Epidemiological and evolutionary management of plant resistance: optimizing the deployment of cultivar mixtures in time and space in agricultural landscapes.

Frédéric Fabre,Ludovic Mailleret,Benoît Moury,Elsa Rousseau

doi:10.1111/eva.12304

Abstract

The management of genes conferring resistance to plant–pathogens should make it possible to control epidemics (epidemiological perspective) and preserve resistance durability (evolutionary perspective). Resistant and susceptible cultivars must be strategically associated according to the principles of cultivar mixture (within a season) and rotation (between seasons). We explored these questions by modeling the evolutionary and epidemiological processes shaping the dynamics of a pathogen population in a landscape composed of a seasonal cultivated compartment and a reservoir compartment hosting pathogen year-round. Optimal deployment strategies depended mostly on the molecular basis of plant–pathogen interactions and on the agro-ecological context before resistance deployment, particularly epidemic intensity and landscape connectivity. Mixtures were much more efficient in landscapes in which between-field infections and infections originating from the reservoir were more prevalent than within-field infections. Resistance genes requiring two mutations of the pathogen avirulence gene to be broken down, rather than one, were particularly useful when infections from the reservoir predominated. Combining mixture and rotation principles were better than the use of the same mixture each season as (i) they controlled epidemics more effectively in situations in which within-field infections or infections from the reservoir were frequent and (ii) they fulfilled the epidemiological and evolutionary perspectives.

Highlights

Integrating the principles governing natural ecosystems into crop protection strategies should be a powerful way to face the challenge of doubling crop production in the four decades while decreasing the environmental impact of agriculture (Tilman 1999)
We analyzed a model explicitly linking the epidemiological and population genetics processes occurring at nested levels of biological organization: (i) within-host population genetics and evolutionary processes and (ii) between-host epidemiological processes
If we assume that the initial pathogen population has never been exposed to a resistant cultivar, the model describes, at the landscape scale, the dynamics of emergence of a resistance-breaking pathogen and the associated epidemiological dynamics during a succession of cropping seasons in which the resistant cultivar can be sown in variable proportions

Summary

Introduction

Integrating the principles governing natural ecosystems into crop protection strategies should be a powerful way to face the challenge of doubling crop production in the four decades while decreasing the environmental impact of agriculture (Tilman 1999). Functional diversity in disease resistance decreases disease spread (Mundt 2002; Garrett et al 2009). This approach has been successful in the control of powdery mildew in barley and blast disease in rice (Wolfe 1985; Zhu et al 2000). The molecular dissection of these interactions for viruses has revealed that (i) one or two nucleotide substitutions in virus avirulence genes are often sufficient to overcome resistance genes (Jenner et al 2002; Kang et al 2005; Fraile et al 2011; Moury et al 2011) and (ii) these substitutions have variable fitness costs in susceptible plants (Ayme et al 2006; Janzac et al 2010)

Methods

Results

Conclusion