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A near complete haplotype-phased genome of the dikaryotic wheat stripe rust fungus Puccinia striiformis f. sp. tritici reveals high inter-haplotype diversity

View ORCID ProfileBenjamin Schwessinger, View ORCID ProfileJana Sperschneider, View ORCID ProfileWilliam S. Cuddy, Diana P. Garnica, View ORCID ProfileMarisa E. Miller, Jennifer M. Taylor, View ORCID ProfilePeter N. Dodds, View ORCID ProfileMelania Figueroa, Park F. Robert, View ORCID ProfileJohn Rathjen
doi: https://doi.org/10.1101/192435
Benjamin Schwessinger
aResearch School of Biology, The Australian National University, Acton 2601, ACT, Australia
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  • For correspondence: benjamin.schwessinger@anu.edu.au
Jana Sperschneider
bCentre for Environment and Life Sciences, CSIRO Agriculture and Food, Perth, WA, Australia
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William S. Cuddy
cPlant Breeding Institute, Faculty of Agriculture and Environment, The University of Sydney, Narellan, NSW, Australia
dElizabeth Macarthur Agricultural Institute, NSW Department of Primary Industries, Woodbridge Road, Menangle, NSW, 2568, Australia
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  • For correspondence: benjamin.schwessinger@anu.edu.au will.cuddy@dpi.nsw.gov.au
Diana P. Garnica
aResearch School of Biology, The Australian National University, Acton 2601, ACT, Australia
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Marisa E. Miller
fDepartment of Plant Pathology, University of Minnesota, St. Paul, MN, USA
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Jennifer M. Taylor
hBlack Mountain Laboratories, CSIRO Agriculture and Food, Canberra, ACT, Australia
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Peter N. Dodds
hBlack Mountain Laboratories, CSIRO Agriculture and Food, Canberra, ACT, Australia
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  • ORCID record for Peter N. Dodds
Melania Figueroa
fDepartment of Plant Pathology, University of Minnesota, St. Paul, MN, USA
gStakman-Borlaug Center for Sustainable Plant Health, University of Minnesota, St. Paul, MN, USA
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Park F. Robert
cPlant Breeding Institute, Faculty of Agriculture and Environment, The University of Sydney, Narellan, NSW, Australia
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John Rathjen
aResearch School of Biology, The Australian National University, Acton 2601, ACT, Australia
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Abstract

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 diploidaware assembly of the wheat stripe rust fungus Puccinia striiformis f. sp. tritici based on long-reads using the FALCON-Unzip assembler. RNA-seq datasets 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 1.5 Mb) and provides phased haplotype information for over 92% of the genome. Comparisons of the phase blocks revealed high inter-haplotype diversity of over 6%. More than 25% of all genes lack a clear allelic counterpart. When investigating 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 leads to allelic variation and the presence of genes lacking allelic counterparts. Non-allelic 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 present 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.

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Posted December 07, 2017.
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A near complete haplotype-phased genome of the dikaryotic wheat stripe rust fungus Puccinia striiformis f. sp. tritici reveals high inter-haplotype diversity
Benjamin Schwessinger, Jana Sperschneider, William S. Cuddy, Diana P. Garnica, Marisa E. Miller, Jennifer M. Taylor, Peter N. Dodds, Melania Figueroa, Park F. Robert, John Rathjen
bioRxiv 192435; doi: https://doi.org/10.1101/192435
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A near complete haplotype-phased genome of the dikaryotic wheat stripe rust fungus Puccinia striiformis f. sp. tritici reveals high inter-haplotype diversity
Benjamin Schwessinger, Jana Sperschneider, William S. Cuddy, Diana P. Garnica, Marisa E. Miller, Jennifer M. Taylor, Peter N. Dodds, Melania Figueroa, Park F. Robert, John Rathjen
bioRxiv 192435; doi: https://doi.org/10.1101/192435

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