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 [4].

The study by Cécilia Fontyn and collaborators [5] 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.

REFERENCES

[1] 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

[2] 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

[3] 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

[4] 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

[5] 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