Mitochondrial-nuclear coadaptation revealed through mtDNA replacements in Saccharomyces cerevisiae

Tuc H M Nguyen,Heather L Fiumera,Swati Paliwal,Andrew Ziesel,Sargunvir Sondhi

doi:10.1186/s12862-020-01685-6

Tuc H M Nguyen, Heather L Fiumera + Show 3 more

Open Access

https://doi.org/10.1186/s12862-020-01685-6

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Journal: BMC ecology	Publication Date: Sep 25, 2020
Citations: 20	License type: open-access

Affiliation: Binghamton University, Banasthali University

Abstract

BackgroundMitochondrial function requires numerous genetic interactions between mitochondrial- and nuclear- encoded genes. While selection for optimal mitonuclear interactions should result in coevolution between both genomes, evidence for mitonuclear coadaptation is challenging to document. Genetic models where mitonuclear interactions can be explored are needed.ResultsWe systematically exchanged mtDNAs between 15 Saccharomyces cerevisiae isolates from a variety of ecological niches to create 225 unique mitochondrial-nuclear genotypes. Analysis of phenotypic profiles confirmed that environmentally-sensitive interactions between mitochondrial and nuclear genotype contributed to growth differences. Exchanges of mtDNAs between strains of the same or different clades were just as likely to demonstrate mitonuclear epistasis although epistatic effect sizes increased with genetic distances. Strains with their original mtDNAs were more fit than strains with synthetic mitonuclear combinations when grown in media that resembled isolation habitats.ConclusionsThis study shows that natural variation in mitonuclear interactions contributes to fitness landscapes. Multiple examples of coadapted mitochondrial-nuclear genotypes suggest that selection for mitonuclear interactions may play a role in helping yeasts adapt to novel environments and promote coevolution.

Highlights

Mitochondrial function requires numerous genetic interactions between mitochondrial- and nuclearencoded genes
As mitochondrial DNA (mtDNA) diverge in different populations of a species, selection should favor coevolved nuclear alleles that help maintain important mitochondrial activities. These coevolved mitochondrial-nuclear allele pairs may be disrupted resulting in reduced fitness in the hybrids and/or F2 progeny in a type of Bateson-Dobzhansky-Muller (BDM) incompatibility that leads to reproductive isolation
A mitonuclear strain collection allows for direct assessment of mitonuclear interactions To explore how mitonuclear interactions contribute to phenotypic differences in S. cerevisiae, we chose 15 isolates that were available as haploid derivatives [59]

Summary

Introduction

Mitochondrial function requires numerous genetic interactions between mitochondrial- and nuclearencoded genes. As mtDNAs diverge in different populations of a species, selection should favor coevolved nuclear alleles that help maintain important mitochondrial activities During hybridization, these coevolved mitochondrial-nuclear (mitonuclear) allele pairs may be disrupted resulting in reduced fitness in the hybrids and/or F2 progeny in a type of Bateson-Dobzhansky-Muller (BDM) incompatibility that leads to reproductive isolation. Hybridization experiments in other taxa have revealed mitonuclear incompatibilities, including flies [12,13,14,15,16,17], wasps [18, 19], plants [20], nematodes [21, 22], yeasts [23,24,25,26], mice [27], and mammalian cell lines [28,29,30] This growing body of literature lends support to the idea that BDM-type mitonuclear incompatibilities can contribute to, and even initiate, speciation [31]

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