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Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici

Pathogens cause significant challenges to global food security. On annual crops, pathogens must re-infect from environmental sources in every growing season. Fungal pathogens have evolved mixed reproductive strategies to cope with the distinct challenges of colonizing growing plants. However, how pa...

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Autores principales: Singh, Nikhil Kumar, Karisto, Petteri, Croll, Daniel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Microbiology Society 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8627204/
https://www.ncbi.nlm.nih.gov/pubmed/34617882
http://dx.doi.org/10.1099/mgen.0.000678
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author Singh, Nikhil Kumar
Karisto, Petteri
Croll, Daniel
author_facet Singh, Nikhil Kumar
Karisto, Petteri
Croll, Daniel
author_sort Singh, Nikhil Kumar
collection PubMed
description Pathogens cause significant challenges to global food security. On annual crops, pathogens must re-infect from environmental sources in every growing season. Fungal pathogens have evolved mixed reproductive strategies to cope with the distinct challenges of colonizing growing plants. However, how pathogen diversity evolves during growing seasons remains largely unknown. Here, we performed a deep hierarchical sampling in a single experimental wheat field infected by the major fungal pathogen Zymoseptoria tritici. We analysed whole genome sequences of 177 isolates collected from 12 distinct cultivars replicated in space at three time points of the growing season to maximize capture of genetic diversity. The field population was highly diverse with 37 SNPs per kilobase, a linkage disequilibrium decay within 200–700 bp and a high effective population size. Using experimental infections, we tested a subset of the collected isolates on the dominant cultivar planted in the field. However, we found no significant difference in virulence of isolates collected from the same cultivar compared to isolates collected on other cultivars. About 20 % of the isolate genotypes were grouped into 15 clonal groups. Pairs of clones were disproportionally found at short distances (<5 m), consistent with experimental estimates for per-generation dispersal distances performed in the same field. This confirms predominant leaf-to-leaf transmission during the growing season. Surprisingly, levels of clonality did not increase over time in the field although reproduction is thought to be exclusively asexual during the growing season. Our study shows that the pathogen establishes vast and stable gene pools in single fields. Monitoring short-term evolutionary changes in crop pathogens will inform more durable strategies to contain diseases.
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spelling pubmed-86272042021-11-29 Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici Singh, Nikhil Kumar Karisto, Petteri Croll, Daniel Microb Genom Research Articles Pathogens cause significant challenges to global food security. On annual crops, pathogens must re-infect from environmental sources in every growing season. Fungal pathogens have evolved mixed reproductive strategies to cope with the distinct challenges of colonizing growing plants. However, how pathogen diversity evolves during growing seasons remains largely unknown. Here, we performed a deep hierarchical sampling in a single experimental wheat field infected by the major fungal pathogen Zymoseptoria tritici. We analysed whole genome sequences of 177 isolates collected from 12 distinct cultivars replicated in space at three time points of the growing season to maximize capture of genetic diversity. The field population was highly diverse with 37 SNPs per kilobase, a linkage disequilibrium decay within 200–700 bp and a high effective population size. Using experimental infections, we tested a subset of the collected isolates on the dominant cultivar planted in the field. However, we found no significant difference in virulence of isolates collected from the same cultivar compared to isolates collected on other cultivars. About 20 % of the isolate genotypes were grouped into 15 clonal groups. Pairs of clones were disproportionally found at short distances (<5 m), consistent with experimental estimates for per-generation dispersal distances performed in the same field. This confirms predominant leaf-to-leaf transmission during the growing season. Surprisingly, levels of clonality did not increase over time in the field although reproduction is thought to be exclusively asexual during the growing season. Our study shows that the pathogen establishes vast and stable gene pools in single fields. Monitoring short-term evolutionary changes in crop pathogens will inform more durable strategies to contain diseases. Microbiology Society 2021-10-07 /pmc/articles/PMC8627204/ /pubmed/34617882 http://dx.doi.org/10.1099/mgen.0.000678 Text en © 2021 The Authors https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
spellingShingle Research Articles
Singh, Nikhil Kumar
Karisto, Petteri
Croll, Daniel
Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici
title Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici
title_full Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici
title_fullStr Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici
title_full_unstemmed Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici
title_short Population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen Zymoseptoria tritici
title_sort population-level deep sequencing reveals the interplay of clonal and sexual reproduction in the fungal wheat pathogen zymoseptoria tritici
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8627204/
https://www.ncbi.nlm.nih.gov/pubmed/34617882
http://dx.doi.org/10.1099/mgen.0.000678
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