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Lee H-Y, Chou J-Y, Cheong L, Chang N-H, Yang S-Y, Leu1 J-Y. Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135: 1065-1073

Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan.
Cell (Impact Factor: 32.24). 01/2009; 135(6):1065-73. DOI: 10.1016/j.cell.2008.10.047
Source: PubMed

ABSTRACT

Hybrids between species are usually unviable or sterile. One possible mechanism causing reproductive isolation is incompatibility between genes from different species. These "speciation" genes are interacting components that cannot function properly when mixed with alleles from other species. To test whether such genes exist in two closely related yeast species, we constructed hybrid lines in which one or two chromosomes were derived from Saccharomyces bayanus, and the rest were from Saccharomyces cerevisiae. We found that the hybrid line with Chromosome 13 substitution was completely sterile and identified Aep2, a mitochondrial protein encoded on Chromosome 13, to cause the sporulation defect as S. bayanus AEP2 is incompatible with S. cerevisiae mitochondria. This is caused by the inability of S. bayanus Aep2 protein to regulate the translation of the S. cerevisiae OLI1 mRNA. We speculate that AEP2 and OLI1 have evolved during the adaptation of S. bayanus to nonfermentable carbon sources, thereby driving speciation.

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    • "Deleterious effects of hybridization on fitness resulting from mitonuclear epistatic interactions have been recently described in a number of species. Together, these studies have established requirements for demonstrating that mitonuclear epistasis causes interpopulation hybrid dysfunction (e.g., Breeuwer and Werren 1995; Tiffin et al. 2001; Levin 2003; Sackton et al. 2003; Bolnick and Near 2005; Zeyl et al. 2005; Ellison and Burton 2006; Fishman and Willis 2006; Dowling et al. 2007; Ellison and Burton 2008a, 2008b; Ellison et al. 2008; Lee et al. 2008; Niehuis et al. 2008; Gagnaire et al. 2012; Gibson et al. 2013; Hoekstra et al. 2013; Meiklejohn et al. 2013; Gershoni et al. 2014). First, genetic variation must exist between the nuclear genomes and the mitochondrial genomes of the two populations. "
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    ABSTRACT: In order to identify the earliest genetic changes that precipitate species formation, it is useful to study genetic incompatibilities that cause only mild dysfunction when incompatible alleles are combined in an inter-population hybrid. Such hybridization within the nematode species Caenorhabditis briggsae has been suggested to result in selection against certain combinations of nuclear and mitochondrial alleles, raising the possibility that mitochondrial-nuclear (mitonuclear) epistasis reduces hybrid fitness. To test this hypothesis, cytoplasmic-nuclear hybrids (cybrids) were created to purposefully disrupt any epistatic interactions. Experimental analysis of the cybrids suggests that mitonuclear discord can result in decreased fecundity, increased lipid content, and increased mitochondrial reactive oxygen species levels. Many of these effects were asymmetric with respect to cross direction, as expected if cytoplasmic-nuclear Dobzhansky-Muller incompatibilities exist. One such effect is consistent with the interpretation that disrupting coevolved mitochondrial and nuclear loci impacts mitochondrial function and organismal fitness. These findings enhance efforts to study the genesis, identity, and maintenance of genetic incompatibilities that precipitate the speciation process.
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    • "Backcross studies on this species have revealed that hybrid breakdown can be attributed to the nuclear-mitochondrial interactions, raising the possibility that mitonuclear incompatibilities may represent an important mechanism of reproductive isolation and speciation (Burton and Barreto 2012). Mitonuclear mismatch also produced sterile hybrids between the yeast species Saccharomyces cerevisiae and S. bayanus (Lee et al. 2008), and hybrid breakdown between species of Nasonia wasps (Ellison et al. 2008), Drosophila (Sackton et al. 2003), centrarchid fishes (Bolnick et al. 2008) and several plant species (Bomblies 2010 and references therein). Studies on Drosophila that have manipulated nuclear and mitochondrial genetic variation have found that mitonuclear epistasis is an important force in shaping longevity variation (James and Ballard 2003; Rand et al. 2006; Maklakov et al. 2006; Ballard et al. 2007; Clancy 2008; Dowling et al. 2009). "
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    • "The effects on F1 hybrids however are often unpredictable ; hybrids can display hybrid vigor — increased fitness in certain traits relative to the parental species (Livesay, 1930; Manwell et al., 1963; McDaniel and Grimwood, 1971) — but more commonly display defects. In many cases, defects in hybrids are linked to incompatibilities between nuclear and mitochondrial genomes (Liepins and Hennen, 1977; Edmands and Burton, 1999; Sackton et al., 2003; Ellison and Burton, 2006, 2008a; Ellison et al., 2008; Lee et al., 2008; Niehuis et al., 2008). While a hybrid's nuclear DNA is inherited from both parents (and therefore both species), its mitochondrial DNA is inherited from only one parent (in most cases, the mother). "
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