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

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

Oat crown rust, caused by the fungus Pucinnia coronata f. sp. avenae, is a devastating disease that impacts worldwide oat production. For much of its life cycle, P. coronata f. sp. avenae 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 P. coronata f. sp. avenae isolates, 12SD80 and 12NC29, from long-read sequences. In total, we assembled 603 primary contigs for 12SD80, for a total assembly length of 99.16 Mbp, and 777 primary contigs for 12NC29, for a total length of 105.25 Mbp; 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 coexpressed 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 P. coronata f. sp. avenae. IMPORTANCE Disease management strategies for oat crown rust are challenged by the rapid evolution of Puccinia coronata f. sp. avenae, which renders resistance genes in oat varieties ineffective. Despite the economic importance of understanding P. coronata f. sp. avenae, resources to study the molecular mechanisms under- pinning pathogenicity and the emergence of new virulence traits are lacking. Such limitations are partly due to the obligate biotrophic lifestyle of P. coronata f. sp. avenae 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 P. coronata f. sp. avenae.

Original languageEnglish (US)
Article numbere01650-17
JournalmBio
Volume9
Issue number1
DOIs
StatePublished - Jan 1 2018

Fingerprint

Crowns
Haplotypes
Virulence
Genome
Fungi
Genome Size
Haploidy
Disease Management
Life Cycle Stages
Single Nucleotide Polymorphism
Avena
Life Style
Alleles
Genotype
Economics
Technology
Population
Genes

Keywords

  • Effectors
  • Genomics
  • Oat
  • Rust fungi
  • Virulence

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

Cite this

Miller, M. E., Zhang, Y., Omidvar, V., Sperschneider, J., Schwessinger, B., Raley, C., ... Figueroa, M. (2018). De novo assembly and phasing of dikaryotic genomes from two isolates of puccinia coronata f. Sp. avenae, the causal agent of oat crown rust. mBio, 9(1), [e01650-17]. https://doi.org/10.1128/mBio.01650-17

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

In: mBio, Vol. 9, No. 1, e01650-17, 01.01.2018.

Research output: Contribution to journalArticle

Miller, ME, Zhang, Y, Omidvar, V, Sperschneider, J, Schwessinger, B, Raley, C, Palmer, JM, Garnica, D, Upadhyaya, N, Rathjen, J, Taylor, JM, Park, RF, Dodds, PN, Hirsch, CD, Kianian, SF & Figueroa, M 2018, 'De novo assembly and phasing of dikaryotic genomes from two isolates of puccinia coronata f. Sp. avenae, the causal agent of oat crown rust', mBio, vol. 9, no. 1, e01650-17. https://doi.org/10.1128/mBio.01650-17
Miller, Marisa E. ; Zhang, Ying ; Omidvar, Vahid ; Sperschneider, Jana ; Schwessinger, Benjamin ; Raley, Castle ; Palmer, Jonathan M. ; Garnica, Diana ; Upadhyaya, Narayana ; Rathjen, John ; Taylor, Jennifer M. ; Park, Robert F. ; Dodds, Peter N. ; Hirsch, Cory D. ; Kianian, Shahryar F. ; Figueroa, Melania. / De novo assembly and phasing of dikaryotic genomes from two isolates of puccinia coronata f. Sp. avenae, the causal agent of oat crown rust. In: mBio. 2018 ; Vol. 9, No. 1.
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abstract = "Oat crown rust, caused by the fungus Pucinnia coronata f. sp. avenae, is a devastating disease that impacts worldwide oat production. For much of its life cycle, P. coronata f. sp. avenae 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 P. coronata f. sp. avenae isolates, 12SD80 and 12NC29, from long-read sequences. In total, we assembled 603 primary contigs for 12SD80, for a total assembly length of 99.16 Mbp, and 777 primary contigs for 12NC29, for a total length of 105.25 Mbp; 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 coexpressed 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 P. coronata f. sp. avenae. IMPORTANCE Disease management strategies for oat crown rust are challenged by the rapid evolution of Puccinia coronata f. sp. avenae, which renders resistance genes in oat varieties ineffective. Despite the economic importance of understanding P. coronata f. sp. avenae, resources to study the molecular mechanisms under- pinning pathogenicity and the emergence of new virulence traits are lacking. Such limitations are partly due to the obligate biotrophic lifestyle of P. coronata f. sp. avenae 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 P. coronata f. sp. avenae.",
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T1 - De novo assembly and phasing of dikaryotic genomes from two isolates of puccinia coronata f. Sp. avenae, the causal agent of oat crown rust

AU - Miller, Marisa E.

AU - Zhang, Ying

AU - Omidvar, Vahid

AU - Sperschneider, Jana

AU - Schwessinger, Benjamin

AU - Raley, Castle

AU - Palmer, Jonathan M.

AU - Garnica, Diana

AU - Upadhyaya, Narayana

AU - Rathjen, John

AU - Taylor, Jennifer M.

AU - Park, Robert F.

AU - Dodds, Peter N.

AU - Hirsch, Cory D.

AU - Kianian, Shahryar F.

AU - Figueroa, Melania

PY - 2018/1/1

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N2 - Oat crown rust, caused by the fungus Pucinnia coronata f. sp. avenae, is a devastating disease that impacts worldwide oat production. For much of its life cycle, P. coronata f. sp. avenae 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 P. coronata f. sp. avenae isolates, 12SD80 and 12NC29, from long-read sequences. In total, we assembled 603 primary contigs for 12SD80, for a total assembly length of 99.16 Mbp, and 777 primary contigs for 12NC29, for a total length of 105.25 Mbp; 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 coexpressed 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 P. coronata f. sp. avenae. IMPORTANCE Disease management strategies for oat crown rust are challenged by the rapid evolution of Puccinia coronata f. sp. avenae, which renders resistance genes in oat varieties ineffective. Despite the economic importance of understanding P. coronata f. sp. avenae, resources to study the molecular mechanisms under- pinning pathogenicity and the emergence of new virulence traits are lacking. Such limitations are partly due to the obligate biotrophic lifestyle of P. coronata f. sp. avenae 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 P. coronata f. sp. avenae.

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KW - Effectors

KW - Genomics

KW - Oat

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KW - Virulence

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