Abstract
Exceptions to the generally accepted rules that plant mitochondrial genomes are strictly maternally inherited and that within-individual sequence diversity in those genomes, i.e., heteroplasmy, should be minimal are becoming increasingly apparent especially with regard to sequence-level heteroplasmy. These findings raise questions about the potential significance of such heteroplasmy for plant mitochondrial genome evolution. Still studies quantifying the amount and consequences of sequence heteroplasmy in natural populations are rare. In this study, we report pervasive sequence heteroplasmy in natural populations of wild carrot, a close relative of the cultivated crop. In order to assay directly for this heteroplasmy, we implemented a quantitative PCR assay that can detect and quantify intra-individual SNP variation in two mitochondrial genes (Cox1 and Atp9). We found heteroplasmy in > 60% of all wild carrot populations surveyed and in > 30% of the 140 component individuals that were genotyped. Heteroplasmy ranged from a very small proportion of the total genotype (e.g., 0.995:0.005) to near even mixtures (e.g., 0.590:0.410) in some individuals. These results have important implications for the role of intra-genomic recombination in the generation of plant mitochondrial genome genotypic novelty. The consequences of such recombination are evident in the results of this study through analysis of the degree of linkage disequilibrium (LD) between the SNP sites at the two genes studied.
Highlights
Mitochondrial heteroplasmy is the co-occurrence of two or more divergent mitochondrial genotypes within an individual, and for the purpose of this study, we consider heteroplasmy at the level of DNA sequence variation, often single nucleotide polymorphisms (SNPs), for one or more mitochondrial genes recognizing that the broader definition can include structural variation and substoichiometric molecules thoroughly discussed in a nice review by Woloszynska [1]
Szklarczyk et al [15] have demonstrated the presence of Atp9 heteroplasmy in two cultivated petaloid, cytoplasmic male sterility (CMS) carrot lines and their respective fertile maintainer lines. These results suggest the possibility that natural populations of D. c. ssp. carota could harbor levels of mitochondrial genome heteroplasmy sufficient to influence the evolution of that genome and its utility as a genetic resource for carrot breeders
The current results suggest that at least low-level heteroplasmy of the mitochondrial genome, defined as such, is quite common among individuals found over much of the distribution of wild carrot in the eastern U.S, if not more widely
Summary
Mitochondrial heteroplasmy is the co-occurrence of two or more divergent mitochondrial genotypes within an individual, and for the purpose of this study, we consider heteroplasmy at the level of DNA sequence variation, often single nucleotide polymorphisms (SNPs), for one or more mitochondrial genes recognizing that the broader definition can include structural variation and substoichiometric molecules thoroughly discussed in a nice review by Woloszynska [1]. Mitochondrial Heteroplasmy in Wild Carrot uni-parental inheritance should result in sequence homoplasmy, or within-individual genetic homogeneity, by preventing the mixing of differing mitochondrial genomes at fertilization. As McCauley [2] points out in a recent Tansley Review, it is becoming increasingly apparent that bi-parental inheritance via occasional paternal transmission (leakage) of plant mitochondrial genomes can generate heteroplasmy and within-individual mitochondrial genome diversity. The occurrence of such heteroplasmy can enhance the possibility that intermolecular recombination between divergent genetic partners will result in novel multi-locus genotypic combinations of potential significance for plant mitochondrial genome evolution. Given that gynodioecy is the second most common mode of reproduction in angiosperms [5], the potential significance for the evolution of the mating system and the plant mitochondrial genome is quite intriguing
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