Publications by authors named "Tatiana Giraud"

117 Publications

Population genomics reveals molecular determinants of specialization to tomato in the polyphagous fungal pathogen Botrytis cinerea in France.

Phytopathology 2021 Apr 8. Epub 2021 Apr 8.

INRAE, 27057, BGPI, Paris, Île-de-France, France;

Many fungal plant pathogens encompass multiple populations specialized on different plant species. Understanding the factors underlying pathogen adaptation to their hosts is a major challenge of evolutionary microbiology, and it should help preventing the emergence of new specialized pathogens on novel hosts. Previous studies have shown that French populations of the grey mould pathogen Botrytis cinerea parasitizing tomato and grapevine are differentiated from each other, and have higher aggressiveness on their host-of-origin than on other hosts, indicating some degree of host specialization in this polyphagous pathogen. Here, we aimed at identifying the genomic features underlying the specialization of B. cinerea populations to tomato and grapevine. Based on whole genome sequences of 32 isolates, we confirmed the subdivision of B. cinerea pathogens into two genetic clusters on grapevine and another, single cluster on tomato. Levels of genetic variation in the different clusters were similar, suggesting that the tomato-specific cluster has not recently emerged following a bottleneck. Using genome scans for selective sweeps and divergent selection, tests of positive selection based on polymorphism and divergence at synonymous and non-synonymous sites and analyses of presence/absence variation, we identified several candidate genes that represent possible determinants of host specialization in the tomato-associated population. This work deepens our understanding of the genomic changes underlying the specialization of fungal pathogen populations.
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http://dx.doi.org/10.1094/PHYTO-07-20-0302-FIDOI Listing
April 2021

Europe as a bridgehead in the worldwide invasion history of grapevine downy mildew, Plasmopara viticola.

Curr Biol 2021 Mar 22. Epub 2021 Mar 22.

SAVE, INRAE, Bordeaux Sciences Agro, Université de Bordeaux, 33140 Villenave d'Ornon, France. Electronic address:

Europe is the historical cradle of viticulture, but grapevines (Vitis vinifera) have been increasingly threatened by pathogens of American origin. The invasive oomycete Plasmopara viticola causes downy mildew, one of the most devastating grapevine diseases worldwide. Despite major economic consequences, its invasion history remains poorly understood. We analyzed a comprehensive dataset of ∼2,000 samples, collected from the most important wine-producing countries, using nuclear and mitochondrial gene sequences and microsatellite markers. Population genetic analyses revealed very low genetic diversity in invasive downy mildew populations worldwide and little evidence of admixture. All the invasive populations originated from only one of the five native North American lineages, the one parasitizing wild summer grape (V. aestivalis). An approximate Bayesian computation-random forest approach allowed inferring the worldwide invasion scenario of P. viticola. After an initial introduction into Europe, invasive European populations served as a secondary source of introduction into vineyards worldwide, including China, South Africa, and twice independently, Australia. Only the invasion of Argentina probably represents a tertiary introduction, from Australia. Our findings provide a striking example of a global pathogen invasion resulting from secondary dispersal of a successful invasive population. Our study will also help designing quarantine regulations and efficient breeding for resistance against grapevine downy mildew.
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http://dx.doi.org/10.1016/j.cub.2021.03.009DOI Listing
March 2021

Size variation of the non-recombining region on the mating-type chromosomes in the fungal Podospora anserina species complex.

Mol Biol Evol 2021 Feb 8. Epub 2021 Feb 8.

Ecologie Systématique Evolution, CNRS, Université Paris-Saclay, 91400, France AgroParisTech, Orsay.

Sex chromosomes often carry large non-recombining regions that can extend progressively over time, generating evolutionary strata of sequence divergence. However, some sex chromosomes display an incomplete suppression of recombination. Large genomic regions without recombination and evolutionary strata have also been documented around fungal mating-type loci, but have been studied in only a few fungal systems. In the model fungus Podospora anserina (Ascomycota, Sordariomycetes), the reference S strain lacks recombination across a 0.8 Mb region around the mating-type locus. The lack of recombination in this region ensures that nuclei of opposite mating types are packaged into a single ascospore (pseudo-homothallic lifecycle). We found evidence for a lack of recombination around the mating-type locus in the genomes of 10 P. anserina strains and six closely related pseudo-homothallic Podospora species. Importantly, the size of the non-recombining region differed between strains and species, as indicated by the heterozygosity levels around the mating-type locus and experimental selfing. The non-recombining region is probably labile and polymorphic, differing in size and precise location within and between species, resulting in occasional, but infrequent, recombination at a given base pair. This view is also supported by the low divergence between mating types, and the lack of strong linkage disequilibrium, chromosomal rearrangements, trans-specific polymorphism and genomic degeneration. We found a pattern suggestive of evolutionary strata in P. pseudocomata. The observed heterozygosity levels indicate low but non-null outcrossing rates in nature in these pseudo-homothallic fungi. This study adds to our understanding of mating-type chromosome evolution and its relationship to mating systems.
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http://dx.doi.org/10.1093/molbev/msab040DOI Listing
February 2021

The taxonomy of the model filamentous fungus .

MycoKeys 2020 25;75:51-69. Epub 2020 Nov 25.

Systematic Biology, Department of Organismal Biology, Uppsala University, Norbyvägen 18D, 752 36 Uppsala, Sweden Uppsala Univeristy Uppsala Sweden.

The filamentous fungus has been used as a model organism for more than 100 years and has proved to be an invaluable resource in numerous areas of research. Throughout this period, has been embroiled in a number of taxonomic controversies regarding the proper name under which it should be called. The most recent taxonomic treatment proposed to change the name of this important species to . The results of past name changes of this species indicate that the broader research community is unlikely to accept this change, which will lead to nomenclatural instability and confusion in literature. Here, we review the phylogeny of the species closely related to and provide evidence that currently available marker information is insufficient to resolve the relationships amongst many of the lineages. We argue that it is not only premature to propose a new name for based on current data, but also that every effort should be made to retain as the current name to ensure stability and to minimise confusion in scientific literature. Therefore, we synonymise with and suggest that either the type species of be moved to from or that all species within the Podosporaceae be placed in the genus .
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http://dx.doi.org/10.3897/mycokeys.75.55968DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7710671PMC
November 2020

Pattern and causes of the establishment of the invasive bacterial potato pathogen Dickeya solani and of the maintenance of the resident pathogen D. dianthicola.

Mol Ecol 2021 01 4;30(2):608-624. Epub 2020 Dec 4.

Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Paris-Saclay University, Gif-sur-Yvette, France.

Invasive pathogens can be a threat when they affect human health, food production or ecosystem services, by displacing resident species, and we need to understand the cause of their establishment. We studied the patterns and causes of the establishment of the pathogen Dickeya solani that recently invaded potato agrosystems in Europe by assessing its invasion dynamics and its competitive ability against the closely related resident D. dianthicola species. Epidemiological records over one decade in France revealed the establishment of D. solani and the maintenance of the resident D. dianthicola in potato fields exhibiting blackleg symptoms. Using experimentations, we showed that D. dianthicola caused a higher symptom incidence on aerial parts of potato plants than D. solani, while D. solani was more aggressive on tubers (i.e. with more severe symptoms). In co-infection assays, D. dianthicola outcompeted D. solani in aerial parts, while the two species co-existed in tubers. A comparison of 76 D. solani genomes (56 of which have been sequenced here) revealed balanced frequencies of two previously uncharacterized alleles, VfmB and VfmB , at the vfmB virulence gene. Experimental inoculations showed that the VfmB population was more aggressive on tubers, while the VfmB population outcompeted the VfmB population in stem lesions, suggesting an important role of the vfmB virulence gene in the ecology of the pathogens. This study thus brings novel insights allowing a better understanding of the pattern and causes of the D.solani invasion into potato production agrosystems, and the reasons why the endemic D. dianthicola nevertheless persisted.
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http://dx.doi.org/10.1111/mec.15751DOI Listing
January 2021

Recombination suppression and evolutionary strata around mating-type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes.

New Phytol 2021 03 1;229(5):2470-2491. Epub 2020 Dec 1.

Ecologie Systematique Evolution, Batiment 360, Université Paris-Saclay, CNRS, AgroParisTech, Orsay, 91400, France.

Genomic regions determining sexual compatibility often display recombination suppression, as occurs in sex chromosomes, plant self-incompatibility loci and fungal mating-type loci. Regions lacking recombination can extend beyond the genes determining sexes or mating types, by several successive steps of recombination suppression. Here we review the evidence for recombination suppression around mating-type loci in fungi, sometimes encompassing vast regions of the mating-type chromosomes. The suppression of recombination at mating-type loci in fungi has long been recognized and maintains the multiallelic combinations required for correct compatibility determination. We review more recent evidence for expansions of recombination suppression beyond mating-type genes in fungi ('evolutionary strata'), which have been little studied and may be more pervasive than commonly thought. We discuss testable hypotheses for the ultimate (evolutionary) and proximate (mechanistic) causes for such expansions of recombination suppression, including (1) antagonistic selection, (2) association of additional functions to mating-type, such as uniparental mitochondria inheritance, (3) accumulation in the margin of nonrecombining regions of various factors, including deleterious mutations or transposable elements resulting from relaxed selection, or neutral rearrangements resulting from genetic drift. The study of recombination suppression in fungi could thus contribute to our understanding of recombination suppression expansion across a broader range of organisms.
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http://dx.doi.org/10.1111/nph.17039DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7898863PMC
March 2021

[The domestication of Penicillium cheese fungi].

C R Biol 2020 Oct 9;343(2):155-176. Epub 2020 Oct 9.

Ecologie Systématique et Evolution, CNRS, AgroParisTech, Université Paris-Saclay, 91400 Orsay, France.

Domestication is the process of organism evolution under selection by humans, and as such has been a model for studying adaptation since Charles Darwin. Here we review recent studies on the genomics of adaptation and domestication syndrome in two cheese-making fungal lineages, Penicillium roqueforti used for maturing blue cheeses, and the Penicillium camemberti species complex used for making soft cheeses such as Camembert and Brie. Comparative genomics have revealed horizontal gene transfers involved in convergent adaptation to cheese. Population genomics have identified differentiated populations with contrasted traits, several populations having independently been domesticated for cheese making in both P. roqueforti and the Penicillium camemberti species complex, and having undergone bottlenecks. The different cheese populations have acquired traits beneficial for cheese making in comparison to non-cheese populations, regarding color, spore production, growth rates on cheese, salt tolerance, lipolysis, proteolysis, volatile compound or toxin production and/or competitive ability. The cheese populations also show degeneration for some unused functions such as decreased ability of sexual reproduction or of growth under harsh conditions. These recent findings have fundamental importance for our understanding of adaptation and have applied interest for strain improvement.
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http://dx.doi.org/10.5802/crbiol.15DOI Listing
October 2020

Threat to Asian wild apple trees posed by gene flow from domesticated apple trees and their "pestified" pathogens.

Mol Ecol 2020 12 27;29(24):4925-4941. Epub 2020 Oct 27.

IRHS-UMR1345, Université d'Angers, INRAE, Institut Agro, Beaucouzé, France.

Secondary contact between crops and their wild relatives poses a threat to wild species, not only through gene flow between plants, but also through the dispersal of crop pathogens and genetic exchanges involving these pathogens, particularly those that have become more virulent by indirect selection on resistant crops, a phenomenon known as "pestification." Joint analyses of wild and domesticated hosts and their pathogens are essential to address this issue, but such analyses remain rare. We used population genetics approaches, demographic inference and pathogenicity tests on host-pathogen pairs of wild or domesticated apple trees from Central Asia and their main fungal pathogen, Venturia inaequalis, which itself has differentiated agricultural and wild-type populations. We confirmed the occurrence of gene flow from cultivated (Malus domestica) to wild (Malus sieversii) apple trees in Asian forests, potentially threatening the persistence of Asian wild apple trees. Pathogenicity tests demonstrated the pestification of V. inaequalis, the agricultural-type population being more virulent on both wild and domesticated trees. Single nucleotide polymorphism (SNP) markers and the demographic modelling of pathogen populations revealed hybridization following secondary contact between agricultural and wild-type fungal populations, and dispersal of the agricultural-type pathogen population in wild forests, increasing the threat of disease in the wild apple species. We detected an SNP potentially involved in pathogen pestification, generating an early stop codon in a gene encoding a small secreted protein in the agricultural-type fungal population. Our findings, based on joint analyses of paired host and pathogen data sets, highlight the threat posed by cultivating a crop near its centre of origin, in terms of pestified pathogen invasions in wild plant populations and introgression in the wild-type pathogen population.
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http://dx.doi.org/10.1111/mec.15677DOI Listing
December 2020

Domestication of the Emblematic White Cheese-Making Fungus Penicillium camemberti and Its Diversification into Two Varieties.

Curr Biol 2020 Nov 24;30(22):4441-4453.e4. Epub 2020 Sep 24.

Ecologie Systematique et Evolution, Universite Paris-Saclay, CNRS, AgroParisTech, 91400 Orsay, France.

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 amounts 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 effects on cheese making.
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http://dx.doi.org/10.1016/j.cub.2020.08.082DOI Listing
November 2020

Identification of the First Oomycete Mating-type Locus Sequence in the Grapevine Downy Mildew Pathogen, Plasmopara viticola.

Curr Biol 2020 Oct 13;30(20):3897-3907.e4. Epub 2020 Aug 13.

SAVE, INRAE, Bordeaux Sciences Agro, Université de Bordeaux, F-33140 Villenave d'Ornon, France. Electronic address:

Mating types are self-incompatibility systems that promote outcrossing in plants, fungi, and oomycetes. Mating-type genes have been widely studied in plants and fungi but have yet to be identified in oomycetes, eukaryotic organisms closely related to brown algae that cause many destructive animal and plant diseases. We identified the mating-type locus of Plasmopara viticola, the oomycete responsible for grapevine downy mildew, one of the most damaging grapevine diseases worldwide. Using a genome-wide association approach, we identified a 570-kb repeat-rich non-recombining region controlling mating types, with two highly divergent alleles. We showed that one mating type was homozygous, whereas the other was heterozygous at this locus. The mating-type locus encompassed 40 genes, including one encoding a putative hormone receptor. Functional studies will, however, be required to validate the function of these genes and find the actual determinants of mating type. Our findings have fundamental implications for our understanding of the evolution of mating types, as they reveal a unique determinism involving an asymmetry of heterozygosity, as in sex chromosomes and unlike other mating-type systems. This identification of the mating-type locus in such an economically important crop pathogen also has applied implications, as outcrossing facilitates rapid evolution and resistance to harsh environmental conditions.
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http://dx.doi.org/10.1016/j.cub.2020.07.057DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7116238PMC
October 2020

Anther-smut fungi from more contaminated sites in Chernobyl show lower infection ability and lower viability following experimental irradiation.

Ecol Evol 2020 Jul 26;10(13):6409-6420. Epub 2020 May 26.

Ecologie Systematique Evolution CNRS Université Paris-Saclay Orsay France.

The long-term contamination that followed the nuclear disaster at Chernobyl provides a case study for the effects of chronic ionizing radiation on living organisms and on their ability to tolerate or evolve resistance to such radiation. Previously, we studied the fertility and viability of early developmental stages of a castrating plant pathogen, the anther-smut fungus isolated from field sites varying over 700-fold in degree of radioactive contamination. Neither the budding rate of haploid spores following meiosis nor the karyotype structure varied with increasing radiation levels at sampling sites. Here, we assessed the ability of the same strains to perform their whole life cycle, up to the production of symptoms in the plants, that is, the development of anthers full of fungal spores; we also assessed their viability under experimental radiation. Fungal strains from more contaminated sites had no lower spore numbers in anthers or viability, but infected host plants less well, indicating lower overall fitness due to radioactivity exposure. These findings improve our understanding of the previous field data, in which the anther-smut disease prevalence on plants caused by was lower at more contaminated sites. Although the fungus showed relatively high resistance to experimental radiation, we found no evidence that increased resistance to radiation has evolved in populations from contaminated sites. Fungal strains from more contaminated sites even tolerated or repaired damage from a brief acute exposure to γ radiation less well than those from non- or less contaminated sites. Our results more generally concur with previous studies in showing that the fitness of living organisms is affected by radiation after nuclear disasters, but that they do not rapidly evolve higher tolerance.
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http://dx.doi.org/10.1002/ece3.6376DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7381591PMC
July 2020

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

Mol Ecol 2020 03 8;29(6):1154-1172. Epub 2020 Mar 8.

Ecologie Systematique Evolution, Batiment 360, AgroParisTech, CNRS, Universite Paris-Saclay, Orsay, France.

Study of the congruence of population genetic structure between hosts and pathogens gives important insights into their shared phylogeographical and coevolutionary histories. We studied the population genetic structure of castrating anther-smut fungi (genus Microbotryum) and of their host plants, the Silene nutans species complex, and the morphologically and genetically closely related Silene italica, which can be found in sympatry. Phylogeographical 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 single nucleotide polymorphisms. 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 that previously inferred for the host plant and probably 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 individual host-pathogen pairs contribute to a better understanding of co-evolutionary histories between hosts and pathogens in natural ecosystems, in which such studies remain scarce.
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http://dx.doi.org/10.1111/mec.15387DOI Listing
March 2020

Differential Gene Expression between Fungal Mating Types Is Associated with Sequence Degeneration.

Genome Biol Evol 2020 04;12(4):243-258

Department of Biology, Amherst College, Amherst, MA.

Degenerative mutations in non-recombining regions, such as in sex chromosomes, may lead to differential expression between alleles if mutations occur stochastically in one or the other allele. Reduced allelic expression due to degeneration has indeed been suggested to occur in various sex-chromosome systems. However, whether an association occurs between specific signatures of degeneration and differential expression between alleles has not been extensively tested, and sexual antagonism can also cause differential expression on sex chromosomes. The anther-smut fungus Microbotryum lychnidis-dioicae is ideal for testing associations between specific degenerative signatures and differential expression because 1) there are multiple evolutionary strata on the mating-type chromosomes, reflecting successive recombination suppression linked to mating-type loci; 2) separate haploid cultures of opposite mating types help identify differential expression between alleles; and 3) there is no sexual antagonism as a confounding factor accounting for differential expression. We found that differentially expressed genes were enriched in the four oldest evolutionary strata compared with other genomic compartments, and that, within compartments, several signatures of sequence degeneration were greater for differentially expressed than non-differentially expressed genes. Two particular degenerative signatures were significantly associated with lower expression levels within differentially expressed allele pairs: upstream insertion of transposable elements and mutations truncating the protein length. Other degenerative mutations associated with differential expression included nonsynonymous substitutions and altered intron or GC content. The association between differential expression and allele degeneration is relevant for a broad range of taxa where mating compatibility or sex is determined by genes located in large regions where recombination is suppressed.
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http://dx.doi.org/10.1093/gbe/evaa028DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7150583PMC
April 2020

Independent domestication events in the blue-cheese fungus Penicillium roqueforti.

Mol Ecol 2020 07 3;29(14):2639-2660. Epub 2020 Feb 3.

Ecologie Systématique et Evolution, CNRS, AgroParisTech, Ecologie Systématique Evolution, Université Paris-Saclay, Orsay, France.

Domestication provides an excellent framework for studying adaptive divergence. Using population genomics and phenotypic assays, we reconstructed the domestication history of the blue cheese mould 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 with all types of blue cheese worldwide except 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.
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http://dx.doi.org/10.1111/mec.15359DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7497015PMC
July 2020

Cause and Effectors: Whole-Genome Comparisons Reveal Shared but Rapidly Evolving Effector Sets among Host-Specific Plant-Castrating Fungi.

mBio 2019 11 5;10(6). Epub 2019 Nov 5.

Department of Biology, Program on Disease Evolution, University of Louisville, Louisville, Kentucky, USA

Plant pathogens utilize a portfolio of secreted effectors to successfully infect and manipulate their hosts. It is, however, still unclear whether changes in secretomes leading to host specialization involve mostly effector gene gains/losses or changes in their sequences. To test these hypotheses, we compared the secretomes of three host-specific castrating anther smut fungi (), two being sister species. To address within-species evolution, which might involve coevolution and local adaptation, we compared the secretomes of strains from differentiated populations. We experimentally validated a subset of signal peptides. Secretomes ranged from 321 to 445 predicted secreted proteins (SPs), including a few species-specific proteins (42 to 75), and limited copy number variation, i.e., little gene family expansion or reduction. Between 52% and 68% of the SPs did not match any Pfam domain, a percentage that reached 80% for the small secreted proteins, indicating rapid evolution. In comparison to background genes, we indeed found SPs to be more differentiated among species and strains, more often under positive selection, and highly expressed ; repeat-induced point mutations (RIPs) had no role in effector diversification, as SPs were not closer to transposable elements than background genes and were not more RIP affected. Our study thus identified both conserved core proteins, likely required for the pathogenic life cycle of all species, and proteins that were species specific or evolving under positive selection; these proteins may be involved in host specialization and/or coevolution. Most changes among closely related host-specific pathogens, however, involved rapid changes in sequences rather than gene gains/losses. Plant pathogens use molecular weapons to successfully infect their hosts, secreting a large portfolio of various proteins and enzymes. Different plant species are often parasitized by host-specific pathogens; however, it is still unclear whether the molecular basis of such host specialization involves species-specific weapons or different variants of the same weapons. We therefore compared the genes encoding secreted proteins in three plant-castrating pathogens parasitizing different host plants, producing their spores in plant anthers by replacing pollen. We validated our predictions for secretion signals for some genes and checked that our predicted secreted proteins were often highly expressed during plant infection. While we found few species-specific secreted proteins, numerous genes encoding secreted proteins showed signs of rapid evolution and of natural selection. Our study thus found that most changes among closely related host-specific pathogens involved rapid adaptive changes in shared molecular weapons rather than innovations for new weapons.
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http://dx.doi.org/10.1128/mBio.02391-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6831777PMC
November 2019

The complex evolutionary history of apricots: Species divergence, gene flow and multiple domestication events.

Mol Ecol 2019 12 22;28(24):5299-5314. Epub 2019 Nov 22.

UMR BFP, INRA-Université de Bordeaux, Villenave d'Ornon, France.

Domestication is an excellent model to study diversification and this evolutionary process can be different in perennial plants, such as fruit trees, compared to annual crops. Here, we inferred the history of wild apricot species divergence and of apricot domestication history across Eurasia, with a special focus on Central and Eastern Asia, based on microsatellite markers and approximate Bayesian computation. We significantly extended our previous sampling of apricots in Europe and Central Asia towards Eastern Asia, resulting in a total sample of 271 cultivated samples and 306 wild apricots across Eurasia, mainly Prunus armeniaca and Prunus sibirica, with some Prunus mume and Prunus mandshurica. We recovered wild Chinese species as genetically differentiated clusters, with P. sibirica being divided into two clusters, one possibly resulting from hybridization with P. armeniaca. Central Asia also appeared as a diversification centre of wild apricots. We further revealed at least three domestication events, without bottlenecks, that gave rise to European, Southern Central Asian and Chinese cultivated apricots, with ancient gene flow among them. The domestication event in China possibly resulted from ancient hybridization between wild populations from Central and Eastern Asia. We also detected extensive footprints of recent admixture in all groups of cultivated apricots. Our results thus show that apricot is an excellent model for studying speciation and domestication in long-lived perennial fruit trees.
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http://dx.doi.org/10.1111/mec.15296DOI Listing
December 2019

Higher Gene Flow in Sex-Related Chromosomes than in Autosomes during Fungal Divergence.

Mol Biol Evol 2020 03;37(3):668-682

Ecologie Systematique Evolution, Batiment 360, Univ. Paris-Sud, AgroParisTech, CNRS, Université Paris-Saclay, Orsay, France.

Nonrecombining sex chromosomes are widely found to be more differentiated than autosomes among closely related species, due to smaller effective population size and/or to a disproportionally large-X effect in reproductive isolation. Although fungal mating-type chromosomes can also display large nonrecombining regions, their levels of differentiation compared with autosomes have been little studied. Anther-smut fungi from the Microbotryum genus are castrating pathogens of Caryophyllaceae plants with largely nonrecombining mating-type chromosomes. Using whole genome sequences of 40 fungal strains, we quantified genetic differentiation among strains isolated from the geographically overlapping North American species and subspecies of Silene virginica and S. caroliniana. We inferred that gene flow likely occurred at the early stages of divergence and then completely stopped. We identified large autosomal genomic regions with chromosomal inversions, with higher genetic divergence than the rest of the genomes and highly enriched in selective sweeps, supporting a role of rearrangements in preventing gene flow in genomic regions involved in ecological divergence. Unexpectedly, the nonrecombining mating-type chromosomes showed lower divergence than autosomes due to higher gene flow, which may be promoted by adaptive introgressions of less degenerated mating-type chromosomes. The fact that both mating-type chromosomes are always heterozygous and nonrecombining may explain such patterns that oppose to those found for XY or ZW sex chromosomes. The specific features of mating-type chromosomes may also apply to the UV sex chromosomes determining sexes at the haploid stage in algae and bryophytes and may help test general hypotheses on the evolutionary specificities of sex-related chromosomes.
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http://dx.doi.org/10.1093/molbev/msz252DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7038665PMC
March 2020

Population genomics revealed cryptic species within host-specific zombie-ant fungi (Ophiocordyceps unilateralis).

Mol Phylogenet Evol 2019 11 13;140:106580. Epub 2019 Aug 13.

Ecologie Systématique Evolution, Univ. Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, 91400 Orsay, France.

The identification and delimitation of species boundaries are essential for understanding speciation and adaptation processes and for the management of biodiversity as well as development for applications. Ophiocordyceps unilateralis sensu lato is a complex of fungal pathogens parasitizing Formicine ants, inducing zombie behaviors in their hosts. Previous taxonomic works with limited numbers of samples and markers led to the "one ant-one fungus" paradigm, resulting in the use of ant species as a proxy for fungal identification. Here, a population genomics study with sampling on three ant species across Thailand supported the existence of host-specific species in O. unilateralis s.l. with no footprints of long term introgression despite occasional host shifts and first-generation hybrids. We further detected genetic clusters within the previously delimited fungal species, with each little footprints of recombination, suggesting high levels of inbreeding. The clusters within each of O. camponoti-leonardi and O. camponoti-saundersi were supported by differentiation throughout the genome, suggesting they may constitute further cryptic species parasitizing the same host, challenging the one ant-one fungus paradigm. These genetic clusters had different geographical ranges, supporting different biogeographic influences between the north/center and the south of Thailand, reinforcing the scenario in which Thailand endured compartmentation during the latest Pleistocene glacial cycles.
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http://dx.doi.org/10.1016/j.ympev.2019.106580DOI Listing
November 2019

Understanding Adaptation, Coevolution, Host Specialization, and Mating System in Castrating Anther-Smut Fungi by Combining Population and Comparative Genomics.

Annu Rev Phytopathol 2019 08 23;57:431-457. Epub 2019 Jul 23.

Ecologie Systématique Evolution, Univ. Paris-Sud, AgroParisTech, CNRS, Université Paris-Saclay, 91400 Orsay, France; email:

Anther-smut fungi provide a powerful system to study host-pathogen specialization and coevolution, with hundreds of species specialized on diverse Caryophyllaceae plants, castrating their hosts through manipulation of the hosts' reproductive organs to facilitate disease transmission. fungi have exceptional genomic characteristics, including dimorphic mating-type chromosomes, that make this genus anexcellent model for studying the evolution of mating systems and their influence on population genetics structure and adaptive potential. Important insights into adaptation, coevolution, host specialization, and mating system evolution have been gained using anther-smut fungi, with new insights made possible by the recent advent of genomic approaches. We illustrate with case studies how using a combination of comparative genomics, population genomics, and transcriptomics approaches enables the integration of different evolutionary perspectives across different timescales. We also highlight current challenges and suggest future studies that will contribute to advancing our understanding of the mechanisms underlying adaptive processes in populations of fungal pathogens.
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http://dx.doi.org/10.1146/annurev-phyto-082718-095947DOI Listing
August 2019

Sympatry and interference of divergent pathogen species.

Ecol Evol 2019 May 12;9(9):5457-5467. Epub 2019 Apr 12.

Department of Biology University of Virginia Charlottesville Virginia.

The impact of infectious diseases in natural ecosystems is strongly influenced by the degree of pathogen specialization and by the local assemblies of potential host species. This study investigated anther-smut disease, caused by fungi in the genus , among natural populations of plants in the Caryophyllaceae. A broad geographic survey focused on sites of the disease on multiple host species in sympatry. Analysis of molecular identities for the pathogens revealed that sympatric disease was most often due to co-occurrence of distinct, host-specific anther-smut fungi, rather than localized cross-species disease transmission. Flowers from sympatric populations showed that the spores were frequently moved between host species. Experimental inoculations to simulate cross-species exposure to the pathogens in these plant communities showed that the anther-smut pathogen was less able to cause disease on its regular host when following exposure of the plants to incompatible pathogens from another host species. These results indicate that multi-host/multi-pathogen communities are common in this system and they involve a previously hidden mechanism of interference between fungi, which likely affects both pathogen and host distributions.
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http://dx.doi.org/10.1002/ece3.5140DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6509394PMC
May 2019

Convergent recombination cessation between mating-type genes and centromeres in selfing anther-smut fungi.

Genome Res 2019 06 1;29(6):944-953. Epub 2019 May 1.

Ecologie Systématique Evolution, Bâtiment 360, Univ. Paris-Sud, AgroParisTech, CNRS, Université Paris-Saclay, 91400 Orsay, France.

The degree of selfing has major impacts on adaptability and is often controlled by molecular mechanisms determining mating compatibility. Changes in compatibility systems are therefore important evolutionary events, but their underlying genomic mechanisms are often poorly understood. Fungi display frequent shifts in compatibility systems, and their small genomes facilitate elucidation of the mechanisms involved. In particular, linkage between the pre- and postmating compatibility loci has evolved repeatedly, increasing the odds of gamete compatibility under selfing. Here, we studied the mating-type chromosomes of two anther-smut fungi with unlinked mating-type loci despite a self-fertilization mating system. Segregation analyses and comparisons of high-quality genome assemblies revealed that these two species displayed linkage between mating-type loci and their respective centromeres. This arrangement renders the same improved odds of gamete compatibility as direct linkage of the two mating-type loci under the automictic mating (intratetrad selfing) of anther-smut fungi. Recombination cessation was found associated with a large inversion in only one of the four linkage events. The lack of -specific polymorphism at genes located in nonrecombining regions and linkage date estimates indicated that the events of recombination cessation occurred independently in the two sister species. Our study shows that natural selection can repeatedly lead to similar genomic patterns and phenotypes, and that different evolutionary paths can lead to distinct yet equally beneficial responses to selection. Our study further highlights that automixis and gene linkage to centromeres have important genetic and evolutionary consequences, while being poorly recognized despite being present in a broad range of taxa.
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http://dx.doi.org/10.1101/gr.242578.118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6581054PMC
June 2019

Little Evidence of Antagonistic Selection in the Evolutionary Strata of Fungal Mating-Type Chromosomes (.

G3 (Bethesda) 2019 06 5;9(6):1987-1998. Epub 2019 Jun 5.

Ecologie Systématique Evolution, Univ. Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, 91400 Orsay, France

Recombination suppression on sex chromosomes often extends in a stepwise manner, generating evolutionary strata of differentiation between sex chromosomes. Sexual antagonism is a widely accepted explanation for evolutionary strata, postulating that sets of genes beneficial in only one sex are successively linked to the sex-determining locus. The anther-smut fungus has mating-type chromosomes with evolutionary strata, only some of which link mating-type genes. Male and female roles are non-existent in this fungus, but mating-type antagonistic selection can also generate evolutionary strata, although the life cycle of the fungus suggests it should be restricted to few traits. Here, we tested the hypothesis that mating-type antagonism may have triggered recombination suppression beyond mating-type genes in by searching for footprints of antagonistic selection in evolutionary strata not linking mating-type loci. We found that these evolutionary strata (i) were not enriched in genes upregulated in the haploid phase, where cells are of alternative mating types, (ii) carried no gene differentially expressed between mating types, and (iii) carried no genes displaying footprints of specialization in terms of protein sequences (d/d) between mating types after recommended filtering. Without filtering, eleven genes showed signs of positive selection in the strata not linking mating-type genes, which constituted an enrichment compared to autosomes, but their functions were not obviously involved in antagonistic selection. Thus, we found no strong evidence that antagonistic selection has contributed to extending recombination suppression beyond mating-type genes. Alternative hypotheses should therefore be explored to improve our understanding of the sex-related chromosome evolution.
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http://dx.doi.org/10.1534/g3.119.400242DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6553529PMC
June 2019

Multiple infections, relatedness and virulence in the anther-smut fungus castrating Saponaria plants.

Mol Ecol 2018 12 22;27(23):4947-4959. Epub 2018 Nov 22.

Ecologie Systématique Evolution, Univ. Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, Orsay, France.

Multiple infections (co-occurrence of multiple pathogen genotypes within an individual host) can have important impacts on diseases. Relatedness among pathogens can affect the likelihood of multiple infections and their consequences through kin selection. Previous studies on the castrating anther-smut fungus Microbotryum lychnidis-dioicae have shown that multiple infections occur in its host plant Silene latifolia. Relatedness was high among fungal genotypes within plants, which could result from competitive exclusion between unrelated fungal genotypes, from population structure or from interactions between plant and fungal genotypes for infection ability. Here, we aimed at disentangling these hypotheses using M. saponariae and its host Saponaria officinalis, both experimentally tractable for these questions. By analysing populations using microsatellite markers, we also found frequent occurrence of multiple infections and high relatedness among strains within host plants. Infections resulting from experimental inoculations in the greenhouse also revealed high relatedness among strains co-infecting host plants, even in clonally replicated plant genotypes, indicating that high relatedness within plants did not result merely from plant x fungus interactions or population structure. Furthermore, hyphal growth in vitro was affected by the presence of a competitor growing nearby and by its genetic similarity, although this latter effect was strain-dependent. Altogether, our results support the hypothesis that relatedness-dependent competitive exclusion occurs in Microbotryum fungi within plants. These microorganisms can thus respond to competitors and to their level of relatedness.
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http://dx.doi.org/10.1111/mec.14911DOI Listing
December 2018

A genome scan of diversifying selection in Ophiocordyceps zombie-ant fungi suggests a role for enterotoxins in co-evolution and host specificity.

Mol Ecol 2018 09 29;27(18):3582-3598. Epub 2018 Aug 29.

Ecologie Systématique Evolution, Université Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, Orsay, France.

Identification of the genes underlying adaptation sheds light on the biological functions targeted by natural selection. Searches for footprints of positive selection, in the form of rapid amino acid substitutions, and the identification of species-specific genes have proved to be powerful approaches to identifying the genes involved in host specialization in plant-pathogenic fungi. We used an evolutionary comparative genomic approach to identify genes underlying host adaptation in the ant-infecting genus Ophiocordyceps, which manipulates ant behaviour. A comparison of the predicted genes in the genomes of species from three species complexes-O. unilateralis, O. australis and O. subramanianii-revealed an enrichment in pathogenesis-associated functions, including heat-labile enterotoxins, among species-specific genes. Furthermore, these genes were overrepresented among those displaying significant footprints of positive selection. Other categories of genes suspected to be important for virulence and pathogenicity in entomopathogenic fungi (e.g., chitinases, lipases, proteases, core secondary metabolism genes) were much less represented, although a few candidate genes were found to evolve under positive selection. An analysis including orthologs from other entomopathogenic fungi in a broader context showed that positive selection on enterotoxins was specific to the ant-infecting genus Ophiocordyceps. Together with previous studies reporting the overexpression of an enterotoxin during behavioural manipulation in diseased ants, our findings suggest that heat-labile enterotoxins are important effectors in host adaptation and co-evolution in the Ophiocordyceps entomopathogenic fungi.
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http://dx.doi.org/10.1111/mec.14813DOI Listing
September 2018

Co-occurrence among three divergent plant-castrating fungi in the same Silene host species.

Mol Ecol 2018 Jul 21. Epub 2018 Jul 21.

Laboratoire Ecologie Systématique et Evolution, Univ. Paris Sud, CNRS, AgroParisTech, Université Paris Saclay, Orsay, France.

The competitive exclusion principle postulates that different species can only coexist in sympatry if they occupy distinct ecological niches. The goal of this study was to understand the geographical distribution of three species of Microbotryum anther-smut fungi that are distantly related but infect the same host plants, the sister species Silene vulgaris and S. uniflora, in Western Europe. We used microsatellite markers to investigate pathogen distribution in relation to host specialization and ecological factors. Microbotryum violaceo-irregulare was only found on S. vulgaris at high elevations in the Alps. Microbotryum lagerheimii could be subdivided into two genetically differentiated clusters, one on S. uniflora in the UK and the second on S. vulgaris in the Alps and Pyrenees. The most abundant pathogen species, M. silenes-inflatae, could be subdivided into four genetic clusters, co-occurring in the Alps, the UK and the Pyrenees, and was found on both S. vulgaris and S. uniflora. All three fungal species had high levels of homozygosity, in agreement with the selfing mating system generally observed in anther-smut fungi. The three pathogen species and genetic clusters had large range overlaps, but occurred at sites with different elevations, temperatures and precipitation levels. The three Microbotryum species thus do not appear to be maintained by host specialization or geographic allopatry, but instead may occupy different ecological niches in terms of environmental conditions.
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http://dx.doi.org/10.1111/mec.14805DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6340787PMC
July 2018

Multiple convergent supergene evolution events in mating-type chromosomes.

Nat Commun 2018 05 21;9(1):2000. Epub 2018 May 21.

Ecologie Systématique Evolution, Bâtiment 360, Univ. Paris-Sud, AgroParisTech, CNRS, Université Paris-Saclay, 91400, Orsay, France.

Convergent adaptation provides unique insights into the predictability of evolution and ultimately into processes of biological diversification. Supergenes (beneficial gene linkage) are striking examples of adaptation, but little is known about their prevalence or evolution. A recent study on anther-smut fungi documented supergene formation by rearrangements linking two key mating-type loci, controlling pre- and post-mating compatibility. Here further high-quality genome assemblies reveal four additional independent cases of chromosomal rearrangements leading to regions of suppressed recombination linking these mating-type loci in closely related species. Such convergent transitions in genomic architecture of mating-type determination indicate strong selection favoring linkage of mating-type loci into cosegregating supergenes. We find independent evolutionary strata (stepwise recombination suppression) in several species, with extensive rearrangements, gene losses, and transposable element accumulation. We thus show remarkable convergence in mating-type chromosome evolution, recurrent supergene formation, and repeated evolution of similar phenotypes through different genomic changes.
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http://dx.doi.org/10.1038/s41467-018-04380-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5962589PMC
May 2018

Gene Presence-Absence Polymorphism in Castrating Anther-Smut Fungi: Recent Gene Gains and Phylogeographic Structure.

Genome Biol Evol 2018 04;10(5):1298-1314

Department Génétique et Ecologie Evolutives, Ecologie Systématique Evolution, Bâtiment 360, Univ. Paris-Sud, AgroParisTech, CNRS, Université Paris-Saclay, Orsay, France.

Gene presence-absence polymorphisms segregating within species are a significant source of genetic variation but have been little investigated to date in natural populations. In plant pathogens, the gain or loss of genes encoding proteins interacting directly with the host, such as secreted proteins, probably plays an important role in coevolution and local adaptation. We investigated gene presence-absence polymorphism in populations of two closely related species of castrating anther-smut fungi, Microbotryum lychnidis-dioicae (MvSl) and M. silenes-dioicae (MvSd), from across Europe, on the basis of Illumina genome sequencing data and high-quality genome references. We observed presence-absence polymorphism for 186 autosomal genes (2% of all genes) in MvSl, and only 51 autosomal genes in MvSd. Distinct genes displayed presence-absence polymorphism in the two species. Genes displaying presence-absence polymorphism were frequently located in subtelomeric and centromeric regions and close to repetitive elements, and comparison with outgroups indicated that most were present in a single species, being recently acquired through duplications in multiple-gene families. Gene presence-absence polymorphism in MvSl showed a phylogeographic structure corresponding to clusters detected based on SNPs. In addition, gene absence alleles were rare within species and skewed toward low-frequency variants. These findings are consistent with a deleterious or neutral effect for most gene presence-absence polymorphism. Some of the observed gene loss and gain events may however be adaptive, as suggested by the putative functions of the corresponding encoded proteins (e.g., secreted proteins) or their localization within previously identified selective sweeps. The adaptive roles in plant and anther-smut fungi interactions of candidate genes however need to be experimentally tested in future studies.
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http://dx.doi.org/10.1093/gbe/evy089DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5967549PMC
April 2018

Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism.

Proc Natl Acad Sci U S A 2017 07 19;114(27):7067-7072. Epub 2017 Jun 19.

Ecologie Systématique Evolution, Univ. Paris Sud, AgroParisTech, CNRS, Université Paris-Saclay, 91400 Orsay, France;

Sex chromosomes can display successive steps of recombination suppression known as "evolutionary strata," which are thought to result from the successive linkage of sexually antagonistic genes to sex-determining genes. However, there is little evidence to support this explanation. Here we investigate whether evolutionary strata can evolve without sexual antagonism using fungi that display suppressed recombination extending beyond loci determining mating compatibility despite lack of male/female roles associated with their mating types. By comparing full-length chromosome assemblies from five anther-smut fungi with or without recombination suppression in their mating-type chromosomes, we inferred the ancestral gene order and derived chromosomal arrangements in this group. This approach shed light on the chromosomal fusion underlying the linkage of mating-type loci in fungi and provided evidence for multiple clearly resolved evolutionary strata over a range of ages (0.9-2.1 million years) in mating-type chromosomes. Several evolutionary strata did not include genes involved in mating-type determination. The existence of strata devoid of mating-type genes, despite the lack of sexual antagonism, calls for a unified theory of sex-related chromosome evolution, incorporating, for example, the influence of partially linked deleterious mutations and the maintenance of neutral rearrangement polymorphism due to balancing selection on sexes and mating types.
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http://dx.doi.org/10.1073/pnas.1701658114DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5502610PMC
July 2017