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Characterizing the genetic and molecular basis of hybrid incompatibilities is a first step toward understanding their evolutionary origins. We fine mapped the nuclear restorer (Rf ) of cytoplasm-dependent anther sterility in Mimulus hybrids by identifying and targeting regions of the Mimulus guttatus genome containing large numbers of candidate pentatricopeptide repeat genes (PPRs). The single Mendelian locus Rf was first isolated to a 1.3-cM region on linkage group 7 that spans the genome's largest cluster of PPRs, then split into two tightly linked loci (Rf1 and Rf2) by ,10 recombination events in a large (N = 6153) fine-mapping population. Progeny testing of fertile recombinants demonstrated that a dominant M. guttatus allele at each Rf locus was sufficient to restore fertility. Each Rf locus spans a physical region containing numerous PPRs with high homology to each other, suggesting recent tandem duplication or transposition. Furthermore, these PPRs have higher homology to restorers in distantly related taxa (petunia and rice) than to PPRs elsewhere in the Mimulus genome. These results suggest that the cytoplasmic male sterility (CMS)-PPR interaction is highly conserved across flowering plants. In addition, given our theoretical understanding of cytonuclear coevolution, the finding that hybrid CMS results from interactions between a chimeric mitochondrial transcript that is modified by Rf loci identified as PPRs is consistent with a history of selfish mitochondrial evolution and compensatory nuclear coevolution within M. guttatus. [ABSTRACT FROM AUTHOR]

It is generally assumed that mitochondrial genomes are uniparentally transmitted, homoplasmic and nonrecombining. However, these assumptions draw largely from early studies on animal mitochondrial DNA (mtDNA). In this review, we show that plants, animals and fungi are all characterized by episodes of biparental inheritance, recombination among genetically distinct partners, and selfish elements within the mitochondrial genome, but that the extent of these phenomena may vary substantially across taxa. We argue that occasional biparental mitochondrial transmission may allow organisms to achieve the best of both worlds by facilitating mutational clearance but continuing to restrict the spread of selfish genetic elements. We also show that methodological biases and disproportionately allocated study effort are likely to have influenced current estimates of the extent of biparental inheritance, heteroplasmy and recombination in mitochondrial genomes from different taxa. Despite these complications, there do seem to be discernible similarities and differences in transmission dynamics and likelihood of recombination of mtDNA in plant, animal and fungal taxa that should provide an excellent opportunity for comparative investigation of the evolution of mitochondrial genome dynamics. [ABSTRACT FROM AUTHOR]

Intraspecific coevolution between selfish elements and suppressors may promote interspecific hybrid incompatibility, but evidence of this process is rare. Here, we use genomic data to test alternative models for the evolution of cytonuclear hybrid male sterility in Mimulus. In hybrids between Iron Mountain (IM) Mimulus guttatus × Mimulus nasutus, two tightly linked M. guttatus alleles (Rf1/Rf2) each restore male fertility by suppressing a local mitochondrial male-sterility gene (IM-CMS). Unlike neutral models for the evolution of hybrid incompatibility loci, selfish evolution predicts that the Rf alleles experienced strong selection in the presence of IM-CMS. Using whole-genome sequences, we compared patterns of population-genetic variation in Rf at IM to a neighbouring population that lacks IM-CMS. Consistent with local selection in the presence of IM-CMS, the Rf region shows elevated FST, high local linkage disequilibrium and a distinct haplotype structure at IM, but not at Cone Peak (CP), suggesting a recent sweep in the presence of IM-CMS. In both populations, Rf2 exhibited lower polymorphism than other regions, but the low-diversity outliers were different between CP and IM. Our results confirm theoretical predictions of ubiquitous cytonuclear conflict in plants and provide a population-genetic mechanism for the evolution of a common form of hybrid incompatibility. [ABSTRACT FROM AUTHOR]