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De novo assembly and phasing of dikaryotic genomes from two isolates of Puccinia coronata f. sp. avenae, the causal agent of oat crown rust

View ORCID ProfileMarisa E. Miller, Ying Zhang, Vahid Omidvar, Jana Sperschneider, View ORCID ProfileBenjamin Schwessinger, Castle Raley, Jonathan M. Palmer, Diana Garnica, Narayana Upadhyaya, John Rathjen, Jennifer M. Taylor, Robert F. Park, Peter N. Dodds, Cory D. Hirsch, Shahryar F. Kianian, Melania Figueroa
doi: https://doi.org/10.1101/179226
Marisa E. Miller
aDepartment of Plant Pathology, University of Minnesota, St. Paul, MN, USA
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Ying Zhang
bSupercomputing Institute for Advanced Computational Research, University of Minnesota, Minneapolis, MN, USA
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Vahid Omidvar
aDepartment of Plant Pathology, University of Minnesota, St. Paul, MN, USA
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Jana Sperschneider
cCentre for Environment and Life Sciences, Commonwealth Scientific and Industrial Research Organisation, Agriculture and Food, Perth, WA, Australia
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Benjamin Schwessinger
dResearch School of Biology, Australian National University, Canberra, ACT, Australia
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Castle Raley
eLeidos Biomedical Research, MD, USA
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Jonathan M. Palmer
fCenter for Forest Mycology Research, Northern Research Station, USDA Forest Service, Madison, WI
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Diana Garnica
gAgriculture and Food, Commonwealth Scientific and Industrial Research Organisation, Canberra, ACT, Australia
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Narayana Upadhyaya
hPlant Breeding Institute, Faculty of Agriculture and Environment, School of Life and Environmental Sciences, The University of Sydney, Narellan, NSW, Australia
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John Rathjen
dResearch School of Biology, Australian National University, Canberra, ACT, Australia
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Jennifer M. Taylor
gAgriculture and Food, Commonwealth Scientific and Industrial Research Organisation, Canberra, ACT, Australia
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Robert F. Park
hPlant Breeding Institute, Faculty of Agriculture and Environment, School of Life and Environmental Sciences, The University of Sydney, Narellan, NSW, Australia
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Peter N. Dodds
gAgriculture and Food, Commonwealth Scientific and Industrial Research Organisation, Canberra, ACT, Australia
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Cory D. Hirsch
aDepartment of Plant Pathology, University of Minnesota, St. Paul, MN, USA
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Shahryar F. Kianian
aDepartment of Plant Pathology, University of Minnesota, St. Paul, MN, USA
iUSDA-ARS Cereal Disease Laboratory, St. Paul, MN, USA
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  • For correspondence: figue031@umn.edu shahryar.kianian@ars.usda.gov
Melania Figueroa
aDepartment of Plant Pathology, University of Minnesota, St. Paul, MN, USA
jStakman-Borlaug Center for Sustainable Plant Health, University of Minnesota, St. Paul, MN, USA
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  • For correspondence: figue031@umn.edu shahryar.kianian@ars.usda.gov
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Abstract

Oat crown rust, caused by the fungus Puccinia coronata f. sp. avenae (Pca), is a devastating disease that impacts worldwide oat production. For much of its life cycle, Pca is dikaryotic, with two separate haploid nuclei that may vary in virulence genotype, highlighting the importance of understanding haplotype diversity in this species. We generated highly contiguous de novo genome assemblies of two Pca isolates, 12SD80 and 12NC29, from long-read sequences. In total, we assembled 603 primary contigs for a total assembly length of 99.16 Mbp for 12SD80 and 777 primary contigs with a total length of 105.25 Mbp for 12NC29, and approximately 52% of each genome was assembled into alternate haplotypes. This revealed structural variation between haplotypes in each isolate equivalent to more than 2% of the genome size, in addition to about 260,000 and 380,000 heterozygous single-nucleotide polymorphisms in 12SD80 and 12NC29, respectively. Transcript-based annotation identified 26,796 and 28,801 coding sequences for isolates 12SD80 and 12NC29, respectively, including about 7,000 allele pairs in haplotype-phased regions. Furthermore, expression profiling revealed clusters of co-expressed secreted effector candidates, and the majority of orthologous effectors between isolates showed conservation of expression patterns. However, a small subset of orthologs showed divergence in expression, which may contribute to differences in virulence between 12SD80 and 12NC29. This study provides the first haplotype-phased reference genome for a dikaryotic rust fungus as a foundation for future studies into virulence mechanisms in Pca.

Importance Disease management strategies for oat crown rust are challenged by the rapid evolution of Puccinia coronata f. sp. avenae (Pca), which renders resistance genes in oat varieties ineffective. Despite the economic importance of understanding Pca, resources to study the molecular mechanisms underpinning pathogenicity and emergence of new virulence traits are lacking. Such limitations are partly due to the obligate biotrophic lifestyle of Pca as well as the dikaryotic nature of the genome, features that are also shared with other important rust pathogens. This study reports the first release of a haplotype-phased genome assembly for a dikaryotic fungal species and demonstrates the amenability of using emerging technologies to investigate genetic diversity in populations of Pca.

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Posted August 25, 2017.
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De novo assembly and phasing of dikaryotic genomes from two isolates of Puccinia coronata f. sp. avenae, the causal agent of oat crown rust
Marisa E. Miller, Ying Zhang, Vahid Omidvar, Jana Sperschneider, Benjamin Schwessinger, Castle Raley, Jonathan M. Palmer, Diana Garnica, Narayana Upadhyaya, John Rathjen, Jennifer M. Taylor, Robert F. Park, Peter N. Dodds, Cory D. Hirsch, Shahryar F. Kianian, Melania Figueroa
bioRxiv 179226; doi: https://doi.org/10.1101/179226
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De novo assembly and phasing of dikaryotic genomes from two isolates of Puccinia coronata f. sp. avenae, the causal agent of oat crown rust
Marisa E. Miller, Ying Zhang, Vahid Omidvar, Jana Sperschneider, Benjamin Schwessinger, Castle Raley, Jonathan M. Palmer, Diana Garnica, Narayana Upadhyaya, John Rathjen, Jennifer M. Taylor, Robert F. Park, Peter N. Dodds, Cory D. Hirsch, Shahryar F. Kianian, Melania Figueroa
bioRxiv 179226; doi: https://doi.org/10.1101/179226

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