Epigenetic modifications affect the rate of spontaneous mutations in a pathogenic fungus

Mutations are the source of genetic variation and the substrate for evolution. Genome-widemutation rates appear to be affected by selection and are probably adaptive. Mutation ratesare also known to vary along genomes, possibly in response to epigenetic modifications, butcausality is only assumed. In this study we determine the direct impact of epigenetic mod-ifications and temperature stress on mitotic mutation rates in a fungal pathogen using amutation accumulation approach. Deletion mutants lacking epigenetic modifications confirmthat histone mark H3K27me3 increases whereas H3K9me3 decreases the mutation rate.Furthermore, cytosine methylation in transposable elements (TE) increases the mutation rate15-fold resulting in significantly less TE mobilization. Also accessory chromosomes havesignificantly higher mutation rates. Finally, wefind that temperature stress substantiallyelevates the mutation rate. Taken together, wefind that epigenetic modifications andenvironmental conditions modify the rate and the location of spontaneous mutations in thegenome and alter its evolutionary trajectory

On variant discovery in genomes of fungal plant pathogens

Comparative genome analyses of eukaryotic pathogens including fungi and oomycetes have revealed extensive variability in genome composition and structure. The genomes of individuals from the same population can exhibit different numbers of chromosomes and different organization of chromosomal segments, defining so-called accessory compartments that have been shown to be crucial to pathogenicity in plant-infecting fungi. This high level of structural variation confers a methodological challenge for population genomic analyses. Variant discovery from population sequencing data is typically achieved using established pipelines based on the mapping of short reads to a reference genome. These pipelines have been developed, and extensively used, for eukaryote genomes of both plants and animals, to retrieve single nucleotide polymorphisms and short insertions and deletions. However, they do not permit the inference of large-scale genomic structural variation, as this task typically requires the alignment of complete genome sequences. Here, we compare traditional variant discovery approaches to a pipeline based on de novo genome assembly of short read data followed by whole genome alignment, using simulated data sets with properties mimicking that of fungal pathogen genomes. We show that the latter approach exhibits levels of performance comparable to that of read-mapping based methodologies, when used on sequence data with sufficient coverage. We argue that this approach further allows additional types of genomic diversity to be explored, in particular as long-read third-generation sequencing technologies are becoming increasingly available to generate population genomic data

Dynamics of transposable elements in recently diverged fungal pathogens: lineage-specific transposable element content and efficiency of genome defences

Transposable elements (TEs) impact genome plasticity, architecture and evolution in fungal plant pathogens. The wide range of TE content observed in fungal genomes reflects diverse efficacy of host-genome defence mechanisms that can counter-balance TE expansion and spread. Closely related species can harbour drastically different TE repertoires, suggesting variation in the efficacy of genome defences. The evolution of fungal effectors, which are crucial determinants of pathogenicity, has been linked to the activity of TEs in pathogen genomes. Here we describe how TEs have shaped genome evolution of the fungal wheat pathogen Zymoseptoria tritici and four closely related species. We compared de novo TE annotations and Repeat-Induced Point mutation signatures in thirteen genomes from the Zymoseptoria species-complex. Then, we assessed the relative insertion ages of TEs using a comparative genomics approach. Finally, we explored the impact of TE insertions on genome architecture and plasticity. The thirteen genomes of Zymoseptoria species reflect different TE dynamics with a majority of recent insertions. TEs associate with distinct genome compartments in all Zymoseptoria species, including chromosomal rearrangements, genes showing presence/absence variation and effectors. European Z. tritici isolates have reduced signatures of Repeat-Induced Point mutations compared to Iranian isolates and closely related species. Our study supports the hypothesis that ongoing but moderate TE mobility in Zymoseptoria species shapes pathogen genome evolution.Competing Interest StatementThe authors have declared no competing interest

Interspecific gene exchange introduces high genetic variability in crop pathogen

Genome analyses have revealed a profound role of hybridization and introgression in the evolution of many eukaryote lineages, including fungi. The impact of recurrent introgression on fungal evolution however remains elusive. Here, we analyzed signatures of introgression along the genome of the fungal wheat pathogen Zymoseptoria tritici. We applied a comparative population genomics approach, including genome data from five Zymoseptoria species, to characterize the distribution and composition of introgressed regions representing segments with an exceptional haplotype pattern. These regions are found throughout the genome, comprising five percent of the total genome and overlapping with > 1000 predicted genes. We performed window-based phylogenetic analyses along the genome to distinguish regions which have a monophyletic or non-monophyletic origin with Z. tritici sequences. A majority of non-monophyletic windows overlap with the highly variable regions suggesting that these originate from introgression. We verified that incongruent gene genealogies do not result from incomplete lineage sorting (ILS) by comparing the observed and expected length distribution of haplotype blocks resulting from ILS. Although protein-coding genes are not enriched in these regions, we identify 18 that encode putative virulence determinants. Moreover, we find an enrichment of transposable elements (TEs) in these regions implying that hybridization may contribute to the horizontal spread of TEs. We detected a similar pattern in the closely related species Zymoseptoria ardabiliae, suggesting that hybridization is widespread among these closely related grass pathogens. Overall, our results demonstrate a significant impact of recurrent hybridization on overall genome evolution of this important wheat pathogen

A thousand-genome panel retraces the global spread and adaptation of a major fungal crop pathogen

Human activity impacts the evolutionary trajectories of many species worldwide. Global trade of agricultural goods contributes to the dispersal of pathogens reshaping their genetic makeup and providing opportunities for virulence gains. Understanding how pathogens surmount control strategies and cope with new climates is crucial to predicting the future impact of crop pathogens. Here, we address this by assembling a global thousand-genome panel of Zymoseptoria tritici, a major fungal pathogen of wheat reported in all production areas worldwide. We identify the global invasion routes and ongoing genetic exchange of the pathogen among wheat-growing regions. We find that the global expansion was accompanied by increased activity of transposable elements and weakened genomic defenses. Finally, we find significant standing variation for adaptation to new climates encountered during the global spread. Our work shows how large population genomic panels enable deep insights into the evolutionary trajectory of a major crop pathogen

Interspecific gene exchange as a driver of adaptive evolution in fungi

Throughout evolutionary history in the kingdom Fungi, taxa have exchanged genetic information among species, as revealed in particular by analyses of genome sequences. In fungi, hybridization can occur by sexual mating or by fusion of vegetative structures giving rise to new species or leaving traces of introgression in the genome. Furthermore, gene exchange can occur by horizontal gene transfer between species and can even include organisms outside the kingdom Fungi. In several cases, interspecific gene exchange has been instrumental in rapid adaptive evolution of fungal species and has notably played a role in the emergence of new pathogens. Here we summarize mechanisms and examples of gene exchange in fungi with a particular focus on the genomic context. We emphasize the need for and potential of applying population genetic approaches to better understand the processes and the impact of interspecific gene exchange in rapid adaptive evolution and species diversification. The broad occurrence of gene exchange among fungal species challenges our species concepts in the kingdom Fungi. Expected final online publication date for the Annual Review of Microbiology Volume 72 is September 8, 2018. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates

Crop-to-wild gene flow and its fitness consequences for a wild fruit tree: towards a comprehensive conservation strategy of the wild apple in Europe

Abstract Crop-to-wild gene flow can reduce the fitness and genetic integrity of wild species. Malus sylvestris, the European crab-apple fruit tree in particular, is threatened by the disappearance of its habitat and by gene flow from its domesticated relative, Malus domestica. With the aims of evaluating threats for M. sylvestris and of formulating recommendations for its conservation, we studied here, using microsatellite markers and growth experiments: (i) hybridization rates in seeds and trees from a French forest and in seeds used for replanting crab apples in agrosystems and in forests, (ii) the impact of the level of M. domestica ancestry on individual tree fitness and (iii) pollen dispersal abilities in relation to crop-to-wild gene flow. We found substantial contemporary crop-to-wild gene flow in crab-apple tree populations and superior fitness of hybrids compared to wild seeds and seedlings. Using paternity analyses, we showed that pollen dispersal could occur up to 4 km and decreased with tree density. The seed network furnishing the wild apple reintroduction agroforestry programmes was found to suffer from poor genetic diversity, introgressions and species misidentification. Overall, our findings indicate supported threats for the European wild apple steering us to provide precise recommendations for its conservation

Crop-to-wild gene flow and its fitness consequences for a wild fruit tree : Towards a comprehensive conservation strategy of the wild apple in Europe

Crop-to-wild gene flow can reduce the fitness and genetic integrity of wild species. Malus sylvestris, the European crab-apple fruit tree in particular, is threatened by the disappearance of its habitat and by gene flow from its domesticated relative, Malus domestica. With the aims of evaluating threats for M.sylvestris and of formulating recommendations for its conservation, we studied here, using microsatellite markers and growth experiments: (i) hybridization rates in seeds and trees from a French forest and in seeds used for replanting crab apples in agrosystems and in forests, (ii) the impact of the level of M.domestica ancestry on individual tree fitness and (iii) pollen dispersal abilities in relation to crop-to-wild gene flow. We found substantial contemporary crop-to-wild gene flow in crab-apple tree populations and superior fitness of hybrids compared to wild seeds and seedlings. Using paternity analyses, we showed that pollen dispersal could occur up to 4km and decreased with tree density. The seed network furnishing the wild apple reintroduction agroforestry programmes was found to suffer from poor genetic diversity, introgressions and species misidentification. Overall, our findings indicate supported threats for the European wild apple steering us to provide precise recommendations for its conservation

Data from: Crop-to-wild gene flow and its fitness consequences for a wild fruit tree: towards a comprehensive conservation strategy of the wild apple in Europe

Crop-to-wild gene flow can reduce the fitness and genetic integrity of wild species. Malus sylvestris, the European crabapple fruit tree, in particular is threatened by the disappearance of its habitat and by gene flow from its domesticated relative, Malus domestica. With the aims of evaluating threats for M. sylvestris and of formulating recommendations for its conservation, we studied here, using microsatellite markers and growth experiments: i) hybridization rates in seeds and trees from a French forest and in seeds used for replanting crabapples in agrosystems and in forests, ii) the impact of the level of M. domestica ancestry on individual fitness tree, and iii) pollen dispersal abilities in relationship with crop-to-wild gene flow. We found substantial contemporary crop-to-wild gene flow in crabapple tree populations and superior fitness of hybrids compared to wild seeds and seedlings. Using paternity analyses, we showed that pollen dispersal could occur up to 4 km and decreased with tree density. The seed network furnishing the wild apple reintroduction agroforestry programs was found to suffer from poor genetic diversity, introgressions, and species misidentification. Overall, our findings indicate supported threats for the European wild apple steering us to provide precise recommendations for its conservation

Population genetic structure of four regional populations of the barley pathogen Pyrenophora teres f. maculata in Iran is characterized by high genetic diversity and sexual recombination

The leaf spot form of the barley disease net blotch, caused by the fungus Pyrenophora teres f. maculata (PTM), is an increasingly important foliar disease of barley. Studies of population genetic structure and reproductive mode are necessary to make predictions of the evolutionary potential of the pathogen. Sources of resistance to PTM have been found in Iranian landraces, which may have the potential to improve plant breeding efforts. However, little is known about the population genetic structure of this fungus in Iran. In this study, we analysed the frequency of the mating type genes to assess the potential for sexual mating of PTM collected from four provinces-Khuzestan, Hamadan, Golestan, and East Azerbaijan-and we investigated the population genetic structure using seven simple sequence repeat markers. High genotype diversity, linkage equilibrium, and equal ratios of mating types frequencies in the PTM populations at Khuzestan and Hamadan support the occurrence of sexual reproduction in these populations, while in Golestan and East Azerbaijan populations, significant gametic disequilibrium and relatively low genotype diversity suggest a higher incidence of clonality or different demographic histories. Unequal mating type frequencies in Golestan confirm a predominance of asexual reproduction. Finally, we found significant evidence for strong population structure with most of the genetic variation represented within regional populations (89%). Overall, our study provides evidence for high genetic variation in Iranian PTM populations, which may be the basis for rapid adaptive evolution in this pathosystem. This highlights the need for integrated efforts to control the disease