Biology subjects

Hartmann, F. E.

Publications and source records attributed to Hartmann, F. E..

12 recordsLinked to original sources

bioRxiv2026

Recombination persists near the mating-type locus in pseudo-homothallic Cladorrhinum fungi (Sordariales)

Recombination suppression has evolved repeatedly across eukaryotes around sex-determining and mating-type loci. Recent theoretical models proposed that such suppression can evolve due to various effects of recessive deleterious mutations, predicting that it should only evolve in lineages experiencing extended diploid phases. Ascomycete fungi provide a powerful system to test this prediction, as pseudo-homothallic ascomycetes maintain prolonged diploid-like phases, while most other ascomycetes have a predominant haploid phase. Megabase-scale non-recombining regions have in fact been reported around the mating-type locus in the four pseudo-homothallic ascomycete lineages studied to date. Here, we studied a previously unexplored lineage of Sordariales, formerly referred to as Podospora australis and suggested to be pseudo-homothallic. Combining genome sequencing, phylogenomic analyses and life-cycle characterization, we identified and described two distinct species and reassigned them to the Cladorrhinum genus. We showed that the two species produce large proportions of self-fertile ascospore-derived mycelia, but the frequencies varied substantially among four strains, and with a selfing progeny, indicating large variation in the extent of the diploid-like phase. By analysing the genomes of five wild strains and of selfing progenies, we did not detect any footprints of large recombination suppression (no heterozygosity, rearrangements or repeated elements). This may be due to the smaller proportion of the life cycle spent in a diploid-like stage compared to other pseudo-homothallic species, or to other features of the life cycle, in agreement with theoretical models. In addition, our results decouple the evolution of pseudo-homothallism from that of recombination suppression, showing that there is no fundamental developmental constraint forcing their joint evolution.

evolutionary biology↗

bioRxiv2025

Stepwise recombination suppression around the mating-type locus associated with a diploid-like life cycle in Schizothecium fungi

Recombination suppression often evolves around sex-determining loci and extends stepwise, resulting in adjacent regions with different levels of divergence between sex chromosomes, called evolutionary strata. In Ascomycota fungi, evolutionary strata have been found around the mating-type (MAT) locus only in pseudo-homothallic species, i.e., with a diploid-like lifecycle and mycelia carrying nuclei of both mating types. In contrast, no recombination suppression has been observed in fungi with a haploid-like lifecycle, such as heterothallic fungi (with mycelial colonies of a single mating type each). Here, we investigated the evolution of recombination suppression in a clade of dung fungi encompassing 16 pseudo-homothallic and three heterothallic sibling species from the Schizothecium genus (Ascomycota, Sordariales). The analysis of genetic divergence based on genome sequencing indicated recombination suppression around the MAT locus in all investigated 13 pseudo-homothallic species. The non-recombining region ranged from 600 kb to 1.6 Mb and harbored multiple evolutionary strata, varying in size and number among species. The separation of alleles associated with alternative mating types in gene genealogies across strains within species, the high linkage disequilibrium and an inversion in one species supported the lack of recombination in the MAT-proximal region in pseudo-homothallic species. The overall lack of trans-specific polymorphism suggested multiple independent events of recombination suppression or the occurrence of rare events of recombination or genic conversion. Progeny analyses showed the occurrence of recombination close to the MAT locus in heterothallic strains. We thus revealed here multiple and likely independent evolutionary strata, associated with an extended diploid-like stage in Schizothecium fungi, which provides a good model for research on sex-related chromosome evolution.

evolutionary biology↗

bioRxiv2025

Huge genetic diversity of Schizothecium tetrasporum (Wint.). N. Lundq.: delimitation of 18 species distributed into three complexes through genome sequencing

Analyses of the genetic diversity of well-studied fungi of the Sordariales order, such as Neurospora spp. and Podospora anserina (syn. Triangularia anserina), have shown that the species classically defined by morphology are often complexes of cryptic species. Here, we report on the species delimitation among 76 strains producing mycelium and sexual reproductive structures identical to those of the pseudo-homothallic Sordariales species Schizothecium tetrasporum (syn. Neoschizothecium tetrasporum). Their whole genomes were sequenced as well as those of six strains closely related to Schizothecium tetrasporum but producing eight-spored asci instead of four-spored ones. The clustering based on the Average Nucleotide Identity (ANI) between the genomes identified eighteen species grouped into three clades, which were further supported by a phylogenetic tree constructed with whole genome Single Nucleotide Polymorphisms (SNPs). Based on their contrasting breeding systems and their large evolutionary distances, we considered the three clades as distinct species complexes. Indeed, two of them, the Schizothecium tetrasporum and Schizothecium pseudotetrasporum complexes, contains pseudo-homothallic species producing four-spored asci, while the third one, which we named Schizothecium octosporum, contains heterothallic species producing eight-spored asci. Surprisingly it was nestled between the two complexes of pseudo-homothallic species. Our data reveals thus a huge genetic diversity of the Schizothecium tetrasporum morpho-species and a convergent evolution of pseudo-homothallism or reversion to heterothallism within the complexes. An epitype for Schizothecium tetrasporum sensus stricto is defined and the seventeen new Schizothecium species are formally described.

microbiology↗

bioRxiv2024

Sheltered load in fungal mating-type chromosomes revealed by fitness experiments

Sex chromosomes and mating-type chromosomes can carry large regions with suppressed recombination. As a result of a lower efficacy of selection, recessive deleterious mutations are expected to accumulate in these non-recombining regions. Multiple genomic analyses have indirectly inferred the presence of deleterious mutations in sex and mating-type chromosomes, but direct experimental evidence remains scarce. Here, we performed fitness assays in fungi with megabase-large and young non-recombining regions around the mating-type locus, using three Sordariales species, to test whether heterokaryons (diploid-like, heterozygous at the mating-type locus) exhibited a fitness advantage over homokaryons (haploid-like, with a single mating-type allele), in terms of spore germination dynamics or mycelium growth speed, under different conditions of light and temperature. We found a faster growth of heterokaryons compared to one of the homokaryons for Podospora anserina at 18{degrees}C and for Schizothecium tetrasporum and Schizothecium tritetrasporum at 22{degrees}C under light. These findings suggest the presence of a sheltered load, i.e., recessive deleterious mutations at the heterozygous state in or near non-recombining regions, associated to a specific mating-type allele. Genomic analyses indeed suggested that the non-recombining regions around the mating-type locus likely carries heterozygous deleterious mutations, while the rest of the genome was mostly homozygous. We also showed that the difference in growth rates did not result from different numbers or densities of nuclei between homokaryons and heterokaryons. Leveraging the experimental assets of fungi, allowing cultivating separately haploid-like and diploid-like life stages, our experiments provided one of the rare direct experimental evidence of sheltered load around mating-compatibility loci, which is crucial for our understanding of sex-related chromosome evolution. Social Media AbstractExperimental evidence for sheltered load around the mating-type locus in filamentous fungi: slower growth of haploid versus diploid-like mycelia, revealing recessive deleterious mutations, in Podospora anserina and other Sordariales fungi.

evolutionary biology↗

bioRxiv2024

Million years old recombination suppression and balancing selection in a region linked to the mating-type locus in the invasive chestnut blight fungal pathogen Cryphonectria parasitica

Recombination suppression can evolve in sex or mating-type chromosomes, or in autosomal supergenes, with different haplotypes being maintained by balancing selection. In the invasive chestnut blight fungus Cryphonectria parasitica, a genomic region was suggested to lack recombination and to be partially linked to the mating-type (MAT) locus based on segregation analyses. Using hundreds of available C. parasitica genomes and generating new high-quality genome assemblies, we show that a ca. 1.2 Mb genomic region proximal to the mating-type locus lacks recombination, with the segregation of two highly differentiated haplotypes in balanced proportions in invasive populations. High-quality genome assemblies further revealed an inversion in one of the haplotypes in the invaded range. The two haplotypes were estimated to have diverged 1.5 million years ago, and each harboured specific genes, some of which likely belonging to Starship elements, that are large mobile elements, mobilized by tyrosine recombinases, able to move accessory genes, and involved in adaptation in multiple fungi. The MAT-proximal region carried genes upregulated under virus infection or vegetative incompatibility reaction. In the native range, the MAT-proximal region also appeared to have a different evolutionary history than the rest of the genome. In all continents, the MAT-Proximal region was enriched in non-synonymous substitutions, in gene presence/absence polymorphism, in tyrosine recombinases and in transposable elements. This study thus sheds light on a case of a large non-recombining region partially linked to a mating compatibility locus, with likely balancing selection maintaining differentiated haplotypes, possibly involved in adaptation in a devastating tree pathogen.

evolutionary biology↗

bioRxiv2023

High-quality genome assemblies of four members of the Podospora anserina species complex

The filamentous fungus Podospora anserina is a model organism used extensively in the study of molecular biology, senescence, prion biology, meiotic drive, mating-type chromosome evolution, and plant biomass degradation. It has recently been established that P. anserina is a member of a complex of seven, closely related species. In addition to P. anserina, high-quality genomic resources are available for two of these taxa. Here we provide chromosome-level annotated assemblies of the four remaining species of the complex, as well as a comprehensive dataset of annotated assemblies from a total of 28 Podospora genomes. We find that all seven species have genomes of around 35 Mbp arranged in seven chromosomes that are mostly collinear and less than 2% divergent from each other at genic regions. We further attempt to resolve their phylogenetic relationships, finding significant levels of phylogenetic conflict as expected from a rapid and recent diversification. SignificanceHere we provide a dataset of 28 annotated genomes from the P. anserina species complex, including chromosome-level assemblies of four species that lacked a reference genome. With this dataset in hand, biologists can take advantage of the molecular tools available for P. anserina to study evolutionary dynamics at the interphase between micro- and macroevolution, with particular emphasis on trait evolution, genome architecture, and speciation.

genomics↗

bioRxiv2020

Machine-learning predicts genomic determinants of meiosis-driven structural variation in a eukaryotic pathogen

Species harbor extensive structural variation underpinning recent adaptive evolution and major disease phenotypes. Most sequence rearrangements are generated non-randomly along the genome through non-allelic recombination and transposable element activity. However, the causality between genomic features and the induction of new rearrangements is poorly established. Here, we analyze a global set of telomere-to-telomere genome assemblies of a major fungal pathogen of wheat to establish a nucleotide-level map of structural variation. We show that the recent emergence of pesticide resistance has been disproportionally driven by rearrangements. We used machine-learning to train a model on structural variation events based on 30 chromosomal sequence features. We show that base composition and gene density are the major determinants of structural variation. Low-copy LINE and Gypsy retrotransposons explain most inversion, indel and duplication events. We retrain our model on Arabidopsis thaliana and show that our modelling approach can be extended to more complex genomes. Finally, we analyzed complete genomes of haploid offspring in a four-generation pedigree. Meiotic crossover locations were enriched for newly generated structural variation consistent with crossovers being mutational hotspots. The model trained on species-wide structural variation predicted the position of >74% of the newly generated variants along the pedigree. The predictive power highlights causality between specific sequence features and the induction of chromosomal rearrangements. Our work demonstrates that training sequence-derived models can accurately identify regions of intrinsic DNA instability in eukaryotic genomes.

genomics↗

bioRxiv2020

Mapping the adaptive landscape of a major agricultural pathogen reveals evolutionary constraints across heterogeneous environments

The adaptive potential of pathogens in novel or heterogeneous environments underpins the risk of disease epidemics. Antagonistic pleiotropy or differential resource allocation among life-history traits can constrain pathogen adaptation. However, we lack understanding how the genetic architecture of individual traits can generate trade-offs. Here, we report a large-scale study based on 145 global strains of the fungal wheat pathogen Zymoseptoria tritici from four continents. We measured 50 life-history traits, including virulence and reproduction on 12 different wheat hosts and growth responses to several abiotic stressors. To elucidate the genetic basis of adaptation, we used multi-trait genome-wide association mapping. We show that most traits are governed by polygenic architectures and are highly heritable suggesting that adaptation proceeds mainly through allele frequency shifts at many loci. We identified numerous pleiotropic SNPs with conflicting effects on host colonization and survival in stressful environments. Such genetic constraints are likely limiting the pathogens ability to cause host damage and could be exploited for pathogen control. In contrast, adaptation to abiotic stress factors was likely facilitated by synergistic pleiotropy. Our study illustrates how comprehensive mapping of life-history trait architectures across diverse environments allows to predict evolutionary trajectories of pathogens confronted with environmental perturbations.

evolutionary biology↗

bioRxiv2020

A population-level invasion by transposable elements in a fungal pathogen

AO_SCPLOWBSTRACTC_SCPLOWGenome evolution is driven by the activity of transposable elements (TEs). The spread of TEs can have deleterious effects including the destabilization of genome integrity and expansions. However, the precise triggers of genome expansions remain poorly understood because genome size evolution is typically investigated only among deeply divergent lineages. Here, we use a large population genomics dataset of 284 individuals from populations across the globe of Zymoseptoria tritici, a major fungal wheat pathogen. We built a robust map of genome-wide TE insertions and deletions to track a total of 2,456 polymorphic loci within the species. We show that purifying selection substantially depressed TE frequencies in most populations but some rare TEs have recently risen in frequency and likely confer benefits. We found that specific TE families have undergone a substantial genome-wide expansion from the pathogens center of origin to more recently founded populations. The most dramatic increase in TE insertions occurred between a pair of North American populations collected in the same field at an interval of 25 years. We find that both genome-wide counts of TE insertions and genome size have increased with colonization bottlenecks. Hence, the demographic history likely played a major role in shaping genome evolution within the species. We show that both the activation of specific TEs and relaxed purifying selection underpin this incipient expansion of the genome. Our study establishes a model to recapitulate TE-driven genome evolution over deeper evolutionary timescales.

genomics↗

bioRxiv2020

Congruent population genetic structures and divergence histories in anther-smut fungi and their host plants Silene italica and the S. nutans species complex

The study of population genetic structure congruence between hosts and pathogens gives important insights into their shared phylogeographic and coevolutionary histories. We studied the population genetic structure of castrating anther-smut fungi (Microbotryum genus) and of their host plants, the Silene nutans species complex, and the morphologically and genetically close S. italica, which can be found in sympatry. Phylogeographic population genetic structure related to persistence in separate glacial refugia has been recently revealed in the S. nutans plant species complex across Western Europe, identifying several distinct lineages. We genotyped 171 associated plant-pathogen pairs of anther-smut fungi and their host plant individuals using microsatellite markers and plant chloroplastic SNPs. We found clear differentiation between fungal populations parasitizing S. nutans and S. italica plants. The population genetic structure of fungal strains parasitizing the S. nutans plant species complex mirrored the host plant genetic structure, suggesting that the pathogen was isolated in glacial refugia together with its host and/or that it has specialized on the plant genetic lineages. Using random forest approximate Bayesian computation (ABC-RF), we found that the divergence history of the fungal lineages on S. nutans was congruent with the one previously inferred for the host plant and likely occurred with ancient but no recent gene flow. Genome sequences confirmed the genetic structure and the absence of recent gene flow between fungal genetic lineages. Our analyses of host-pathogen individual pairs contribute to a better understanding of co-evolutionary histories between hosts and pathogens in natural ecosystems, in which such studies are still scarce.

evolutionary biology↗

bioRxiv2018

Transposable element insertions shape gene regulation and melanin production in a fungal pathogen

Background\n\nVariation in gene expression contributes to phenotypic diversity within species and adaptation. However, very few cases of adaptive regulatory changes have been reported and the mechanisms underlying variation in gene expression remain largely unexplored. Fungal pathogen genomes are highly plastic and harbour numerous insertions of transposable elements, which can potentially contribute to gene expression regulation. In this work we elucidated how transposable elements contribute to variation of melanin accumulation, a quantitative adaptive trait of fungal pathogens that is involved in survival under stress conditions.\n\nResults\n\nWe demonstrated that differential transcriptional regulation of the gene encoding the transcription factor Zmr1, which controls expression of the genes in the melanin biosynthetic gene cluster, is responsible for variation in melanin accumulation in the fungal plant pathogen Zymoseptoria tritici. We show that differences in melanin levels between two strains of Z. tritici are due to two levels of transcriptional regulation: 1) variation in the promoter sequence of Zmr1, and 2) an insertion of transposable elements upstream of the Zmr1 promoter. Remarkably, independent insertions of transposable elements upstream of Zmr1 occurred in 9% of Z. tritici strains from around the world and negatively regulated Zmr1 expression, contributing to melanin accumulation variation.\n\nConclusions\n\nOur studies demonstrate that different layers of transcriptional control fine-tune the synthesis of melanin. These regulatory mechanisms potentially evolved to balance the fitness costs associated with melanin production against its positive contribution to survival in stressful environments.

molecular biology↗

bioRxiv2018

A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch

O_LICultivar-strain specificity in the wheat-Zymoseptoria tritici pathosystem determines the infection outcome and is controlled by resistance genes on the host side, of which many have been identified. However, on the pathogen side, the molecular determinants of specificity are largely unknown.\nC_LIO_LIWe used genetic mapping, targeted gene disruption and allele swapping to characterize the recognition of the new avirulence factor Avr3D1. We then combined population genetic and comparative genomic analyses to estimate the evolutionary trajectory of Avr3D1.\nC_LIO_LIAvr3D1 is specifically recognized by cultivars harboring the resistance gene Stb7 and triggers a strong defence response without preventing pathogen infection and reproduction. Avr3D1 resides in a cluster of putative effector genes located in a region populated by independent transposable element insertions. The gene is present in all 132 investigated strains and is highly polymorphic, with a total of 30 different protein variants. We demonstrated that certain amino acid mutations in Avr3D1 led to evasion of recognition.\nC_LIO_LIThese results demonstrate that quantitative resistance and gene-for-gene interactions are not mutually exclusive per se. Location of avirulence genes in highly plastic genomic regions likely facilitates accelerated evolution that enables escape from recognition by resistance proteins.\nC_LI

plant biology↗