A chromosome-level, fully phased genome asssembly of the oat crown rust fungus Puccinia coronata f. sp. avenae: A resource to enable comparative genomics in cereal rusts

Authors: HENNINGSEN, EVA - University Of Minnesota; HEWITT, TIM - Commonwealth Scientific And Industrial Research Organisation (CSIRO); DUGYALA, SHESHANKA - University Of Minnesota; NAZARENO, ERIC - University Of Minnesota; GILBERT, ERIN - Bayer Cropscience; LI, FENG - University Of Minnesota; Kianian, Shahryar; STEFFENSON, BRIAN - University Of Minnesota; DODDS, PETER - Commonwealth Scientific And Industrial Research Organisation (CSIRO); SPERSCHNEIDER, JANA - Commonwealth Scientific And Industrial Research Organisation (CSIRO); FIGUEROA, MELANIA - Commonwealth Scientific And Industrial Research Organisation (CSIRO)

Submitted to: G3, Genes/Genomes/Genetics
Publication Type: Pre-print Publication
Publication Acceptance Date: 5/19/2022
Publication Date: 6/22/2022
Citation: Henningsen, E.C., Hewitt, T., Dugyala, S., Nazareno, E., Gilbert, E., Li, F., Kianian, S., Steffenson, B.J., Dodds, P.N., Sperschneider, J., Figueroa, M. 2022. A chromosome-level, fully phased genome asssembly of the oat crown rust fungus Puccinia coronata f. sp. avenae: A resource to enable comparative genomics in cereal rusts. G3, Genes/Genomes/Genetics. 12(8). https://doi.org/10.1093/g3journal/jkac149.
DOI: https://doi.org/10.1093/g3journal/jkac149

Interpretive Summary: Oat crown rust, caused by Puccinia coronata f. sp. avenae (Pca), is a major disease of cultivate oat and has global impact on grain production. Disease management strategies for oat crown rust rely heavily on breeding for race-specific resistance. However, Pca rapidly evolves virulence to new resistance genes and field populations are highly polymorphic with high numbers of races (pathotypes), which limits the efficacy of this approach. This has coincided with a dramatic decline in US oat production. Here we utilized advanced genome sequencing technologies and computational tools to assemble the complete genome of this pathogen. This genome assembly can be directly compared to that of other rust species, such as wheat stem and leaf rust, to better understand the evolutionary relationship of these major pathogens and devise more sustainable control methods. The outcomes of this study underscore the value of genomic-based approaches to characterize pathogen evolution.

Technical Abstract: Advances in sequencing technologies as well as development of algorithms and workflows have made it possible to generate fully phased genome references for organisms with non-haploid genomes such as dikaryotic rust fungi. To enable discovery of pathogen effectors and further our understanding of virulence evolution, we generated a chromosome-scale assembly for each of the two nuclear genomes of the oat crown rust pathogen, Puccinia coronata f. sp. avenae (Pca). This resource complements two previous released partially phased genome references of Pca, which display virulence traits absent in the isolate of historic race 203 (isolate Pca203) which was selected for this genome project. A fully phased, chromosome-level reference for Pca203 was generated using PacBio reads and Hi-C data and a recently developed pipeline named NuclearPhaser for phase assignment of contigs and phase switch correction. With 18 chromosomes in each haplotype and a total size of 208.10 Mbp, Pca203 has the same number of chromosomes as other cereal rust fungi such as Puccinia graminis f. sp. tritici and Puccinia triticina, the causal agents of wheat stem rust and wheat leaf rust, respectively. The Pca203 reference marks the third fully-phased chromosome-level assembly of a cereal rust to date. Here, we demonstrate that the chromosomes of these three Puccinia species are syntenous and that chromosomal size variations are primarily due to differences in repeat element content.