bioRxiv Science⌕ Search

Biology subjects

Rodriguez de la Vega, R. C.

Publications and source records attributed to Rodriguez de la Vega, R. C..

15 recordsLinked to original sources

Improving the benchmark of variant calling in clonal bacteria using more realistic in silico genomes, the case of Mycobacterium tuberculosis

The democratisation of Whole Genome Sequencing data in bacterial genomics requires the benchmarking of associated analytical methodologies such as reference-based variant calling. Current variant calling benchmarks rely either on de novo assembled natural genomes, for which true variants are inferred using a genome aligner, or on genomes evolved in silico by incorporating short variants on reference genomes. We introduce Maketube, a method for evolving realistic genomes of the Mycobacterium tuberculosis complex with the full diversity of variants verified in natural isolates, and describe benchmarking results using Maketube-evolved genomes. We document that Maketube-evolved genomes satisfyingly mimic Mtbc complex genomes. Using Maketube-evolved genomes, we show that genome aligners miss up to 7.5% of the variants, which implies that benchmarkings with natural de novo assembled genomes are biased. Second, we show that recall of popular variant calling pipelines MTBseq, TB-Profiler, and our in-house genomic pipeline genotube, was overestimated by 1 to 10% in benchmarkings relying on simplistic in silico-evolved genomes, and that slight but significant differences in performance exist between pipelines. Finally, we provide evidence that variants are missed in duplicated regions and in regions flanking sequences absent in the reference (displaced insertion sequences or sequences deleted during the evolution of the reference). Altogether, realistic in silico-evolved genomes such as Maketube-derived ones are precious tools for reliable genomic tools benchmarking. We provide new evidence that structural variants interfere with variant-calling, both because of the additional sequences they contain, but also because of misalignments around insertions.

bioinformatics↗

Structure-based phylogenetic analysis reveals multiple events of convergent evolution of cysteine-rich antimicrobial peptides in legume-rhizobium symbiosis

Nitrogen is essential for plant growth, yet its availability often limits agricultural productivity. Some legumes have evolved a unique ability to form symbiotic relationships with nitrogen-fixing soil bacteria called rhizobia, enabling them to thrive in nitrogen-deficient soils. In five legume clades, an exploitive strategy has evolved in which rhizobia undergo Terminal Bacteroid Differentiation (TBD), where the bacteria become larger, polyploid, and have a permeabilized membrane. Terminally differentiated bacteria are associated with higher N2-fixation and, thus, a higher return on investment to the plant. In several members of the IRLC (Inverted Repeat-Lacking Clade) and the Dalbergioid clades of legumes, this differentiation process is triggered by a set of apparently unrelated plant antimicrobial peptides with membrane-damaging activity, known as Nodule-specific Cysteine-Rich (NCR) peptides. However, whether NCR peptides are also implicated in symbiotic TBD in other legume clades and whether they are evolutionarily related remains unknown. Here, to address the molecular identity of NCR peptides and their evolution in different legume clades, we performed inter- and intra-clade comparisons of NCR peptides in representative species of four TBD-inducing legume clades. First, we collected genomic and proteomic data of species for which NCR peptides are known (1523 NCR peptides). We then used sequence similarity-based clustering to regroup the NCR peptides, resulting in over 400 different NCR clusters, each clade-specific. We obtained Hidden Markov Models for each cluster and used them to predict NCR peptides in 21 legume genomes (6 clades), including newly generated deep-sequenced root and nodule RNA-seq data of Indigofera argentea (Indigoferoid clade) and newly assembled high-quality transcriptomes of Lupinus luteus and Lupinus mariae-josephae (Genistoid clade), using tailored gene prediction pipeline and transcriptome matching. This resulted in 3710 NCR peptides in species that induce TBD. To date, the rapid diversification of NCR peptides that reduces the sequence similarities has masked the origin of NCR peptide evolution. We obtained high-confidence structural models for one sequence of each cluster. We performed structure-based clustering and phylogenetics, which resulted in 23 superclusters (14 inter-clade and nine clade-specific) that we represent in a structural distance-based tree. Our study revealed that the evolution of NCR peptides is a mix of divergent and convergent processes within each clade. We further chose nine independently evolved NCR peptides to test in vitro whether they are functional analogs in symbiosis. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=145 HEIGHT=200 SRC="FIGDIR/small/675119v1_ufig1.gif" ALT="Figure 1"> View larger version (50K): org.highwire.dtl.DTLVardef@8d1698org.highwire.dtl.DTLVardef@c65b98org.highwire.dtl.DTLVardef@a75994org.highwire.dtl.DTLVardef@ea1a73_HPS_FORMAT_FIGEXP M_FIG Overview of the experimental and computational workflow for NCR peptide detection, characterization, and structural analysis. Nodule and root samples from Indigofera argentea (8 weeks post-inoculation) were collected and subjected to RNA extraction, library preparation, and Illumina PE150 sequencing. Raw RNA-seq reads from two Lupinus species were also included (Lupinus luteus and Lupinus mariae-josephae). Bacteroid differentiation of I. argentea was assessed by flow cytometry and confocal microscopy. Transcriptomes were assembled de novo and analyzed for differential gene expression between root and nodule tissues. NCR peptides were identified from them and other legume genomes and transcriptomes using the SPADA pipeline and HMM profiles from NCR clusters of the known NCR peptides. The putative NCR peptides were filtered based on conserved cysteine motifs, length, and nodule expression to build an exhaustive NCR peptide database. 3D structural predictions of NCR clusters were performed using AlphaFold2 (pLDDT >70), followed by structural clustering (Foldseek) and phylogenetic analysis (Foldtree). Functional validation involved flow cytometry and antimicrobial assays (against Eschericha coli, Sinorhizobium meliloti, and Bacillus subtilis), enabling structural and evolutionary characterization of NCR peptides. The green box at the top represents the experimental analysis, the blue box represents the sequence-based computational pipeline, the red box represents the structure-based computational pipeline, and the grey box at the bottom left represents the functional validation and interpretation of the results. C_FIG

evolutionary biology↗

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↗

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↗

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↗

Taxonomic distribution of SbmA/BacA and BacA-like antimicrobial peptide transporters suggests independent recruitment and convergent evolution in host-microbe interactions

Small, antimicrobial peptides are often produced by eukaryotes to control bacterial populations in both pathogenic and mutualistic symbioses. These include proline-rich mammalian immune peptides and cysteine-rich peptides produced by legume plants in symbiosis with rhizobia. The fitness of the bacterial partner is dependent upon their ability to persist in the presence of these antimicrobial peptides. In the case of Escherichia coli and Mycobacterium tuberculosis pathogens and nitrogen-fixing legume symbionts (rhizobia), the ability to survive exposure to these peptides depends on peptide transporters called SbmA (also known as BacA) or BclA (for BacA-like). However, how broadly these transporters are distributed amongst bacteria, and their evolutionary history, is poorly understood. Here, we used hidden Markov models, phylogenetic analysis, and sequence similarity networks to examine the distribution of SbmA/BacA and BclA proteins across a representative set of 1,255 species from across the domain Bacteria. We identified a total of 71 and 177 SbmA/BacA and BclA proteins, respectively. Phylogenetic and sequence similarity analyses suggest that these protein families likely did not evolve from a common ancestor and that their functional similarity is instead a result of convergent evolution. In vitro sensitivity assays using the legume peptide NCR247 and several of the newly-identified BclA proteins confirmed that transport of antimicrobial peptides is a common feature of this protein family. Analysis of the taxonomic distribution of these proteins showed that SbmA/BacA orthologs were encoded only by species in the phylum Pseudomonadota and that they were primarily identified in just two orders: Hyphomicrobiales (class Alphaproteobacteria) and Enterobacterales (class Gammaproteobacteria). BclA orthologs were somewhat more broadly distributed and were found in clusters across four phyla. These included several orders of the phyla Pseudomonadota and Cyanobacteriota, as well as the order Mycobacteriales (phylum Actinomycetota) and the class Negativicutes (phylum Bacillota). Notably, many of the clades enriched for species encoding BacA or BclA orthologs also include many species known to interact with eukaryotic hosts in mutualistic or pathogenic interactions. Collectively, these observations suggest that SbmA/BacA and BclA proteins have been repeatedly co-opted to facilitate both mutualistic and pathogenic associations with eukaryotic hosts by allowing bacteria to cope with host-encoded antimicrobial peptides.

microbiology↗

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↗

Horizontal transfers between fungal Fusarium species contributed to successive outbreaks of coffee wilt disease

Outbreaks of fungal disease have devastated plants and animals throughout history. Over the past century, the repeated emergence of coffee wilt disease caused by the fungal pathogen Fusarium xylarioides severely impacted coffee production across sub-Saharan Africa. To improve the disease management of such pathogens, it is crucial to understand their genetic structure and evolutionary potential. We compared the genomes of 13 historic strains spanning six decades and multiple disease outbreaks to investigate population structure and host specialisation. We found F. xylarioides comprises at least four distinct lineages: one host-specific to Coffea arabica, one to C. canephora var. robusta, and two historic lineages isolated from various Coffea species. Mapping variation onto a new long-read reference genome showed that host-specificity appears to be acquired through horizontal transfer of effector genes from members of the F. oxysporum species complex. This species complex is known to cause wilt disease in over 100 plant species. Multiple transfers into the F. xylarioides populations matched to different parts of the F. oxysporum mobile pathogenicity chromosome and were enriched in effector genes and transposons. Effector genes in this region and other horizontally transferred carbohydrate-active enzymes important in the breakdown of plant cell walls were shown by transcriptomics to be highly expressed during infection of C. arabica by the fungal arabica strains. Widespread sharing of specific transposons between F. xylarioides and F. oxysporum, and the presence of large Starship elements, indicate that transposons were involved in horizontal transfers. Our results support the hypothesis that horizontal gene transfers contributed to the repeated emergence of this fungal disease.

evolutionary biology↗

Dynamics of transposable element accumulation in the non-recombining regions of mating-type chromosomes in anther-smut fungi

BackgroundTransposable element (TE) activity is generally deleterious to the host fitness, such that TE copies are often purged by selection, which is facilitated when meiotic recombination reshuffles variation among loci. In the absence of recombination, the number of TE insertions usually increases, but the dynamics of such TE accumulations is unknown. ResultsIn this study, we investigated the temporal dynamics of TE accumulation in the non-recombining genomic regions of 15 Microbotryum species, leveraging on a unique dataset of 21 independent evolutionary strata of recombination cessation of different ages. We show that TEs rapidly accumulated in regions lacking recombination, but that the TE content reached a plateau at ca. 50% of occupied base pairs by 1.5 MY following recombination suppression. The same TE superfamilies have repeatedly expanded in independently evolved non-recombining regions, in particular rolling-circle replication elements (Helitrons), despite being scarce before recombination suppression. The most abundant elements, long-terminal repeat (LTR) retrotransposons of the Copia and Ty3 superfamilies, expanded through transposition bursts affecting both the non-recombining regions of mating-type chromosomes and autosomes, thus suggesting that non-recombining regions constitute a reservoir of TEs that transpose to recombining regions. Based on LTR sequence divergence within and among copies, we could distinguish bursts of transposition from gene conversion. ConclusionOur study supports the TE reservoir hypothesis, by showing that TE accumulation in non-recombining has a genome-wide impact. TEs accumulated through bursts, and following a non-linear, decelerating dynamics, thus improving our knowledge on genome evolution, particularly in association with sex or mating-type chromosomes.

evolutionary biology↗

Stepwise recombination suppression around the mating-type locus in the fungus Schizothecium tetrasporum (Ascomycota, Sordariales)

Recombination is often suppressed at sex-determining loci in plants and animals, and at self-incompatibility or mating-type loci in plants and fungi. In fungal ascomycetes, recombination suppression around the mating-type locus is associated with pseudo-homothallism, i.e., the production of self-fertile dikaryotic sexual spores carrying the two opposite mating types. This has been well studied in two species complexes from different families of Sordariales: Podospora anserina and Neurospora tetrasperma. However, it is unclear whether this intriguing convergent association holds in other species. We show here that Schizothecium tetrasporum, a fungus from a third family in the order Sordariales, also produces mostly self-fertile dikaryotic spores carrying the two opposite mating types. This was due to a high frequency of second meiotic division segregation at the mating-type locus, indicating the occurrence of a single and systematic crossing-over event between the mating-type locus and the centromere, as in P. anserina. The mating-type locus has the typical Sordariales organization, plus a MAT1-1-1 pseudogene in the MAT1-2 haplotype. High-quality genome assemblies of opposite mating types and segregation analyses revealed a suppression of recombination in a region of 1.3 Mb around the mating-type locus. We detected three evolutionary strata, displaying a stepwise extension of recombination suppression, but no rearrangement or transposable element accumulation in the non-recombining region. Our findings indicate a convergent evolution of self-fertile dikaryotic sexual spores across multiple ascomycete fungi. The particular pattern of meiotic segregation at the mating-type locus was associated with recombination suppression around this locus, that had extended stepwise. This association is consistent with a recently proposed mechanism of deleterious allele sheltering through recombination suppression around a permanently heterozygous locus. AUTHOR SUMMARYRecombination allows faster adaptation and the purging of deleterious mutation but is often paradoxically lacking in sex chromosomes. It has been recently recognized that recombination can also be suppressed on fungal mating-type chromosomes, but the evolutionary explanation and the proximal mechanism of this phenomenon remain unclear. By studying here the sexual biology of a poorly studied mold living in rabbit dung, we reveal a striking convergence in three distant fungal lineages of an independently evolved association between the production of self-fertile sexual spores (carrying two nuclei with opposite mating types), a particular segregation of the mating-type locus and the lack of recombination on mating-type chromosomes, having evolved stepwise. Such a convergent association suggests causal relationships and will contribute to unveil the evolutionary causes of recombination suppression. Graphical summary O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=174 SRC="FIGDIR/small/500756v2_ufig1.gif" ALT="Figure 1"> View larger version (40K): org.highwire.dtl.DTLVardef@1cea706org.highwire.dtl.DTLVardef@378c41org.highwire.dtl.DTLVardef@d90297org.highwire.dtl.DTLVardef@1391c74_HPS_FORMAT_FIGEXP M_FIG C_FIG

evolutionary biology↗

Domestication of different varieties in the cheese-making fungus Geotrichum candidum

Domestication is an excellent model for studying adaptation processes, involving recent adaptation and diversification, convergence following adaptation to similar conditions, as well as degeneration of unused functions. Geotrichum candidum is a fungus used for cheese making and is also found in other environments such as soil and plants. By analyzing whole-genome data from 98 strains, we found that all strains isolated from cheese formed a monophyletic clade. Within the cheese clade, we identified three genetically differentiated populations and we detected footprints of recombination and admixture. The genetic diversity in the cheese clade was similar as that in the wild clade, suggesting the lack of strong bottlenecks. Commercial starter strains were scattered across the cheese clade, thus not constituting a single clonal lineage. The cheese populations were phenotypically differentiated from other populations, with a slower growth on all media, even cheese, a prominent production of typical cheese volatiles and a lower proteolytic activity. One of the cheese clusters encompassed all soft goat cheese strains, suggesting an effect of cheese-making practices on differentiation. Another of the cheese populations seemed to represent a more advanced stage of domestication, with stronger phenotypic differentiation from the wild clade, harboring much lower genetic diversity, and phenotypes more typical of cheese fungi, with denser and fluffier colonies and a greater ability of excluding cheese spoiler fungi. Cheese populations lacked two beta lactamase-like genes present in the wild clade, involved in xenobiotic clearance, and displayed higher contents of transposable elements, likely due to relaxed selection. Our findings suggest the existence of genuine domestication in G. candidum, which led to diversification into different varieties with contrasted phenotypes. Some of the traits acquired by cheese strains indicate convergence with other, distantly related fungi used for cheese maturation.

genetics↗

Footprints of domestication in dry-cured meat Penicillium fungi: convergent specific phenotypes and horizontal gene transfers

Some fungi have been domesticated for food production, with genetic differentiation between populations from food and wild environments, and food populations often acquiring beneficial traits through horizontal gene transfers (HGTs). Studying their adaptation to human-made substrates are of fundamental and applied importance, for understanding adaptation processes and for further strain improvement. We studied here the population structures and phenotypes of two distantly related Penicillium species used for dry-cured meat production, P. nalgiovense, the most common species in the dry-cured meat food industry, and P. salamii, used locally by farms. Both species displayed low genetic diversity, lacking differentiation between strains isolated from dry-cured meat and those from other environments. Nevertheless, the strains collected from dry-cured meat within each species displayed slower proteolysis and lipolysis than their wild conspecifics, and those of P. nalgiovense were whiter. Phenotypically, the non-dry-cured meat strains were more similar to their sister species than to their conspecific dry-cured meat strains, indicating an evolution of specific phenotypes in dry-cured meat strains. A comparison of available Penicillium genomes from various environments revealed HGTs, particularly between P. nalgiovense and P. salamii (representing almost 1.5 Mb of cumulative length). HGTs additionally involved P. biforme, also found in dry-cured meat products. We further detected positive selection based on amino-acid changes. Our findings suggest that selection by humans has shaped the P. salamii and P. nalgiovense populations used for dry-cured meat production, which constitutes domestication. Several genetic and phenotypic changes were similar in P. salamii, P. nalgiovense, and P. biforme, indicating convergent adaptation to the same human-made environment. Our findings have implications for fundamental knowledge on adaptation and for the food industry: the discovery of different phenotypes and of two mating types paves the way for strain improvement by conventional breeding, to elucidate the genomic bases of beneficial phenotypes and to generate diversity.

evolutionary biology↗

Onset and stepwise extensions of recombination suppression are common in mating-type chromosomes of Microbotryum anther-smut fungi

Sex chromosomes and mating-type chromosomes can display large genomic regions without recombination. Recombination suppression often extended stepwise with time away from the sex- or mating-type-determining genes, generating evolutionary strata of differentiation between alternative sex or mating-type chromosomes. In anther-smut fungi of the Microbotryum genus, recombination suppression evolved repeatedly, linking the two mating-type loci and extended multiple times in regions distal to the mating-type genes. Here, we obtained high-quality genome assemblies of alternative mating types for four Microbotryum fungi. We found an additional event of independent chromosomal rearrangements bringing the two mating-type loci on the same chromosome followed by recombination suppression linking them. We also found, in a new clade analysed here, that recombination suppression between the two mating-type loci occurred in several steps, with first an ancestral recombination suppression between one of the mating-type locus and its centromere; later, completion of recombination suppression up to the second mating-type locus occurred independently in three species. The estimated dates of recombination suppression between the mating-type loci ranged from 0.15 to 3.58 million years ago. In total, this makes at least nine independent events of linkage between the mating-type loci across the Microbotryum genus. Several mating-type locus linkage events occurred through the same types of chromosomal rearrangements, where similar chromosome fissions at centromeres represent convergence in the genomic changes leading to the phenotypic convergence. These findings further highlight Microbotryum fungi as excellent models to study the evolution of recombination suppression.

evolutionary biology↗

Domestication of the emblematic white cheese-making fungus Penicillium camemberti and its diversification into two varieties

Domestication involves recent adaptation under strong human selection and rapid diversification, and therefore constitutes a good model for studies of these processes. We studied the domestication of the emblematic white mold Penicillium camemberti, used for the maturation of soft cheeses, such as Camembert and Brie, about which surprisingly little was known, despite its economic and cultural importance. Whole genome-based analyses of genetic relationships and diversity revealed that an ancient domestication event led to the emergence of the gray-green P. biforme mold used in cheese-making, by divergence from the blue-green wild P. fuscoglaucum fungus. Another much more recent domestication event led to the generation of the P. camemberti clonal lineage as a sister group to P. biforme. Penicillium biforme displayed signs of phenotypic adaptation to cheese-making relative to P. fuscoglaucum, in terms of whiter color, faster growth on cheese medium under cave conditions, lower levels of toxin production and greater ability to prevent the growth of other fungi. The P. camemberti lineage displayed even stronger signs of domestication for all these phenotypic features. We also identified two differentiated P. camemberti varieties, apparently associated with different kinds of cheeses, and with contrasted phenotypic features in terms of color, growth, toxin production and competitive ability. We have, thus, identified footprints of domestication in these fungi, with genetic differentiation between cheese and wild populations, bottlenecks and specific phenotypic traits beneficial for cheese-making. This study has not only fundamental implications for our understanding of domestication but can also have important impacts on cheese-making.

evolutionary biology↗

Independent domestication events in the blue-cheese fungus Penicillium roqueforti

Domestication provides an excellent framework for studying adaptive divergence. Using population genomics and phenotypic assays, we reconstructed the domestication history of the blue cheese mold Penicillium roqueforti. We showed that this fungus was domesticated twice independently. The population used in Roquefort originated from an old domestication event associated with weak bottlenecks and exhibited traits beneficial for pre-industrial cheese production (slower growth in cheese and greater spore production on bread, the traditional multiplication medium). The other cheese population originated more recently from the selection of a single clonal lineage, was associated to all types of blue cheese worldwide but Roquefort, and displayed phenotypes more suited for industrial cheese production (high lipolytic activity, efficient cheese cavity colonization ability and salt tolerance). We detected genomic regions affected by recent positive selection and putative horizontal gene transfers. This study sheds light on the processes of rapid adaptation and raises questions about genetic resource conservation.

evolutionary biology↗