Three decades of rust surveys in the United States reveal drastic virulence changes in oat crown rust

Authors: Moreau, Erin; Riddle, Jakob; NAZARENO, ERIC - University Of Minnesota; Kianian, Shahryar

Submitted to: Plant Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/7/2023
Publication Date: 5/2/2024
Citation: Moreau, E.L., Riddle, J.M., Nazareno, E.S., Kianian, S. 2024. Three decades of rust surveys in the United States reveal drastic virulence changes in oat crown rust. Plant Disease. https://doi.org/10.1094/PDIS-09-23-1956-RE.
DOI: https://doi.org/10.1094/PDIS-09-23-1956-RE

Interpretive Summary: One of the most important diseases affecting oat production worldwide is oat crown rust caused by the fungus Puccinia coronata f. sp. avenae (Pca). The USDA, ARS, Cereal Disease Laboratory conducts annual oat crown rust surveys by collecting Pca samples from across oat growing regions in the United States and determining their virulence to resistance genes that protect against the disease in oat varieties. Over 5,000 Pca samples from the past 30 years of surveys were analyzed to determine how the pathogen’s virulence has changed over time. The results showed that the pathogen is highly variable with most Pca samples demonstrating a unique virulence profile. Additionally, Pca is overcoming more oat resistance genes used in the survey analysis every year, from an average of 9.3/30 resistance genes in 1993 to 20/30 resistance genes in 2022. Isolates collected from northern states had more virulences than isolates from southern states in seven of the years, which further supports sexual recombination in the presence of alternate host, common buckthorn, present in these states, as a contributing factor. Virulence significantly increased for 23 and decreased for 4 of the 40 resistance genes tested over the past 30 years. Sixteen resistance genes have been almost completely defeated, with over 90% of isolates virulent to them in the past few years. Strong correlations between several resistance genes also support previous studies showing that some are redundant, with different names designating the same or very similar gene. Understanding how Pca is changing over time is essential for determining which resistance genes to use in breeding for development of oat crown rust resistant cultivars for sustainable and profitable oat production.

Technical Abstract: To better understand how the pathogenicity of the oat crown rust pathogen, Puccinia coronata f. sp. avenae (Pca), has changed in the United States, 30 years of USDA survey isolates (n=5,436) tested on 30-40 differential lines were analyzed for overall and Pc resistance gene specific virulence trends and correlations. Pca is incredibly pathologically diverse with 88% of races represented by a single isolate. There are a slightly higher proportion of unique races from the Northern Region of the US and for a fourth of the years. Northern region isolates were significantly more virulent than Southern isolates which supports the idea that sexual recombination in this region is mediated by the alternate host as a major factor in creating new races. However, there is also support for regular isolate movement between North and South regions as isolates in the United States are steadily accumulating virulences at a rate of 0.35 virulences per year. Virulence significantly increased for 23 and decreased for 4 of the 40 differential lines. In the past few years, virulence has reached 90% or greater for 16 differential lines. There were also strong correlations in virulence for certain Pc genes that are likely identical, allelic, or target the same or closely linked pathogen effectors (e.g. Pc39, Pc55, and Pc71), and the results were largely in concordance with recent GWAS effector studies using USDA isolate subsets. Understanding changes in Pca pathogenicity is essential for the responsible deployment and management of Pc resistance genes for sustainable and profitable oat production.