Section: Infections
Topic: Biology of interactions, Evolution, Plant biology

Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of French wheat leaf rust populations

10.24072/pcjournal.264 - Peer Community Journal, Volume 3 (2023), article no. e39.

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Plant pathogens are constantly evolving and adapting to their environment, including their host. Virulence alleles emerge, and then increase, and sometimes decrease in frequency within pathogen populations in response to the fluctuating selection pressures imposed by the deployment of resistance genes. In some cases, these strong selection pressures cannot fully explain the evolution observed in pathogen populations. A previous study on the French population of Puccinia triticina, the causal agent of wheat leaf rust, showed that two major pathotypes — groups of isolates with a particular combination of virulences — predominated but then declined over the 2005-2016 period. The relative dynamics and the domination of these two pathotypes — 166 317 0 and 106 314 0 —, relative to the other pathotypes present in the population at a low frequency although compatible, i.e. virulent on several varieties deployed, could not be explained solely by the frequency of Lr genes in the landscape. Within these two pathotypes, we identified two main genotypes that emerged in succession. We assessed three components of aggressiveness — infection efficiency, latency period and sporulation capacity — for 44 isolates representative of the four P. triticina pathotype-genotype combinations. We showed, for both pathotypes, that the more recent genotypes were more aggressive than the older ones. Our findings were highly consistent for the various components of aggressiveness for pathotype 166 317 0 grown on Michigan Amber — a ‘naive’ cultivar never grown in the landscape — or on Apache — a ‘neutral’ cultivar, which does not affect the pathotype frequency in the landscape and therefore was postulated to have no or minor selection effect on the population composition. For pathotype 106 314 0, the most recent genotype had a shorter latency period on several of the cultivars most frequently grown in the landscape, but not on ‘neutral’ and ‘naive’ cultivars. We conclude that the quantitative components of aggressiveness can be significant drivers of evolution in pathogen populations. A gain in aggressiveness stopped the decline in frequency of a pathotype, and subsequently allowed an increase in frequency of this pathotype in the pathogen population, providing evidence that adaptation to a changing varietal landscape not only affects virulence but can also lead to changes in aggressiveness.

Published online:
DOI: 10.24072/pcjournal.264
Type: Research article
Keywords: Aggressiveness, quantitative phenotyping, genotype evolution, host adaptation, Puccinia triticina
Keywords: Aggressiveness, quantitative phenotyping, genotype evolution, host adaptation, Puccinia triticina
Fontyn, Cécilia 1; Meyer, Kevin JG 1; Boixel, Anne-Lise 1; Delestre, Ghislain 1; Piaget, Emma 1; Picard, Corentin 1; Suffert, Frédéric 1; Marcel, Thierry C 1; Goyeau, Henriette 1

1 Université Paris-Saclay, INRAE, UR BIOGER, 91120 Palaiseau, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Fontyn, C\'ecilia and Meyer, Kevin JG and Boixel, Anne-Lise and Delestre, Ghislain and Piaget, Emma and Picard, Corentin and Suffert, Fr\'ed\'eric and Marcel, Thierry C and Goyeau, Henriette},
     title = {Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of {French} wheat leaf rust populations},
     journal = {Peer Community Journal},
     eid = {e39},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.264},
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AU  - Meyer, Kevin JG
AU  - Boixel, Anne-Lise
AU  - Delestre, Ghislain
AU  - Piaget, Emma
AU  - Picard, Corentin
AU  - Suffert, Frédéric
AU  - Marcel, Thierry C
AU  - Goyeau, Henriette
TI  - Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of French wheat leaf rust populations
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
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DO  - 10.24072/pcjournal.264
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%A Fontyn, Cécilia
%A Meyer, Kevin JG
%A Boixel, Anne-Lise
%A Delestre, Ghislain
%A Piaget, Emma
%A Picard, Corentin
%A Suffert, Frédéric
%A Marcel, Thierry C
%A Goyeau, Henriette
%T Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of French wheat leaf rust populations
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%R 10.24072/pcjournal.264
%F 10_24072_pcjournal_264
Fontyn, Cécilia; Meyer, Kevin JG; Boixel, Anne-Lise; Delestre, Ghislain; Piaget, Emma; Picard, Corentin; Suffert, Frédéric; Marcel, Thierry C; Goyeau, Henriette. Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of French wheat leaf rust populations. Peer Community Journal, Volume 3 (2023), article  no. e39. doi : 10.24072/pcjournal.264.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.infections.100074

Conflict of interest of the recommender and peer reviewers:
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.

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