Academic journal article Genetics

Mitochondrial-Nuclear Epistasis Contributes to Phenotypic Variation and Coadaptation in Natural Isolates of Saccharomyces Cerevisiae

Academic journal article Genetics

Mitochondrial-Nuclear Epistasis Contributes to Phenotypic Variation and Coadaptation in Natural Isolates of Saccharomyces Cerevisiae

Article excerpt

MITOCHONDRIAL energy production, which affects vir- tually every aspect of cellular fitness, requires the par- ticipation of two genomes. The mitochondrial genome encodes for essential components of the oxidative phosphorylation ma- chinery and mitochondrial ribosomal RNAs and transfer RNAs. The nuclear genome encodes nearly 1000 proteins that are imported to the organelle where they compose the majority of the mitochondrial proteome. Specific interactions between components of both genomes are required at many levels, in- cluding mitochondrial DNA (mtDNA) replication, repair, and inheritance and transcription, translation, and assembly of the electron transport chain components. The respiratory com- plexes themselves are heterogeneous, composed of both nu- clear and mitochondrially encoded proteins. Over evolutionary time, these interactions have been optimized, in part, to regu- late production of the reactive oxygen species (ROS) that are the by-products of mitochondrial respiration.

Allelic variation in both genomes can affect mt-n inter- actions and alter mitochondrial fitness. These interactions have been shown to have direct consequences on health- related and life-history phenotypes in several taxa. In insects such as Drosophila and Callosobruchus (seed beetle), ex- changing mtDNA variants between distinct populations has led to lowered metabolic rate (Arnqvist et al. 2010), de- creased egg-to-adult survival (Dowling et al. 2007a; Montooth et al. 2010), and shortened life span (Clancy 2008; Zhu et al. 2014). Interpopulation hybrids of the marine copepod Tigriopus suffered compromised oxidative phosphorylation (OXPHOS) capacities (Ellison and Burton 2006, 2008b) and reduced mitochondrial transcription (Ellison and Burton 2008a), most likely influenced by interactions between alleles of the nuclear- encoded RNA polymerase and mtDNA variants (Ellison and Burton 2010).

The importance of mt-n epistasis extends well past ar- thropods. In mice, mt-n epistasis is known to affect cognition (Roubertoux et al. 2003), ROS (Fetterman et al. 2013), and respiratory functions (Betancourt et al. 2014) as well as tissue- specific selection for mtDNA variants (Jenuth et al. 1997). Interactions between mt and n genomes likely contribute to cytoplasmic male sterility in plants (Hu et aL 2014) and disease presentation and aging in humans (Tranah 2011; Wallace and Chalkia 2013; Wolff et al. 2014), suggesting that mt-n epistasis is important in most eukaryotes.

Between species, incompatibilities between mitochondrial and nuclear genomes can be quite severe. Introgression of mtDNAs from Drosophila simulaos to D. melanogaster had sig- nificant effects on respiratory complexes (Sackton et aL 2003), development (Montooth et al. 2010), and aging (Rand et al. 2006). Disrupted oxidative phosphorylation pathways were observed in F2 male hybrids of Nasonia wasps (Ellison et al. 2008; Niehuis et al. 2008; Koevoets et al. 2012a). Activities of OXPHOS complexes in human cell lines harboring mtDNAs from other primates were reduced by as much as 90% (Barrientos et al. 2000). Similarly, respiratory capabilities of murine (Dey et al. 2000; Yamaoka et al. 2000; McKenzie et al. 2003) or amphibian (Liepins and Hennen 1977) xenomito- chondrial cybrids were drastically reduced. Interspecific mt-n incompatibilities between yeasts in the Saccharomyces sensu stricto genus can lead to complete respiratory deficiencies (Sulo et al. 2003; Lee et al. 2008; Chou et aL 2010; but see Prochazka et aL 2012). While incompatibilities between spe- cies generally leads to a decline in fitness, mt-n incompatibil- ities do not always tightly align with genetic distance; larger epistatic responses to mtDNA exchanges were observed within D. melanogaster populations than between species (Montooth et al. 2010). The Dobzhansky-Muller-type mt-n incompatibil- ities that sometimes exist between species may have contrib- uted to spéciation events (Trier et aL 2014; Wolff et al. …

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