Impact of ploidy and pathogen life cycle on resistance durability

Saubin, Méline; Mita, Stéphane De; Zhu, Xiao Feng; Sudret, Bruno; Halkett, Fabien

doi:10.24072/pcjournal.10

Cited by 8 publications

(26 citation statements)

References 92 publications

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“…By contrast, once the resistance is overcome, the virulent allele(s) spread massively in the landscape (over both resistant and susceptible hosts) and the avirulent allele collapses rapidly, even in individuals living on susceptible hosts (Saubin et al, 2021). Such modelling work is in accordance with our observations.…”

Section: A Point Mutation and A Large Deletion Were Combined During R...supporting

confidence: 90%

“…Alleles conferring virulence are subjected mostly to drift as long as they are in the heterozygous state. In this respect, a recent modelling study on the dynamics of resistance breakdown highlighted that the diploid state leads to much more unpredictable evolutionary trajectories, with a delayed time for fixation of the virulence compared with haploids (Saubin et al, 2021). This phenomenon is further marked in pathogens such as M. larici-populina that require an alternate host to complete their life cycle.…”

Section: A Point Mutation and A Large Deletion Were Combined During R...mentioning

confidence: 99%

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A point mutation and large deletion at the candidate avirulence locus AvrMlp7 in the poplar rust fungus correlate with poplar RMlp7 resistance breakdown

et al. 2021

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The deployment of plant varieties carrying resistance genes (R) exerts strong selection pressure on pathogen populations. Rapidly evolving avirulence genes (Avr) allow pathogens to escape R‐mediated plant immunity through a variety of mechanisms, leading to virulence. The poplar rust fungus Melampsora larici‐populina is a damaging pathogen of poplars in Europe. It underwent a major adaptive event in 1994, with the breakdown of the poplar RMlp7 resistance gene. Population genomics studies identified a locus in the genome of M. larici‐populina that probably corresponds to the candidate avirulence gene AvrMlp7. Here, to further characterize this effector, we used a population genetics approach on a comprehensive set of 281 individuals recovered throughout a 28‐year period encompassing the resistance breakdown event. Using two dedicated molecular tools, genotyping at the candidate locus highlighted two different alterations of a predominant allele found mainly before the resistance breakdown: a nonsynonymous mutation and a complete deletion of this locus. This results in six diploid genotypes: three genotypes related to the avirulent phenotype and three related to the virulent phenotype. The temporal survey of the candidate locus revealed that both alterations were found in association during the resistance breakdown event. They pre‐existed before the breakdown in a heterozygous state with the predominant allele cited above. Altogether, these results suggest that the association of both alterations at the candidate locus AvrMlp7 drove the poplar rust adaptation to RMlp7‐mediated immunity. This study demonstrates for the first time a case of adaptation from standing genetic variation in rust fungi during a qualitative resistance breakdown.

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Section: A Point Mutation and A Large Deletion Were Combined During R...supporting

confidence: 90%

Section: A Point Mutation and A Large Deletion Were Combined During R...mentioning

confidence: 99%

A point mutation and large deletion at the candidate avirulence locus AvrMlp7 in the poplar rust fungus correlate with poplar RMlp7 resistance breakdown

et al. 2021

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“…Despite the potentially major impact of the pathogen reproduction system on the epidemiological and evolutionary control provided by resistance deployment strategies, this impact has been little studied and is poorly understood. Genetic recombination is considered in only three (Sapoukhina et al, 2009; Xu, 2012; Crété et al, 2020) of the 69 models reviewed by Rimbaud et al (2021) and in a recent study by Saubin et al (2021). These studies considered pathogens with mixed reproduction systems, but they did not compare purely clonal reproduction with mixed reproduction systems, all other things being equal.…”

Section: Introductionmentioning

confidence: 99%

“…They highlighted the role of the fitness cost of resistance in superpathogen persistence (Xu, 2012), and in the efficacy of rotation (Crété et al, 2020) and mixture (Xu, 2012; Sapoukhina et al, 2009) strategies. In addition, Saubin et al (2021) assessed the impact of ploidy on resistance durability, revealing that resistance durability was greater, but more variable, for diploid pathogens.…”

Section: Introductionmentioning

confidence: 99%

“…Genetic recombination is considered in only three (Sapoukhina et al, 2009;Xu, 2012;Crété et al, 2020) of the 69 models reviewed by Rimbaud et al (2021) and in a recent study by Saubin et al (2021). These studies considered pathogens with mixed reproduction systems, but they did not compare purely clonal reproduction with mixed reproduction systems, all other things being equal.…”

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confidence: 99%

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

Zaffaroni

Rimbaud

Rey

et al. 2023

Preprint

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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).

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Neutral genetic structuring of pathogen populations during rapid adaptation

Saubin,

Stoeckel,

Tellier

et al. 2024

Journal of Heredity

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Pathogen species are experiencing strong joint demographic and selective events, especially when they adapt to a new host, for example through overcoming plant resistance. Stochasticity in the founding event and the associated demographic variations hinder our understanding of the expected evolutionary trajectories and the genetic structure emerging at both neutral and selected loci. What would be the typical genetic signatures of such a rapid adaptation event is not elucidated. Here, we build a demogenetic model to monitor pathogen population dynamics and genetic evolution on two host compartments (susceptible and resistant). We design our model to fit two plant pathogen life cycles, ‘with’ and ‘without’ host alternation. Our aim is to draw a typology of eco-evolutionary dynamics. Using time-series clustering, we identify three main scenarios: 1) small variations in the pathogen population size and small changes in genetic structure, 2) a strong founder event on the resistant host that in turn leads to the emergence of genetic structure on the susceptible host, and 3) evolutionary rescue that results in a strong founder event on the resistant host, preceded by a bot- tleneck on the susceptible host. We pinpoint differences between life cycles with notably more evolutionary rescue ‘with’ host alternation. Beyond the selective event itself, the demographic trajectory imposes specific changes in the genetic structure of the pathogen population. Most of these genetic changes are transient, with a signature of resistance overcoming that vanishes within a few years only. Considering time-series is therefore of utmost importance to accurately decipher pathogen evolution.

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Impact of ploidy and pathogen life cycle on resistance durability

Cited by 8 publications

References 92 publications

A point mutation and large deletion at the candidate avirulence locus AvrMlp7 in the poplar rust fungus correlate with poplar RMlp7 resistance breakdown

A point mutation and large deletion at the candidate avirulence locus AvrMlp7 in the poplar rust fungus correlate with poplar RMlp7 resistance breakdown

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

Neutral genetic structuring of pathogen populations during rapid adaptation

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