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      Genome Structure and Reproductive Behaviour Influence the Evolutionary Potential of a Fungal Phytopathogen

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          Modern agriculture favours the selection and spread of novel plant diseases. Furthermore, crop genetic resistance against pathogens is often rendered ineffective within a few years of its commercial deployment. Leptosphaeria maculans, the cause of phoma stem canker of oilseed rape, develops gene-for-gene interactions with its host plant, and has a high evolutionary potential to render ineffective novel sources of resistance in crops. Here, we established a four-year field experiment to monitor the evolution of populations confronted with the newly released Rlm7 resistance and to investigate the nature of the mutations responsible for virulence against Rlm7. A total of 2551 fungal isolates were collected from experimental crops of a Rlm7 cultivar or a cultivar without Rlm7. All isolates were phenotyped for virulence and a subset was genotyped with neutral genetic markers. Virulent isolates were investigated for molecular events at the AvrLm4-7 locus. Whilst virulent isolates were not found in neighbouring crops, their frequency had reached 36% in the experimental field after four years. An extreme diversity of independent molecular events leading to virulence was identified in populations, with large-scale Repeat Induced Point mutations or complete deletion of AvrLm4-7 being the most frequent. Our data suggest that increased mutability of fungal genes involved in the interactions with plants is directly related to their genomic environment and reproductive system. Thus, rapid allelic diversification of avirulence genes can be generated in L. maculans populations in a single field provided that large population sizes and sexual reproduction are favoured by agricultural practices.

          Author Summary

          Plant disease resistance often relies on simple “gene-for-gene” systems and, in the pathogen, a mutation in a single “avirulence” gene matching the plant resistance gene is sufficient to render the resistance ineffective. In agricultural systems, breeding for resistance is challenged by both the high evolutionary potential of the pathogen and the large scale of crop production; together, these factors encourage “breakdown” of novel sources of resistance soon after their deployment. Here, we established a four-year field experiment to evaluate the mechanisms and speed with which a fungal pathogen of oilseed rape, Leptosphaeria maculans renders ineffective the novel resistance gene Rlm7. The pathogen showed a very high evolutionary potential; the proportion of isolates in the population that were virulent against Rlm7 increased from 0 to 36% in four years. The experiment demonstrated that an extremely diverse range of molecular events leading to virulence, from more or less extensive nucleotide mutations or deletions to complete gene deletion, can occur in a single field. These results suggest that the genomic environment of the avirulence gene and the reproductive regime of the pathogen promote mutability at a single locus to produce virulence. Cropping practices that promote large pathogen populations and encourage sexual reproduction therefore favour rapid adaptation of the pathogen to the novel resistance.

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          Most cited references 38

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              A method is presented by which the gene diversity (heterozygosity) of a subdivided population can be analyzed into its components, i.e., the gene diversities within and between subpopulations. This method is applicable to any population without regard to the number of alleles per locus, the pattern of evolutionary forces such as mutation, selection, and migration, and the reproductive method of the organism used. Measures of the absolute and relative magnitudes of gene differentiation among subpopulations are also proposed.

                Author and article information

                Role: Editor
                PLoS Pathog
                PLoS Pathog
                PLoS Pathogens
                Public Library of Science (San Francisco, USA )
                November 2012
                November 2012
                8 November 2012
                : 8
                : 11
                [1 ]INRA, UR 1290 Bioger, Campus AgroParisTech, Thiverval-Grignon, France
                [2 ]AgroParisTech, Campus AgroParisTech, Thiverval-Grignon, France
                [3 ]INRA, UMR 1248 AGIR, Castanet Tolosan, France
                [4 ]CETIOM, Campus AgroParisTech, Thiverval-Grignon, France
                University of Melbourne, Australia
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: LG JNA MHB. Performed the experiments: GD IF MM JC MHB FP. Analyzed the data: GD TR LG JNA IF MM MHB FP. Wrote the paper: GD TR LG MHB.


                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Pages: 15
                This work was funded by the ANR project CEDRE (ANR-PADD-005), the CASDAR Project 05391(2006–09) « Mise au point et utilisation d'outils de biovigilance et de gestion durable des résistances variétales aux pathogènes », and a grant from the Santé des Plantes et Environnement (SPE) INRA department. G. Daverdin was funded by the French ministry of research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Research Article
                Crop Diseases
                Evolutionary Biology
                Population Genetics
                Host-Pathogen Interaction
                Plant Microbiology

                Infectious disease & Microbiology


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