Changes in aggressiveness in pathotypes of wheat leaf rust
Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of French wheat leaf rust populations
Recommendation: posted 05 April 2023, validated 06 April 2023
Gladieux, P. (2023) Changes in aggressiveness in pathotypes of wheat leaf rust. Peer Community In Infections, 100074. https://doi.org/10.24072/pci.infections.100074
Understanding the ecological and evolutionary factors underlying the spread of new fungal pathogen populations can inform the development of more effective management strategies. In plant pathology, pathogenicity is generally presented as having two components: ‘virulence’ (qualitative pathogenicity) and aggressiveness (quantitative pathogenicity). Changes in virulence in response to the deployment of new resistant varieties are a major driver of the spread of new populations (called pathotypes, or races) in modern agrosystems, and the genomic (i.e. proximal) and eco-evolutionary (i.e. ultimate) factors underlying these changes are well-documented [1,2,3]. By contrast, the role of changes in aggressiveness in the spread of pathotypes remains little known .
The study by Cécilia Fontyn and collaborators  set out to characterize changes in aggressiveness for isolates of two pathotypes of the wheat leaf rust (Puccinia triticina) that have been dominant in France during the 2005-2016 period. Isolates were genetically characterized using multilocus microsatellite typing and phenotypically characterized for three components of aggressiveness on wheat varieties: infection efficiency, latency period, and sporulation capacity. Using experiments that represent quite a remarkable amount of work and effort, Fontyn et al. showed that each dominant pathotype consisted of several genotypes, including common genotypes whose frequency changed over time. For each pathotype, the genotypes that were more common initially were replaced by a more aggressive genotype. Together, these results show that changes in the genetic composition of populations of fungal plant pathogens can be associated with, and may be caused by, changes in the quantitative components of pathogenicity. This study also illustrates how extensive, decade-long monitoring of fungal pathogen populations, such as the one conducted for wheat leaf rust in France, represents a very valuable resource for research.
 Brown, J. K. (1994). Chance and selection in the evolution of barley mildew. Trends in Microbiology, 2(12), 470-475. https://doi.org/10.1016/0966-842x(94)90650-5
 Daverdin, G., Rouxel, T., Gout, L., Aubertot, J. N., Fudal, I., Meyer, M., Parlange, F., Carpezat, J., & Balesdent, M. H. (2012). Genome structure and reproductive behaviour influence the evolutionary potential of a fungal phytopathogen. PLoS Pathogens, 8(11), e1003020. https://doi.org/10.1371/journal.ppat.1003020
 Gladieux, P., Feurtey, A., Hood, M. E., Snirc, A., Clavel, J., Dutech, C., Roy, M., & Giraud, T. (2015). The population biology of fungal invasions.Molecular Ecology, 24(9), 1969-86. https://doi.org/10.1111/mec.13028
 Fontyn, C., Zippert, A. C., Delestre, G., Marcel, T. C., Suffert, F., & Goyeau, H. (2022). Is virulence phenotype evolution driven exclusively by Lr gene deployment in French Puccinia triticina populations?. Plant Pathology, 71(7), 1511-1524. https://doi.org/10.1111/ppa.13599
 Fontyn, C., Meyer, K. J., Boixel, A. L., Delestre, G., Piaget, E., Picard, C., Suffer, F., Marcel, T.C., & Goyeau, H. (2022). Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of French wheat leaf rust populations. bioRxiv, 2022.08.29.505401, ver. 3 peer-reviewed and recommended by Peer Community in Infections. https://doi.org/10.1101/2022.08.29.505401
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
This research was supported by a PhD fellowship from the INRAE department ‘Santé des Plantes et Environnement’ (SPE) and from the French Ministry of Education and Research (MESRI) awarded to Cécilia Fontyn for the 2018-2022 period. It was also supported by several French FSOV (‘Fonds de Soutien à l’Obtention Végétale’) grants (FSOV 2004 K, 2008 G, 2012 Q) and by the European Commission, Research and Innovation under the Horizon 2020 program (RUSTWATCH 2018-2022, Grant Agreement no. 773311-2)
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/2022.08.29.505401
Version of the preprint: 2
Author's Reply, 02 Mar 2023
Decision by Pierre Gladieux, posted 01 Dec 2022, validated 01 Dec 2022
Dear Dr. Marcel, Dear all,
Your preprint entitled "Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of French wheat leaf rust populations,» which you submitted to PCI-Infections, has been reviewed. The comments of the reviewers are included at the bottom of this letter.
I enjoyed reading your manuscript, which represents a large amount of experimental work and presents interesting and insightful results. However, based on the comments of the reviewers and my assessment, your manuscript will require revisions before further consideration for a recommendation.
One main concern raised by reviewer 1 is the nature and presentation of statistical analyses. Please review your analyzes and their presentation and modify your conclusions accordingly.
Another concern raised by reviewer 1 is the content and length of the discussion. Four pages of results and ten pages of discussion seem highly unbalanced indeed.
Both reviewers and I (see below) also expressed various concerns regarding the hypothesis at the core of this study. After reading your preprint, I have the impression that you are not testing the hypothesis described in the abstract or introduction but another, which also has its merits but needs to be better introduced.
The central hypothesis of the article is unclear for several reasons:
- The introduction suggests that changes in aggressiveness are caused by quantitative resistance. For instance, line 102 reads: « the quantitative resistance genes introgressed into new wheat cultivars at the same time as qualitative resistance genes may also exert a selection pressure in favor of more aggressive pathotypes .» However, as underlined by both reviewers, the connection between natural selection for increased aggressiveness and quantitative resistance of the host is unclear: do we need to invoke quantitative resistance to explain the evolution of aggressiveness? Then, if the hypothesis is that quantitative resistance is at the origin of the variations of aggressiveness, why never mention - and test the effect of - the variations of quantitative resistance between the hosts included in the annual survey and the experiments? Finally, this sentence also conveys the idea that the genetic bases of quantitative and qualitative resistance would be distinct, just like the genetic bases of virulence or aggressiveness, which is probably an unnecessary simplification, as pointed out by reviewer 2.
- As I struggled to understand your hypothesis, I read Fontyn et al. 2022 doi.org/10.1111/ppa.13599. In this article, if I understand correctly, you formulate the hypothesis according to which the pathotypes 166 317 0 and 106 314 0 correspond to generalist lineages, whose greater aggressiveness allows them to outcompete several other compatible pathotypes virulent against the Lr genes carried by the most widely grown cultivars (9th paragraph of the discussion, starting with « PCA revealed… »). You take up this hypothesis in the introduction to your preprint L112-118. Based on this hypothesis, I expected to see a comparison between the major pathotypes and the other pathotypes. Instead, I observed that you were interested in the genotypic diversity of pathotypes and that you tested the hypothesis of a role of aggressiveness in the temporal dynamics of genotypes underlying the same pathotype.
I have highlighted some reviewer comments here, but I invite you to consider each in your revised preprint.
L132 and L232-236: you used five cultivars widely grown over the study period. How many resistance genes matching virulence in the pathotypes do each of these cultivars carry?
L235: « were among the 35 most frequently grown cultivars in the French landscape during the 2006-2016 period. ». How frequent are they? What is the frequency of the 35th most frequently grown cultivar?