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

Title: Duplications and losses in gene families of rust pathogens highlight putative effectors

Abstract

Rust fungi are a group of fungal pathogens that cause some of the world's most destructive diseases of trees and crops. A shared characteristic among rust fungi is obligate biotrophy, the inability to complete a lifecycle without a host. This dependence on a host species likely affects patterns of gene expansion, contraction, and innovation within rust pathogen genomes. The establishment of disease by biotrophic pathogens is reliant upon effector proteins that are encoded in the fungal genome and secreted from the pathogen into the host's cell apoplast or within the cells. This study uses a comparative genomic approach to elucidate putative effectors and determine their evolutionary histories. We used OrthoMCL to identify nearly 20,000 gene families in proteomes of 16 diverse fungal species, which include 15 basidiomycetes and one ascomycete. We inferred patterns of duplication and loss for each gene family and identified families with distinctive patterns of expansion/contraction associated with the evolution of rust fungal genomes. To recognize potential contributors for the unique features of rust pathogens, we identified families harboring secreted proteins that: (i) arose or expanded in rust pathogens relative to other fungi, or (ii) contracted or were lost in rust fungal genomes. While the origin ofmore » rust fungi appears to be associated with considerable gene loss, there are many gene duplications associated with each sampled rust fungal genome. We also highlight two putative effector gene families that have expanded in Cqf that we hypothesize have roles in pathogenicity.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [3];  [2];  [6];  [7]
  1. Univ. of Florida, Gainesville, FL (United States). Plant Molecular and Cellular Biology Program
  2. US Dept. of Agriculture (USDA)., Saucier, MS (United States). Southern Research Station, Southern Inst. of Forest Genetics
  3. Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Forest Sciences
  4. Univ. de Lorraine, Champenoux (France). Interactions Arbres/Microorganismes, Lab. d'Excellence ARBRE, INRA-Nancy, UMR Inst. National de la Recherche Agronomique
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. Univ. of Florida, Gainesville, FL (United States). Plant Molecular and Cellular Biology Program; Univ. of Florida, Gainesville, FL (United States). Biology Dept.; Univ. of Florida, Gainesville, FL (United States). Genetics Inst.
  7. Univ. of Florida, Gainesville, FL (United States). Plant Molecular and Cellular Biology Program; Univ. of Florida, Gainesville, FL (United States). Genetics Inst.; Univ. of Florida, Gainesville, FL (United States). School of Forest Resources and Conservation
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1469147
Report Number(s):
LBNL-178026
Journal ID: ISSN 1664-462X; ir:178026
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 5; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; effectors; rustpathogens; secretome; genome evolution; comparative genomics

Citation Formats

Pendleton, Amanda L., Smith, Katherine E., Feau, Nicolas, Martin, Francis M., Grigoriev, Igor V., Hamelin, Richard, Nelson, C. Dana, Burleigh, J. Gordon, and Davis, John M. Duplications and losses in gene families of rust pathogens highlight putative effectors. United States: N. p., 2014. Web. doi:10.3389/fpls.2014.00299.
Pendleton, Amanda L., Smith, Katherine E., Feau, Nicolas, Martin, Francis M., Grigoriev, Igor V., Hamelin, Richard, Nelson, C. Dana, Burleigh, J. Gordon, & Davis, John M. Duplications and losses in gene families of rust pathogens highlight putative effectors. United States. https://doi.org/10.3389/fpls.2014.00299
Pendleton, Amanda L., Smith, Katherine E., Feau, Nicolas, Martin, Francis M., Grigoriev, Igor V., Hamelin, Richard, Nelson, C. Dana, Burleigh, J. Gordon, and Davis, John M. Thu . "Duplications and losses in gene families of rust pathogens highlight putative effectors". United States. https://doi.org/10.3389/fpls.2014.00299. https://www.osti.gov/servlets/purl/1469147.
@article{osti_1469147,
title = {Duplications and losses in gene families of rust pathogens highlight putative effectors},
author = {Pendleton, Amanda L. and Smith, Katherine E. and Feau, Nicolas and Martin, Francis M. and Grigoriev, Igor V. and Hamelin, Richard and Nelson, C. Dana and Burleigh, J. Gordon and Davis, John M.},
abstractNote = {Rust fungi are a group of fungal pathogens that cause some of the world's most destructive diseases of trees and crops. A shared characteristic among rust fungi is obligate biotrophy, the inability to complete a lifecycle without a host. This dependence on a host species likely affects patterns of gene expansion, contraction, and innovation within rust pathogen genomes. The establishment of disease by biotrophic pathogens is reliant upon effector proteins that are encoded in the fungal genome and secreted from the pathogen into the host's cell apoplast or within the cells. This study uses a comparative genomic approach to elucidate putative effectors and determine their evolutionary histories. We used OrthoMCL to identify nearly 20,000 gene families in proteomes of 16 diverse fungal species, which include 15 basidiomycetes and one ascomycete. We inferred patterns of duplication and loss for each gene family and identified families with distinctive patterns of expansion/contraction associated with the evolution of rust fungal genomes. To recognize potential contributors for the unique features of rust pathogens, we identified families harboring secreted proteins that: (i) arose or expanded in rust pathogens relative to other fungi, or (ii) contracted or were lost in rust fungal genomes. While the origin of rust fungi appears to be associated with considerable gene loss, there are many gene duplications associated with each sampled rust fungal genome. We also highlight two putative effector gene families that have expanded in Cqf that we hypothesize have roles in pathogenicity.},
doi = {10.3389/fpls.2014.00299},
journal = {Frontiers in Plant Science},
number = ,
volume = 5,
place = {United States},
year = {Thu Jun 26 00:00:00 EDT 2014},
month = {Thu Jun 26 00:00:00 EDT 2014}
}

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

Citation Metrics:
Cited by: 39 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

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

Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites
journal, January 1997

  • Nielsen, H.; Engelbrecht, J.; Brunak, S.
  • Protein Engineering Design and Selection, Vol. 10, Issue 1, p. 1-6
  • DOI: 10.1093/protein/10.1.1

The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis
journal, March 2008


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

Fruiting body production in basidiomycetes
journal, August 2000


Challenges and progress towards understanding the role of effectors in plant–fungal interactions
journal, August 2012

  • Rafiqi, Maryam; Ellis, Jeffrey G.; Ludowici, Victoria A.
  • Current Opinion in Plant Biology, Vol. 15, Issue 4
  • DOI: 10.1016/j.pbi.2012.05.003

The genome sequence of the rice blast fungus Magnaporthe grisea
journal, April 2005

  • Dean, Ralph A.; Talbot, Nicholas J.; Ebbole, Daniel J.
  • Nature, Vol. 434, Issue 7036
  • DOI: 10.1038/nature03449

Host-Parasite Coevolutionary Conflict Between Arabidopsis and Downy Mildew
journal, December 2004


Phytophthora Genome Sequences Uncover Evolutionary Origins and Mechanisms of Pathogenesis
journal, September 2006


Prediction of Potential GPI-modification Sites in Proprotein Sequences
journal, September 1999

  • Eisenhaber, Birgit; Bork, Peer; Eisenhaber, Frank
  • Journal of Molecular Biology, Vol. 292, Issue 3
  • DOI: 10.1006/jmbi.1999.3069

TreeFix: Statistically Informed Gene Tree Error Correction Using Species Trees
journal, November 2012

  • Wu, Yi-Chieh; Rasmussen, Matthew D.; Bansal, Mukul S.
  • Systematic Biology, Vol. 62, Issue 1
  • DOI: 10.1093/sysbio/sys076

Lignin-modifying enzymes in filamentous basidiomycetes - ecological, functional and phylogenetic review
journal, February 2010

  • Lundell, Taina K.; Mäkelä, Miia R.; Hildén, Kristiina
  • Journal of Basic Microbiology, Vol. 50, Issue 1
  • DOI: 10.1002/jobm.200900338

URec: a system for unrooted reconciliation
journal, December 2006


Fungal Effector Proteins
journal, September 2009


Diversity and Evolution of Effector Loci in Natural Populations of the Plant Pathogen Melampsora lini
journal, July 2009

  • Barrett, L. G.; Thrall, P. H.; Dodds, P. N.
  • Molecular Biology and Evolution, Vol. 26, Issue 11
  • DOI: 10.1093/molbev/msp166

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


Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens
journal, November 2007

  • Xu, J.; Saunders, C. W.; Hu, P.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 47
  • DOI: 10.1073/pnas.0706756104

The structure and function of fungal laccases
journal, January 1994


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

The Genomics of Obligate (and Nonobligate) Biotrophs
journal, September 2012


Effectors of biotrophic fungi and oomycetes: pathogenicity factors and triggers of host resistance
journal, September 2009


InterPro in 2011: new developments in the family and domain prediction database
journal, November 2011

  • Hunter, S.; Jones, P.; Mitchell, A.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr948

Small proteins of plant-pathogenic fungi secreted during host colonization
journal, December 2005


Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche
journal, October 2012

  • Morin, E.; Kohler, A.; Baker, A. R.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 43
  • DOI: 10.1073/pnas.1206847109

The Plant Cell Wall-Decomposing Machinery Underlies the Functional Diversity of Forest Fungi
journal, July 2011


A Bayesian Approach for Fast and Accurate Gene Tree Reconstruction
journal, July 2010

  • Rasmussen, M. D.; Kellis, M.
  • Molecular Biology and Evolution, Vol. 28, Issue 1
  • DOI: 10.1093/molbev/msq189

Multiple Multi-Copper Oxidase Gene Families in Basidiomycetes – What for?
journal, April 2011


The plant immune system
journal, November 2006

  • Jones, Jonathan D. G.; Dangl, Jeffery L.
  • Nature, Vol. 444, Issue 7117
  • DOI: 10.1038/nature05286

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

Role of laccase in the biology and virulence of
journal, October 2004


Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation: Coevolution in a wild host-pathogen system
journal, February 2012


Life with 6000 Genes
journal, October 1996


Insight into trade-off between wood decay and parasitism from the genome of a fungal forest pathogen
journal, March 2012


Genome sequencing provides insight into the reproductive biology, nutritional mode and ploidy of the fern pathogen Mixia osmundae
journal, December 2013

  • Toome, Merje; Ohm, Robin A.; Riley, Robert W.
  • New Phytologist, Vol. 202, Issue 2
  • DOI: 10.1111/nph.12653

Genome Evolution in Plant Pathogenic and Symbiotic Fungi
book, January 2009


RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees
journal, December 2004


Winter Storm, Maine Coast
journal, March 1977


An ultrastructural comparison of monokaryotic and dikaryotic haustoria formed by the fusiform rust fungus Cronartium quercuum f.sp. fusiforme
journal, December 1982

  • Gray, D. J.; Amerson, H. V.; Dyke, C. G. Van
  • Canadian Journal of Botany, Vol. 60, Issue 12
  • DOI: 10.1139/b82-352

Recent progress in discovery and functional analysis of effector proteins of fungal and oomycete plant pathogens
journal, August 2009

  • Ellis, Jeffrey G.; Rafiqi, Maryam; Gan, Pamela
  • Current Opinion in Plant Biology, Vol. 12, Issue 4
  • DOI: 10.1016/j.pbi.2009.05.004

Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001

  • Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
  • Journal of Molecular Biology, Vol. 305, Issue 3
  • DOI: 10.1006/jmbi.2000.4315

Genome size variation in the pine fusiform rust pathogen Cronartium quercuum f.sp. fusiforme as determined by flow cytometry
journal, November 2010

  • Anderson, Claire L.; Kubisiak, Thomas L.; Nelson, C. Dana
  • Mycologia, Vol. 102, Issue 6
  • DOI: 10.3852/10-040

MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004


A genomic map enriched for markers linked to Avr1 in Cronartium quercuum f.sp. fusiforme
journal, March 2011

  • Kubisiak, Thomas L.; Anderson, Claire L.; Amerson, Henry V.
  • Fungal Genetics and Biology, Vol. 48, Issue 3
  • DOI: 10.1016/j.fgb.2010.09.008

Filamentous plant pathogen effectors in action
journal, October 2013

  • Giraldo, Martha C.; Valent, Barbara
  • Nature Reviews Microbiology, Vol. 11, Issue 11
  • DOI: 10.1038/nrmicro3119

Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence
journal, July 2000

  • Emanuelsson, Olof; Nielsen, Henrik; Brunak, Søren
  • Journal of Molecular Biology, Vol. 300, Issue 4
  • DOI: 10.1006/jmbi.2000.3903

Using transcription of six Puccinia triticina races to identify the effective secretome during infection of wheat
journal, January 2014

  • Bruce, Myron; Neugebauer, Kerri A.; Joly, David L.
  • Frontiers in Plant Science, Vol. 4
  • DOI: 10.3389/fpls.2013.00520

Nutrient uptake in rust fungi: how sweet is parasitic life?
journal, February 2011


Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy
journal, April 2011

  • Letunic, I.; Bork, P.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr201

Comparative analysis of secreted protein evolution using expressed sequence tags from four poplar leaf rusts (Melampsora spp.)
journal, January 2010


Phylogenetic Relationships among the Pine Stem Rust Fungi (Cronartium and Peridermium spp.)
journal, March 1998

  • Vogler, Detlev R.; Bruns, Thomas D.
  • Mycologia, Vol. 90, Issue 2
  • DOI: 10.2307/3761300

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

Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78
journal, May 2004

  • Martinez, Diego; Larrondo, Luis F.; Putnam, Nik
  • Nature Biotechnology, Vol. 22, Issue 6
  • DOI: 10.1038/nbt967

Magnaporthe grisea Pth11p Is a Novel Plasma Membrane Protein That Mediates Appressorium Differentiation in Response to Inductive Substrate Cues
journal, October 1999

  • DeZwaan, Todd M.; Carroll, Anne M.; Valent, Barbara
  • The Plant Cell, Vol. 11, Issue 10
  • DOI: 10.1105/tpc.11.10.2013

A sand fly salivary protein acts as a neutrophil chemoattractant
journal, May 2021

  • Guimaraes-Costa, Anderson B.; Shannon, John P.; Waclawiak, Ingrid
  • Nature Communications, Vol. 12, Issue 1
  • DOI: 10.1038/s41467-021-23002-5

Phylogenetic relationships among the pine stem rust fungi ( Cronartium and Peridermium spp.)
journal, March 1998


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


Magnaporthe grisea Pth11p Is a Novel Plasma Membrane Protein That Mediates Appressorium Differentiation in Response to Inductive Substrate Cues
journal, October 1999

  • DeZwaan, Todd M.; Carroll, Anne M.; Valent, Barbara
  • The Plant Cell, Vol. 11, Issue 10
  • DOI: 10.2307/3871094

InterPro in 2011: new developments in the family and domain prediction database
journal, May 2012

  • Hunter, S.; Jones, P.; Mitchell, A.
  • Nucleic Acids Research, Vol. 40, Issue 10
  • DOI: 10.1093/nar/gks456

Prediction of Potential GPI-modification Sites in Proprotein Sequences
journal, September 1999

  • Eisenhaber, Birgit; Bork, Peer; Eisenhaber, Frank
  • Journal of Molecular Biology, Vol. 292, Issue 3
  • DOI: 10.1006/jmbi.1999.3069

Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence
journal, July 2000

  • Emanuelsson, Olof; Nielsen, Henrik; Brunak, Søren
  • Journal of Molecular Biology, Vol. 300, Issue 4
  • DOI: 10.1006/jmbi.2000.3903

Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001

  • Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
  • Journal of Molecular Biology, Vol. 305, Issue 3
  • DOI: 10.1006/jmbi.2000.4315

Fruiting body production in basidiomycetes
journal, August 2000


Nutrient uptake in rust fungi: how sweet is parasitic life?
journal, February 2011


Small proteins of plant-pathogenic fungi secreted during host colonization
journal, December 2005


Role of laccase in the biology and virulence of
journal, October 2004


A genomic map enriched for markers linked to Avr1 in Cronartium quercuum f.sp. fusiforme
journal, March 2011

  • Kubisiak, Thomas L.; Anderson, Claire L.; Amerson, Henry V.
  • Fungal Genetics and Biology, Vol. 48, Issue 3
  • DOI: 10.1016/j.fgb.2010.09.008

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

Recent progress in discovery and functional analysis of effector proteins of fungal and oomycete plant pathogens
journal, August 2009

  • Ellis, Jeffrey G.; Rafiqi, Maryam; Gan, Pamela
  • Current Opinion in Plant Biology, Vol. 12, Issue 4
  • DOI: 10.1016/j.pbi.2009.05.004

Challenges and progress towards understanding the role of effectors in plant–fungal interactions
journal, August 2012

  • Rafiqi, Maryam; Ellis, Jeffrey G.; Ludowici, Victoria A.
  • Current Opinion in Plant Biology, Vol. 15, Issue 4
  • DOI: 10.1016/j.pbi.2012.05.003

Biosynthesis of fungal melanins and their importance for human pathogenic fungi
journal, March 2003


The genome sequence of the rice blast fungus Magnaporthe grisea
journal, April 2005

  • Dean, Ralph A.; Talbot, Nicholas J.; Ebbole, Daniel J.
  • Nature, Vol. 434, Issue 7036
  • DOI: 10.1038/nature03449

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

The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis
journal, March 2008


Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78
journal, May 2004

  • Martinez, Diego; Larrondo, Luis F.; Putnam, Nik
  • Nature Biotechnology, Vol. 22, Issue 6
  • DOI: 10.1038/nbt967

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

Filamentous plant pathogen effectors in action
journal, October 2013

  • Giraldo, Martha C.; Valent, Barbara
  • Nature Reviews Microbiology, Vol. 11, Issue 11
  • DOI: 10.1038/nrmicro3119

Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture
journal, November 2022


Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens
journal, November 2007

  • Xu, J.; Saunders, C. W.; Hu, P.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 47
  • DOI: 10.1073/pnas.0706756104

Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche
journal, October 2012

  • Morin, E.; Kohler, A.; Baker, A. R.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 43
  • DOI: 10.1073/pnas.1206847109

RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees
journal, December 2004


Diversity and Evolution of Effector Loci in Natural Populations of the Plant Pathogen Melampsora lini
journal, July 2009

  • Barrett, L. G.; Thrall, P. H.; Dodds, P. N.
  • Molecular Biology and Evolution, Vol. 26, Issue 11
  • DOI: 10.1093/molbev/msp166

A Bayesian Approach for Fast and Accurate Gene Tree Reconstruction
journal, July 2010

  • Rasmussen, M. D.; Kellis, M.
  • Molecular Biology and Evolution, Vol. 28, Issue 1
  • DOI: 10.1093/molbev/msq189

Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy
journal, April 2011

  • Letunic, I.; Bork, P.
  • Nucleic Acids Research, Vol. 39, Issue suppl
  • DOI: 10.1093/nar/gkr201

InterPro in 2011: new developments in the family and domain prediction database
journal, May 2012

  • Hunter, S.; Jones, P.; Mitchell, A.
  • Nucleic Acids Research, Vol. 40, Issue 10
  • DOI: 10.1093/nar/gks456

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

Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites
journal, January 1997

  • Nielsen, H.; Engelbrecht, J.; Brunak, S.
  • Protein Engineering Design and Selection, Vol. 10, Issue 1, p. 1-6
  • DOI: 10.1093/protein/10.1.1

TreeFix: Statistically Informed Gene Tree Error Correction Using Species Trees
journal, November 2012

  • Wu, Yi-Chieh; Rasmussen, Matthew D.; Bansal, Mukul S.
  • Systematic Biology, Vol. 62, Issue 1
  • DOI: 10.1093/sysbio/sys076

Melampsora larici-populina Transcript Profiling During Germination and Timecourse Infection of Poplar Leaves Reveals Dynamic Expression Patterns Associated with Virulence and Biotrophy
journal, July 2011

  • Duplessis, Sébastien; Hacquard, Stéphane; Delaruelle, Christine
  • Molecular Plant-Microbe Interactions, Vol. 24, Issue 7
  • DOI: 10.1094/mpmi-01-11-0006

A Comprehensive Analysis of Genes Encoding Small Secreted Proteins Identifies Candidate Effectors in Melampsora larici-populina (Poplar Leaf Rust)
journal, March 2012

  • Hacquard, Stéphane; Joly, David L.; Lin, Yao-Cheng
  • Molecular Plant-Microbe Interactions, Vol. 25, Issue 3
  • DOI: 10.1094/mpmi-09-11-0238

The structure and function of fungal laccases
journal, January 1994


OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
journal, September 2003


Magnaporthe grisea Pth11p Is a Novel Plasma Membrane Protein That Mediates Appressorium Differentiation in Response to Inductive Substrate Cues
journal, October 1999

  • DeZwaan, Todd M.; Carroll, Anne M.; Valent, Barbara
  • The Plant Cell, Vol. 11, Issue 10
  • DOI: 10.1105/tpc.11.10.2013

Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation: Coevolution in a wild host-pathogen system
journal, February 2012


Effectors of biotrophic fungi and oomycetes: pathogenicity factors and triggers of host resistance
journal, September 2009


Insight into trade-off between wood decay and parasitism from the genome of a fungal forest pathogen
journal, March 2012


Genome sequencing provides insight into the reproductive biology, nutritional mode and ploidy of the fern pathogen Mixia osmundae
journal, December 2013

  • Toome, Merje; Ohm, Robin A.; Riley, Robert W.
  • New Phytologist, Vol. 202, Issue 2
  • DOI: 10.1111/nph.12653

Host-Parasite Coevolutionary Conflict Between Arabidopsis and Downy Mildew
journal, December 2004


Phytophthora Genome Sequences Uncover Evolutionary Origins and Mechanisms of Pathogenesis
journal, September 2006


The Plant Cell Wall-Decomposing Machinery Underlies the Functional Diversity of Forest Fungi
journal, July 2011


Funding Sequencing Efforts
journal, February 1997


An ultrastructural comparison of monokaryotic and dikaryotic haustoria formed by the fusiform rust fungus Cronartium quercuum f.sp. fusiforme
journal, December 1982

  • Gray, D. J.; Amerson, H. V.; Dyke, C. G. Van
  • Canadian Journal of Botany, Vol. 60, Issue 12
  • DOI: 10.1139/b82-352

The Genomics of Obligate (and Nonobligate) Biotrophs
journal, September 2012


Fungal Effector Proteins
journal, September 2009


MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004


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


Multiple Multi-Copper Oxidase Gene Families in Basidiomycetes – What for?
journal, April 2011


Winter Storm, Maine Coast
journal, March 1977


Using transcription of six Puccinia triticina races to identify the effective secretome during infection of wheat
journal, January 2014

  • Bruce, Myron; Neugebauer, Kerri A.; Joly, David L.
  • Frontiers in Plant Science, Vol. 4
  • DOI: 10.3389/fpls.2013.00520

Genome size variation in the pine fusiform rust pathogen Cronartium quercuum f.sp. fusiforme as determined by flow cytometry
journal, November 2010

  • Anderson, Claire L.; Kubisiak, Thomas L.; Nelson, C. Dana
  • Mycologia, Vol. 102, Issue 6
  • DOI: 10.3852/10-040

Works referencing / citing this record:

A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements
journal, January 2017

  • Hartmann, Fanny E.; Sánchez-Vallet, Andrea; McDonald, Bruce A.
  • The ISME Journal, Vol. 11, Issue 5
  • DOI: 10.1038/ismej.2016.196

Plant Innate Immune Response: Qualitative and Quantitative Resistance
journal, January 2016

  • Kushalappa, Ajjamada C.; Yogendra, Kalenahalli N.; Karre, Shailesh
  • Critical Reviews in Plant Sciences, Vol. 35, Issue 1
  • DOI: 10.1080/07352689.2016.1148980

The emergence of the multi‐species NIP1 effector in Rhynchosporium was accompanied by high rates of gene duplications and losses
journal, April 2019

  • Mohd‐Assaad, Norfarhan; McDonald, Bruce A.; Croll, Daniel
  • Environmental Microbiology, Vol. 21, Issue 8
  • DOI: 10.1111/1462-2920.14583

Host-microbe and microbe-microbe interactions in the evolution of obligate plant parasitism
journal, January 2015

  • Kemen, Ariane C.; Agler, Matthew T.; Kemen, Eric
  • New Phytologist, Vol. 206, Issue 4
  • DOI: 10.1111/nph.13284

Advances in understanding obligate biotrophy in rust fungi
journal, February 2019

  • Lorrain, Cécile; Gonçalves dos Santos, Karen Cristine; Germain, Hugo
  • New Phytologist, Vol. 222, Issue 3
  • DOI: 10.1111/nph.15641

Rapid turnover of effectors in grass powdery mildew (Blumeria graminis)
journal, October 2017

  • Menardo, Fabrizio; Praz, Coraline R.; Wicker, Thomas
  • BMC Evolutionary Biology, Vol. 17, Issue 1
  • DOI: 10.1186/s12862-017-1064-2

Comparative genome analysis and genome evolution of members of the magnaporthaceae family of fungi
journal, February 2016


Network analysis exposes core functions in major lifestyles of fungal and oomycete plant pathogens
journal, December 2019


Genome sequence of the plant growth promoting endophytic yeast Rhodotorula graminis WP1
journal, September 2015


Rapid turnover of effectors in grass powdery mildew (Blumeria graminis)
text, January 2017

  • Menardo, Fabrizio; Praz, Coraline R.; Wicker, Thomas
  • BioMed Central
  • DOI: 10.5167/uzh-144168

Rapid turnover of effectors in grass powdery mildew (Blumeria graminis)
journal, October 2017

  • Menardo, Fabrizio; Praz, Coraline R.; Wicker, Thomas
  • BMC Evolutionary Biology, Vol. 17, Issue 1
  • DOI: 10.1186/s12862-017-1064-2

Network analysis exposes core functions in major lifestyles of fungal and oomycete plant pathogens
journal, December 2019


Genome sequence of the plant growth promoting endophytic yeast Rhodotorula graminis WP1
journal, September 2015


Genomic Patterns Of Positive Selection At The Origin Of Rust Fungi
text, January 2015