Genome-Enabled Analysis of Population Dynamics and Virulence-Associated Loci in the Oat Crown Rust Fungus Puccinia coronata f. sp. avenae

Tim C. Hewitt; Eva C. Henningsen; Danilo Pereira; Kerensa McElroy; Eric S. Nazareno; Sheshanka Dugyala; Hoa Nguyen-Phuc; Feng Li; Marisa E. Miller; Botma Visser; Zacharias A. Pretorius; Willem H. P. Boshoff; Jana Sperschneider; Eva H. Stukenbrock; Shahryar F. Kianian; Peter N. Dodds; Melania Figueroa

doi:10.1094/MPMI-09-23-0126-FI

Molecular Plant-Microbe Interactions (Mar 2024)

Genome-Enabled Analysis of Population Dynamics and Virulence-Associated Loci in the Oat Crown Rust Fungus Puccinia coronata f. sp. avenae

Tim C. Hewitt,
Eva C. Henningsen,
Danilo Pereira,
Kerensa McElroy,
Eric S. Nazareno,
Sheshanka Dugyala,
Hoa Nguyen-Phuc,
Feng Li,
Marisa E. Miller,
Botma Visser,
Zacharias A. Pretorius,
Willem H. P. Boshoff,
Jana Sperschneider,
Eva H. Stukenbrock,
Shahryar F. Kianian,
Peter N. Dodds,
Melania Figueroa

Affiliations

Tim C. Hewitt: Commonwealth Scientific and Industrial Research Organisation, Agriculture and Food, Canberra, ACT 2600, Australia
Eva C. Henningsen: Commonwealth Scientific and Industrial Research Organisation, Agriculture and Food, Canberra, ACT 2600, Australia
Danilo Pereira: Christian Albrechts University of Kiel, 24118 Kiel, Germany
Kerensa McElroy: Commonwealth Scientific and Industrial Research Organisation, Agriculture and Food, Canberra, ACT 2600, Australia
Eric S. Nazareno: Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108, U.S.A.
Sheshanka Dugyala: Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108, U.S.A.
Hoa Nguyen-Phuc: Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108, U.S.A.
Feng Li: Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108, U.S.A.
Marisa E. Miller: Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108, U.S.A.
Botma Visser: Department of Plant Sciences, University of the Free State, Bloemfontein 9300, South Africa
Zacharias A. Pretorius: Department of Plant Sciences, University of the Free State, Bloemfontein 9300, South Africa
Willem H. P. Boshoff: Department of Plant Sciences, University of the Free State, Bloemfontein 9300, South Africa
Jana Sperschneider: Commonwealth Scientific and Industrial Research Organisation, Agriculture and Food, Canberra, ACT 2600, Australia
Eva H. Stukenbrock: Christian Albrechts University of Kiel, 24118 Kiel, Germany
Shahryar F. Kianian: Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108, U.S.A.
Peter N. Dodds: Commonwealth Scientific and Industrial Research Organisation, Agriculture and Food, Canberra, ACT 2600, Australia
Melania Figueroa: Commonwealth Scientific and Industrial Research Organisation, Agriculture and Food, Canberra, ACT 2600, Australia

DOI: https://doi.org/10.1094/MPMI-09-23-0126-FI
Journal volume & issue: Vol. 37, no. 3
pp. 290 – 303

Abstract

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Puccinia coronata f. sp. avenae (Pca) is an important fungal pathogen causing crown rust that impacts oat production worldwide. Genetic resistance for crop protection against Pca is often overcome by the rapid virulence evolution of the pathogen. This study investigated the factors shaping adaptive evolution of Pca using pathogen populations from distinct geographic regions within the United States and South Africa. Phenotypic and genome-wide sequencing data of these diverse Pca collections, including 217 isolates, uncovered phylogenetic relationships and established distinct genetic composition between populations from northern and southern regions from the United States and South Africa. The population dynamics of Pca involve a bidirectional movement of inoculum between northern and southern regions of the United States and contributions from clonality and sexuality. The population from South Africa is solely clonal. A genome-wide association study (GWAS) employing a haplotype-resolved Pca reference genome was used to define 11 virulence-associated loci corresponding to 25 oat differential lines. These regions were screened to determine candidate Avr effector genes. Overall, the GWAS results allowed us to identify the underlying genetic factors controlling pathogen recognition in an oat differential set used in the United States to assign pathogen races (pathotypes). Key GWAS findings support complex genetic interactions in several oat lines, suggesting allelism among resistance genes or redundancy of genes included in the differential set, multiple resistance genes recognizing genetically linked Avr effector genes, or potentially epistatic relationships. A careful evaluation of the composition of the oat differential set accompanied by the development or implementation of molecular markers is recommended. [Graphic: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Published in Molecular Plant-Microbe Interactions

ISSN: 0894-0282 (Print); 1943-7706 (Online)
Publisher: The American Phytopathological Society
Country of publisher: United States
LCC subjects: Science: Microbiology; Science: Botany
Website: https://apsjournals.apsnet.org/journal/mpmi

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