DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

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 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 effectorsmore » 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.« less

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [5];  [6];  [6]; ORCiD logo [7];  [8];  [4]
  1. Australian National Univ., Acton, ACT (Australia). Research School of Biology
  2. Commonwealth Scientific and Industrial Research Organization (CSIRO), Perth ACT (Australia). Dept. of Agriculture & Food. Centre for Environment and Life Sciences
  3. Univ. of Sydney, Narellan, NSW (Australia). Faculty of Agriculture and Environment. Plant Breeding Inst. Elizabeth Macarthur Agricultural Inst, Menangle, NSW (Australia). Department of Primary Industries
  4. Australian National Univ., Acton, ACT (Australia). Research School of Biology
  5. Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Plant Pathology
  6. Commonwealth Scientific and Industrial Research Organization (CSIRO), Canberra ACT (Australia). Agriculture & Food. Black Mountain Laboratories
  7. Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Plant Pathology. Stakman-Borlaug Center for Sustainable Plant Health
  8. Univ. of Sydney, Narellan, NSW (Australia). Faculty of Agriculture and Environment. Plant Breeding Inst.
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1626146
Grant/Contract Number:  
AC02-05CH11231; LT000674/2012; DE150101897; MIN-22-058; 2017-67012-26117
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology (ASM)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; Microbiology; Dikaryon; basidiomycetes; genomics; plant pathogens

Citation Formats

Schwessinger, Benjamin, Sperschneider, Jana, Cuddy, William S., Garnica, Diana P., Miller, Marisa E., Taylor, Jennifer M., Dodds, Peter N., Figueroa, Melania, Park, Robert F., and Rathjen, John P. A Near-Complete Haplotype-Phased Genome of the Dikaryotic Wheat Stripe Rust Fungus Puccinia striiformis f. sp. tritici Reveals High Interhaplotype Diversity. United States: N. p., 2018. Web. doi:10.1128/mbio.02275-17.
Schwessinger, Benjamin, Sperschneider, Jana, Cuddy, William S., Garnica, Diana P., Miller, Marisa E., Taylor, Jennifer M., Dodds, Peter N., Figueroa, Melania, Park, Robert F., & Rathjen, John P. A Near-Complete Haplotype-Phased Genome of the Dikaryotic Wheat Stripe Rust Fungus Puccinia striiformis f. sp. tritici Reveals High Interhaplotype Diversity. United States. https://doi.org/10.1128/mbio.02275-17
Schwessinger, Benjamin, Sperschneider, Jana, Cuddy, William S., Garnica, Diana P., Miller, Marisa E., Taylor, Jennifer M., Dodds, Peter N., Figueroa, Melania, Park, Robert F., and Rathjen, John P. Tue . "A Near-Complete Haplotype-Phased Genome of the Dikaryotic Wheat Stripe Rust Fungus Puccinia striiformis f. sp. tritici Reveals High Interhaplotype Diversity". United States. https://doi.org/10.1128/mbio.02275-17. https://www.osti.gov/servlets/purl/1626146.
@article{osti_1626146,
title = {A Near-Complete Haplotype-Phased Genome of the Dikaryotic Wheat Stripe Rust Fungus Puccinia striiformis f. sp. tritici Reveals High Interhaplotype Diversity},
author = {Schwessinger, Benjamin and Sperschneider, Jana and Cuddy, William S. and Garnica, Diana P. and Miller, Marisa E. and Taylor, Jennifer M. and Dodds, Peter N. and Figueroa, Melania and Park, Robert F. and Rathjen, John P.},
abstractNote = {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 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.},
doi = {10.1128/mbio.02275-17},
journal = {mBio (Online)},
number = 1,
volume = 9,
place = {United States},
year = {2018},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 70 works
Citation information provided by
Web of Science

Figures / Tables:

FIG 1 FIG 1: The Pst-104E genome assembly is highly contiguous and complete. (A) Comparison of the Pst-104E primary and haplotig assemblies with the two most complete publicly available P. striiformis f. sp. tritici genome assemblies, Pst-78 and Pst-130. The histograms and the left y axis show log10 counts of contigs withinmore » each size bin. The dots and the right y axis show the cumulative sizes of small to large sorted contig lengths. Each dot represents a single contig of the given size, shown on the x axis. Each plot also shows the number of contigs or scaffolds, total assembly size, N50 of the assembly, and NG50 assuming a genome size of 85 Mb. NG50 is the N50 of an assembly considering the estimated genome size instead of the actual assembly size. This enables comparisons between different-sized assemblies. (B) Genome completeness was assessed using benchmarking universal single-copy orthologs (BUSCOs) for Basidiomycota (odb9) as proxy. The graph shows BUSCO results for Pst-104E primary (p), haplotig (h), and nonredundantly combined (ph) assemblies, in comparison to all publicly available P. striiformis f. sp. tritici genome assemblies with gene models, including Pst-78, Pst-130, Pst-21, Pst-43, Pst-0821, and Pst-887. The analysis was performed on the protein level, using publicly available gene models. An asterisk indicates the actual number of identified BUSCOs for the complete Pst-104E ph assembly before filtering gene models for similarity with genes related to transposable elements.« less

Save / Share:

Works referenced in this record:

Leaf Rust of Cultivated Barley: Pathology and Control
journal, August 2015


Improved Prediction of Signal Peptides: SignalP 3.0
journal, July 2004

  • Dyrløv Bendtsen, Jannick; Nielsen, Henrik; von Heijne, Gunnar
  • Journal of Molecular Biology, Vol. 340, Issue 4, p. 783-795
  • DOI: 10.1016/j.jmb.2004.05.028

Diversity of Puccinia striiformis on Cereals and Grasses
journal, September 2011


BRAKER1: Unsupervised RNA-Seq-Based Genome Annotation with GeneMark-ET and AUGUSTUS: Table 1.
journal, November 2015


LOCALIZER: subcellular localization prediction of both plant and effector proteins in the plant cell
journal, March 2017

  • Sperschneider, Jana; Catanzariti, Ann-Maree; DeBoer, Kathleen
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep44598

Characterization and comparative analysis of the genome of Puccinia sorghi Schwein, the causal agent of maize common rust
journal, March 2018

  • Rochi, Lucia; Diéguez, María José; Burguener, Germán
  • Fungal Genetics and Biology, Vol. 112
  • DOI: 10.1016/j.fgb.2016.10.001

PacBio-LITS: a large-insert targeted sequencing method for characterization of human disease-associated chromosomal structural variations
journal, March 2015


eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences
journal, November 2015

  • Huerta-Cepas, Jaime; Szklarczyk, Damian; Forslund, Kristoffer
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1248

Replacement of the European wheat yellow rust population by new races from the centre of diversity in the near-Himalayan region
journal, July 2015

  • Hovmøller, M. S.; Walter, S.; Bayles, R. A.
  • Plant Pathology, Vol. 65, Issue 3
  • DOI: 10.1111/ppa.12433

Genome analysis and avirulence gene cloning using a high-density RADseq linkage map of the flax rust fungus, Melampsora lini
journal, August 2016

  • Anderson, Claire; Khan, Muhammad Adil; Catanzariti, Ann-Maree
  • BMC Genomics, Vol. 17, Issue 1
  • DOI: 10.1186/s12864-016-3011-9

Worldwide population structure of the wheat rust fungus Puccinia striiformis in the past
journal, February 2016


Database resources of the National Center for Biotechnology Information
journal, November 2018

  • Sayers, Eric W.; Agarwala, Richa; Bolton, Evan E.
  • Nucleic Acids Research, Vol. 47, Issue D1
  • DOI: 10.1093/nar/gky1069

Global status of stripe rust: a review of historical and current threats
journal, February 2011


The Top 10 fungal pathogens in molecular plant pathology: Top 10 fungal pathogens
journal, April 2012


inStrain profiles population microdiversity from metagenomic data and sensitively detects shared microbial strains
journal, January 2021

  • Olm, Matthew R.; Crits-Christoph, Alexander; Bouma-Gregson, Keith
  • Nature Biotechnology, Vol. 39, Issue 6
  • DOI: 10.1038/s41587-020-00797-0

Combined Evidence Annotation of Transposable Elements in Genome Sequences
journal, January 2005


Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014


SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011

  • Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
  • Nature Methods, Vol. 8, Issue 10
  • DOI: 10.1038/nmeth.1701

Isolation and characterization of the novel Pseudomonas stutzeri bacteriophage 8P
journal, January 2021


Genome-scale model reconstruction of the methylotrophic yeast Ogataea polymorpha
text, January 2021


Assemblytics: a web analytics tool for the detection of variants from an assembly
journal, June 2016


Repbase Update, a database of repetitive elements in eukaryotic genomes
journal, June 2015


Molecular profiling of microbial community structure and their CAZymes via metagenomics, from Tsomgo lake in the Eastern Himalayas
journal, April 2021


featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
journal, November 2013


Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors
journal, November 2015

  • Rawlings, Neil D.; Barrett, Alan J.; Finn, Robert
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1118

Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
journal, March 2021


Full-length transcriptome assembly from RNA-Seq data without a reference genome
journal, May 2011

  • Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran
  • Nature Biotechnology, Vol. 29, Issue 7
  • DOI: 10.1038/nbt.1883

Heterozygosity, Heteromorphy, and Phylogenetic Trees in Asexual Eukaryotes
journal, September 1996


CASSPER is a semantic segmentation-based particle picking algorithm for single-particle cryo-electron microscopy
journal, February 2021


eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences
text, January 2016

  • Jaime, Huerta-Cepas,; Damian, Szklarczyk,; Kristoffer, Forslund,
  • Oxford University Press
  • DOI: 10.5167/uzh-120037

Century-Old Mystery of Puccinia striiformis Life History Solved with the Identification of Berberis as an Alternate Host
journal, May 2010


Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis
journal, November 2006

  • Kämper, Jörg; Kahmann, Regine; Bölker, Michael
  • Nature, Vol. 444, Issue 7115
  • DOI: 10.1038/nature05248

InterProScan 5: genome-scale protein function classification
journal, January 2014


The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat
journal, October 2016

  • Plissonneau, Clémence; Stürchler, Alessandra; Croll, Daniel
  • mBio, Vol. 7, Issue 5
  • DOI: 10.1128/mBio.01231-16

The Fungal Tree of Life: from Molecular Systematics to Genome-Scale Phylogenies
journal, October 2017


ApoplastP : prediction of effectors and plant proteins in the apoplast using machine learning
journal, December 2017

  • Sperschneider, Jana; Dodds, Peter N.; Singh, Karam B.
  • New Phytologist, Vol. 217, Issue 4
  • DOI: 10.1111/nph.14946

Yellow Rust Epidemics Worldwide Were Caused by Pathogen Races from Divergent Genetic Lineages
journal, June 2017

  • Ali, Sajid; Rodriguez-Algaba, Julian; Thach, Tine
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.01057

The genome sequence and effector complement of the flax rust pathogen Melampsora lini
journal, March 2014

  • Nemri, Adnane; Saunders, Diane G. O.; Anderson, Claire
  • Frontiers in Plant Science, Vol. 5
  • DOI: 10.3389/fpls.2014.00098

Fundamental wheat stripe rust research in the 21 st century
journal, August 2016


Role of Alternate Hosts in Epidemiology and Pathogen Variation of Cereal Rusts
journal, August 2016


Phased diploid genome assembly with single-molecule real-time sequencing
journal, October 2016

  • Chin, Chen-Shan; Peluso, Paul; Sedlazeck, Fritz J.
  • Nature Methods, Vol. 13, Issue 12
  • DOI: 10.1038/nmeth.4035

Fast Genome-Wide Functional Annotation through Orthology Assignment by eggNOG-Mapper
text, January 2017

  • Huerta-Cepas, Jaime; Forslund, Kristoffer; Coelho, Luis Pedro
  • Oxford University Press
  • DOI: 10.5167/uzh-140372

Evolution within the fungal genus Verticillium is characterized by chromosomal rearrangement and gene loss: Evolution within the fungal genus Verticillium
journal, January 2018

  • Shi-Kunne, Xiaoqian; Faino, Luigi; van den Berg, Grardy C. M.
  • Environmental Microbiology, Vol. 20, Issue 4
  • DOI: 10.1111/1462-2920.14037

The coffee leaf rust pathogen Hemileia vastatrix : one and a half centuries around the tropics: Coffee leaf rust caused by Hemileia vastatrix
journal, January 2017

  • Talhinhas, Pedro; Batista, Dora; Diniz, Inês
  • Molecular Plant Pathology, Vol. 18, Issue 8
  • DOI: 10.1111/mpp.12512

Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici: Puccinia striiformis , yellow rust
journal, May 2014

  • Chen, Wanquan; Wellings, Colin; Chen, Xianming
  • Molecular Plant Pathology, Vol. 15, Issue 5
  • DOI: 10.1111/mpp.12116

Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

Effector proteins of rust fungi
journal, August 2014

  • Petre, Benjamin; Joly, David L.; Duplessis, Sébastien
  • Frontiers in Plant Science, Vol. 5
  • DOI: 10.3389/fpls.2014.00416

IPython: A System for Interactive Scientific Computing
journal, January 2007

  • Perez, Fernando; Granger, Brian E.
  • Computing in Science & Engineering, Vol. 9, Issue 3
  • DOI: 10.1109/MCSE.2007.53

Comparative Analysis Highlights Variable Genome Content of Wheat Rusts and Divergence of the Mating Loci
journal, December 2016

  • Cuomo, Christina A.; Bakkeren, Guus; Khalil, Hala Badr
  • G3: Genes|Genomes|Genetics, Vol. 7, Issue 2
  • DOI: 10.1534/g3.116.032797

Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown
journal, August 2016

  • Pertea, Mihaela; Kim, Daehwan; Pertea, Geo M.
  • Nature Protocols, Vol. 11, Issue 9
  • DOI: 10.1038/nprot.2016.095

Matplotlib: A 2D Graphics Environment
journal, January 2007


MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

The Top 10 fungal pathogens in molecular plant pathology: Corrigendum
journal, July 2012


Python for Scientific Computing
journal, January 2007


The NumPy Array: A Structure for Efficient Numerical Computation
journal, March 2011

  • van der Walt, Stéfan; Colbert, S. Chris; Varoquaux, Gaël
  • Computing in Science & Engineering, Vol. 13, Issue 2
  • DOI: 10.1109/MCSE.2011.37

MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013

  • Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1183

A Puccinia striiformis f. sp. tritici secreted protein activates plant immunity at the cell surface
journal, April 2017


GenomeScope: fast reference-free genome profiling from short reads
journal, March 2017


Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen
journal, June 2016

  • Faino, Luigi; Seidl, Michael F.; Shi-Kunne, Xiaoqian
  • Genome Research, Vol. 26, Issue 8
  • DOI: 10.1101/gr.204974.116

Obligate biotrophy features unraveled by the genomic analysis of rust fungi
journal, May 2011

  • Duplessis, S.; Cuomo, C. A.; Lin, Y. -C.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 22
  • DOI: 10.1073/pnas.1019315108

Ensembl Genomes 2016: more genomes, more complexity
journal, November 2015

  • Kersey, Paul Julian; Allen, James E.; Armean, Irina
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1209

Field pathogenomics reveals the emergence of a diverse wheat yellow rust population
journal, February 2015


Research investment implications of shifts in the global geography of wheat stripe rust
journal, September 2015


PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments
journal, July 2006

  • Suyama, M.; Torrents, D.; Bork, P.
  • Nucleic Acids Research, Vol. 34, Issue Web Server
  • DOI: 10.1093/nar/gkl315

Versatile and open software for comparing large genomes
journal, January 2004

  • Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L.
  • Genome Biology, Vol. 5, Issue 2, R12
  • DOI: 10.1186/gb-2004-5-2-r12

Erratum: Evolution and genome architecture in fungal plant pathogens
journal, December 2017


A Tale of Genome Compartmentalization: The Evolution of Virulence Clusters in Smut Fungi
journal, February 2016

  • Dutheil, Julien Y.; Mannhaupt, Gertrud; Schweizer, Gabriel
  • Genome Biology and Evolution, Vol. 8, Issue 3
  • DOI: 10.1093/gbe/evw026

STAR: ultrafast universal RNA-seq aligner
journal, October 2012


Using Hierarchical Clustering of Secreted Protein Families to Classify and Rank Candidate Effectors of Rust Fungi
journal, January 2012


Pybedtools: a flexible Python library for manipulating genomic datasets and annotations
journal, September 2011


An overview of genetic rust resistance: From broad to specific mechanisms
journal, July 2017


Circos: An information aesthetic for comparative genomics
journal, June 2009


High genome heterozygosity and endemic genetic recombination in the wheat stripe rust fungus
journal, October 2013

  • Zheng, Wenming; Huang, Lili; Huang, Jinqun
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms3673

Considering Transposable Element Diversification in De Novo Annotation Approaches
journal, January 2011


BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs
journal, June 2015


Dating the molecular clock in fungi – how close are we?
journal, February 2010


The host-pathogen interaction between wheat and yellow rust induces temporally coordinated waves of gene expression
journal, May 2016

  • Dobon, Albor; Bunting, Daniel C. E.; Cabrera-Quio, Luis Enrique
  • BMC Genomics, Vol. 17, Issue 1
  • DOI: 10.1186/s12864-016-2684-4

Easyfig: a genome comparison visualizer
journal, January 2011


Characterization and functional analysis of phytoene synthase gene family in tobacco
journal, January 2021


dbCAN: a web resource for automated carbohydrate-active enzyme annotation
journal, May 2012

  • Yin, Yanbin; Mao, Xizeng; Yang, Jincai
  • Nucleic Acids Research, Vol. 40, Issue W1
  • DOI: 10.1093/nar/gks479

Breeding cereals for rust resistance in Australia
journal, August 2008


Strategies for Wheat Stripe Rust Pathogenicity Identified by Transcriptome Sequencing
journal, June 2013


The past, present and future of breeding rust resistant wheat
journal, November 2014

  • Ellis, Jeffrey G.; Lagudah, Evans S.; Spielmeyer, Wolfgang
  • Frontiers in Plant Science, Vol. 5
  • DOI: 10.3389/fpls.2014.00641

E ffector P: predicting fungal effector proteins from secretomes using machine learning
journal, December 2015

  • Sperschneider, Jana; Gardiner, Donald M.; Dodds, Peter N.
  • New Phytologist, Vol. 210, Issue 2
  • DOI: 10.1111/nph.13794

Reduction in the sex ability of worldwide clonal populations of Puccinia striiformis f.sp. tritici
journal, October 2010

  • Ali, Sajid; Leconte, Marc; Walker, Anne-Sophie
  • Fungal Genetics and Biology, Vol. 47, Issue 10
  • DOI: 10.1016/j.fgb.2010.07.002

Sexual structures and recombination of the wheat rust fungus Puccinia striiformis on Berberis vulgaris
journal, September 2014

  • Rodriguez-Algaba, Julian; Walter, Stephanie; Sørensen, Chris K.
  • Fungal Genetics and Biology, Vol. 70
  • DOI: 10.1016/j.fgb.2014.07.005

Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans
journal, September 2009

  • Haas, Brian J.; Kamoun, Sophien; Zody, Michael C.
  • Nature, Vol. 461, Issue 7262
  • DOI: 10.1038/nature08358

The two-speed genomes of filamentous pathogens: waltz with plants
journal, December 2015

  • Dong, Suomeng; Raffaele, Sylvain; Kamoun, Sophien
  • Current Opinion in Genetics & Development, Vol. 35
  • DOI: 10.1016/j.gde.2015.09.001

SimpleSynteny: a web-based tool for visualization of microsynteny across multiple species
journal, May 2016

  • Veltri, Daniel; Wight, Martha Malapi; Crouch, Jo Anne
  • Nucleic Acids Research, Vol. 44, Issue W1
  • DOI: 10.1093/nar/gkw330

The Irish Potato Famine Pathogen Phytophthora infestans Translocates the CRN8 Kinase into Host Plant Cells
journal, August 2012


Phakopsora pachyrhizi , the causal agent of Asian soybean rust
journal, March 2010


Data Structures for Statistical Computing in Python
conference, January 2010


Estimating Synonymous and Nonsynonymous Substitution Rates Under Realistic Evolutionary Models
journal, January 2000


The Top 10 fungal pathogens in molecular plant pathology: Top 10 fungal pathogens
journal, March 2012


The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat
text, January 2016


The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000
journal, January 2000


ARS2/MAGL signaling in glioblastoma stem cells promotes self-renewal and M2-like polarization of tumor-associated macrophages
journal, June 2020


A unified classification system for eukaryotic transposable elements
journal, December 2007

  • Wicker, Thomas; Sabot, François; Hua-Van, Aurélie
  • Nature Reviews Genetics, Vol. 8, Issue 12
  • DOI: 10.1038/nrg2165

Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments
journal, January 2008


Fast Genome-Wide Functional Annotation through Orthology Assignment by eggNOG-Mapper
journal, April 2017

  • Huerta-Cepas, Jaime; Forslund, Kristoffer; Coelho, Luis Pedro
  • Molecular Biology and Evolution, Vol. 34, Issue 8
  • DOI: 10.1093/molbev/msx148

BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010


Advances and Challenges in Computational Prediction of Effectors from Plant Pathogenic Fungi
journal, May 2015


Estimation of Nucleotide Substitution Rates in Eurotiomycete Fungi
journal, December 2002


StringTie enables improved reconstruction of a transcriptome from RNA-seq reads
journal, February 2015

  • Pertea, Mihaela; Pertea, Geo M.; Antonescu, Corina M.
  • Nature Biotechnology, Vol. 33, Issue 3
  • DOI: 10.1038/nbt.3122

CodingQuarry: highly accurate hidden Markov model gene prediction in fungal genomes using RNA-seq transcripts
journal, March 2015


Proteinortho: Detection of (Co-)orthologs in large-scale analysis
journal, April 2011


CRN13 candidate effectors from plant and animal eukaryotic pathogens are DNA-binding proteins which trigger host DNA damage response
journal, December 2015

  • Ramirez-Garcés, Diana; Camborde, Laurent; Pel, Michiel J. C.
  • New Phytologist, Vol. 210, Issue 2
  • DOI: 10.1111/nph.13774

Puccinia coronata f. sp. avenae : a threat to global oat production : Oat crown rust fungus
journal, December 2017

  • Nazareno, Eric S.; Li, Feng; Smith, Madeleine
  • Molecular Plant Pathology, Vol. 19, Issue 5
  • DOI: 10.1111/mpp.12608

The Sequence Alignment/Map format and SAMtools
journal, June 2009


Draft Genome Sequence of Medusavirus Stheno, Isolated from the Tatakai River of Uji, Japan
journal, January 2021

  • Yoshida, Koki; Zhang, Ruixuan; Garcia, Kimberly G.
  • Microbiology Resource Announcements, Vol. 10, Issue 1
  • DOI: 10.1128/mra.01323-20

Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium
journal, March 2010

  • Ma, Li-Jun; van der Does, H. Charlotte; Borkovich, Katherine A.
  • Nature, Vol. 464, Issue 7287
  • DOI: 10.1038/nature08850

Puccinia striiformis in Australia: a review of the incursion, evolution, and adaptation of stripe rust in the period 1979 - 2006
journal, January 2007

  • Wellings, C. R.
  • Australian Journal of Agricultural Research, Vol. 58, Issue 6
  • DOI: 10.1071/AR07130

The relation of recombination to mutational advance
journal, May 1964


HISAT: a fast spliced aligner with low memory requirements
journal, March 2015

  • Kim, Daehwan; Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 12, Issue 4
  • DOI: 10.1038/nmeth.3317

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Works referencing / citing this record:

MARPLE, a point-of-care, strain-level disease diagnostics and surveillance tool for complex fungal pathogens
journal, August 2019

  • Radhakrishnan, Guru V.; Cook, Nicola M.; Bueno-Sancho, Vanessa
  • BMC Biology, Vol. 17, Issue 1
  • DOI: 10.1186/s12915-019-0684-y

De Novo Genome Assembly and Comparative Genomics of the Barley Leaf Rust Pathogen Puccinia hordei Identifies Candidates for Three Avirulence Genes
journal, August 2019

  • Chen, Jiapeng; Wu, Jingqin; Zhang, Peng
  • G3: Genes|Genomes|Genetics, Vol. 9, Issue 10
  • DOI: 10.1534/g3.119.400450

Whole-genome sequencing of Puccinia striiformis f. sp. tritici mutant isolates identifies avirulence gene candidates
journal, March 2020


Pathotypic and molecular evolution of contemporary population of Puccinia striiformis f. sp. tritici in Egypt during 2016-2018
journal, November 2018

  • Draz, Ibrahim Sobhy
  • Journal of Phytopathology, Vol. 167, Issue 1
  • DOI: 10.1111/jph.12770

Distinct Life Histories Impact Dikaryotic Genome Evolution in the Rust Fungus Puccinia striiformis Causing Stripe Rust in Wheat
journal, April 2020

  • Schwessinger, Benjamin; Chen, Yan-Jun; Tien, Richard
  • Genome Biology and Evolution, Vol. 12, Issue 5
  • DOI: 10.1093/gbe/evaa071

Flax rust infection transcriptomics reveals a transcriptional profile that may be indicative for rust Avr genes
journal, December 2019


TaAMT2;3a, a wheat AMT2-type ammonium transporter, facilitates the infection of stripe rust fungus on wheat
journal, June 2019


Pathogen Detection and Microbiome Analysis of Infected Wheat Using a Portable DNA Sequencer
journal, January 2019


The need for speed: compartmentalized genome evolution in filamentous phytopathogens: Multiple 'speeds' in phytopathogen genomes
journal, December 2018

  • Frantzeskakis, Lamprinos; Kusch, Stefan; Panstruga, Ralph
  • Molecular Plant Pathology, Vol. 20, Issue 1
  • DOI: 10.1111/mpp.12738

Genome expansion by allopolyploidization in the fungal strain Coniochaeta 2T2.1 and its exceptional lignocellulolytic machinery
journal, September 2019

  • Mondo, Stephen J.; Jiménez, Diego Javier; Hector, Ronald E.
  • Biotechnology for Biofuels, Vol. 12, Issue 1
  • DOI: 10.1186/s13068-019-1569-6

Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation
journal, November 2019


Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.