Within- and Between-Species Adaptation of Rust Fungi – WABSARF

The study of host-pathogen interactions is an active and diversified field of biology with many connections in functional and evolutionary biology and in ecology. In particular, genome evolution is an essential topic in the study of pathological systems due to the fast pace of their evolution. Directional selection is expected to be pervasive in the molecular evolution of pathogenic species due to the intense and permanent selective pressures they undergo. Therefore, the search for the signatures of adaptation in the genomes of species involved in host-pathogen interactions can give insight into the dynamics of this particular form of biotic interactions.

Besides, the study of the molecular bases of adaptation is a major field of research on its own. It is an essential topic in evolutionary biology since the modern synthesis of the theory of evolution. Since then and the dispute over the neutralist and selectionist theories of molecular evolution, much theoretical and experimental research has been devoted to molecular evolution. In the recent years, the interest in molecular evolution has actually been renewed by the possibility of examining genome-wide patterns of molecular diversity, allowing to detect the signatures of adaptation with unprecedented power and resolution. Due to the high likelihood to observe natural selection at work, host-pathogen interactions are an excellent model to address the mechanisms of molecular evolution.

Therefore, whether the original question is to understand the dynamics of host-pathogen interactions or to study the mechanisms of molecular adaptation by themselves, the search for the signatures of adaptation at a genome-wide scale in species involved in pathogenic interactions is a topical prospect. There are two levels to detect natural selection: intraspecific and interspecific. At the intraspecific level, selection is frequently detected through the deformation of the allele frequency spectrum within the framework of the population genetics theory. At the interspecific level, detection of selection relies on phylogenetic tools, most commonly based on an excess of non-synonymous (relatively to synonymous) substitutions.

In this project we are interested in rust fungi, a widespread and diversified clade of Basidiomycotina pathogenic fungi that pose a serious threat to their host plants (including many crop species). They have a complex life cycle that can involve two different, unrelated host species. They are biotrophes (grow in and feed on living host tissues). Among rust fungi, the Melampsora genus, for which considerable taxonomic and epidemiological knowledge as well as genomic data are available, includes a well documented variety of host specificity.

Our aims are to provide the community with a panorama of genomic diversity and species divergence in the genus, detect positive selection at both levels in order to identify determinants of potential coevolution with hosts, and compare these levels to draw conclusions about the general process of molecular adaptation in rust fungi. To this aim, we make use of the knowledge, expertise and material collection of INRA Nancy and the expertise in evolutionary genomics of the applicant. We will focus on a clade of 15 Melampsora species specialized on hosts of the Populus genus. All species will be sequenced and the signatures of past positive selection will be searched along the phylogeny. For three of these species, within-species polymorphism will be examined in order to detect the signatures of recent events of adaptation.

The project will yield candidate genes and information on genome evolution in rust fungi and will represent a reference study for other pathogenic fungi, for which studies of molecular evolution are still relatively scarce. The dissemination of conceptual and practical knowledge on the analysis of molecular evolution will be reinforced by a methodological training course held during the course of the project.