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The genetic basis of rapid plant pathogen evolution

English title The genetic basis of rapid plant pathogen evolution
Applicant Croll Daniel
Number 173265
Funding scheme Project funding (Div. I-III)
Research institution Institut de Biologie Université de Neuchâtel
Institution of higher education University of Neuchatel - NE
Main discipline Genetics
Start/End 01.08.2017 - 30.04.2021
Approved amount 549'680.00
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All Disciplines (4)

Discipline
Genetics
Botany
Agricultural and Forestry Sciences
Ecology

Keywords (6)

Genome-wide association mapping; Zymoseptoria tritici; Selection scans; Population genomics; Plant pathogens; Fungi

Lay Summary (German)

Lead
Pflanzenkrankheiten stellen eine ernsthafte Bedrohung der weltweiten Nahrungssicherheit dar. Die Züchtung von natürlichen Resistenzen gegen Pathogene hat in vielen Nutzpflanzen zu beachtlichen Erfolgen geführt. Gewisse Pathogene zeigen jedoch ein bedrohliches Potential, innerhalb kurzer Zeit Resistenzmechanismen zu überwinden. Unser Forschungsprojekt wird die Prozesse studieren, die zu schneller Anpassung von Pathogenen führen und nach Mechanismen suchen, die solche Anpassungsprozesse eindämmen können.
Lay summary

Inhalt und Ziele des Forschungsprojekts 

Wir haben in den letzten Jahren Methoden entwickelt, die uns erlauben Anpassungsprozesse in Pathogenen präzise nachzuvollziehen. Zu diesen Methoden gehören die Analyse einer grossen Anzahl vollständig sequenzierter Erbgüter (Genomen) von Pathogenpopulationen.

In diesem Projekt werden wir den Erreger erforschen, der für die Septoria-Blattdürre, die wichtigste Krankheit von Weizen, verantwortlich ist. Der erste Teil des Projekts wird aufzeigen, welche Gene im Pathogen so mutiert haben, dass sie bestimmte Resistenzen im Weizen überwinden können. Diese Analysen werden anhand von genomweiten Assoziationsstudien (GWAS) durchgeführt. Der zweite Teil des Projekts wird aufzeigen, welche Regionen im Genom der Pathogene für den Befall eines Weizenfelds verantwortlich sind. Unser besonderes Interesse gilt den Faktoren, welche die Anpassung beschleunigen oder Verlangsamen können.

Wissenschaftlicher und gesellschaftlicher Kontext des Forschungsprojekts 

Die Bekämpfung von Pflanzenkrankheiten ist eine weltweit prioritäre Aufgabe sowohl auf der ökonomischen wie auch auf der ökologischen Ebene. Das Projekt beschäftigt sich mit Anpassungsprozessen in Pathogenen, die bei Getreide zu grossen Ernteverlusten führen können. Die präzise Charakterisierung von Anpassungsprozessen wird erlauben, dauerhafte Strategien zur Krankheitseindämmung zu entwickeln. 

 
Direct link to Lay Summary Last update: 21.04.2017

Responsible applicant and co-applicants

Employees

Project partner

Publications

Publication
Emergence and diversification of a highly invasive chestnut pathogen lineage across southeastern Europe
Stauber Lea, Badet Thomas, Feurtey Alice, Prospero Simone, Croll Daniel (2021), Emergence and diversification of a highly invasive chestnut pathogen lineage across southeastern Europe, in eLife, 1.
Histone H3K27 methylation perturbs transcriptional robustness and underpins dispensability of highly conserved genes in fungi
Tralamazza Sabina Moser, Abraham Leen Nachira, Correa Benedito, Croll Daniel (2021), Histone H3K27 methylation perturbs transcriptional robustness and underpins dispensability of highly conserved genes in fungi, Cold Spring Harbor Laboratory, bioRxiv.
Machine-learning predicts genomic determinants of meiosis-driven structural variation in a eukaryotic pathogen
Badet Thomas, Fouche Simone, Hartmann Fanny E, Zala Marcello, Croll Daniel (2021), Machine-learning predicts genomic determinants of meiosis-driven structural variation in a eukaryotic pathogen, Cold Spring Harbor Laboratory, bioRxiv.
Rapid sequence evolution driven by transposable elements at a virulence locus in a fungal wheat pathogen
Singh Nikhil Kumar, Badet Thomas, Abraham Leen N, Croll Daniel (2021), Rapid sequence evolution driven by transposable elements at a virulence locus in a fungal wheat pathogen, in BMC Genomics, 1.
Soil composition and plant genotype determine benzoxazinoid-mediated plant-soil feedbacks in cereals
Cadot Selma, Gfeller Valentin, Hu Lingfei, Singh Nikhil, Sánchez-Vallet Andrea, Glauser Gaétan, Croll Daniel, Erb Matthias, van der Heijden Marcel G. A., Schlaeppi Klaus (2021), Soil composition and plant genotype determine benzoxazinoid-mediated plant-soil feedbacks in cereals, Cold Spring Harbor Laboratory, bioRxiv.
Tackling microbial threats in agriculture with integrative imaging and computational approaches
Singh Nikhil Kumar, Dutta Anik, Puccetti Guido, Croll Daniel (2021), Tackling microbial threats in agriculture with integrative imaging and computational approaches, in Computational and Structural Biotechnology Journal, 1.
The complex genomic basis of rapid convergent adaptation to pesticides across continents in a fungal plant pathogen
Hartmann Fanny E., Vonlanthen Tiziana, Singh Nikhil~Kumar, McDonald Megan, Milgate Andrew, Croll Daniel (2021), The complex genomic basis of rapid convergent adaptation to pesticides across continents in a fungal plant pathogen, in Molecular Ecology, 1.
A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici
Badet Thomas, Oggenfuss Ursula, Abraham Leen, McDonald Bruce A., Croll Daniel (2020), A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici, in BMC Biology, 18(1), 12-12.
A population-level invasion by transposable elements in a fungal pathogen
U Oggenfuss, T Badet, T Wicker, FE Hartmann, NK Singh, LN Abraham, P Karisto, T Vonlanthen, CC Mundt, BA McDonald, D Croll (2020), A population-level invasion by transposable elements in a fungal pathogen, Cold Spring Harbor, bioRxiv.
Comparative genomics analyses of lifestyle transitions at the origin of an invasive fungal pathogen in the genus Cryphonectria
Stauber Lea, Prospero Simone, Croll Daniel (2020), Comparative genomics analyses of lifestyle transitions at the origin of an invasive fungal pathogen in the genus Cryphonectria, in mSphere, 1.
Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici
Singh Nikhil Kumar, Chanclud Emilie, Croll Daniel (2020), Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici, Cold Spring Harbor Laboratory, bioRxiv.
Stress-Driven Transposable Element De-repression Dynamics and Virulence Evolution in a Fungal Pathogen
Fouché Simone, Badet Thomas, Oggenfuss Ursula, Plissonneau Clémence, Francisco Carolina Sardinha, Croll Daniel (2020), Stress-Driven Transposable Element De-repression Dynamics and Virulence Evolution in a Fungal Pathogen, in Molecular Biology and Evolution, 37(1), 221-239.
The rise and fall of genes: origins and functions of plant pathogen pangenomes
Badet Thomas, Croll Daniel (2020), The rise and fall of genes: origins and functions of plant pathogen pangenomes, in Current Opinion in Plant Biology, 56, 65-73.

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Effectome 2019 Talk given at a conference Parasites within parasites : how transposable elements drive effector evolution 23.10.2019 Lauret, France Croll Daniel; Badet Thomas;
SMBE Poster Transposable elements as drivers of intra-specific evolution of genome architecture 21.07.2019 Manchester, Great Britain and Northern Ireland Badet Thomas; Croll Daniel;
IS-MPMI 2019 Talk given at a conference Parasites within parasites : how transposable elements drive the evolution of plant pathogenic fungi 14.07.2019 Glasgow, Great Britain and Northern Ireland Badet Thomas; Singh Nikhil; Croll Daniel;
Experimental approaches to test for coevolution Poster Genetic basis of fungal pathogenicity 22.04.2018 Gif-sur-Yvette, France Croll Daniel; Singh Nikhil;
Experimental approaches to test for coevolution Poster Unravelling pathogen evolution breaking down crop resistance in agricultural ecosystems 22.04.2018 Gif-sur-Yvette, France Croll Daniel; Chanclud Emilie;
Experimental approaches to test for coevolution Talk given at a conference How pathogens rapidly surmount plant resistance in agricultural ecosystems 22.04.2018 Gif-sur-Yvette, France Croll Daniel;
Zymoseptoria tritici community meeting Poster The genetic basis of host-­‐pathogen interactions 05.09.2017 Kiel, Germany Singh Nikhil;
Zymoseptoria tritici community meeting Talk given at a conference How variation in the genome speeds up the evolution of Zymoseptoria tritici 05.09.2017 Kiel, Germany Croll Daniel;
The Sainsbury Laboratory Summer School 2017 Talk given at a conference Retracing pathogen genome evolution during rapid disease emergence 07.08.2017 Norwich, Great Britain and Northern Ireland Croll Daniel;


Self-organised

Title Date Place
Host-Microbes Genomics Meeting 2017 08.09.2017 Neuchâtel, Switzerland

Communication with the public

Communication Title Media Place Year
Media relations: radio, television CQFD RTS1 Western Switzerland 2017

Associated projects

Number Title Start Funding scheme
183365 Ultra High Performance Liquid Chromatography-High Resolution Tandem Mass Spectrometry (UHPLC-HRMS/MS) for metabolomics and identification of bioactive molecules 01.10.2019 R'EQUIP

Abstract

Plants and pathogens are locked in arms races to detect invasion and to disable host resistance, respectively. A key evolutionary step for pathogens is to evolve effectors, which are small proteins that specifically target and disable the plant immune system. The effector content is a major determinant of the pathogen's host range and evolutionary potential. The ability of hosts to detect specific pathogen effectors is expected to lead to strong directional selection on pathogen populations. However, for most plant pathogenic fungi, the content in effector genes and their evolutionary trajectory are poorly known. Plants in agricultural ecosystems are attacked by a multitude of microbial pathogens. Rapid evolution in pathogens poses a significant threat to food security. What enables pathogens to overcome disease resistance of crops and cause damage is poorly understood. In this project, we will use the highly polymorphic pathogen of wheat Zymoseptoria tritici as a model. The wheat genome encodes a large number of uncharacterized resistance factors against the pathogen. The very large population sizes of the pathogen enabled the rapid evolution of fungicide resistance and virulence on previously resistant wheat cultivars. However, it is largely unknown what loci in the pathogen genome contribute to virulence on wheat. We also lack an understanding how selection, imposed by the host’s ability to detect the pathogen, impacts the evolutionary trajectory of pathogen populations. The major goal of the proposed research is to establish a comprehensive understanding of the loci in the pathogen genome that contribute to virulence evolution. The first set of experiments will map phenotypic traits of the pathogen to loci in the genome using genome-wide association studies (GWAS). For this, we will create a highly diverse mapping population from an experimental wheat field site. We will measure the ability of fungal strains to cause disease on a series of different wheat cultivars in greenhouse experiments. We will also assay the mapping population for the ability to tolerate abiotic stress factors and quantify the secretion of secondary metabolites, which likely play a role in ecological interactions during infection. Whole genome sequencing will provide a highly dense set of genetic markers for association mapping. The second set of experiments takes a “reverse ecology” approach to identify targets of selection in pathogen populations. For this, we will collect pathogen strains in replicated plots of multiple wheat cultivars grown at the same experimental wheat field site. Pathogen genotypes better adapted to cause disease on a specific wheat cultivar are expected to accumulate over the growing season. We will perform a large-scale sequencing study to detect responses to selection in pathogen populations by identifying consistent allele frequency changes over time. Finally, we will combine knowledge gained from the first and second part of this project. Importantly, we will be able to disentangle loci segregating adaptive genetic variation to cause disease from loci responding to selection pressure to colonize the same host. In principle, pathogen loci contributing to virulence on a specific host (identified by GWAS) should match the targets of selection on the same host in the field experiments. However, mismatches in the identity of loci recovered by the two approaches will provide important insights into how ecological factors impact the evolution of host specialization. This project will identify key mechanisms driving rapid plant pathogen evolution. Knowledge generated in this project will advance the functional understanding of fungal pathogenesis and inform sustainable strategies to manage disease in agricultural ecosystems.
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