Genome structure and reproductive behaviour influence the evolutionary potential of a fungal phytopathogen.

Guillaume Daverdin,Jean-Noël Aubertot,Thierry Rouxel,Julien Carpezat,Marie-Hélène Balesdent,Michel Meyer,Francis Parlange,Lilian Gout,Isabelle Fudal,Alex Andrianopoulos

doi:10.1371/journal.ppat.1003020

Abstract

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.

Highlights

Fungi are the most important pathogens of cultivated plants, with significant economic, food security and environmental impacts, the latter being due to the large quantities of fungicides used to control plant diseases [1]
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

Summary

Introduction

Fungi are the most important pathogens of cultivated plants, with significant economic, food security and environmental impacts, the latter being due to the large quantities of fungicides used to control plant diseases [1]. In contrast to fungicide use, genetic resistance against pathogens in crops is an environmentally friendly strategy to control diseases. Effective resistance has been provided by the introduction of major resistance (R) genes into crop genotypes [2]. Fungal pathogens have an incredible plasticity with which they can respond to their environment. Their ability to adapt to changes in their environment and to disseminate these adaptations makes them very successful in countering crop defenses and control methods [1]. The rapid emergence of new strains able to render ineffective new R genes is a common feature of fungal phytopathogens [3]

Methods

Results

Discussion

Conclusion