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Plant Physiol. Apr 2010; 152(4): 1960–1970.
Published online Feb 5, 2010. doi:  10.1104/pp.109.152827
PMCID: PMC2850037

Extensive Rearrangement of the Arabidopsis Mitochondrial Genome Elicits Cellular Conditions for Thermotolerance1,[W][OA]

Abstract

Three nuclear genes involved in plant mitochondrial recombination surveillance have been previously identified. Simultaneous disruption of two of these genes, MutS Homolog1 (MSH1) and RECA3, results in extensive rearrangement of the mitochondrial genome and dramatic changes in plant growth. We have capitalized on these changes in mitochondrial genome organization to understand the role mitochondria play in plant cellular and developmental processes. Transcript profiling of the double mutants grown under normal conditions revealed differential regulation of numerous nuclear genes involved in stress responses together with increased levels of polyadenylated mitochondrial transcripts. We show that extensive rearrangement of the mitochondrial genome in Arabidopsis (Arabidopsis thaliana) directly elicits physiological stress responses in plants, with msh1 recA3 double mutants exhibiting enhanced thermotolerance. Likewise, we show that mitochondrial transcriptional changes are associated with genome recombination, so that differential gene modulation is accomplished, at least in part, through altered gene copy number.

Plant mitochondrial genomes are characterized by unusually high levels of recombination that produce a multipartite genome structure, novel sequence chimeras (Schnable and Wise, 1998), foreign DNA insertions (Xiong et al., 2008), and altered relative copy numbers of portions of the genome (Kmiec et al., 2006). Mitochondrial genome recombination involves both large-sized (greater than 1 kb) repeats that mediate high-frequency reciprocal DNA exchange to produce subgenomic DNA molecules (Mackenzie and McIntosh, 1999) and intermediate-sized repeats that participate in low-frequency DNA exchange. This latter recombination process produces asymmetric DNA exchange and only one of the predicted recombination products (Shedge et al., 2007). Intermediate-sized repeats also mediate rapid stoichiometric changes in the genome (Arrieta-Montiel et al., 2009), referred to as substoichiometric shifting (Small et al., 1987).

Three nuclear genes have been shown to influence recombination within the plant mitochondrial genome: MutS Homolog1 (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 effects on the genome and plant phenotype (Sandhu et al., 2007). Over 33 sites within the genome simultaneously become recombinationally active with MSH1 disruption (Arrieta-Montiel et al., 2009), with several plant developmental processes altered. Likewise, RNA interference-mediated suppression of MSH1 expression in five other plant species results in mitochondrial genome rearrangements and similarly aberrant plant phenotypes (Sandhu et al., 2007; X. Feng and S. Mackenzie, unpublished data).

In this study, we combined msh1 and recA3 mutations in Arabidopsis (Arabidopsis thaliana) to determine how plants respond to even more extensive destabilization of the mitochondrial genome. We report evidence of a programmed stress response conditioned by changes in nuclear gene expression, specific modulation of mitochondrial transcription, and an enhanced heat tolerance phenotype.

RESULTS

The msh1 recA3 Double Mutant Has a Highly Destabilized Mitochondrial Genome

The double mutant shows extensive mitochondrial genome rearrangement (Arrieta-Montiel et al., 2009). Patterns of recombination activity at intermediate repeats throughout the genome differed between msh1 and recA3 single mutants and msh1 recA3 double mutants. While asymmetric DNA exchange occurs at all repeats ranging in size from 108 to 556 bp (33 repeats) in the msh1 mutant (Arrieta-Montiel et al., 2009), this activity was observed at only four repeats in the recA3 mutants (Fig. 1). In the msh1 recA3 double mutant, recombination at most repeats involved reciprocal exchange and a more extensive rearrangement pattern than in the msh1 single mutant. The more extensive hybridization pattern also provided an indication of enhanced gene copy numbers in some regions of the double mutant genome. Results are shown in Figure 1 for three repeats. The double mutants show reduced growth rate, delayed flowering, reduced fertility, and low seed set (Shedge et al., 2007). The intensified phenotype of the double mutant relative to single mutants implies that MSH1 and RECA3 are important components of distinct mitochondrial genome maintenance processes (Shedge et al., 2007).

Figure 1.
Mitochondrial genome rearrangements in msh1, recA3, and msh1 recA3. DNA gel-blot analysis of total genomic DNA (BamHI) shows DNA recombination activity. Three repeats, F, D, and Q, are recombinationally active in the mutants, resulting in amplification ...

The Double Mutant Was Altered in Its Transcript Profile

Underlying phenotypic differences in the msh1 recA3 double mutant are numerous changes in gene expression, evident by transcript profiling of msh1, recA3, and msh1 recA3 (Supplemental Table S3). Transcript profiles were generated from flowering, aboveground tissues of plants grown at 16-h daylength and 24°C. Comparative profile analysis of the single and double mutants showed only mild gene expression changes in recA3 in response to mitochondrial genome rearrangement, while msh1 and the double mutant showed profound changes in gene expression (Fig. 2A). These transcript profiles shared only about 10% transcript changes in common, indicating distinct cellular conditions associated with the two mitochondrial states.

Figure 2.
Gene expression is altered by mitochondrial genomic changes. A, Venn diagram representation of genes altered in their expression, relative to Col-0, and shared between the msh1 recA3 double mutant, msh1 single mutant, and recA3 single mutant. Data are ...

Predominant among transcript changes shared by msh1 and the double mutant are genes involved in organellar (mitochondria and plastid) processes and responses to stimuli, including hormonal metabolism and signaling. Ontology surveys of genes altered predominantly in the msh1 recA3 double mutant indicated a broad range of gene classes, several involved in organellar functions, transcription regulation, unfolded protein-binding activity, and stress responses (Fig. 2B). The relationship of mitochondrial functions to cell division and stress response processes is not well defined, but the striking reproducibility of mitochondrial genome changes, phenotypes, and transcript changes in the double mutants suggests conserved pathway connections.

The msh1 recA3 Double Mutant Displays Pronounced Thermotolerance

Transcript profiling of the double mutant indicated enhanced expression of a large number of genes previously identified in stress responses. Consequently, wild-type, single mutant, and double mutant plants were subjected to heat stress under controlled growth conditions. In three different experiments, nine, 10, and 12 double mutant plants were grown together with wild-type and single mutant plants at 24°C for 8 weeks and subjected to heat stress of 37°C for approximately 24 h. Following heat treatment, the plants were returned to normal growing conditions at 24°C. While 100% of the wild-type and single mutant plants died, 71% (22 of 31) of the double mutant plants resumed normal growth and reproduction (Fig. 3A; Supplemental Fig. S1).

Figure 3.
Evidence of heat tolerance in the msh1 recA3 double mutant. A, Plants were subjected to 37°C for approximately 24 h and then returned to normal growing conditions. The photograph was taken 14 d following return to 24°C. B, Eight-week-old ...

A second set of heat stress experiments was also conducted. Wild-type ecotype Columbia (Col-0), msh1, recA3, and msh1 recA3 plants (eight to 10 each) were subjected to gradual temperature elevation, increasing temperature 1°C per day from 24°C, under controlled growth conditions. The double mutant displayed enhanced thermotolerance, reaching sustained ambient temperatures of 32°C before showing any obvious phenotypic effect, while single mutants were comparable to the wild type in susceptibility to heat stress (Fig. 3, B and C). Double mutants were able to flower and set seed at 32°C before succumbing to temperature stress after nearly 3 weeks of treatment (Fig. 3B).

Under normal growing conditions, msh1 recA3 double mutants exhibit a range of phenotypic variation, likely corresponding to the extent of mitochondrial genome rearrangement in individual plants. Generally, DNA sampling of double mutants was from individual plants, not pooled samples, but it was not feasible to prepare DNA samples from unusually small or weak plants, and sequence deletions may go undetected. While some double mutants show a moderately altered plant phenotype, a few display more severely stunted growth and reproductive dysfunction and die before completing their normal life cycle. This variation likely accounts for some of the plant loss observed in the double mutant heat treatment experiment. Cellular conditions accounting for the observed heat acclimation in double mutants are assumed to derive from the mitochondrial genome rearrangements and consequent gene expression changes.

It is important to point out that the extensive mitochondrial rearrangements observed in the msh1 recA3 double mutant are present in plants with or without heat stress. However, these mitochondrial rearrangements are not present in Col-0 plants that have been subjected to heat stress. We have carried out similar mitochondrial genome analysis of heat-treated Col-0 plants and observed no evidence of enhanced mitochondrial genomic rearrangement.

Cellular Stress Response Is Primed in the msh1 recA3 Double Mutant under Normal Conditions

Cellular conditions associated with mitochondrial genome alteration in the msh1 recA3 double mutant overlap with those of wild-type plants that have been subjected to heat stress. A second transcript profiling experiment was conducted with 8-week-old plants grown under 8-h daylength to compare untreated wild-type and double mutant plants versus heat-treated (37°C for 2 h) wild-type and double mutant plants (Supplemental Table S4). Microarray analysis using false discovery rate (FDR) values of less than 0.1 identified approximately 1,100 genes responsive to heat in the wild-type plants that were likewise differentially regulated in untreated double mutant plants (Fig. 4A; Table I). While gene expression changes for over 85% (952 genes) of these 1,100 genes correlated between untreated double mutant and heat-treated wild-type plants, expression of the remaining 15% (153 genes) was anticorrelated. Of the 952 genes, over 11% were up-regulated more than 2-fold and over 2% were down-regulated more than 2-fold in the double mutant. Individual gene analysis within the latter noncorrespondence category showed that while a majority of the genes in this group did not appear to be associated with known stress response pathways, a few genes with putative stress-responsive functions in this group were significantly up-regulated in the untreated double mutant but down-regulated in the heat-treated wild type (Supplemental Table S1).

Figure 4.
Stress response appears to be primed in the msh1 recA3 double mutant. A, Venn diagram representation of the genes altered in their expression, relative to the wild type (WT) under normal conditions, and shared between the wild type subjected to heat stress ...
Table I.
Sample list of genes (with fold change values relative to untreated wild type) involved in the primed heat stress response in the msh1 recA3 double mutant (Mut) at 0- and 2-h heat stress versus Col-0 (Wt) at 2-h heat stress (FDR < 0.1)

Transcriptional response elicited by heat stress in the msh1 recA3 double mutant was higher than that in wild-type plants. The 952 genes responding in common between heat-treated wild-type and untreated double mutant plants showed greater response in the double mutants when subjected to heat stress (Fig. 4B). This analysis also indicated an additional 6,598 genes that were differentially regulated in wild-type plants when subjected to heat stress. Approximately 90% of these genes were similarly responsive in the double mutant under heat stress. A group of 697 genes were differentially regulated in only the untreated double mutant. Of these, 56 genes were up-regulated and nine genes were down-regulated more than 2-fold, with several having stress-responsive functions (Table III).

Table III.
Sample list of mitochondria-encoded genes and ORFs that are up-regulated in the msh1 recA3 double mutants under normal conditions (FDR < 0.1)

Heat Stress-Associated Polyadenylation of Mitochondrial Transcripts Increases in the msh1 recA3 Double Mutant under Normal Conditions

Plant mitochondrial gene expression does not appear to be regulated primarily at the level of transcription initiation (Holec et al., 2006). However, one important means of transcript regulation involves RNA turnover, with polyadenylation participating in the degradation of mitochondrial transcripts (Holec et al., 2006). Microarray-based transcript profiling to identify heat stress response in wild-type plants has shown increases in the levels of several mitochondrially encoded transcripts (Adamo et al., 2008). Polyadenylated transcripts are preferentially selected in library preparation for Affymetrix microarray experiments, so we assumed that the appearance of up-regulation in mitochondrial transcripts in our experiments was due to their enhanced polyadenylation. Polyadenylated mitochondrial transcripts induced by heat have been shown to be truncated and inactive (Adamo et al., 2008). Plant mitochondrial genomes are also characterized by a number of unidentified open reading frames (ORFs) that are thought to be nonexpressing (Marienfeld et al., 1997). In our studies, heat-induced polyadenylation was also increased for some of these ORF-derived transcripts (Fig. 5; Table II). Similar transcript changes were observed in the msh1 recA3 double mutant grown under normal conditions (Table III), and these effects were enhanced under heat stress conditions. Therefore, we were interested in learning whether mitochondrial gene expression is influenced in the double mutant.

Figure 5.
Expression levels of a subset of mitochondrial transcripts in msh1 recA3 double mutant (dm) versus wild-type (wt) plants. The graphs were generated from quantitative RT-PCR analyses showing an increase in the expression of total mitochondrial transcripts ...
Table II.
Sample list of genes (fold change values compared with untreated wild type) with putative stress-responsive functions up-regulated exclusively in the untreated msh1 recA3 double mutant

Steady-State Mitochondrial Transcripts Are Increased in the msh1 recA3 Double Mutant

While microarray analysis provided evidence for increased levels of polyadenylated mitochondrial transcripts, these experiments did not address the status of full-length mitochondrial transcripts in the double mutant with and without heat treatment. To examine this, full-length and polyadenylated mitochondrial transcripts from wild-type and double mutant plants were surveyed by quantitative reverse transcription (RT)-PCR analysis under normal and heat stress conditions. Separate cDNA templates were prepared from treated and untreated wild-type and double mutant plants using oligo(dT) and random primers. Transcripts amplified using random primers were shown to represent full-length transcripts in an earlier expression analysis (Arrieta-Montiel et al., 2009). Experiments focused on a collection of 25 mitochondrial transcripts that included ORFs, mitochondrial respiratory chain complex components, and ribosomal genes. Results for all 25 genes showed that the amount of total transcript (polyadenylated + full length) in the msh1 recA3 double mutant was higher than in wild-type plants under both treated and untreated conditions (Figs. 1 and and5).5). For most genes tested, this tendency could be attributed to an increases in full-length transcripts under both normal and heat-stressed conditions, with only four genes showing increased transcript levels due to polyadenylation under heat stress. Quantitative PCR analysis to measure DNA copy number of several of these mitochondrial genes in the msh1 recA3 double mutant showed correspondence between increases in gene copy number and increased transcript levels (Table IV; Fig. 1). In some cases, it was only possible to conduct these experiments with pooled plants, because of the small size of the double mutant plant. Therefore, we conducted experiments for four of the genes, Cob, Atp1, Ccb254, and Atp8, by measuring copy number in pooled and individual plants, and we observed identical trends in both cases. These observations suggest that substoichiometric shifting activity of the msh1 recA3 mitochondrial genome produces alterations in genotype that may directly influence mitochondrial gene expression patterns via steady-state transcript levels.

Table IV.
List of mitochondria-encoded genes and ORFs with fold changes in copy number and transcript level, comparing msh1 recA3 double mutant with Col-0 under normal conditions

DISCUSSION

The msh1 recA3 Double Mutant Mitochondrial Genome Represents Widespread Genomic Rearrangement

The msh1 recA3 double mutant displays extensive levels of mitochondrial genome rearrangement. Mitochondrial DNA exchange occurs at over 33 identified repeat regions, with what appears to be more extensive rearrangement than is observed in the msh1 single mutant (Arrieta-Montiel et al., 2009). While changes in mitochondrial genome configuration that occur with MSH1 disruption produce several distinct plant phenotypes, including cytoplasmic male sterility and leaf variegation (Sandhu et al., 2007), that may arise naturally under conditions for MSH1 suppression, it seems unlikely that the severe growth phenotype observed in the double mutant would occur under natural conditions. However, the cellular conditions created in the double mutant provide an opportunity to identify previously unknown stress response loci that participate in thermotolerance.

The msh1 recA3 Double Mutant Appears To Be Primed for Stress Response

Transcript profiling experiments showed dramatic gene expression changes in the double mutant. Alterations in organellar and stress response functions were surprisingly distinct from the changes elicited by disruption of MSH1. Comparison of the double mutant and wild-type plants under normal and heat stress conditions showed that a significant stress response was already primed (Prime-A-Plant Group, 2006) within the double mutant under nonstress conditions.

Predominant within this primed response were heat shock proteins. These included up-regulation of genes encoding mitochondrially localized HSP23.5, HSP23.6, HSP70, and HSP90; cytosolic HSP70 and BP1; and chloroplastic HSP70 and HSP90 (Table I; for review, see Timperio et al., 2008). In addition, several J class heat shock proteins that play important roles as cellular stress sensors (Rajan and D'Silva, 2009) were up-regulated in the double mutant. Reactive oxygen species (ROS)-responsive genes influenced in the double mutant included mitochondria-localized AOX1a and NDB2, suggested to have a broad role in cellular stress response (Giraud et al., 2008), and ROS-scavenging GADPH and catalases. Stress-responsive transcription factors such as NF-X1, involved in heat acclimation (Larkindale and Vierling, 2008), WRKY, involved in pathogen defense signaling (for review, see Eulgem and Somssich, 2007), and DREB2B, responsive to desiccation and high-salinity stress (Nakashima et al., 2000), were up-regulated. Temperature-induced lipocalin, involved in scavenging harmful lipophilic molecules and thought to participate in plant responses to heat and cold stress (Chi et al., 2009), was prominent in the double mutant under normal growth conditions. Two other genes involved in combined stress responses, a mitochondrial calcium ion-binding protein and a WD-40 repeat family protein, also appeared to be a part of this priming state (Rizhsky et al., 2004).

The priming response observed in the msh1 recA3 double mutant represents an overlap of several known stress response pathways, implying that mitochondria and/or ROS signaling derived from mitochondrial processes participate in these pathways. Rearrangements of the mitochondrial genome in the cucumber (Cucumis sativus) MSC16 mutant appear to result in priming to cold stress by what may be a similar process (Szal et al., 2009). It is not yet clear how mitochondrial genome rearrangement conditions a cellular state that elicits effective phenotypic stress responses. Intracellular signaling via ROS may be one mechanism, but it is also possible that mitochondrial genome rearrangement influences mitochondrial transcription patterns for alternative routes of retrograde signaling. One possibility under investigation is that rearrangements in the double mutant influence the function of mitochondrial complex I. Tobacco (Nicotiana tabacum) CMSII mutants lacking nad7 and complex I activity are enhanced for ozone and biotic stress tolerance (Dutilleul et al., 2003). Likewise, in Arabidopsis lines disrupted in NDUFS4, another component of complex I assembly, plants show enhanced tolerance to salt and osmotic stress (Meyer et al., 2009). The heightened stress response maintained constitutively within the double mutant likely accounts for the aberrant growth phenotypes observed in these plants (Liu et al., 1998).

Steady-State Transcript Levels Increase in msh1 recA3 Mitochondria

We observed evidence of differentially altered steady-state RNA levels within mitochondria of the double mutant. Apparent increases in mitochondrial transcript levels with heat stress in microarray experiments were previously reported to be the consequence of enhanced polyadenylation and turnover of truncated transcripts (Adamo et al., 2008). While polyadenylation increased for some mitochondrial genes in response to heat in our study, most changes involved significant increases in full-length transcripts for several genes/ORFs in the double mutant. We assume that the observed differences in our study relative to Adamo et al. (2008) are due to our survey of a more extensive collection of genes.

Our analysis showed that some changes in steady-state transcript levels correlated with altered DNA copy numbers within the genome, providing evidence of a mechanism by which transcription may be differentially modulated in plant mitochondria. However, in an earlier study in common bean (Phaseolus vulgaris) mitochondria, it was reported that no correlation existed between the number of gene loci and transcript levels (Woloszynska et al., 2006). It is possible that a newly rearranged genome, as we present in the double mutant, has not yet modulated transcription in association with the genomic alterations, or that the gene copy number changes we are observing are greater than were observed previously. Gene-specific modulation of transcription within mitochondria via an organellar (plastid and mitochondrion)-targeted RPOTmp gene has been reported (Kühn et al., 2009). In our microarray analysis, the expression of RPOTmp does not appear to change, but mitochondrially targeted RPOTm is up-regulated more than 2-fold in the double mutant. More extensive analysis of how changes in mitochondrial gene expression influence plant stress response is warranted.

MATERIALS AND METHODS

Arabidopsis Growth and Heat Treatment

Cold-treated Arabidopsis (Arabidopsis thaliana) seeds were sown directly on soil (Metro Mix 360) and kept in growth chambers with 8-h daylength at 24°C for 8 weeks and then transferred to a growth chamber with 16-h daylength at 24°C. For heat treatment experiments, 8-week-old plants were first transferred to a chamber (Percival Scientific) where they were subjected to heat stress at 37°C for approximately 24 h. Following heat treatment, plants were transferred to the greenhouse with 16-h daylength at 24°C.

Mutants

To obtain msh1 recA3 double mutants, crosses were made using recA3-1 (Sail_252_C06) homozygous mutant as the female parent and msh1-1 homozygous mutant as the pollen donor. Heterozygous MSH1-1 msh1-1/recA3-1 recA3-1 plants were first identified by PCR-based genotyping of the segregating F2 population. This genotyping step allowed for higher frequency identification of msh1-1 msh1-1/recA3-1 recA3-1 double mutants than are obtained from double heterozygous F1 plants. The primers used to genotype each locus have been described previously (Shedge et al., 2007).

Molecular Biology Procedures

For microarray experiments, total RNA was extracted from aboveground parts of 8-week-old Col-0 plants and msh1 recA3 double mutant plants (Col-0 background) using the TRIzol (Invitrogen) extraction procedure followed by purification on RNeasy columns (Qiagen). RNAs from two Col-0 and four msh1 recA3 double mutant plants under untreated conditions were each hybridized to individual chips. Similarly, RNAs from three Col-0 and three double mutant plants subjected to heat treatment of 37°C for 2 h were each hybridized to individual chips. Samples were assayed on the Affymetrix GeneChip oligonucleotide ATH1 array according to the manufacturer's instructions.

Bioinformatics

Microarray data have been deposited at ArrayExpress (E-MEXP-1409, E-MEXP-1410, E-MEXP-1411) and GEO (GSE19603). Expression data from Affymetrix GeneChips were normalized using the Robust Multichip Average method (Bolstad et al., 2003) using Bioconductor's (Gentleman et al., 2004) affy package (Gautier et al., 2004). A linear model analysis was conducted using the Limma package (Smyth, 2004), and the P values from the tests of interest were converted to q values to obtain approximate control of the FDR at a specified value (Benjamini et al., 2001). The cutoff q value used for generating the lists of interest in Tables II, III, and andIVIV and Supplemental Table S1 was 10%. For the generation of data in Table I, a cutoff of 10% was used in the P value along with an absolute fold change of greater than 2. The Gene Ontology classification was used and Gene Ontology enrichment analysis of differentially expressed genes was done using GOHyperGAll (Horan et al., 2008).

Quantitative PCR

Total RNA was extracted as described above. Equal amounts of RNA from individual plants were reverse transcribed to two different cDNA preparations, one using oligo(dT) primers and the second using random primers. The cDNAs were used for quantitative PCR with the SYBR GreenER Supermix for the iCycler (Invitrogen). The quantitative PCR data collection and analysis were done using iCycler iQ software (version 3.1) from Bio-Rad. Each sample was run in triplicate and the results were averaged; the entire experiment was repeated. Primers used for the quantitative RT-PCR analysis are provided in Supplemental Table S2. Primers RealAct2F1 (5′-TGTTGCCATTCAGGCCGTTCTTTC-3′) and RealAct2R2 (5′-ACAGTGTGAGACACACCATCACCA-3′) were used for the Actin2 gene that was used as an internal control.

Supplemental Data

The following materials are available in the online version of this article.

  • Supplemental Figure S1. Phenotypes of msh1 and recA3 mutants after heat stress of 37°C for approximately 24 h.
  • Supplemental Table S1. Putative stress-responsive genes in the double mutant that do not correspond with induced heat tolerance.
  • Supplemental Table S2. Primers used to amplify mitochondrial transcript in quantitative RT-PCR analysis.
  • Supplemental Table S3. List of genes with information regarding expression, relative to Col-0, in msh1, recA3, and msh1 recA3.
  • Supplemental Table S4. List of genes with information regarding expression, relative to Col-0 under normal conditions, in msh1 recA3 under normal conditions, Col-0 under heat stress, and msh1 recA3 under heat stress.

Supplementary Material

[Supplemental Data]

Acknowledgments

We thank Sara Vestecka and Chris Hawkins for technical assistance. We also thank Dr. Yuannan Xia and the University of Nebraska, Lincoln, Center for Biotechnology Microarray Core Facility for assistance with microarray experiments.

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