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

Abstract

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 lineagespecific pattern of mitochondrial genetic variation in higher plants.

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

“…Multiple rearrangements among the promoter-contain-ing sequence (from the orf284 region) and other mitochondrial genomic source sequences (including the key sequence cs1 from S284b), involving HR, MMEJ, and cNHEJ, occurred at the specific site downstream of rpl5, generating the transcription-competent pre-structure. Homologous recombination between certain sites in the plant mitochondrial genomes may be reversible and reproducible under the control of some nuclear genes (MSH1 and homologs of RecA and MutS) [33,34], however, the MMEJ-and cNHEJ-based recombination events at the specific sites could be rare, suggesting that these recombinant structures were likely unique evolutionary products. (2) Formation of the CMS-like protogenes (orf367 and orf356) that are expressed but functionally self-inhibitory; (3) Generation of intermediate, functional CMS genes (WA352a/b, WA314) by gradual variations in the protogene sequence and the structures, and acquisition of the biochemical function through emancipating their COX11-interaction potential, coupled with SSS and natural (purifying) selection; (4) Formation of WA352c via further subtle sequence variation, e.g., insertion of the atp6-containing sequence into the downstream of WA352c, of which a part sequence serves as a new signal for transcription termination [10].…”

Extensive Rearrangement of the Arabidopsis Mitochondrial Genome Elicits Cellular Conditions for Thermotolerance

“…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.…”

“…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).…”

“…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.…”

The Chloroplast Triggers Developmental Reprogramming When MUTS HOMOLOG1 Is Suppressed in Plants

“…Disruption of MSH1 enhances recombination at 47 pairs of repeated sequences in the mitochondrial genome of Arabidopsis (Arabidopsis thaliana; Shedge et al, 2007;Arrieta-Montiel et al, 2009;Davila et al, 2011) and gives rise to cytoplasmic male sterility in tomato (Solanum lycopersicum ) and tobacco (Nicotiana tabacum; Sandhu et al, 2007). Within the chloroplast, disruption of MSH1 results in low-frequency DNA rearrangements mediated by recombination, together with altered redox properties of the cell and variegation of the plant .…”