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

International audienceThe 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 trans-specific poly-morphism 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

Influence of multiple infection and relatedness on virulence: Disease dynamics in an experimental plant population and its castrating parasite. PLoS One 2014

Abstract The level of parasite virulence, i.e., the decrease in host's fitness due to a pathogen, is expected to depend on several parameters, such as the type of the disease (e.g., castrating or host-killing) and the prevalence of multiple infections. Although these parameters have been extensively studied theoretically, few empirical data are available to validate theoretical predictions. Using the anther smut castrating disease on Silene latifolia caused by Microbotryum lychnidis-dioicae, we studied the dynamics of multiple infections and of different components of virulence (host death, non-recovery and percentage of castrated stems) during the entire lifespan of the host in an experimental population. We monitored the number of fungal genotypes within plants and their relatedness across five years, using microsatellite markers, as well as the rates of recovery and host death in the population. The mean relatedness among genotypes within plants remained at a high level throughout the entire host lifespan despite the dynamics of the disease, with recurrent new infections. Recovery was lower for plants with multiple infections compared to plants infected by a single genotype. As expected for castrating parasites, M. lychnidis-dioicae did not increase host mortality. Mortality varied across years but was generally lower for plants that had been diseased the preceding year. This is one of the few studies to have empirically verified theoretical expectations for castrating parasites, and to show particularly i) that castrated hosts live longer, suggesting that parasites can redirect resources normally used in reproduction to increase host lifespan, lengthening their transmission phase, and ii) that multiple infections increase virulence, here in terms of non-recovery and host castration

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

Data from: Inference of domestication history and differentiation between early- and late-flowering varieties in pearl millet

Pearl millet (Pennisetum glaucum) is a staple crop in Sahelian Africa. Farmers usually grow varieties with different cycle lengths and complementary functions in Sahelian agrosystems. Both the level of genetic differentiation of these varieties and the domestication history of pearl millet have been poorly studied. We investigated the neutral genetic diversity and population genetic structure of early- and late-flowering domesticated and wild pearl millet populations using 18 microsatellite loci and 8 nucleotide sequences. Strikingly, early- and late-flowering domesticated varieties were not differentiated over their whole distribution area, despite a clear difference in their isolation-by-distance pattern. Conversely, our data brought evidence for two well-differentiated genetic pools in wild pearl millet, allowing us to test scenarios with different numbers and origins of domestication using approximate Bayesian computation (ABC). The ABC analysis showed the likely existence of asymmetric migration between wild and domesticated populations. The model choice procedure indicated that a single domestication from the eastern wild populations was the more likely scenario to explain the polymorphism patterns observed in cultivated pearl millet

Scripts and reference tables of the ABC analysis

Contains the scripts needed to perform the simulations with ABCtoolbox and fastsimcoal for the ABC analysis, and the reference tables for each simulated model. ReadMe files are included in the directories

Polymorphism data

Microsatellite and nucleotide sequence data sets, used in the polymorphism study and the ABC analysis. ReadMe files describing the data are included in the directories

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

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

Blue cheese-making has shaped the population genetic structure of the mould Penicillium roqueforti

Background Penicillium roqueforti is a filamentous fungus used for making blue cheeses worldwide. It also occurs as a food spoiler and in silage and wood. Previous studies have revealed a strong population genetic structure, with specific traits associated with the different populations. Here, we used a large strain collection from worldwide cheeses published recently to investigate the genetic structure of P. roqueforti. Principal findings We found a genetic population structure in P. roqueforti that was consistent with previous studies, with two main genetic clusters (W+C+and W-C-, i.e., with and without horizontal gene transferred regions CheesyTer and Wallaby). In addition, we detected a finer genetic subdivision that corresponded to the environment and to protected designation of origin (PDO), namely the Roquefort PDO. We indeed found evidence for eight genetic clusters, one of the cluster including only strains from other environments than cheeses, and another cluster encompassing only strains from the Roquefort PDO. The W-C-and W+C+cheese clusters were not the most closely related ones, suggesting that there may have been two independent domestication events of P. roqueforti for making blue cheeses. Significance The additional population structure revealed here may be relevant for cheese-makers and for understanding the history of domestication in P. roqueforti

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

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