Article

Incompatibility of Nuclear and Mitochondrial Genomes Causes Hybrid Sterility between Two Yeast Species

Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan.
Cell (Impact Factor: 33.12). 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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    • "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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    ABSTRACT: Products and regulatory motifs of the mitochondrial and nuclear genomes interact closely to enable efficient cellular energy production within mitochondria. Although recent evidences support the prediction that during evolutionary time combinations of these interactions are optimized by selection acting on important life history traits, relatively few studies have directly tested it. The goal of this study was to test the role of mitonuclear interactions in shaping preadult and adult life history traits under age-specific selection in the seed beetle (Acanthoscelides obtectus). In order to disentangle the effects of mitochondria, nuclei and their interaction in the evolutionary response to the long-term laboratory selection for early (E) and late (L) reproduction, we used mitonuclear introgression lines in which E and L mitochondrial genomes were expressed in both E and L nuclear background. We found that mitonuclear genotypes carrying disrupted pair of nuclear and mitochondrial genomes mainly affected preadult life history traits—egg-to-adult viability and developmental time. Neither mitochondria nor their interaction with nuclear genomes had effects on realized fecundity of mated females and longevity of virgin beetles. However, when involved in reproductive activities females and males with disrupted genotypes mostly exhibited reduced longevity. Furthermore, since reproduced males exhibited greater longevity cost than females, our results are in accordance with the mother’s curse hypothesis. Being that for the most life history traits we detected smaller additive mitochondrial genetic effects compared with epistatic mitonuclear effects, we concluded that mitonuclear interactions might be the target of age-specific selection.
    Evolutionary Biology 07/2015; DOI:10.1007/s11692-015-9340-9 · 3.27 Impact Factor
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    • "A second mechanism that contributes to RI is genetic incompatibilities. A special Dobzhansky–Muller incompatibility between nuclear and mitochondrial genomes contributes to postzygotic isolation in F2 hybrids that are derived from rare viable F1 hybrids (Lee et al. 2008; Chou et al. 2010). Additionally, Xu and He (2011) found that genetic incompatibilities affect sporulation efficiency in yeast F2 hybrids more than F2 hybrid growth. "
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    ABSTRACT: Regulatory changes rapidly accumulate between species, and interspecific hybrids often misexpress genes. Hybrid misexpression, expression levels outside the range of both parental species, can result from cis- and trans-acting regulatory changes that interact abnormally in hybrids. Thus misexpressed genes may contribute to hybrid sterility. However in the context of a whole organism, misexpression may not result directly from cis-trans interactions, but rather indirectly from differences between hybrid and parental abundance of cell types. Here we eliminate the confounding effects of cells types by examining gene expression in a sterile interspecific yeast hybrid during meiosis. We investigated gene expression of the yeasts Saccharomyces cerevisiae, S. paradoxus and their hybrid at multiple meiotic stages. Although the hybrid and parents exhibit similar changes in expression levels across meiosis, the hybrid meiotic program occurs earlier than either parent. The timing change produces a heterochronic pattern of misexpression during mid-meiosis. Coincident with the timing of misexpression, we find a transition from predominantly trans-acting to cis-acting expression divergence and an increase in the number of opposing cis-trans changes. However, we find no direct relationship between opposing cis-trans changes and misexpression. Contrary to the notion that cis-trans interactions cause misexpression, a heterochronic shift in the normal meiotic gene expression program produces patterns of misexpression in a yeast hybrid. Our results imply that temporal dynamics of single cell types is important to understanding hybrid misexpression and its relationship to cis-trans interactions.
    Molecular Biology and Evolution 03/2014; DOI:10.1093/molbev/msu098 · 14.31 Impact Factor
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    • "Translation deficiency in hybrids (Lee et al. 2008), poor intron excision (Chou et al. 2010), ribosomal protein divergence (Barreto & Burton 2013, Matthews et al. 1978) "
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    ABSTRACT: Reduced fitness in interpopulation hybrids can be a first indication of genetic incompatibilities that may ultimately lead to reproductive isolation and speciation. A growing number of cases of hybrid breakdown have been traced to incompatibilities between the nuclear genome and the organellar genomes of the mitochondria and chloroplasts. Although these organellar genomes derive from ancient bacterial endosymbioses, they have been vastly reduced in size and now encode relatively few genes. The remaining genes are necessary but not sufficient for organelle function. In fact, most proteins functioning in the organelles are encoded in the nuclear genome and need to be imported after synthesis in the cytosol. The necessary interactions between organelle and nuclear genomes have resulted in some degree of coadaptation within all natural populations. Hybridization brings together previously untested allelic combinations and can disrupt intergenomic coadaptation, resulting in organelle dysfunction and, consequently, hybrid breakdown.
    Annual Review of Ecology Evolution and Systematics 11/2013; 44:281–302. DOI:10.1146/annurev-ecolsys-110512-135758 · 10.98 Impact Factor
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