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First published online April 27, 2007; 10.1105/tpc.106.048355 The Plant Cell 19:1251-1264 (2007) © 2007 American Society of Plant Biologists OPEN ACCESS ARTICLE
Plant Mitochondrial Recombination Surveillance Requires Unusual RecA and MutS Homologs[OA]
a Plant Science Initiative, University of Nebraska, Lincoln, Nebraska 68588-0660 1 To whom correspondence should be addressed. E-mail smackenzie2{at}unl.edu; fax 402-472-3139.
For >20 years, the enigmatic behavior of plant mitochondrial genomes has been well described but not well understood. Chimeric genes appear, and occasionally are differentially replicated or expressed, with significant effects on plant phenotype, most notably on male fertility, yet the mechanisms of DNA replication, chimera formation, and recombination have remained elusive. Using mutations in two important genes of mitochondrial DNA metabolism, we have observed reproducible asymmetric recombination events occurring at specific locations in the mitochondrial genome. Based on these experiments and existing models of double-strand break repair, we propose a model for plant mitochondrial DNA replication, chimeric gene formation, and the illegitimate recombination events that lead to stoichiometric changes. We also address the physiological and developmental effects of aberrant events in mitochondrial genome maintenance, showing that mitochondrial genome rearrangements, when controlled, influence plant reproduction, but when uncontrolled, lead to aberrant growth phenotypes and dramatic reduction of the cell cycle.
The plant mitochondrial genome displays several features that are distinctive to the plant kingdom. These include the incorporation of foreign DNA sequences, a partially linearized genome, split gene sequences requiring RNA trans-splicing for proper expression, large, recombinationally active repeats, a stoichiometrically variable multipartite genome organization, and an unusually high incidence of illegitimate recombination leading to gene chimeras (Adams and Palmer, 2003  ; Knoop, 2004). The linear genome structure and T4 phage-like features (Backert and Borner, 2000) of the genome imply that components of the genome maintenance apparatus may have been acquired over plant evolution (Lang et al., 1999). Furthermore, the linear genome organization would be consistent with a recombination-mediated replication initiation system (Kreuzer, 2005).
More than 20 years of literature exists documenting the recombinogenic nature of the plant mitochondrial genome. This literature includes many examples of aberrant recombination induced by tissue culture conditions (Kanazawa et al., 1994
Several years ago it was demonstrated that commonly observed ghost bands detected by gel blot hybridization of plant mitochondrial DNA represented a population of substoichiometric genomic forms retained generation to generation within the mitochondrial population (Small et al., 1987
To further investigate the evolutionary implications and molecular mechanisms underlying the SSS process in plants, our laboratory identified two nuclear genes that regulate SSS in Arabidopsis thaliana. The first, designated MSH1 (formerly CHM), encodes a homolog of the Eschericha coli MutS mismatch repair component (Abdelnoor et al., 2003
RECA3 Function in Arabidopsis Is Distinct from Other RecA Homologs There exist at least three distinct RecA homologs in the Arabidopsis genome, located on chromosomes 1 (At1g79050), 2 (At2g19490), and 3 (At3g10140). A fourth homolog has also been identified (At3g32920) but appears to represent a pseudogene and is not described here. The three intact loci are designated RECA1, RECA2, and RECA3, respectively. Alignment of their predicted protein sequences to each other and to E. coli RecA revealed several distinct features within RECA3 as detailed in Figure 1 . The three differences indicated are in very strongly conserved motifs (McGrew and Knight, 2003 ). Development of N-terminal gene fusions to green fluorescent protein (GFP) showed that RECA1 is a plastid-targeted protein, RECA2 is dual targeted to mitochondria and plastids, and RECA3 is targeted to mitochondria (Figure 2
). RECA3 has previously been shown to be mitochondrially targeted by a different method and to partially complement the mutagen-sensitive phenotype of the E. coli recA– mutation (Khazi et al., 2003).
Analysis of T-DNA insertion mutations of the three RecA homologs obtained from the Salk Institute and Syngenta indicated that disruption of RECA1 or RECA2 resulted in lethality. However, disruption of the RECA3 locus resulted in viable and phenotypically normal plants displaying reproducible mitochondrial DNA rearrangements.
recA3 Mutations Lead to Mitochondrial Rearrangements Similar, but Not Identical, to Those Occurring in msh1 Mutants
This result is similar to that seen in msh1-1 homozygotes, which also display the nonreciprocal recombination product D and an additional band, corresponding to molecule E, the nonreciprocal recombination product of molecules A and B (Figure 3A). Although this pattern of bands was previously reported (Martinez-Zapater et al., 1992 ; Sakamoto et al., 1996; Abdelnoor et al., 2003), the identity of the fragments was not known. The reciprocal product of molecule E, with a predicted size of 3.61 kb, is not seen. Hybridization with multiple probes from the unique sequences in these regions confirmed the identity of the 1.26-kb band as configuration E and showed that it is not the reciprocal product of molecule D (Figure 3B). These results indicate that the recombination products seen in recA3-1/recA3-1 mutants are a subset of those seen in msh1-1/msh1-1 mutants, and in both mutants, only one of the two possible reciprocal recombinant products accumulates.
Genetic Analysis of RECA3 and MSH1 Action Suggests an Influence on de Novo Mitochondrial Recombination Activity
Gel blot analysis revealed the underlying basis for the two different forms among the RECA3/recA3-1 F1 plants. These plants demonstrate one of two patterns of mitochondrial DNA. While most of the F1 progeny lose molecule D, reversing the mitochondrial atp9 recombination event that had been induced in the mutants, some retain it (Figure 4C). Those plants that retain molecule D also acquire a 1.22-kb molecule designated F (Figure 4C). Although similar in size to the 1.26-kb band seen in msh1-1 mutants, it is not the same fragment. The 1.26-kb band does not hybridize to the 3' end of atp9, while the 1.22-kb band represented as molecule F does not hybridize to the 5' end of atp9. Further analysis of molecule F by PCR and hybridization revealed that it is the reciprocal recombinant of molecule D, as indicated in the figure.
Eight recA3-1/recA3-1 plants are analyzed in Figure 4D. All of these plants have both molecules A and D, assayed by DNA gel blot analysis. However, there are different stoichiometries of these two molecules: plants 2, 5, and 7 show recombinant molecule D in higher stoichiometry than parental molecule A, while plants 1, 3, 4, 6, and 8 contain molecule A in higher copy than molecule D. When these plants were pollinated with the wild type, the results were striking. All the progeny of the plants predominant for molecule D retained molecule D (40 F1 progeny tested from nine different siliques). However, 95% of the progeny from the plants predominant for molecule A lost molecule D (211 out of 223 total progeny from 31 different siliques). The exceptions appeared sporadically, with no more than two seeds in any silique. We suggest that when molecule D is less abundant in a plant than molecule A, reintroduction of the wild-type RECA3 allele causes the loss of molecule D, but when molecule D is the most abundant configuration, it is stable and reciprocal recombination occurs to produce F. The basis for this threshold effect is unknown but could be due to the partitioning of organelles during cell division, known as cytoplasmic sorting, resulting in homoplasmy (Birky, 1983
A similar phenomenon occurs in msh1 mutants. This was first observed by Sakamoto et al. (1996)
RECA3 and MSH1 Have Enhanced Expression in Reproductive Tissues Previous experiments to track the developmental timing of substoichiometric shifting (Johns et al., 1992 ; S.A. Mackenzie, unpublished data) have suggested that nuclear influence on mitochondrial genome configuration may be most pronounced during or immediately preceding flowering. We used quantitative real-time RT-PCR to detect mRNA levels of both RECA3 and MSH1 in roots, mature leaves, young leaves, and unopened flower buds. RNA samples were also prepared from dissected stamens and carpels taken from both unopened flower buds and fully opened flowers. Although both RecA3 and Msh1 transcript levels were nearly undetectable in young roots and mature leaves (data not shown), Figure 5
shows that the genes are expressed in young leaves and flower buds, with levels highest in carpel tissues. In all tissues but ovules, the mRNA levels of MSH1 were lower than RECA3 (Figure 5; data not shown). The data suggest that functional specialization of RECA3 and MSH1 in higher plants may have involved not only adaptations in gene structure but also in gene expression pattern.
RECA3 and MSH1 Function in Distinct Pathways Both recA3 and msh1 mutants undergo mitochondrial genome changes in highly similar but nonidentical patterns, leading us to question whether these two proteins carry out similar functions within the plant mitochondrion. The homologies to bacterial RecA and MutS might suggest that RECA3 is involved in recombination and that MSH1 is involved in mismatch repair. However, we find no evidence for defects in mismatch repair in msh1 mutants, and there is ample precedent for thinking that a MutS homolog does not function in mismatch repair. In yeast, the MutS homolog MSH2 promotes symmetric recombination events in meiosis (Hoffmann et al., 2005 ), and in mammalian cells, the MSH3/MSH5 heterodimer has been found to bind to Holliday junctions during double-strand break repair–mediated recombination (Snowden et al., 2004). Recent results in yeast suggest that MSH1 is not involved in mismatch repair but is involved in stability of the genome and maintenance of homoplasmy (Sia and Kirkpatrick, 2005). The differences observed between msh1 and recA3 mutants in mitochondrial rearrangement patterns and reversibility of phenotype suggest that the genes act in two overlapping but distinct pathways. To test this hypothesis, we generated msh1-1 recA3-1 double mutants. To establish double mutant plants on an unaltered mitochondrial genome, we used recA3-1/recA3-1 mutants as females in crosses to msh1-1/msh1-1 mutants. The resulting double heterozygotes (RECA3 msh1-1/recA3-1 MSH1) had reversed mitochondrial genome configurations resembling the wild type. These plants were selfed, and the homozygous double mutants were identified by genotyping. These plants all had a distinct slow growth, small size, and delayed flowering phenotype. However, to ensure that the mitochondrial genome in these plants had not been altered by passage through a recA3-1 homozygote, these double mutant plants were used to pollinate Columbia-0 (Col-0). This produced plants that appeared completely normal, had inherited wild-type mitochondrial DNA from Col-0, and were heterozygous for both recA2-1 and msh1-1. The F1 progeny were allowed to self, and double mutants were again identified by genotyping. The double mutants obtained in this cross inherited the Col-0 cytoplasm, so the effect of simultaneous inactivation of both RECA3 and MSH1 on the mitochondrial genome could be assessed. All double mutant plants (>50 plants evaluated) were highly pronounced in phenotype, as shown in Figure 6 , with slower growth rate, small size and delayed flowering (Figure 6A), reduced mitotic index (Figure 6B), reduced fertility, and low seed set (Figure 6C). The second generation plants, derived by selfing, were even more pronounced in phenotype. The mitochondrial genome of the double mutants appeared to consist of the Col-0 wild-type pattern superimposed on the msh1-associated pattern, together with the recA3-associated pattern (Figure 7 ). These observations support the hypothesis that these two genes act in distinct but overlapping pathways, and their simultaneous loss results in a higher degree of genome instability.
Plant Mitochondrial SSS Is Controlled by at Least Two Nuclear Genes That Have Undergone Specialization We have presented evidence to suggest that two nuclear genes, RECA3 and MSH1, are uniquely adapted in plants to control mitochondrial genome maintenance. While both genes have maintained sequence features strongly reminiscent of their bacterial counterparts, several modifications have occurred in both genes that appear to be conserved in plants. We have described some of the distinguishing features of the RECA3 protein sequence in this study and recently reported novel features of MSH1, including well-conserved protein domains and an unusual fusion with a GIY-YIG endonuclease (Abdelnoor et al., 2006 ). Other essential recombination controls within the mitochondrial and plastid genomes appear to be performed by at least two additional recA homologs in Arabidopsis.
The SSS Phenomenon and Its Control Appear to Be Timed with the Transition to Reproduction in Plants
The RNA interference–mediated suppression of MSH1 expression in tobacco (Nicotiana tabacum) and tomato (Solanum lycopersicum) results in a condition of CMS (Sandhu et al., 2007 While loss of MSH1 or RECA3 functions individually can result in a fairly mild and sustainable plant phenotype, loss of the two functions simultaneously has profound effects on the plant, particularly with regard to growth rate and reproduction. More detailed analysis of the msh1-1 recA3-1 double mutants is currently underway to understand cell cycle and redox status of these plants, but it is clear that while the influence of SSS may be predominantly at the reproductive stage, the mitochondrial genome instability effected in the double mutant influences all stages of plant growth and development.
The SSS Process Appears to Be Associated with Nuclear Regulation of de Novo, Mitochondrial, Nonhomologous Recombination: A Proposed Model
Our model links mitochondrial DNA replication, the generation of chimeric genes, and the nonreciprocal recombination between short repeated sequences resulting in altered stoichiometry and expression of the chimeras. We propose that double-strand breaks are central to all these processes. When double-strand breaks occur, they can be repaired in a number of ways (Aguilera, 2001
In wild-type Arabidopsis, repeats of up to 560 bp are not recombinationally active, while repeats of 6.5 and 4.2 kb are (Unseld et al., 1997
We further suggest that strand-invasion events at the long repeats are initiation sites for recombination-dependent replication (RDR). RDR requires coordination of the DNA ends to ensure that reciprocal and symmetric events occur, thus replicating the complete genome (Stohr and Kreuzer, 2002 By contrast, when recA3 or msh1 mutations render the recombination surveillance system nonfunctional, homeologous and asymmetric events occur, shifting the stoichiometry of various segments of the genome. We propose that the events reproducibly observed in the mutants resemble low frequency, sporadic events that occur in wild populations to effect substoichiometric shifting and CMS. Consistent with this hypothesis, we can detect both recombination products in mutant plants and even in wild-type plants by PCR (data not shown), but these molecules are rare, as indicated by their apparent absence on blots. This model applies whether the genomic molecules are circular or linear. Strand invasion events that lead to RDR could result in theta replication, rolling circle replication, or more complex T4-like events, depending on the molecules involved and their topologies. Still not understood are the detailed mechanisms that result in differential replication or instability of some of the recombination products, evident as asymmetric recombination within the recA3 and msh1 mutants during de novo generation of these novel recombinant molecules. A remaining question is why there are so few distinct recombination events in the mutants. We suggest that double-strand breakage hot spots likely exist in a few locations, which lead to gene conversion in the wild type and recombination in the mutants. Other aberrant events may occur sporadically at additional locations in the mutants, but if they are infrequent they would be lost by cytoplasmic sorting. Thus, only the most frequent aberrant events will be seen, unless large populations or many generations are examined. Alternatively, localized cruciforms in the DNA, localized melting due to high transcriptional activity, or stalling replication forks could account for the sites of DNA exchange, although any of these alternative events would likewise need to occur at high frequency at specific locations.
A model for the double-strand break–mediated events is diagrammed in Figure 8
. Following strand invasion at a short repeat to establish a D loop, DNA synthesis will convert any mutations, thus maintaining the sequence identity of the short repeats. Branch migration will allow heterology to be detected, resulting in unwinding of the invading strand and resulting in synthesis-dependent strand annealing to complete gene conversion of the short repeat. On the other hand, if heterology is not detected, establishment of a replication fork will result in production of one of two possible reciprocal recombination products. Normally rare, this becomes frequent in the mutants. Why the same nonreciprocal recombinant is always produced is unknown. It may be due to asymmetry in the processing of the breakage site leading to the initial strand invasion event, asymmetry in resolution of the intermediates, or differential replication of the products. Some of these have been described in other systems (Villemure et al., 1997
There are several possible fates for the broken end that has not invaded. It could be degraded, undergo NHEJ, or invade another DNA molecule (Stohr and Kreuzer, 2002 ; Shcherbakov et al., 2006). If it invades the asymmetric recombination product and initiates replication, regeneration of the parental molecule would occur. If it invades the recombinant molecule, the reciprocal recombinant would be produced. In the mutants, this evidently occurs at a low frequency, to account for the occasional appearance of the reciprocal recombination product in RECA3/recA3-1 backcross heterozygotes. One possible explanation is that the two broken ends are normally coordinated, leading to gene conversion at short repeats and establishment of two replication forks at long repeats to initiate RDR. If RECA3 and MSH1 are involved in selecting which pathway the intermediate follows, then disruption at either locus could lead to establishment of only one replication fork due to poor detection of heterologies, poor coordination of the ends, or both, resulting in the asymmetric recombination products seen in the mutants. Our model predicts a hotspot for breakage events at atp9. It is interesting that the two defective copies of atp9 in the mitochondrial genome represent the 5' and 3' ends of the gene, with no overlap between the sequences (Figure 3A, molecules B and C). These are likely the result of breakage events near the middle of the gene, followed by NHEJ to produce the defective copies now fixed in the population. Recombination between other short repeats in the genome (including some very near the atp9 gene) has not been observed in msh1 or recA3 mutants, again suggesting a hot spot for initiation of strand invasion events in the atp9 gene.
The Acquisition of Aberrant Repeats in the Genome and the SSS Process They Mediate Likely Comprise Major Components of Plant Mitochondrial Genome Evolution
Using the atp9 and rpl16 repeats as indicators of mitochondrial genome evolution in Arabidopsis, one can hypothesize that double-strand breakage events leading to novel repeated sequences within the genome represents a key step in major mitochondrial genome transitions. Ecotype C24 represents a mitochondrial form prior to the introduction of such a repeat configuration (Figure 9
), and Col-0 represents a mitochondrial type following synthesis and fixation of the novel atp9 chimera near cox3 (Forner et al., 2005
It should be feasible to test for evidence of such mitochondrial genome transitions within other plant species. While in the case of Arabidopsis, these genomic shifts do not appear to confer any obvious phenotypic changes to the plant, one presumes that in natural populations, where CMS may be induced or suppressed in the process, such genomic shifts could provide important adaptive advantages (Mackenzie, 2005 ). It is likely no coincidence that RNA interference suppression of MSH1 in two other plant species gives rise to a CMS phenotype together with mitochondrial rearrangement (Sandhu et al., 2007).
The plant growth phenotype of recA3-1 msh1-1 double mutants suggests that these two genes control different aspects of homology surveillance. The ectopic recombination events seen in the single mutants are distinct, and the double mutants seem to suffer both sets of ectopic recombination. This suggests that while mitochondrial genes may exist in a few different linkage relationships on different molecules in the single mutants, they apparently exist in a large number of linkage relationships, topologies, and stoichiometries in the double mutants. This genomic complexity could interfere with replication efficiency, perhaps accounting for the observed reduction in mitotic index and plant growth rate (Mandal et al., 2005
Arabidopsis thaliana Growth Seeds were plated on 0.5x Murashige and Skoog media and cold treated at 4°C for 5 d to synchronize germination. The seed plates were then transferred to a growth chamber with 16 h of daylight at 22°C. Three-week-old seedlings were transplanted to soil (Metro Mix 360) and kept in 8 h of daylight at 24°C until they started bolting, after which the plants were moved to 16 h of daylight at 24°C. Alternatively, cold-treated seeds were sown directly on soil (Metro Mix 360) and kept in growth chambers at 8 h of daylight at 24°C for 5 to 6 weeks and then transferred to a growth chamber with 16 h of daylight at 24°C. Antibiotic selection was performed by adding kanamycin at 50 µg/mL or glufosinate at 5 µg/mL to the germination plates.
Mutants T-DNA insertions for all three recA homologs were also obtained from the Salk Institute: recA1-1 (Salk_013488), recA1-2 (Salk_072979), and recA1-3 (Salk_020949). For RECA2, the alleles obtained were recA2-1 (Salk_076237), recA2-2 (Salk_068655), and recA2-3 (Salk_118134). Two alleles of RECA3 were obtained: recA3-1 (Sail_252_C06) and recA3-2 (Salk_146388).
Molecular Biology Procedures
Total genomic DNA samples were digested with the restriction enzyme BamHI according to the manufacturer's instructions. Agarose gel electrophoresis, DNA transfer to Hybond N+ nylon membrane (0.45 µm; Amersham), extraction of DNA fragments, labeling of DNA, and filter hybridizations were conducted according to procedures described previously (Janska and Mackenzie, 1993
Genotypes of msh1-1 plants were verified by the SNAP method as described (Drenkard et al., 2000
RT-PCR Primers RealRecA3F2 (5'-ATCTAACATGCATTTCCCGCACGC-3') and RealRecA3R2 (5'-TGGACGCAGACATTGAGACCACTT-3'); RealMsh1F1 (5'-TCATGCGTGTATGTG ATGCGGAGA-3') and RealMsh1R1 (5'-ACTTGACCCTTGCAGTCCTTCCTT-3'); and RealUbqF1 (5'-CACCATTGACAACGTCAAGGCCAA-3') and RealUbqR1 (5'-CACGCAGACGCAAGACCAAATGAA-3') were used for real-time analysis of RECA3, MSH1, and ubiquitin, respectively.
GFP Constructs
Transient Transformation and GFP Expression Assay
Histology
Bioinformatics
Accession Numbers
We thank the ABRC, the Salk Institute, Syngenta, and the Nottingham Arabidopsis Stock Centre for providing mutant seeds. We also thank Guichuan Hou and the Center for Biotechnology Microscopy Core Facility for histology and confocal microscopy services. Tom Clemente generously provided raillery. This work was supported in part by National Science Foundation Grant IOB-0417172 to S.A.M. and A.C.C. and National Science Foundation Grant MCB-0323377 to S.A.M.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Sally A. Mackenzie (smackenzie2{at}unl.edu).
[OA] Open Access articles can be viewed online without a subscription. www.plantcell.org/cgi/doi/10.1105/tpc.106.048355 Received October 18, 2006; Revision received March 4, 2007. accepted April 10, 2007.
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ABSTRACT
INTRODUCTION
rpl16 from molecule D (indicated as Probe 1). Dashed arrows indicate the BamHI fragments corresponding to the bands on the DNA gel blot. Molecules A and B are derived from the published sequence of the Arabidopsis ecotype C24 sequence (accession number 
80% of which display the wild-type pattern (
