Academic journal article Genetics

A Genome-Wide Map of Mitochondrial DNA Recombination in Yeast

Academic journal article Genetics

A Genome-Wide Map of Mitochondrial DNA Recombination in Yeast

Article excerpt

(ProQuest: ... denotes formulae omitted.)

MITOCHONDRIA (mt) are central organelles for various cellular functions including respiration, apoptosis, ion homeostasis, and metabolite biosynthesis. Cellular energy production through oxidative phosphorylation requires the involvement of factors encoded by two different genomes: one located in the nucleus and the other in mitochondria. The interplay between these two genomes is crucial to ensure functionality and these interactions have been associ- ated with phenotypic diversity (Zeyl et al. 2005; Solieri et al. 2008) as well as speciation due to genetic incompatibilities (Lee et al. 2008). The mt genome is a remnant of an ancestral a-proteobacterial symbiont and has undergone an important size reduction by gene transfer to the nucleus (Wallace 2007; Gray 2012). Nevertheless, the cell requires mtDNA to ensure respiration, as it encodes essential subunits of the oxidative phosphorylation pathway. Unlike nuclear genomic DNA, mul- tiple copies of mtDNA are contained in each cell, the number of which varies depending on the species, the tissue (Preuten et al. 2010), or the culture conditions (Shay et al. 1990; Hori et al. 2009). High mtDNA copy number provides a pool of templates for intermolecular recombination, and mt recom- bination is a widespread phenomenon described in plants (Arrieta-Montiel et al. 2009; Galtier 2011), fungi (Dujon et al. 1974; Fourie et al. 2013), protists (Gray et al. 1999), and invertebrates (Ladoukakis and Zouros 2001). In ani- mal mtDNA, although the recombination machinery has been described (Lakshmipathy and Campbell 1999), the common belief was that mtDNA is clonally inherited and devoid of recombination. However, some recent studies have challenged this dogma and evidence of mt recombi- nation has been found in the animal kingdom, from statistical analyses of mtDNA sequences (Eyre-Walker and Awadalla 2001) and direct measurements (D'aurelio 2004; Kraytsberg et al. 2004).

Saccharomyces cerevisiae has proved to be a relevant model for mitochondrial genetics due to its functional sim- ilarity with the human mtDNA and the ability to directly manipulate the mt genome. Yeast is also able to grow in the absence of functional mitochondria and to spontane- ously produce respiratory-deficient mutants called petite mutants, in which the whole mtDNA or part of it is deleted. Additionally, the first mitochondrial genes to be sequenced originated from yeast and a full mtDNA genome sequence has been available since 1998 (Foury et al. 1998), a few years after the release of the nuclear genome (Goffeau et al. 1996). The major fraction of the yeast mt genome is organized as linear concatemers of 85-kb-long molecules suggested to originate from circular monomers (reviewed in Solieri 2010). Concatemers are predominantly present in mother cells and nondividing cells, while the monomers have been described to be located in the growing buds (Ling and Shibata 2002; Solieri 2010; Shibata and Ling 2007). The mt genome is composed of seven genes involved in oxidative phosphorylation (COX1, COX2, COX3, ATP6, ATP8, ATP9, and COB) and a gene coding for a ribosomal protein (VAR1). It also contains the mt small and large ri- bosomal RNA (rRNA) genes and 24 transfer RNA (tRNA) genes (Foury et al. 1998). Its copy number per cell ranges from 50 to 200 (Solieri 2010) and contrary to the mamma- lian mtDNA it is biparentally inherited after mating, allow- ing for recombination, although this heteroplasmic state is transient for only ^20 generations. Yeast mt recombination has been described since the 1970s (Dujon et al. 1974). After mating, the parental mitochondria fuse, forming a sin- gle organelle throughout the newly formed zygote, with a rapid mixing of the mt proteins (Figure 1A). Subsequently, the parental mtDNAs are in the same compartment but they cannot diffuse freely through the mt reticulum, and the recombinants' genome can thus be found only at the medial bud where both genomes are in direct physical contact (Figure 1A) (Strausberg and Perlman 1978; Zinn et al. …

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