Assessing the fitness consequences of mitonuclear interactions in natural populations

Hill, Geoffrey E.; Havird, Justin C.; Sloan, Daniel B.; Burton, Ronald S.; Greening, Chris; Dowling, Damian K.

doi:10.1111/brv.12493

Cited by 105 publications

(131 citation statements)

References 227 publications

(299 reference statements)

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“…Although we do find clear additive effects of some plasmotypes, the majority of the plasmotype derived variation manifests as epistasis in the traits we measured which is in line with previous research in plants, animals, and fungi (Zeyl et al, 2005; Dowling et al, 2007; Montooth et al, 2010; Joseph et al, 2013; Roux et al, 2016). Also in line with studies of mitonuclear interactions in animals is the observation that phenotypic variation due to plasmotypic variation becomes more pronounced under fluctuating and stressful conditions (Dowling et al, 2007; Hoekstra et al, 2013; Mossman et al, 2016; Hill et al, 2019). Both our results and previous work suggests that multilevel interactions (i.e.…”

Section: Introductory Paragraphmentioning

confidence: 55%

Reciprocal cybrids reveal how organellar genomes affect plant phenotypes

Flood

Theeuwen

Schneeberger

et al. 2018

Preprint

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27 28 29 30 2Introductory paragraph: 31 Assessing the impact of variation in chloroplast and mitochondrial DNA (collectively termed the 32 plasmotype) on plant phenotypes is challenging due to the difficulty in separating their effect from 33 nuclear derived variation (the nucleotype). Haploid inducer lines can be used as efficient plasmotype 34 donors to generate new plasmotype-nucleotype combinations (cybrids) (Ravi et al., 2014). We generated 35 a panel comprising all possible cybrids of seven Arabidopsis thaliana accessions and extensively 36 phenotyped these lines for 1859 phenotypes under stable and fluctuating conditions. We show that 37 natural variation in the plasmotype results in additive as well as epistatic effects across all phenotypic 38 categories. Plasmotypes which induce more additive phenotypic changes also cause more significant 39 epistatic effects, suggesting a possible common basis for both additive and epistatic effects. On average 40 epistatic interactions explained twice as much of the variance in phenotypes as additive plasmotype 41 effects. The impact of plasmotypic variation was also more pronounced under fluctuating and stressful 42 environmental conditions. Thus, the phenotypic impact of variation in plasmotypes is the outcome of 43 multilevel Nucleotype X Plasmotype X Environment interactions and, as such, the plasmotype is likely 44 to serve as a reservoir of variation which is only exposed under certain conditions. The production of 45 cybrids using haploid inducers is a quick and precise method for assessing the phenotypic effects of 46 natural variation in organellar genomes. It will facilitate efficient screening of unique nucleotype-47 plasmotype combinations to both improve our understanding of natural variation in nucleotype 48 plasmotype interactions and identify favourable combinations to improve plant performance. 49Chloroplasts and mitochondria play essential roles in metabolism, cellular homeostasis and 50 environmental sensing (Petrillo et al., 2014; Chan et al., 2016). Their genomes contain only a limited set 51 of genes whose functioning requires tight coordination with the nucleus through signaling pathways that 52 modulate nuclear and organellar gene expression (Petrillo et al., 2014; Kleine and Leister, 2016). 53 Plasmotype variation can be strongly additive, such as in the case of chloroplast encoded herbicide 54 tolerance (Flood et al., 2016), or can manifest in complex cytonuclear interactions as non-additive, non-55 linear effects (epistasis), such as found for secondary metabolites (Joseph et al., 2013). The phenotypic 56 consequences of epistasis can be detected when a plasmotype causes phenotypic effects in 57 combination with some, but not all nuclear backgrounds. Recent studies suggest that cytonuclear 58 epistasis is the main route through which variation in the plasmotype is expressed (Zeyl et al., 2005; 59 3 Montooth et al. , 2010; Joseph et al., 2013; Joseph et al., 2013; Tang et al., 2014; Roux et al., 2016; 60 Mossman et al., 2019) an...

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Section: Introductory Paragraphmentioning

confidence: 55%

Reciprocal cybrids reveal how organellar genomes affect plant phenotypes

Flood

Theeuwen

Schneeberger

et al. 2018

Preprint

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“…(Galtier et al 2009, Lamb et al 2018, Morales et al 2015, Ruiz-Pesini et al 2004). It is difficult to disentangle the effects of selection from the effects of demographic processes using genomic data alone without using phenotypic data to support the role of selection (Hill et al 2018, Walsh & Lynch 2018). Our study population of collared flycatchers went through a recent bottleneck as they colonized the island of Öland about fifty years ago followed by a drastic population expansion (Kardos et al 2017).…”

Section: Discussionmentioning

confidence: 99%

Divergent mitochondrial and nuclear OXPHOS genes are candidates for genetic incompatibilities inFicedulaFlycatchers

Valk

et al. 2019

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Hybrid dysfunction is an important source of reproductive isolation between emerging species. Bateson-Dobzhansky-Muller incompatibilities are theoretically well-recognized as the underlying cause of low hybrid dysfunction. However, especially in wild populations, little empirical evidence exists for which genes are involved in such incompatibilities. The relative role of ecological divergence in causing the build-up of genetic incompatibilities in relation to other processes such as genomic conflict therefore remains largely unknown. Genes involved in energy metabolism are potential candidates for genetic incompatibilities, since energy metabolism depends on co-expression of mitochondrial DNA (mtDNA) and nuclear DNA (nDNA) leading to mitonuclear coadaptation. When mitochondrial and nuclear genes lacking a co-evolutionary history appear together in hybrids, incompatibilities could arise.Ficedulaflycatcher F1 hybrids have a higher resting metabolic rate (RMR) compared to the parental species, which could be a sign of genetic incompatibilities between energy metabolism genes that diverged in response to environmental differences while the species were in allopatry. Based on sequences of 15 mitochondrial genes of 264 individuals, we show that the two species have divergent mtDNA caused by the build-up of mainly synonymous mutations and a few non-synonymous mutations. Pied flycatcher mitogenomes show evidence of non-neutrality, indicating a selective sweep or population expansion. There is little variation in the nuclear OXPHOS-related proteins and no significant deviation from neutrality, however, specific codon identified sites might be under positive selection in both mitochondrial and nuclear genes encoding OXPHOS proteins for complex I and III. Taken together, these diverged mitonuclear genes therefore constitute possible candidates underlying, at least part of the genetic incompatibilities that cause hybrid dysfunction in crosses between collared and pied flycatchers.

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“…Heteroplasmy among the hundreds of mitochondrial DNA (mtDNA) molecules found within a cell (Stewart and Chinnery 2015;Hahn and Zuryn 2019), differential distribution of disease-causing mtDNA among tissues (Boulet et al 1992), and modifier alleles within the mitochondrial genome (Elliott et al 2008;Wei et al 2017) magnify the problem of interpreting effects of different mtDNA alterations. Mito-nuclear interactions and environmental effects may also determine the outcome of mitochondrial DNA mutations (Wolff et al 2014;Matilainen et al 2017;Hill et al 2019). Beyond the obvious importance of determining the genetic etiology of symptoms in the clinical setting, the rapidly increasing prominence of direct-to-consumer genetic testing (Phillips et al 2018) calls for an improved understanding of which mtDNA polymorphisms might affect human health (Blell and Hunter 2019).…”

Section: Introductionmentioning

confidence: 99%

A novel phylogenetic analysis and machine learning predict pathogenicity of human mtDNA variants

Dunn

Akpinar

Carlson³

et al. 2020

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Linking mitochondrial DNA (mtDNA) mutations to patient outcomes remains a formidable challenge. The multicopy nature and potential heteroplasmy of the mitochondrial genome, differential distribution of mutant mtDNAs among various tissues, genetic interactions among alleles, and environmental effects currently hamper clinical efforts to diagnose mitochondrial disease. Multiple sequence alignments are often deployed to estimate the potential significance of mitochondrial variants. However, factors including sample set bias, alignment errors, and sequencing errors currently limit the utility of multiple sequence alignments in pathogenicity prediction. Here, we describe an approach to assessment of site-specific conservation and variant acceptability that is reliant upon ancestral phylogenetic predictions and minimizes current alignment limitations. Using the output of our approach, we deploy machine learning in order to predict the pathogenicity of thousands of human mtDNA variants not yet linked to disease. Our work demonstrates that a substantial portion of mtDNA variants not yet characterized as harmful are, in fact, likely to be deleterious. Our findings will be of direct relevance to those at risk of mitochondria-associated illness, but the general applications of our methodology also extend beyond the context of mitochondrial disorders.

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Assessing the fitness consequences of mitonuclear interactions in natural populations

Cited by 105 publications

References 227 publications

Reciprocal cybrids reveal how organellar genomes affect plant phenotypes

Reciprocal cybrids reveal how organellar genomes affect plant phenotypes

Divergent mitochondrial and nuclear OXPHOS genes are candidates for genetic incompatibilities inFicedulaFlycatchers

A novel phylogenetic analysis and machine learning predict pathogenicity of human mtDNA variants

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