PATH2EVOL · Unravelling pathogen evolution breaking down crop resistance in agricultural ecosystems

Unravelling pathogen evolution breaking down crop resistance in agricultural ecosystems

Supplying sufficient and safe food to the growing world population is a major challenge. In modern agriculture, plant diseases are a major drawback on productivity requiring the breeding of resistant crop varieties and/or the deployment of chemical control agents. However, both avenues face severe challenges and societal concerns. Many pathogens can easily evolve resistance to chemicals leading to higher application doses. Concerns over the overall safety of such compounds is a major topic of current discussions. Pathogens can also easily evolve to cause disease on previously resistant plants by acquiring specific mutations in the genome. Plant resistance genes encode proteins that activate the plant immune system by recognizing pathogen-specific virulence factors. Mutations in virulence factors can suffice for pathogens to escape the plant immune system. Promising approaches include genome editing that can accelerate resistance breeding. Here also societal concerns remain about the acceptance of such technology. Our objective has been to apply evolutionary principles to understand the emergence of crop pathogens with the ultimate goal to identify more durable control strategies. We have analyzed a how the dominant pathogen of wheat in Europe, Zymoseptoria tritici, evolves the ability to attack plants. For this, we were interested to analyze the critical stage of infection happening during the colonization of a field. We collected large samples of the pathogen from two fields in Europe and performed large-scale genome sequencing. Using statistical approaches, we analyzed how the pathogens succeeded at the molecular level in the presence of resistant wheat cultivars. Specifically, we identified how specific changes in the frequency of mutations can be related to the success or failure of a pathogen to attack a crop plant. These blooms/collapses cycles of selection of crop pathogens populations taking place since domestication, may have shaped pathogens’ genomes to fasten resistance overcome and guarantee survival. Indeed, previous genomic analyses revealed that plant filamentous pathogens’ genomes are compartmentalized into stable gene-rich and dynamic gene-poor regions and that virulence genes are most likely to locate into the second ones. The evolutionary model of genomic regions evolving at different speeds emerged (i.e. the two-speed genome) and suggest that the genomic regions containing virulence genes evolve faster than the region containing essential genes. However, the roles of this genomic architecture in pathogen adaptation to agro-ecosystems remain unclear and a better understanding of its evolutionary dynamic is now crucial to appropriately deploy disease control strategies.

Data: CORDIS, © European Union