genomic rearrangement that occurs in msh1 and the msh1 recA3 double mutant produces alterations in mitochondrial gene expression. RNA gel blot analysis showed that several transcripts were altered in either size or abundance as a consequence of recombination (Figure 5). However, transcript changes were not observed for all genes. For example, three additional mitochondrial genes tested, Atp9, Atp6, and orf 111b, showed no detectable change in transcript level or size (data not shown).

Figure 4.
Reciprocal recombinants can accumulate in the msh1 recA3 double mutant. Experiments using repeats D, K, and I as probes show that parental forms A and B are predominant in Col-0. In the msh1 mutant, only recombinant molecule C accumulates. In the double ...
Figure 5.
Mitochondrial transcription is influenced by DNA rearrangement activity. RNA gel blot analysis of total RNA preparations probed with the mitochondrial coding sequence of orf452, Atp8, and CoxII to demonstrate examples of enhanced transcript levels (orf452 ...

Mitochondrial genome comparisons in Arabidopsis:

Arabidopsis C24, Col-0, and Ler mitochondrial genomes are readily distinguished by numerous DNA polymorphisms, some of which have been characterized in detail. Previous studies by another group showed that at least one novel DNA insertion exists in Col-0 but is absent from C24 (Forner et al. 2005). This insertion was suggested to involve a 9-bp repeat-mediated integration. The sequence in question represents a recombinationally active region (Zaegel et al. 2006; Shedge et al. 2007). Similarly, mitochondrial genomic environments present in Col-0 have seemingly disappeared from the Ler genome (Figure 6). Remarkably, introduction of the msh1 mutation to C24, Col-0, and Ler ecotypes produced genomic changes such that each of the three mitochondrial genomes show evidence of recombination in all regions assayed (Figure 6). Following this observation, we employed PCR-based methods to detect an extremely low-level presence of regions undetectable by gel blot hybridization in the wild type (Table 2). In some cases, the presence of regions could be predicted on the basis of recombination patterns in the msh1 mutant, but in such a small number of cells as to go completely undetected.

Figure 6.
Substoichiometric shifting accounts for DNA polymorphisms distinguishing Arabidopsis ecotypes. Recombination data are presented for two different repeats, B and L. In both panels, molecules A and B are predominant forms in Col-0. Molecule C is the product ...
Evidence for substoichiometric repeat forms in Arabidopsis ecotypes

These results indicate that several features distinguishing the three mitochondrial genomes are largely the consequence of differential substoichiometric shifting across ecotypes under the influence of MSH1. The region reported by Forner et al. (2005) to be present in Col-0 but absent from C24 is present at near-undetectable levels in C24, with its recombination activity evident only in the C24 msh1 mutant (Table 2). Similarly, genomic regions present in Col-0 but absent in Ler were detectable within the Ler msh1 mutant (Figure 6). These observations suggest that much of the mitochondrial variation reported in Arabidopsis ecotypes is the consequence of MSH1-regulated recombination.

While the recombinationally active regions of the Arabidopsis mitochondrial genome were dispersed throughout the genome, some repeats tended to cluster (Figure 1A and Figure 7A). Several regions show repeats organized densely, even overlapping. In fact, the recombinational region suggested by Forner et al. (2005) to be absent from C24 actually encompasses four distinct and active repeats within a 1.8-kb segment (Figure 7B). Given the observed association of recombination frequency with repeat size, these cluster regions are presumed to represent regions of highest DNA exchange activity within the genome.

Figure 7.
Intermediate repeats within the Arabidopsis mitochondrial genome show evidence of clustering. (A) Position of the repeat clusters on the mitochondrial genome map. The y-axis represents the map position with a cluster represented by a symbol. Repeats present ...

Mitochondrial genome comparisons of C24, Col-0, Ler, and their msh1 counterparts allowed us to model the organization of these genomes (Figure 8). From a process of cross-ecotype diagnostic gel blot hybridizations with repeat probes, we postulate that the three genomes, while differing dramatically in their organizations in wild-type lines, appear much more similar in their msh1 counterparts. This similarity emerges from substoichiometric forms present in all three ecotypes that become amplified with the disruption of MSH1 and enhanced ectopic recombination.

Figure 8.
Model representing the mitochondrial genomes of Arabidopsis ecotypes based on diagnostic gel blot hybridization experiments including intermediate repeat regions and an assembly script. The predominant form is represented as the larger forms, with smaller ...


Loss of MSH1 in Arabidopsis results in extensive changes in mitochondrial genome configuration and altered gene expression:

The impact of MSH1 on DNA exchange activity within the Arabidopsis mitochondrial genome is wide-ranging, influencing the activity of every identifiable repeat in the genome within a size range of ~100–600 bp. The pervasive nature of mitochondrial rearrangement in the msh1 mutant suggests that the gene participates in defining the mitochondrial genome organization that is inherited within a lineage. This influence by MSH1 was demonstrated in cross-ecotype comparisons within Arabidopsis. Loss of MSH1 activity in C24, Col-0, and Ler leads to stoichiometric changes that essentially obviate polymorphisms between the genomes. From these results we postulate that a significant proportion of the within-species mitochondrial DNA polymorphisms observed in plants may be the consequence of low-frequency recombination and substoichiometric changes within genomes that are otherwise quite similar or even identical in sequence.

The influence of MSH1 in establishing genomic stoichiometric relationships also affected mitochondrial transcription. Transcriptional modulation occurs as the apparent consequence of altered gene copy number or local environment during genomic shifting. In fact, cross-ecotype variation in mitochondrial transcription has already been shown genetically to be the consequence, at least in part, of mitochondrial genome configuration (Forner et al. 2008). Thus, MSH1 appears to play a significant role in plant mitochondrial genome diversity by controlling low-frequency, asymmetric recombination and, hence, genetic variation that is observed within plant mitochondrial genomes (Small et al. 1989).

A model for MSH1 action:

Results presented here and in a previous study (Shedge et al. 2007) suggest that MSH1 influences the fate of double-strand breaks and strand invasion within near-perfect repeats of a given size range. MSH1 apparently limits successful DNA exchange, so that recombination at intermediate repeats is extremely low but detectable in wild type, and unsuccessful events presumably result in gene conversion events that would account for the continued maintenance of sequence identity in the repeats. Disruption of MSH1 permits high-frequency DNA exchange and massive reorganization of the genome. Remarkably, this reorganization in C24, Col-0, and Ler leads to very similar genome organizations in the three ecotypes, perhaps eventually producing a “default” organization with final DNA configurations approaching more uniform levels. The process by which these three mitochondrial genomes assume distinct, ecotype-specific, heritable genome configurations with the participation of MSH1 is a detail for future study.

The observations that we report in Arabidopsis are strikingly similar to previous studies of the common bean (Phaseolus vulgaris L), where the accession line G08063 was shown to derive directly from the maternal parent line POP, although their mitochondrial genomes appear remarkably different in configuration (Janska et al. 1998). In bean, as in Arabidopsis, these mitochondrial genomes were apparently interconvertible via substoichiometric shifting processes, as deduced by more sensitive mapping methods.

For such genomic interconversions to occur, one must assume that successful DNA exchange involves one parental molecule that is substoichiometric and present only in some small fraction of the plant's cells. In Arabidopsis, recombination occurs at a repeat present at nearly undetectable levels in C24 (Forner et al. 2005). Similar substoichiometric recombination has been described in the common bean (Woloszynska and Trojanowski 2009) and pearl millet (Feng et al. 2009) mitochondria. This can be explained by hypothesizing that these events occur only in tissue(s) where the repeats are present in normal copy number. We have speculated that this is the meristem (Arrieta-Montiel et al. 2001). Whether loss of MSH1 can produce a mitochondrial genome configuration in the vegetative tissues of a plant that resembles that of the meristem cells, the elusive “master” chromosome (Lonsdale et al. 1988), is an interesting possibility that merits further testing.

MSH1-associated processes likely account for other mitochondrial rearrangement activity observed in plants:

Massive mitochondrial genome rearrangement in plants has been reported in the past. Many of these reports involved cell suspension cultures (Kemble et al. 1982; Kemble and Shepard 1984; Schmidt et al. 1996). Suspension-culture-associated mitochondrial rearrangements have also been associated with repeat-mediated recombination (Belliard et al. 1979) and likely substoichiometric shifting (Ozias-Akins et al. 1988; Forner et al. 2005). These results, while not conclusive, would be consistent with a model for enhanced mitochondrial recombination under conditions where MSH1 might be reduced in its expression or activity. There are probably other environmental conditions under which modulation of MSH1 could influence mitochondrial genome organization within a plant. Perhaps such conditions permit low-frequency induction of cytoplasmic male sterility (Sandhu et al. 2007) in natural plant populations or, perhaps, the spontaneous reversion to pollen fertility (Janska et al. 1998)? Interestingly, a report made several years ago on maize following crosses to the mutant iojap suggests that these crossing experiments resulted in the emergence of a cytoplasmic male sterile cytoplasm type from a normal fertile cytoplasm (Lemke et al. 1985). These reported observations possibly could be accounted for by a substoichiometric shifting process identical to that reported here.


We thank Hardik Kundariya for excellent technical assistance. This work was funded by a grant from the National Science Foundation (NSF) (MCB 0744104) to S.A.M. and M.P.A.-M. This material was based on work supported by the National Science Foundation while A.C.C. was working at the NSF. Any opinion, finding, conclusions, or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the NSF.


Supporting information is available online at http://www.genetics.org/cgi/content/full/genetics.109.108514/DC1.


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