Effects of pathogen sexual reproduction on the evolutionary and epidemiological control provided by deployment strategies for two major resistance genes in agricultural landscapes

Abstract

Resistant cultivars are of value for protecting crops from disease, but can be rapidly overcome by pathogens. Several strategies have been proposed to delay pathogen adaptation (evolutionary control), while maintaining effective protection (epidemiological control). Resistance genes can be i) combined in the same cultivar (pyramiding), ii) deployed in different cultivars sown in the same field (mixtures) or in different fields (mosaics), or iii) alternated over time (rotations). The outcomes of these strategies have been investigated principally in pathogens displaying pure clonal reproduction, but sexual reproduction may promote the emergence of superpathogens adapted to all the resistance genes deployed. We improved the spatially explicit stochastic modellandsepito include pathogen sexual reproduction, and then investigate the effect of sexual reproduction on evolutionary and epidemiological outcomes across deployment strategies for two major resistance genes. Sexual reproduction only favours the establishment of a superpathogen when single mutant pathogens are present together at a sufficiently high frequency, as in mosaic and mixture strategies. We concluded that, although sexual reproduction may promote the establishment of a superpathogen, it did not affect the optimal strategy recommendations for a wide range of mutation probabilities, associated fitness costs, and landscape organisations (notably the cropping ratio of resistant fields).

Combining single-gene-resistant and pyramided cultivars in agricultural landscape compromises the benefits of pyramiding in most, but not all, productions situations

“…The latter case requires the existence of single mutants pathogens that are: 1) possibly less competitive than wild type ones on susceptible hosts and 2) not able to infect the pyramided cultivar. This explains why, at low mutation probability or high fitness cost of virulence, pyramiding has been proven to be the best strategy in controlling the epidemic and avoiding the breakdown of resistance genes (Lof et al, 2017; Rimbaud et al, 2018b; Zaffaroni et al, 2023). However, our results indicated that concurrently deploying a pyramided cultivar along with single-gene-resistant cultivars, carrying the resistance genes stacked into the pyramid, could often result in a drastic decrease in the evolutionary and epidemiological control provided by pyramiding.…”

“…We used the version of the model presented in Zaffaroni et al (2023). This model simulates the spread and evolution of a pathogen alternating within-season clonal reproduction and between-season sexual reproduction in an heterogeneous agricultural landscape over multiple cropping seasons.…”

“…Simulations were run for 30 cropping seasons of 120 days each. Preliminary trials (Zaffaroni et al, 2023) showed that this simulation horizon was sufficiently long to differentiate the performances of the deployment strategies considered. Note that for each simulation the allocation of cultivars to the fields in the landscape was randomly assigned.…”

“…Indeed, the effects of the probability of mutation and of the fitness cost associated to pathogen virulence have not been explored by Lof et al (2017). Yet, these two parameters, under-investigated in plant pathology, greatly affect the emergence of a super-pathogen adapted to all the deployed resistance genes (Zaffaroni et al, 2023). Moreover, Lof et al (2017) considered only mosaic strategies where the single-gene-resistant cultivars are deployed in different fields, while these could be planted as mixture in the same field.…”

“…Third, the history of pyramiding has led to some of the great successes of plant pathology, such as the control of wheat stem rust (Mundt, 2018). From a theoretical perspective, mathematical models suggest that the pyramiding strategy provides a better evolutionary and epidemiological control than mixture and mosaic strategies, for a variety of pathogen reproductive systems, as soon as no adapted pathogens preexist in the pathogen population and mutations rates are low (Lof et al, 2017; Rimbaud et al, 2018a; Zaffaroni et al, 2023). In this setting, the evolutionary control could be achieved for decades while the epidemiological control increases with the proportion of the fields planted with a pyramided cultivar.…”