Academic journal article Genetics

Mitochondrial Recombination Reveals Mito–Mito Epistasis in Yeast

Academic journal article Genetics

Mitochondrial Recombination Reveals Mito–Mito Epistasis in Yeast

Article excerpt

MITOCHONDRIAL DNA (mtDNA) haplotypes are frequently associated with environmental temperature gradients across eukarya, suggesting that mitochondrial performance plays an important role in adaptation (Mishmar et al. 2003; Lucassen et al. 2006; Chatelain et al. 2011; Scott et al. 2011; Lagisz et al. 2013; Dingley et al. 2014; Melo-Ferreira et al. 2014; Silva et al. 2014; Consuegra et al. 2015; Li et al. 2016). To understand the adaptive potential of mtDNAs, it is necessary to dissect the genetic and environmental factors that influence the functional variation in mtDNAs. This is particularly challenging in systems where mtDNA inheritance is uniparental because the lack of recombination makes it difficult to differentiate between mitochondrial alleles that contribute to functional variation and those that are neutral.

Homologous recombination between mtDNAs should promote the reorganization of mitochondrial genes and increase the efficacy of selection on adaptive loci. Mitochondrial recombination is common in systems with biparental mtDNA inheritance, such as fungi and many plants (Barr et al. 2005; Gualberto and Newton 2017). In Saccharomyces yeasts, the diverse and highly reticulated mtDNAs show signatures of recombination and horizontal gene transfer within and between species (Peris et al. 2014, 2017; Wolters et al. 2015; Wu et al. 2015; Leducq et al. 2017). In predominantly asexual fungi, mitochondrial recombination occurs more frequently than expected (Brankovics et al. 2017). The machinery for homologous recombination is found in the mitochondria of mammals (Dahal et al. 2017) and there is some evidence of mitochondrial recombination in mammals (Piganeau etai. 2004), other vertebrates (Ciborowski et ai 2007; Ujvari et ai 2007; Sammler et ai. 2011; Wang etai. 2015; Park etai. 2016), and invertebrates (Ladoukakis and Zouros 2001; Passamonti et ai. 2003). Mitochondrial recombination occurs with enough frequency that it should play an important role in the evolution of mtDNAs, especially in fungi.

The effects of mitochondrial recombination on selection and adaptive potential are not understood. In Saccharomyces yeasts, mitochondrial recombination can occur in zygotes containing different mtDNAs but, because heteroplasmic mtDNA states are not maintained, a single mtDNA haplotype (either parental or recombinant) becomes fixed after ~20 generations (Berger and Yaffe 2000). Hybrids of Saccharomyces cerevisiae and S. uvarum contained different speciesspecific mtDNA genetic markers, depending on whether the hybrids were created in a laboratory (Verspohl et ai. 2018) or isolated from industrial settings (Masneuf et ai. 1998; Rainieri et ai. 2008), suggesting that environmental conditions influence the selection for mitochondrial alleles or entire mitotypes. Supporting this, mitochondrial allele inheritance during hybridization of S. cerevisiae and S. paradoxus was altered by changing laboratory conditions during matings (Hsu and Chou 2017).

Mitochondrial alleles that participate in mito-nuclear interactions will also influence the adaptive success of recombinant mtDNAs. Mito-nuclear incompatibilities occur between (Sulo et ai. 2003; Chou et ai. 2010; Spirek et ai. 2014) and within (Paliwal et ai. 2014; Hou et ai. 2015) Saccharomyces species and species-specific compatible mito-nuclear genetic combinations were universally maintained in rare, viable meiotic progeny from S. cerevisiae/ S. bayanus hybrids (Lee et ai. 2008). The extent of recombination in these hybrid studies is not known due to the limited number of mitochondrial markers followed. Laboratoryderived isogenic S. paradoxus hybrids containing different recombinant mtDNAs were phenotypically variable, consistent with the presence of functionally distinct mitochondrial or mito-nuclear alleles (Leducq et ai. 2017). Selection on such functional units could explain the existence of recombinant mtDNAs found in natural S. paradoxus hybrids (Leducq et ai. 2017; Peris et ai. …

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