Biology subjects

Giraud, T.

Publications and source records attributed to Giraud, T..

At least 19 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↗

bioRxiv2026

Cheese adaptation beyond Penicillium: contrasting genomic trajectories in the distantly related Nectriaceae molds

Fungal domestication provides a powerful framework for understanding adaptation to human-made environments, yet genomic studies of cheese-associated fungi have largely focused on Penicillium molds. Here, we investigated cheese-associated Nectriaceae, a phylogenetically distant fungal lineage of ascomycetes, by comparing genomes of nine cheese isolates, belonging to five species, with 22 relatives from other environments. Comparative genomic analyses revealed strikingly contrasting evolutionary trajectories in the two cheese-associated genera. Longinectria showed extensive gene family expansions and duplications, particularly affecting nutrient transport, specialised metabolism and fungal recognition, whereas cheese-associated Bisifusarium exhibited genome reduction and contraction of many of the same functional systems. In Bisifusarium domesticum, these reductions extended to biosynthetic gene clusters, carbohydrate-active enzymes and peptidases, consistent with ecological specialisation. We further identified a 75-kb region with >98% nucleotide identity between two cheese-associated Bisifusarium species, strongly supporting recent horizontal transfer. This region contains several genes involved in ion transport and salt tolerance, including functions previously identified in horizontally transferred regions of cheese-associated Penicillium populations. Together, our results reveal multiple genomic routes to cheese association and highlight gene-family turnover, adaptive protein evolution and horizontal gene transfer as complementary mechanisms shaping fungal evolution in anthropogenic environments.

evolutionary biology↗

bioRxiv2026

A recent domestication event in Penicillium biforme, independent of the emblematic cheese mold P. camemberti

Domestication of molds for cheese production has repeatedly shaped Penicillium fungi, most notably giving rise to the emblematic P. camemberti lineage, derived from P. biforme. Here, we identified a new P. biforme lineage, named cheesy, likely selected from P. biforme for food fermentation, including cheese and sausage production. This lineage exhibits evidence of a severe bottleneck, with little nucleotide polymorphism and a single mating type. The cheesy lineage has evolved advantageous traits for cheesemaking: compared to other P. biforme strains and its wild relative P. fuscoglaucum, it displays faster growth on cheese, galactose and lactose media, higher sporulation and germination rates on cheese, elevated lipolytic activity, enhanced inhibition capacities, and produced specific volatile organic compounds. Additionally, P. camemberti and P. biforme cheesy differ in their content of Starship mobile elements, acquired through horizontal transfers. These elements carry cargo genes potentially relevant for adaptation to cheese. Notably, the cheesy lineage has acquired a 20 kb Starship element (Rattus), nested within a much larger 160 kb Starship (Bilge), and carrying cargo genes with predicted functions involved in antagonistic interactions among micro-organisms. SignificanceO_LIWe identified a new Penicillium biforme lineage, named cheesy, which was likely selected from P. biforme for food fermentation (cheese and sausage), genetically and phenotypically different from the emblematic P. camemberti lineage. This lineage suffered from a severe bottleneck, displaying very little nucleotide polymorphism and a single mating type. C_LIO_LIThis newly identified lineage has evolved advantageous traits for cheesemaking; compared to other P. biforme strains and its wild relative P. fuscoglaucum, it displayed faster growth on cheese, galactose and lactose media, higher sporulation and germination rates on cheese, higher lipolytic activity, better inhibition capacities and specific volatile organic compounds. C_LIO_LIPenicillium camemberti and P. biforme cheesy also differed by their content in Starship mobile elements, acquired through horizontal transfers, and carrying cargo genes potentially relevant for adaptation to cheese. C_LIO_LINotably, the cheesy lineage has acquired a specific 20 kb Starship nested within a much larger 160 kb Starship, and likely involved in antagonistic interactions. C_LI

evolutionary biology↗

bioRxiv2026

The fate of mutations on Y chromosomes andautosomes: a unified Wright-Fisher frameworkaccounting for segregation time

Understanding how mutations evolve on Y chromosomes is central to explaining the origin, diversity and persistence of sex chromosomes. Mutations occurring on the Y chromosome in sexual populations experience selective dynamics that differ markedly from those on autosomes, due to a reduced effective population size and the presence of large non-recombining regions containing alleles maintained in a permanently heterozygous state. These specific features alter gene transmission in the Y chromosome population compared to autosomes, even within the same pedigree. Here, we provide a two-sex diploid Wright-Fisher model that explicitly incorporates both sex chromosomes and autosomes within a unified population framework, in order to capture the influence of these specificities on the fate of mutations, not only considering fixation probabilities but also segregation times. We use diffusion approximations and provide analytical and numerical tools to compute these quantities across a wide range of parameters and selection regimes. We recover classical results on fixation probabilities in various scenarios, including purely beneficial, deleterious or overdominant mutations, and extend them in the light of mean segregation time, a key but often overlooked determinant of evolutionary outcomes over finite timescales. In particular, our analyses show that overdominant mutations are overall more likely to fix in observable time windows on the Y chromosome than on autosomes. Individual-based simulations corroborate our approximations and highlight parameter regimes where the theoretical approach is particularly useful, especially for parameter values inducing long segregation times or small fixation probabilities, for which simulations are impractical. Our results provide a comprehensive and tractable framework for clarifying how chromosome-specific features shape evolutionary dynamics beyond fixation probabilities alone.

evolutionary biology↗

bioRxiv2026

Rapid speciation in small populations challenges the dominance of ecological speciation

Speciation - the process by which two lineages become reproductively isolated - plays a key role in the emergence and maintenance of biodiversity. Yet, our understanding of the time it takes for speciation to occur, and of the microevolutionary processes that influence this tempo, remains limited. Here, we thoroughly characterize how population size, mutation rate, local adaptation and migration are expected to influence the duration of speciation, as well as the shape of the "grey zone" of speciation. We show that the relationship between population size and speciation time is indicative of the speciation mode, as faster speciation in smaller populations only occurs in the case of non-ecological speciation. Leveraging genomic estimates of population size and speciation duration across 196 pairs of plant species, we uncover a positive association between population size and speciation duration. Taken together, these results challenge the view that ecological speciation is the source of much of species diversity.

evolutionary biology↗

bioRxiv2025

Stepwise expansion of recombination suppression on sex chromosomes and other supergenes through lower load advantage and deleterious mutation sheltering

Many organisms possess sex chromosomes with non-recombining regions that have expanded progressively. Yet, the causes of this stepwise expansion remain poorly understood. Here, using mathematical modeling and stochastic simulations, we show that the widespread presence of deleterious recessive mutations in genomes can generate several phenomena that can contribute to the evolution of recombination suppression on sex chromosomes. We demonstrate that a significant proportion of new chromosomal inversions, or any other recombination suppressor, are initially advantageous because they carry fewer mutations than average. However, these less-loaded inversions generally fail to fix on autosomes because, as their frequency increases, the recessive deleterious mutations they carry are more likely to occur in a homozygous state, leading to a selective disadvantage. In contrast, the permanent heterozygosity of Y-like sex chromosomes shelters their inversions from this disadvantage, facilitating their fixation and thereby the stepwise expansion of non-recombining regions. Due to this sheltering effect, we show that fixation probabilities are substantially higher on Y-like chromosomes than on autosomes across a wide range of parameters, particularly when segregating deleterious mutations are moderately to strongly recessive, and this is true even after controlling for differences in effective population sizes between those chromosomes. Then, once recombination is suppressed, deleterious mutations accumulate on inversions, which could select for recombination restoration. However, we show that the accumulation of overlapping genomic rearrangements following recombination suppression can prevent its restoration. Overall, our theoretical model proposes a testable framework that may contribute to explaining evolutionary strata on sex and mating-type chromosomes, and other supergenes.

evolutionary biology↗

bioRxiv2025

Loci under balancing selection facilitate the emergence of pseudo-overdominance and recombination suppression

Loci under strong balancing selection, such as sex-determining, mating-type, and self-incompatibility loci, are frequently flanked by regions of suppressed recombination. The reasons why recombination suppression evolves around these loci remain poorly understood. Here, we propose that one reason may be that loci under balancing selection facilitate the emergence of pseudo-overdominance, a phenomenon under which linked partially recessive deleterious mutations in repulsion mimic overdominance. Pseudo-overdominance arises when linkage disequilibrium gradually builds up between recessive deleterious mutations, often due to strong genetic linkage and genetic drift. Once complementary haplotypes form, homozygous and recombinant offspring are selected against because they carry homozygous recessive deleterious mutations. Using individual-based simulations, we demonstrate here that the presence of loci under balancing selection eases the establishment of pseudo-overdominance, by facilitating the maintenance of partially recessive deleterious mutations and linkage disequilibrium in their flanking regions. This occurs particularly in regions with low recombination rates and a high load of partially recessive deleterious mutations, which can be found in specific genomic regions in natural populations. We further show that such resulting pseudo-overdominance can render more likely the evolution of recombination suppression around permanently heterozygous loci, preventing the creation of unfit homozygous recombinant offspring. These results suggest new avenues for understanding the evolution of loci under balancing selection, sex chromosomes and supergenes, and shed new light on the mechanisms driving genome 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↗

bioRxiv2025

EASYstrata: a new workflow to infer evolutionary strata along sex chromosomes and other supergenes

New reference genomes and transcriptomes are increasingly available across the tree of life, opening new avenues to tackle exciting questions. However, there are still challenges associated with annotating genomes and inferring evolutionary processes and with a lack of methodological standardisation. Here, we propose a new workflow designed for evolutionary analyses to overcome these challenges, facilitating the detection of recombination suppression and its consequences in terms of rearrangements and transposable element accumulation. To do so, we assemble multiple bioinformatic steps in a single easy-to-use workflow. We combine state-of-the-art tools to detect transposable elements, annotate genomes, infer gene orthology relationships, compute divergence between sequences, infer evolutionary strata (i.e., footprints of stepwise extension of recombination suppression) and their structural rearrangements, and visualise the results. This workflow, called EASYstrata, was applied to reannotate 42 published genomes from Microbotryum fungi. We show in further case examples from a plant and an animal that we recover the same strata as previously described. While this tool was developed with the goal to infer divergence between sex or mating-type chromosomes, it can be applied to any pair of haplotypes whose patteern of divergence is of interest. This workflow will facilitate the study of non-model species for which newly sequenced phased diploid genomes are becoming available. Contactquentinrougemont@orange.fr

genomics↗

bioRxiv2024

Genetic differentiation in the MAT-proximal region is not sufficient for suppressing recombination in Podospora anserina

Recombination is advantageous over the long-term, as it allows efficient selection and purging deleterious mutations. Nevertheless, recombination suppression has repeatedly evolved in sex chromosomes and mating-type chromosomes. The evolutionary causes for recombination suppression and the proximal mechanisms preventing crossing overs are still poorly understood. Several hypotheses have recently been suggested based on theoretical models, and in particular, that divergence could accumulate neutrally around a sex-determining region and reduce recombination rates, a self-reinforcing process that could foster progressive extension of recombination suppression. The ascomycete fungus Podospora anserina is an excellent model for investigating these questions. A 0.8 Mb region around the mating-type locus is non-recombining, despite being collinear between the two mating types. This fungus is mostly selfing, so that strains are highly homozygous, except in the non-recombining region around the mating-type locus that displays differentiation between mating types. Here, we generated a mutant to test the hypothesis that sequence divergence alone is responsible for recombination cessation. We replaced the mat-idiomorph by the sequence of the mat+ idiomorph, to obtain a strain that is sexually compatible with the mat-reference strain and isogenic to this strain in the MAT-proximal region. Crosses showed that recombination was still suppressed in the MAT-proximal region in the mutant strains, indicating that other proximal mechanisms than inversions or mere sequence divergence are responsible for recombination suppression in this fungus. This finding suggests that selective mechanisms likely acted for suppressing recombination, as the neutral model does not seem to hold, at least in this fungus. ARTICLE SUMMARYIn many organisms, a non-recombining region is observed around the sex-determining locus. In the fungus Podospora anserina, recombination is suppressed within an 800kb region around the mating-type locus. In natural strains, the genome is isogenic between two mating-types, except in this region displaying heterozygosity. To determine if this heterozygosity can be responsible for the lack of recombination, compatible strains were engineered to be isogenic, including in the non-recombining region. Recombination inhibition persisted, indicating that mere sequence divergence does not cause recombination suppression. Our study provides an interesting insight on the molecular and evolutionary causes of recombination inhibition.

genetics↗

bioRxiv2024

Deleterious mutations can contribute to the evolution of recombination suppression between sex chromosomes

Many organisms have sex chromosomes with large non-recombining regions that expand in a stepwise manner, although the underlying reasons remain poorly understood. Recently, we proposed that recombination suppression may evolve in sex chromosomes simply because of the presence of recessive deleterious mutations within genomes. Specifically, we demonstrated that chromosomal inversions suppressing recombination and carrying by chance fewer deleterious mutations than average have a selective advantage. In addition, we showed that the permanent heterozygosity of Y-like sex chromosomes facilitates the fixation of these less-loaded inversions by a sheltering effect, i.e., by preventing the expression of recessive deleterious mutations in a homozygous state when they increase in frequency. In contrast, similar less-loaded inversions in autosomes suffer from a disadvantage in the homozygous state as their frequency increases, preventing their fixation. However, the methodology and significance of our previous study have been questioned. Here, we present new analyses that further reinforce our original claims, demonstrating that the lower-load advantage and the sheltering effect can explain the fixation of inversions on sex chromosomes over a broad range of parameter values. We show that these mechanisms promote the fixation of inversions on Y-like chromosomes at rates exceeding those expected under drift alone. We used, as a control, autosomes with a similar population size as the Y chromosome, which, we argue, provides the appropriate neutral control for the sheltering effect. We also address criticisms regarding our focus on inversions surviving the first 20 generations in a figure of our previous study, and show that these criticisms stemmed from a misunderstanding of what this figure was intended to illustrate. Including all inversions, even those that went extinct within 20 generations, does not alter our conclusions. Overall, the present study offers new support for our theory based on the combination of lower-load advantage and sheltering effect, and addresses the questions about its significance and range of applicability.

evolutionary biology↗

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

A theoretical framework linking the birth-death and protracted birth-death models, with implications for the phylogenetic analysis of diversification

Standard birth-death processes used in macroevolutionary studies assume instantaneous speciation, an unrealistic premise that limits the interpretation of speciation and extinction rates. The protracted birth-death (PBD) model instead assumes that speciation involves two steps: initiation and completion. In order to understand their respective influence on macroevolutionary speciation rates, we compute a standard time-varying birth-death scenario that is "equivalent" to the PBD model in terms of speciation and extinction probabilities. First, we find a sharp decline in the equivalent birth rate near the present, indicating that rates estimated at the tips of phylogenies may not accurately reflect the underlying speciation process. Second, the completion rate controls the timing of the decay rather than the asymptotic equivalent rates. The equivalent birth rate in the past scales with the speciation initiation rate, with a scaling factor depending mostly on the population extinction rate. Our results suggest that the rates of population formation and extinction may often play a larger role than the speed of accumulation of reproductive isolation in modulating speciation rates. Our study establishes a theoretical framework for understanding how microevolutionary processes combine to explain the diversification of species on macroevolutionary time scales.

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↗

bioRxiv2024

Repeated loss of function at HD mating-type genes and of recombination suppression without mating-type locus linkage in anther-smut fungi

A wide diversity of mating systems occur in nature, with frequent evolutionary transitions in mating-compatibility mechanisms. Basidiomycete fungi typically have two mating-type loci controlling mating compatibility, HD and PR, usually residing on different chromosomes. In Microbotryum anther-smut fungi, there have been repeated events of linkage between the two mating-type loci through chromosome fusions, leading to large non-recombining regions. By generating high-quality genome assemblies, we found that two sister Microbotryum species parasitizing Dianthus plants, M. superbum and M. shykoffianum, as well as the distantly related M. scorzonarae, have their HD and PR mating-type loci on different chromosomes, but with the PR mating-type chromosome fused with part of the ancestral HD chromosome. Furthermore, progressive extensions of recombination suppression have generated evolutionary strata. In all three species, rearrangements suggest the existence of a transient stage of HD-PR linkage by whole chromosome fusion, and, unexpectedly, the HD genes lost their function. In M. superbum, multiple natural diploid strains were homozygous, and the disrupted HD2 gene was hardly expressed. Mating tests confirmed that a single genetic factor controlled mating compatibility (i.e. PR) and that haploid strains with identical HD alleles could mate and produce infectious hyphae. The HD genes have therefore lost their function in the control of mating compatibility in these Microbotryum species. While the loss of function of PR genes in mating compatibility has been reported in a few basidiomycete fungi, these are the first documented cases for the loss of mating-type determination by HD genes in heterothallic fungi. The control of mating compatibility by a single genetic factor is beneficial under selfing and can thus be achieved repeatedly, through evolutionary convergence in distant lineages, involving different genomic or similar pathways.

evolutionary biology↗

bioRxiv2024

Generation of diversity in the blue cheese mold Penicillium roqueforti and identification of pleiotropic QTL for key cheese-making phenotypes

Elucidating the genomic architecture of quantitative traits is essential for our understanding of adaptation and for breeding in domesticated organisms. Penicillium roqueforti is the mold used worldwide for the blue cheese maturation, contributing to flavors through proteolytic and lipolytic activities. The two domesticated cheese populations display very little genetic diversity, but are differentiated and carry opposite mating types. We produced haploid F1 progenies from five crosses, using parents belonging to cheese and non-cheese populations. Analyses of high-quality genome assemblies of the parental strains revealed five large translocations, two having occurred via a circular intermediate. Offspring genotyping with genotype-by-sequencing (GBS) revealed several genomic regions with segregation distortion, possibly linked to degeneration in cheese lineages. We found transgressions for several traits relevant for cheese making, with offspring having more extreme trait values than parental strains. We identified quantitative trait loci (QTLs) for colony color, lipolysis, proteolysis, extrolite production, including mycotoxins, but not for growth rates. Some genomic regions appeared rich in QTLs for both lipid and protein metabolism, and other regions for the production of multiple extrolites, indicating that QTLs have pleiotropic impacts. Some QTLs corresponded to known biosynthetic gene clusters, e.g., for the production of melanin or extrolites. F1 hybrids constitute valuable strains for cheese producers, with new traits and genetic diversity, and allowed identifying target genomic regions for traits important in cheese making, paving the way for strain improvement. The findings further contribute to our understanding of the genetic mechanisms underlying rapid adaptation, revealing convergent adaptation targeting major regulators.

evolutionary biology↗

bioRxiv2024

Different metabolite profiles across Penicillium roqueforti populations associated with ecological niche specialisation and domestication

Fungi are known to produce many chemically diversified metabolites, yet their ecological roles are not always fully understood. The blue cheese making fungus Penicillium roqueforti thrives in different ecological niches and is known to produce a wide range of metabolites, including mycotoxins. Three P. roqueforti populations have been domesticated for cheese production and two populations thrive in other anthropized environments, i.e., spoiled food, lumber and silage. Here, we looked for differences in targeted and untargeted metabolite production profiles between populations using HPLC-HR-Q-TOF and UHPLC-Q-TOF-HR-MS/MS. The non-cheese populations produced several fatty acids and different terpenoids, lacking in cheese strains. The Termignon cheese population displayed intermediate metabolite profiles between cheese and non-cheese populations, as previously shown for other traits. The non-Roquefort population, the cheese population with the strongest domestication syndrome, produced the lowest quantities of measured metabolites, including known mycotoxins such as mycophenolic acid (MPA), andrastin A and PR toxin. Its inability to produce MPA was due to a deletion in the mpaC gene, while a premature stop codon in ORF 11 of the PR toxin gene cluster explained its absence and the accumulation of its eremofortin A & B intermediates. In the Roquefort population, we detected no PR toxin nor eremofortins A or B, but found no indel or frameshift mutation, suggesting downregulation. Our results suggest that domesticated cheese populations were selected for lower toxin production while populations from other anthropized environments maintained high metabolite diversity, the bioactivities of these compounds being likely important in these ecological niches.

microbiology↗