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

Abstract 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 epidemiolo...

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Main Authors: Samuel Holden, Guus Bakkeren, John Hubensky, Ramandeep Bamrah, Mehrdad Abbasi, Dinah Qutob, Mei-Lan de Graaf, Sang Hu Kim, Hadley R. Kutcher, Brent D. McCallum, Harpinder S. Randhawa, Muhammad Iqbal, Keith Uloth, Rishi R. Burlakoti, Gurcharn S. Brar
Format: Article
Language:English
Published: BMC 2023-10-01
Series:BMC Biology
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Online Access:https://doi.org/10.1186/s12915-023-01717-9
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author Samuel Holden
Guus Bakkeren
John Hubensky
Ramandeep Bamrah
Mehrdad Abbasi
Dinah Qutob
Mei-Lan de Graaf
Sang Hu Kim
Hadley R. Kutcher
Brent D. McCallum
Harpinder S. Randhawa
Muhammad Iqbal
Keith Uloth
Rishi R. Burlakoti
Gurcharn S. Brar
author_facet Samuel Holden
Guus Bakkeren
John Hubensky
Ramandeep Bamrah
Mehrdad Abbasi
Dinah Qutob
Mei-Lan de Graaf
Sang Hu Kim
Hadley R. Kutcher
Brent D. McCallum
Harpinder S. Randhawa
Muhammad Iqbal
Keith Uloth
Rishi R. Burlakoti
Gurcharn S. Brar
author_sort Samuel Holden
collection DOAJ
description Abstract 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.
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spelling doaj.art-aeb30ed05aa1461ebc0e7a96de55e42f2023-11-20T10:55:31ZengBMCBMC Biology1741-70072023-10-0121111510.1186/s12915-023-01717-9Uncovering the history of recombination and population structure in western Canadian stripe rust populations through mating type allelesSamuel Holden0Guus Bakkeren1John Hubensky2Ramandeep Bamrah3Mehrdad Abbasi4Dinah Qutob5Mei-Lan de Graaf6Sang Hu Kim7Hadley R. Kutcher8Brent D. McCallum9Harpinder S. Randhawa10Muhammad Iqbal11Keith Uloth12Rishi R. Burlakoti13Gurcharn S. Brar14Faculty of Land and Food Systems, The University of British Columbia (UBC)Agriculture and Agri-Food Canada (AAFC), Summerland Research and Development CenterFaculty of Land and Food Systems, The University of British Columbia (UBC)Faculty of Land and Food Systems, The University of British Columbia (UBC)Faculty of Land and Food Systems, The University of British Columbia (UBC)Kent State University, Stark CampusAgriculture and Agri-Food Canada (AAFC), Summerland Research and Development CenterAgriculture and Agri-Food Canada (AAFC), Summerland Research and Development CenterDepartment of Plant Science/Crop Development Centre, University of SaskatchewanAgriculture and Agri-Food Canada (AAFC), Brandon Research and Development CenterAgriculture and Agri-Food Canada (AAFC), Lethbridge Research and Development CenterFaculty of Agricultural, Life & Environmental Sciences, University of AlbertaBritish Columbia Pest Monitoring NetworkAgriculture and Agri-Food Canada (AAFC), Agassiz Research and Development CenterFaculty of Land and Food Systems, The University of British Columbia (UBC)Abstract 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.https://doi.org/10.1186/s12915-023-01717-9Puccinia striiformis f. sp. triticiStripe rustPlant-pathogen interactionsFungal mating typeField pathogenomics
spellingShingle Samuel Holden
Guus Bakkeren
John Hubensky
Ramandeep Bamrah
Mehrdad Abbasi
Dinah Qutob
Mei-Lan de Graaf
Sang Hu Kim
Hadley R. Kutcher
Brent D. McCallum
Harpinder S. Randhawa
Muhammad Iqbal
Keith Uloth
Rishi R. Burlakoti
Gurcharn S. Brar
Uncovering the history of recombination and population structure in western Canadian stripe rust populations through mating type alleles
BMC Biology
Puccinia striiformis f. sp. tritici
Stripe rust
Plant-pathogen interactions
Fungal mating type
Field pathogenomics
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 Puccinia striiformis f. sp. tritici
Stripe rust
Plant-pathogen interactions
Fungal mating type
Field pathogenomics
url https://doi.org/10.1186/s12915-023-01717-9
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