Unravelling pathogen evolution breaking down crop resistance in agricultural ecosystems

Project Information

PATH2EVOL

Grant agreement ID: 799630

DOI

10.3030/799630

Project closed

EC signature date 18 April 2018

Start date 1 July 2018

End date 30 June 2020

Funded under

• EXCELLENT SCIENCE - Marie Skłodowska-Curie Actions

Total cost

€ 175 419,60

EU contribution

€ 175 419,60

Coordinated by

UNIVERSITE DE NEUCHATEL
Switzerland

Periodic Reporting for period 1 - PATH2EVOL (Unravelling pathogen evolution breaking down crop resistance in agricultural ecosystems)

Reporting period: 2018-07-01 to 2020-06-30

Summary of the context and overall objectives of the project

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.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

The project has established vast genomic resources for investigating how pathogens can adapt to attack a major crop. Considering both local scales (individual fields) and continental, as well as nuclear and mitochondrial genomic diversity, we have gained the following insights:

- Individual wheat fields can be colonized by massively diverse pathogen gene pools. The extent of genetic diversity suggests that the studied wheat pathogen is largely unhindered to adapt to individual wheat varieties.

- We identified genomic signatures indicating what mutations were particularly relevant to attack wheat varieties.

- At the continental scale, we find that the pathogen experienced severe bottlenecks to colonize more isolated regions including Oceania. Gene flow in Europe is extensive challenging traditional quarantine measures.

- Analysis of the mitochondrial genome reveals an unexpectedly high diversity that might be relevant for adaptation.


The complete list of output including seminars, conferences, outreach and publications is below:

1.) Talk given at the "Workshop on Ecological Genomics" (Paris, France, 07.2018)

2.) Talk given at the "Meeting on Host-Microbe Genomics" organized at the ETH Zurich (Zurich, Switzerland, 09.2018)

3.) Talk given at the workshop "At the border between ecology and evolution" (Montpellier, France, 03.2019)

4.) Talk given at the "Seminar on Genomics and Evolution of Microbes" at the University of Neuchâtel (Neuchâtel, Switzerland, 04.2019)

5.) Poster presented at the "Zymoseptoria Community Meeting" at the ETH Zürich (Zurich, Switzerland, 07.2019)

6.) Manuscript published as a preprint on bioRxiv "Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici" DOI: https://doi.org/10.1101/2020.07.07.191510

7.) Additional manuscripts are in preparation.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

The project has revealed that crop pathogens establish very large gene pools when colonizing individual fields. Genomic evidence suggests that the pathogen continues to adapt to overcome host resistance. Such genetic variation challenges traditional approaches in relying on resistant crops or classical pesticide application regimes. The available pool of mutations likely harbors already mutations to overcome most challenges presented to the pathogen.

Innovative field monitoring expanding on our approaches will help to predict the risk of local pathogen outbreaks. The genomic knowledge will also enable to breed more durable resistance by integrating the potential pathogen evolution more explicitly.

Analyzing the adaptive landscape of a global wheat pathogen. From continents to individual fields