• 5 years programme (2013-2017)
• Coordinator: Pascal Frey (total: 500 k€). For IGEPP, Frederic Hamelin (22 k€).
• Contact: frederic.hamelin@agrocampus-ouest.fr

Mathematical models for a better understanding of the evolution of forest fungal pathogens

http://www.agence-nationale-recherche.fr/?Projet=ANR-13-BSV7-0011 

Basis and Rationale of the project

The objective of the FunFit project is to confront theoretical mathematical models and biological observations in order to better understand the evolution of biological characters (or life history traits) related to aggressiveness and dispersal abilities of fungal pathogens of forest trees. Three major forest diseases were selected as study models: poplar rust, chestnut blight and oak powdery mildew.

Main issues raised & general objectives

Fungi are among the most frequent damaging agents of plants, in natural and managed ecosystems. In recent years, they have been identified as a major cause of emerging diseases in the context of global change, especially through the introduction of previously absent species in new areas. Understanding this fast-moving epidemiological environment is a key issue and will require greater emphasis on integrative and predictive approaches. Though plant pathology has been increasingly integrating population genetics and genomics, an integrative ecological framework based on adaptive traits is still missing for fungal plant pathogens. In the FunFit project, we aim to fill this gap by establishing a theoretical framework, including conceptual schemes and models, and by developing experimental work on three representative fungal forest pathogens from a trait-based perspective. The premise of FunFit is that characterizing life history traits of fungal forest pathogens, including their variation, plasticity, trade-offs and evolution, will give us better insights into: (i) what makes a fungal pathogen successful, which is a very complementary approach to genomic studies of the determinants of pathogenicity; (ii) population and community dynamics of pathogens, hence ultimately plant disease dynamics and impacts in natural ecosystems.

Methods or technologies used

FunFit encompasses concepts and methods from evolutionary biology, epidemiology and ecology, with strong interactions between modelling and biological studies. It is based on three main tasks, using a trait-based approach at different levels of biological organization: Task 1 - linking disease associated traits and fitness in fungal forest pathogens (individual level); Task 2 -studying the evolution of traits during colonisation/emergence processes (population level); and Task 3 - unravelling how a complex of cryptic species/lineages can last although they share the same spatial niche. All tasks combine theoretical (including modelling) and empirical (experiments and data analysis) approaches in order to enrich a conceptual framework and to test hypotheses using three major fungal pathogens of forest trees: the Chestnut blight fungus Cryphonectria parasitica, the Oak powdery mildew fungus Erysiphe alphitoides, and the Poplar rust fungus Melampsora laricipopulina. Finally, results are expected to (i) contribute to deeper academic knowledge of the ecology of fungi, which constitute a major part of terrestrial biodiversity, and (ii) help knowledgebased management of plant diseases, including pest risk analysis, selection of durable resistance, and biological control. The FunFit project will lead to a significant step forward in the understanding of plant epidemics. It will have major implications in our understanding of how fungi grow, survive and evolve in the ever-changing environmental conditions and how this knowledge can be exploited to reduce fungal infestation and destruction of crops.

Main results

The first results of FunFit project are:

• A theoretical model of optimal infection dynamics for a biotrophic fungus was developed and allows predicting mycelium growth and spore production. This theoretical model fully fits empirical data for the dynamics of in planta mycelium growth and sporulation of the poplar rust fungus.
• We have demonstrated an adaptation to temperature in the Chestnut blight fungus during its migration to northern France.
• We have identified a phenomenon of natural selection on the volume of spores of M. larici- populina during an annual dispersal event of the fungus on wild poplars along the Durance River valley.
• We validated a theoretical model of coexistence of species based on trade-offs in a seasonal environment with empirical observations of the temporal dynamics for the two oak powdery mildew fungi, Erysiphe alphitoides and E. quercicola.

Outstanding feature (or focus) and future

prospect

Our ambition with the FunFit project is to provide significant contributions in fungal ecology and plant pathology, through developments of concepts, methodology and data. The main expected scientific outputs are the following:

• Different models of plant-pathogen interaction: a model of local interaction enabling the assessment of lifetime infection success (i.e. links between traits and fitness) and helping to define what traits should be measured by plant pathologists; an extension of this model into an epidemiological model
• A better understanding of niche differentiation between cryptic species, with a generic model and applications to the oak powdery mildew complex, representative of a major group of plant pathogens
• Insights into evolutionary processes for a few major forest pathogens: Melampsora larici-populina, Cryphonectria parasitica, and Erysiphe alphitoides, representing contrasted disease types, parasitic strategies and life-cycles
• New technical tools: in planta quantification of mycelium by real-time qPCR technique.

The most important output of our project is a conceptual framework for plant pathologists. Obtaining that plant pathology continues opening up to evolutionary and ecological ideas is an ambitious and very challenging goal.

Ultimately, the results of FunFit will both contribute to deeper academic knowledge of fungi, which constitute a major part of terrestrial biodiversity, and help knowledge-based management of plant diseases, with high social and economic impact, including pest risk analysis and selection of durable resistance.

Scientific production and patents

Eight scientific papers in excellent international peer-reviewed journals, in connection with the FunFit project were published, accepted or submitted. Several manuscripts are in preparation and will be submitted shortly. In addition, 17 oral and poster presentations were given by the project partners in national and international conferences.

Partners: http://mycor.nancy.inrae.fr/IAM/, http://www6.bordeaux-aquitaine.inrae.fr/biogeco, https://team.inria.fr/biocore/fr/