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Uncovering the history of recombination and population structure in western Canadian stripe rust populations through mating type alleles

BACKGROUND: The population structure of crop pathogens such as Puccinia striiformis f. sp. tritici (Pst), the cause of wheat stripe rust, is of interest to researchers looking to understand these pathogens on a molecular level as well as those with an applied focus such as disease epidemiology. Cere...

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Autores principales: Holden, Samuel, Bakkeren, Guus, Hubensky, John, Bamrah, Ramandeep, Abbasi, Mehrdad, Qutob, Dinah, de Graaf, Mei-Lan, Kim, Sang Hu, Kutcher, Hadley R., McCallum, Brent D., Randhawa, Harpinder S., Iqbal, Muhammad, Uloth, Keith, Burlakoti, Rishi R., Brar, Gurcharn S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10601111/
https://www.ncbi.nlm.nih.gov/pubmed/37880702
http://dx.doi.org/10.1186/s12915-023-01717-9
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author Holden, Samuel
Bakkeren, Guus
Hubensky, John
Bamrah, Ramandeep
Abbasi, Mehrdad
Qutob, Dinah
de Graaf, Mei-Lan
Kim, Sang Hu
Kutcher, Hadley R.
McCallum, Brent D.
Randhawa, Harpinder S.
Iqbal, Muhammad
Uloth, Keith
Burlakoti, Rishi R.
Brar, Gurcharn S.
author_facet Holden, Samuel
Bakkeren, Guus
Hubensky, John
Bamrah, Ramandeep
Abbasi, Mehrdad
Qutob, Dinah
de Graaf, Mei-Lan
Kim, Sang Hu
Kutcher, Hadley R.
McCallum, Brent D.
Randhawa, Harpinder S.
Iqbal, Muhammad
Uloth, Keith
Burlakoti, Rishi R.
Brar, Gurcharn S.
author_sort Holden, Samuel
collection PubMed
description BACKGROUND: The population structure of crop pathogens such as Puccinia striiformis f. sp. tritici (Pst), the cause of wheat stripe rust, is of interest to researchers looking to understand these pathogens on a molecular level as well as those with an applied focus such as disease epidemiology. Cereal rusts can reproduce sexually or asexually, and the emergence of novel lineages has the potential to cause serious epidemics such as the one caused by the ‘Warrior’ lineage in Europe. In a global context, Pst lineages in Canada were not well-characterized and the origin of foreign incursions was not known. Additionally, while some Pst mating type genes have been identified in published genomes, there has been no rigorous assessment of mating type diversity and distribution across the species. RESULTS: We used a whole-genome/transcriptome sequencing approach for the Canadian Pst population to identify lineages in their global context and evidence tracing foreign incursions. More importantly: for the first time ever, we identified nine alleles of the homeodomain mating type locus in the worldwide Pst population and show that previously identified lineages exhibit a single pair of these alleles. Consistently with the literature, we find only two pheromone receptor mating type alleles. We show that the recent population shift from the ‘PstS1’ lineage to the ‘PstS1-related’ lineage is also associated with the introduction of a novel mating type allele (Pst-b3-HD) to the Canadian population. We also show evidence for high levels of mating type diversity in samples associated with the Himalayan center of diversity for Pst, including a single Canadian race previously identified as ‘PstPr’ (probable recombinant) which we identify as a foreign incursion, most closely related to isolates sampled from China circa 2015. CONCLUSIONS: These data describe a recent shift in the population of Canadian Pst field isolates and characterize homeodomain-locus mating type alleles in the global Pst population which can now be utilized in testing several research questions and hypotheses around sexuality and hybridization in rust fungi. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01717-9.
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spelling pubmed-106011112023-10-27 Uncovering the history of recombination and population structure in western Canadian stripe rust populations through mating type alleles Holden, Samuel Bakkeren, Guus Hubensky, John Bamrah, Ramandeep Abbasi, Mehrdad Qutob, Dinah de Graaf, Mei-Lan Kim, Sang Hu Kutcher, Hadley R. McCallum, Brent D. Randhawa, Harpinder S. Iqbal, Muhammad Uloth, Keith Burlakoti, Rishi R. Brar, Gurcharn S. BMC Biol Research Article BACKGROUND: The population structure of crop pathogens such as Puccinia striiformis f. sp. tritici (Pst), the cause of wheat stripe rust, is of interest to researchers looking to understand these pathogens on a molecular level as well as those with an applied focus such as disease epidemiology. Cereal rusts can reproduce sexually or asexually, and the emergence of novel lineages has the potential to cause serious epidemics such as the one caused by the ‘Warrior’ lineage in Europe. In a global context, Pst lineages in Canada were not well-characterized and the origin of foreign incursions was not known. Additionally, while some Pst mating type genes have been identified in published genomes, there has been no rigorous assessment of mating type diversity and distribution across the species. RESULTS: We used a whole-genome/transcriptome sequencing approach for the Canadian Pst population to identify lineages in their global context and evidence tracing foreign incursions. More importantly: for the first time ever, we identified nine alleles of the homeodomain mating type locus in the worldwide Pst population and show that previously identified lineages exhibit a single pair of these alleles. Consistently with the literature, we find only two pheromone receptor mating type alleles. We show that the recent population shift from the ‘PstS1’ lineage to the ‘PstS1-related’ lineage is also associated with the introduction of a novel mating type allele (Pst-b3-HD) to the Canadian population. We also show evidence for high levels of mating type diversity in samples associated with the Himalayan center of diversity for Pst, including a single Canadian race previously identified as ‘PstPr’ (probable recombinant) which we identify as a foreign incursion, most closely related to isolates sampled from China circa 2015. CONCLUSIONS: These data describe a recent shift in the population of Canadian Pst field isolates and characterize homeodomain-locus mating type alleles in the global Pst population which can now be utilized in testing several research questions and hypotheses around sexuality and hybridization in rust fungi. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01717-9. BioMed Central 2023-10-25 /pmc/articles/PMC10601111/ /pubmed/37880702 http://dx.doi.org/10.1186/s12915-023-01717-9 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Holden, Samuel
Bakkeren, Guus
Hubensky, John
Bamrah, Ramandeep
Abbasi, Mehrdad
Qutob, Dinah
de Graaf, Mei-Lan
Kim, Sang Hu
Kutcher, Hadley R.
McCallum, Brent D.
Randhawa, Harpinder S.
Iqbal, Muhammad
Uloth, Keith
Burlakoti, Rishi R.
Brar, Gurcharn S.
Uncovering the history of recombination and population structure in western Canadian stripe rust populations through mating type alleles
title Uncovering the history of recombination and population structure in western Canadian stripe rust populations through mating type alleles
title_full Uncovering the history of recombination and population structure in western Canadian stripe rust populations through mating type alleles
title_fullStr Uncovering the history of recombination and population structure in western Canadian stripe rust populations through mating type alleles
title_full_unstemmed Uncovering the history of recombination and population structure in western Canadian stripe rust populations through mating type alleles
title_short Uncovering the history of recombination and population structure in western Canadian stripe rust populations through mating type alleles
title_sort uncovering the history of recombination and population structure in western canadian stripe rust populations through mating type alleles
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10601111/
https://www.ncbi.nlm.nih.gov/pubmed/37880702
http://dx.doi.org/10.1186/s12915-023-01717-9
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