Estimating the Fitness Effect of Deleterious Mutations During the Two Phases of the Life Cycle: A New Method Applied to the Root-Rot Fungus Heterobasidion parviporum

Abstract

Many eukaryote species, including taxa such as fungi or algae, have a lifecycle with substantial haploid and diploid phases. A recent theoretical model predicts that such haploid-diploid lifecycles are stable over long evolutionary time scales when segregating deleterious mutations have stronger effects in homozygous diploids than in haploids and when they are partially recessive in heterozygous diploids. The model predicts that effective dominance—a measure that accounts for these two effects—should be close to 0.5 in these species. It also predicts that diploids should have higher fitness than haploids on average. However, an appropriate statistical framework to conjointly investigate these predictions is currently lacking. In this study, we derive a new quantitative genetic model to test these predictions using fitness data of two haploid parents and their diploid offspring, and genome-wide genetic distance between haploid parents. We apply this model to the root-rot basidiomycete fungus Heterobasidion parviporum—a species where the heterokaryotic (equivalent to the diploid) phase is longer than the homokaryotic (haploid) phase. We measured two fitness-related traits (mycelium growth rate and the ability to degrade wood) in both homokaryons and heterokaryons, and we used whole-genome sequencing to estimate nuclear genetic distance between parents. Possibly due to a lack of power, we did not find that deleterious mutations were recessive or more deleterious when expressed during the heterokaryotic phase. Using this model to compare effective dominance among haploid-diploid species where the relative importance of the two phases varies should help better understand the evolution of haploid-diploid life cycles.

Chemical defence responses of Norway spruce to two fungal pathogens

“…Two fungal strains, Heterobasidion parviporum Sä 159–5 (Hp) and Endoconidiophora polonica NFLI 1993‐208/115‐2 (Ep), were used in the inoculation experiment. The Hp isolate was obtained from SLU, Uppsala, and it has previously shown a good ability in phytotoxin production (Hansson et al., 2014) and wood degradation (Clergeot et al., 2019). The Ep strain was collected from a Norway spruce log infested by the bark beetle Polygraphus poligraphus L. (Krokene & Solheim, 1996).…”

Mitonuclear Genetic Interactions in the Basidiomycete Heterobasidion parviporum Involve a Non-conserved Mitochondrial Open Reading Frame

“…Heterokaryon synthesis was implemented with thirty homokaryotic parental isolates sampled at various locations in Eurasia and showing no population structure. We observed that variance of growth rate does not correlate with genetic distance in heterokaryons and that mitochondrial genetic effects account for 35% of phenotypic variance among homokaryons and 3% among heterokaryons (Clergeot et al, 2019). Heterokaryons are more fit than their parents in average, but not more than the fittest parents, suggesting heterozygosity and the masking of deleterious alleles at some of the nuclear loci involved in mitonuclear interactions in the offspring, rather than an intrinsic difference of fitness between the heterokaryons and their parents.…”

“…Data from thirteen H. parviporum homokaryotic isolates out of thirty initially crossed in our previous study (Clergeot et al, 2019), and from 73 pairs of their heterokaryotic offspring were analyzed for mitonuclear epistasis in this study. Heterokaryons of each pair are carrying the same parental haploid nuclei, but mitochondria from either of the two parental isolates (Xu and Wang, 2015; see also Figure 2 in Clergeot et al, 2019).…”

“…Our recent work in Heterobasdion parviporum demonstrated and quantified mitochondrial genetic effects on two fitness proxies in heterokaryons and their parents (Clergeot et al, 2019). Our experimental design was based on heterokaryon synthesis (Olson and Stenlid, 2001), during which mitochondrial DNA is unparentally inherited while nuclei undergo bidirectional exchange, resulting in a pair of heterokaryons with the same haploid nuclei but a different mitochondrial genome (Xu and Wang, 2015).…”

“…The present study is an investigation of the genetic basis of mitonuclear interactions in Heterobasidion parviporum: As phenotyping the heterokaryotic offspring of pairwise crossings of homokaryotic parents in controlled conditions brings a more reliable assessment of the variation resulting from combining different nuclear and mitochondrial alleles (Nguyen et al, 2020), we have revisited our data of heterokaryon variance for growth rate and parental genome sequence polymorphism (Clergeot et al, 2019) in order to identify candidate loci acting in trans across the two genomes. We have been able to single out this way two possible candidates for a nuclear locus encoding proteins involved in molecular trafficking to the mitochondrion (a mitochondrial carrier protein or a mitochondrial calcium uniporter), and a non-conserved mitochondrial locus of unknown function and whose distribution is limited to the Russulales order of Agaricomycetes.…”