Genome-enabled analysis of population dynamics and virulence associated loci in the oat crown rust fungus Puccinia coronata f. sp. avenae

Authors: HEWITT, TIM - Commonwealth Scientific And Industrial Research Organisation (CSIRO); HENNINGSEN, EVA - Commonwealth Scientific And Industrial Research Organisation (CSIRO); PEREIRA, DANILO - Max Planck Institute Of Molecular Plant Physiology; MCELROY, KERENSA - Commonwealth Scientific And Industrial Research Organisation (CSIRO); NAZARENO, ERIC - University Of Minnesota; DUGYALA, SHESHANKA - University Of Minnesota; NGUYEN-PHUC, HOA - University Of Minnesota; LI, FENG - University Of Minnesota; MILLER, MARISA - University Of Minnesota; VISSER, BOTMA - University Of The Free State; PRETORIUS, ZAK - University Of The Free State; BOSHOFF, WILLEM - University Of The Free State; SPERSCHNEIDER, JANA - Max Planck Institute Of Molecular Plant Physiology; STUCKENBROCK, EVA - Max Planck Institute For Plant Breeding Research; Kianian, Shahryar; DODDS, PETER - Commonwealth Scientific And Industrial Research Organisation (CSIRO); FIGUEROA, MELANIA - Commonwealth Scientific And Industrial Research Organisation (CSIRO)

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/9/2023
Publication Date: 3/21/2024
Citation: Hewitt, T., Henningsen, E.C., Pereira, D., Mcelroy, K., Nazareno, E.S., Dugyala, S., Nguyen-Phuc, H., Li, F., Miller, M.E., Visser, B., Pretorius, Z., Boshoff, W., Sperschneider, J., Stuckenbrock, E., Kianian, S., Dodds, P.N., Figueroa, M. 2024. Genome-enabled analysis of population dynamics and virulence associated loci in the oat crown rust fungus Puccinia coronata f. sp. avenae. Molecular Plant-Microbe Interactions. 37(3):290-303. https://doi.org/10.1094/MPMI-09-23-0126-FI.
DOI: https://doi.org/10.1094/MPMI-09-23-0126-FI

Interpretive Summary: Puccinia coronata f. sp. avenae (Pca) is an important foliar pathogen that causes oat crown rust disease, which impacts oat production around the world. Sexual recombination, random (sequential) mutation and somatic hybridization are some of mechanisms allow rust pathogens such as Pca to alter their genetic make-up and gain virulence in otherwise resistant cultivars. Pca shares a similar life cycle with other Puccinia species that infect cereals. This involves alternation between an asexual cereal infection phase mediated by dikaryotic urediniospores (containing two different haploid nuclei), and a sexual phase that occurs on an alternate host. Thus, populations of cereal rust fungi can be highly sexual when the alternate host is present. We recently developed a complete chromosome-level and nuclear-phased reference genome of Pca (Pca203), and here we use this resource to expand on the initial findings reported by Miller et al. (2020) through analysis of a much larger population of US Pca isolates. This reveals a primary role for local sexual reproduction in the Northern US population and extensive migration between southern and northern regions. A GWAS analysis identifies a total of 11 virulence associated genomic interval (VGIs) associated with virulence phenotypes on 25 oat differential lines postulated to carry different Pc genes. Multiple oat lines have several corresponding VGIs, suggesting the presence of multiple Pc genes, many of which overlap between different oat differential lines.t, but in its absence, the asexual phase can persist indefinitely giving rise to long-lived clonal populations.

Technical Abstract: Puccinia coronata f. sp. avenae (Pca) is an important fungal pathogen causing oat crown rust disease 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 the evolutionary capacity of Pca using pathogen populations from distinct geographic regions within the USA and South Africa. Phenotypic and genome-wide sequencing data of these diverse Pca collections was utilised to uncover phylogenetic relationships and established distinct genetic composition between populations from Northern and Southern regions from the USA and South Africa. The population dynamics of Pca involve a bidirectional movement of inoculum between North and South regions of the USA 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 eleven virulence-associated loci corresponding to twenty-five oat differential lines. These regions were screened to determine candidate Avr effector genes. Overall, the GWAS results help characterising the underlying genetics controlling pathogen recognition in an oat differential set used in the USA 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 recognising 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.