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A Near-Complete Haplotype-Phased Genome of the Dikaryotic Wheat Stripe Rust Fungus Puccinia striiformis f. sp. tritici Reveals High Interhaplotype Diversity

Schwessinger, Benjamin; Sperschneider, Jana; Cuddy, William S; Garnica, Diana; Miller, Marisa E; Taylor, Jennifer; Dodds, Peter N; Figueroa, Melania; Park, R.F.; Rathjen, John

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A long-standing biological question is how evolution has shaped the genomic architecture of dikaryotic fungi. To answer this, high-quality genomic resources that enable haplotype comparisons are essential. Short-read genome assemblies for dikaryotic fungi are highly fragmented and lack haplotype-specific information due to the high heterozygosity and repeat content of these genomes. Here, we present a diploid-aware assembly of the wheat stripe rust fungus Puccinia striiformis f. sp. tritici...[Show more]

dc.contributor.authorSchwessinger, Benjamin
dc.contributor.authorSperschneider, Jana
dc.contributor.authorCuddy, William S
dc.contributor.authorGarnica, Diana
dc.contributor.authorMiller, Marisa E
dc.contributor.authorTaylor, Jennifer
dc.contributor.authorDodds, Peter N
dc.contributor.authorFigueroa, Melania
dc.contributor.authorPark, R.F.
dc.contributor.authorRathjen, John
dc.date.accessioned2019-04-08T11:57:16Z
dc.date.available2019-04-08T11:57:16Z
dc.identifier.issn2161-2129
dc.identifier.urihttp://hdl.handle.net/1885/159344
dc.description.abstractA long-standing biological question is how evolution has shaped the genomic architecture of dikaryotic fungi. To answer this, high-quality genomic resources that enable haplotype comparisons are essential. Short-read genome assemblies for dikaryotic fungi are highly fragmented and lack haplotype-specific information due to the high heterozygosity and repeat content of these genomes. Here, we present a diploid-aware assembly of the wheat stripe rust fungus Puccinia striiformis f. sp. tritici based on long reads using the FALCON-Unzip assembler. Transcriptome sequencing data sets were used to infer high-quality gene models and identify virulence genes involved in plant infection referred to as effectors. This represents the most complete Puccinia striiformis f. sp. tritici genome assembly to date (83 Mb, 156 contigs, N50 of 1.5 Mb) and provides phased haplotype information for over 92% of the genome. Comparisons of the phase blocks revealed high interhaplotype diversity of over 6%. More than 25% of all genes lack a clear allelic counterpart. When we investigated genome features that potentially promote the rapid evolution of virulence, we found that candidate effector genes are spatially associated with conserved genes commonly found in basidiomycetes. Yet, candidate effectors that lack an allelic counterpart are more distant from conserved genes than allelic candidate effectors and are less likely to be evolutionarily conserved within the P. striiformis species complex and Pucciniales. In summary, this haplotype-phased assembly enabled us to discover novel genome features of a dikaryotic plant-pathogenic fungus previously hidden in collapsed and fragmented genome assemblies. IMPORTANCE Current representations of eukaryotic microbial genomes are haploid, hiding the genomic diversity intrinsic to diploid and polyploid life forms. This hidden diversity contributes to the organism’s evolutionary potential and ability to adapt to stress conditions. Yet, it is challenging to provide haplotype-specific information at a whole-genome level. Here, we take advantage of long-read DNA sequencing technology and a tailored-assembly algorithm to disentangle the two haploid genomes of a dikaryotic pathogenic wheat rust fungus. The two genomes display high levels of nucleotide and structural variations, which lead to allelic variation and the presence of genes lacking allelic counterparts. Nonallelic candidate effector genes, which likely encode important pathogenicity factors, display distinct genome localization patterns and are less likely to be evolutionary conserved than those which are pres- ent as allelic pairs. This genomic diversity may promote rapid host adaptation and/or be related to the age of the sequenced isolate since last meiosis.
dc.format.mimetypeapplication/pdf
dc.language.isoen_AU
dc.publisherAmerican Society for Microbiology
dc.rightsCreative Commons Attribution License 4.0
dc.rights.urihttps://creativecommons.org/licenses/by/4.0/
dc.sourcemBio
dc.titleA Near-Complete Haplotype-Phased Genome of the Dikaryotic Wheat Stripe Rust Fungus Puccinia striiformis f. sp. tritici Reveals High Interhaplotype Diversity
dc.typeJournal article
local.description.notesImported from ARIES
local.identifier.citationvolume9
dc.date.issued2018
local.identifier.absfor060704 - Plant Pathology
local.identifier.absfor060408 - Genomics
local.identifier.ariespublicationa383154xPUB9552
local.type.statusPublished Version
local.contributor.affiliationSchwessinger, Benjamin, College of Science, ANU
local.contributor.affiliationSperschneider, Jana , Commonwealth Scientific and Industrial Research Organization
local.contributor.affiliationCuddy, William S, University of Sydney
local.contributor.affiliationGarnica, Diana, College of Science, ANU
local.contributor.affiliationMiller, Marisa E, University of Minnesota
local.contributor.affiliationTaylor, Jennifer, CSIRO
local.contributor.affiliationDodds, Peter N, CSIRO
local.contributor.affiliationFigueroa, Melania, University of Minnesota
local.contributor.affiliationPark, R.F., University of Sydney
local.contributor.affiliationRathjen, John, College of Science, ANU
local.bibliographicCitation.issue1
local.identifier.doi10.1128/mBio.02275-17
local.identifier.absseo820507 - Wheat
dc.date.updated2019-03-12T07:21:55Z
local.identifier.scopusID2-s2.0-85043517175
dcterms.accessRightsOpen Access
dc.provenanceJournal: mBio (ESSN: 2150-7511) RoMEO: This is a RoMEO green journal Listed in: DOAJ as an open access journal Author's Pre-print: green tick author can archive pre-print (ie pre-refereeing) Author's Post-print: green tick author can archive post-print (ie final draft post-refereeing) Publisher's Version/PDF: green tick author can archive publisher's version/PDF General Conditions: Authors retain copyright On funder's repositories, institutional repository or subject-based repositories, after publication of article Publisher's version/PDF may be used Published source must be acknowledged Creative Commons Attribution License 4.0
CollectionsANU Research Publications

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