Increased virulence of Puccinia coronata f. sp.avenae populations through allele frequency changes at multiple putative Avr loci

Pathogen populations are expected to evolve virulence traits in response to resistance deployed in agricultural settings. However, few temporal datasets have been available to characterize this process at the population level. Here, we examined two temporally separated populations of Puccinia corona...

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Published in:	PLoS genetics Vol. 16; no. 12; p. e1009291
Main Authors:	Miller, Marisa E, Nazareno, Eric S, Rottschaefer, Susan M, Riddle, Jakob, Dos Santos Pereira, Danilo, Li, Feng, Nguyen-Phuc, Hoa, Henningsen, Eva C, Persoons, Antoine, Saunders, Diane G O, Stukenbrock, Eva, Dodds, Peter N, Kianian, Shahryar F, Figueroa, Melania
Format:	Journal Article
Language:	English
Published:	United States Public Library of Science 28-12-2020 Public Library of Science (PLoS)
Subjects:	Asexuality Avena - microbiology Biology and Life Sciences Diseases and pests Epidemics Evolution Fungi Gene Frequency Genes Genes, Fungal Genetic aspects Genetic diversity Genomes Hybridization Infections Leucine Medicine and Health Sciences Mutation Oats Pathogens Physiological aspects Plant diseases Plant population genetics Polymorphism, Genetic Population Population genetics Principal components analysis Puccinia - genetics Puccinia - pathogenicity Puccinia coronata avenae Pucciniales Recombination Rust diseases Rust fungi Selection, Genetic Virulence Virulence (Microbiology) Virulence - genetics United Kingdom United States > US North America
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Abstract	Pathogen populations are expected to evolve virulence traits in response to resistance deployed in agricultural settings. However, few temporal datasets have been available to characterize this process at the population level. Here, we examined two temporally separated populations of Puccinia coronata f. sp. avenae (Pca), which causes crown rust disease in oat (Avena sativa) sampled from 1990 to 2015. We show that a substantial increase in virulence occurred from 1990 to 2015 and this was associated with a genetic differentiation between populations detected by genome-wide sequencing. We found strong evidence for genetic recombination in these populations, showing the importance of the alternate host in generating genotypic variation through sexual reproduction. However, asexual expansion of some clonal lineages was also observed within years. Genome-wide association analysis identified seven Avr loci associated with virulence towards fifteen Pc resistance genes in oat and suggests that some groups of Pc genes recognize the same pathogen effectors. The temporal shift in virulence patterns in the Pca populations between 1990 and 2015 is associated with changes in allele frequency in these genomic regions. Nucleotide diversity patterns at a single Avr locus corresponding to Pc38, Pc39, Pc55, Pc63, Pc70, and Pc71 showed evidence of a selective sweep associated with the shift to virulence towards these resistance genes in all 2015 collected isolates.
AbstractList	Pathogen populations are expected to evolve virulence traits in response to resistance deployed in agricultural settings. However, few temporal datasets have been available to characterize this process at the population level. Here, we examined two temporally separated populations of Puccinia coronata f. sp. avenae (Pca), which causes crown rust disease in oat (Avena sativa) sampled from 1990 to 2015. We show that a substantial increase in virulence occurred from 1990 to 2015 and this was associated with a genetic differentiation between populations detected by genome-wide sequencing. We found strong evidence for genetic recombination in these populations, showing the importance of the alternate host in generating genotypic variation through sexual reproduction. However, asexual expansion of some clonal lineages was also observed within years. Genome-wide association analysis identified seven Avr loci associated with virulence towards fifteen Pc resistance genes in oat and suggests that some groups of Pc genes recognize the same pathogen effectors. The temporal shift in virulence patterns in the Pca populations between 1990 and 2015 is associated with changes in allele frequency in these genomic regions. Nucleotide diversity patterns at a single Avr locus corresponding to Pc38, Pc39, Pc55, Pc63, Pc70, and Pc71 showed evidence of a selective sweep associated with the shift to virulence towards these resistance genes in all 2015 collected isolates. R genes generally encode intracellular immune receptor proteins of the nucleotide binding leucine rich repeat (NB-LRR) class, which recognize pathogen ‘effector’ proteins that are delivered into host cells during infection to suppress host basal defenses and facilitate infection [1,3]. [...]plants and pathogens engage in a co-evolutionary battle, where new resistance traits in the host are countered by gain-of-virulence traits in the pathogen. Somatic hybridization, as shown in the broadly virulent Ug99 lineage of Pgt, is another mechanism that contributes to genetic variation in rusts [15]. [...]there are multiple processes that can play a role in the evolution of rust fungi and their precise contribution has not yet been determined. [...]sexual recombination is thought to contribute to variation in the US population of Pca. R genes generally encode intracellular immune receptor proteins of the nucleotide binding leucine rich repeat (NB-LRR) class, which recognize pathogen ‘effector’ proteins that are delivered into host cells during infection to suppress host basal defenses and facilitate infection [1,3]. [...]plants and pathogens engage in a co-evolutionary battle, where new resistance traits in the host are countered by gain-of-virulence traits in the pathogen. Somatic hybridization, as shown in the broadly virulent Ug99 lineage of Pgt, is another mechanism that contributes to genetic variation in rusts [15]. [...]there are multiple processes that can play a role in the evolution of rust fungi and their precise contribution has not yet been determined. [...]sexual recombination is thought to contribute to variation in the US population of Pca. Pathogen populations are expected to evolve virulence traits in response to resistance deployed in agricultural settings. However, few temporal datasets have been available to characterize this process at the population level. Here, we examined two temporally separated populations of Puccinia coronata f. sp. avenae ( Pca ), which causes crown rust disease in oat ( Avena sativa ) sampled from 1990 to 2015. We show that a substantial increase in virulence occurred from 1990 to 2015 and this was associated with a genetic differentiation between populations detected by genome-wide sequencing. We found strong evidence for genetic recombination in these populations, showing the importance of the alternate host in generating genotypic variation through sexual reproduction. However, asexual expansion of some clonal lineages was also observed within years. Genome-wide association analysis identified seven Avr loci associated with virulence towards fifteen Pc resistance genes in oat and suggests that some groups of Pc genes recognize the same pathogen effectors. The temporal shift in virulence patterns in the Pca populations between 1990 and 2015 is associated with changes in allele frequency in these genomic regions. Nucleotide diversity patterns at a single Avr locus corresponding to Pc38 , Pc39 , Pc55 , Pc63 , Pc70 , and Pc71 showed evidence of a selective sweep associated with the shift to virulence towards these resistance genes in all 2015 collected isolates. Pathogen populations are expected to evolve virulence traits in response to resistance deployed in agricultural settings. However, few temporal datasets have been available to characterize this process at the population level. Here, we examined two temporally separated populations of Puccinia coronata f. sp. avenae ( Pca ), which causes crown rust disease in oat ( Avena sativa ) sampled from 1990 to 2015. We show that a substantial increase in virulence occurred from 1990 to 2015 and this was associated with a genetic differentiation between populations detected by genome-wide sequencing. We found strong evidence for genetic recombination in these populations, showing the importance of the alternate host in generating genotypic variation through sexual reproduction. However, asexual expansion of some clonal lineages was also observed within years. Genome-wide association analysis identified seven Avr loci associated with virulence towards fifteen Pc resistance genes in oat and suggests that some groups of Pc genes recognize the same pathogen effectors. The temporal shift in virulence patterns in the Pca populations between 1990 and 2015 is associated with changes in allele frequency in these genomic regions. Nucleotide diversity patterns at a single Avr locus corresponding to Pc38 , Pc39 , Pc55 , Pc63 , Pc70 , and Pc71 showed evidence of a selective sweep associated with the shift to virulence towards these resistance genes in all 2015 collected isolates. The rust fungus Puccinia coronata f. sp. avenae ( Pca ), which causes crown rust disease, decimates oat ( Avena sativa ) production in many countries of the world. While the use of genetic resistance in crop breeding programs is the most sustainable disease management strategy to control plant disease, the release of oat varieties that display genetic resistance to Pca infection is hindered by rapid evolution of this pathogen. This study aims to determine demography and determinants of adaptive evolution in Pca to minimize the risk of disease outbreaks and enhance resistance gene stewardship. We recently published two high quality genome references of P . coronata f. sp. avenae . Here, we used these resources to direct a population genomics-based study of two temporally distant sets of pathogen collections to study genotypic changes that may explain the most recent oat crown rust epidemics across the continental US. We found that the population of Pca in 1990 is significantly different to that collected in 2015 at both genotypic and phenotypic levels. Our findings are consistent with the role of sexual and asexual reproduction in the Pca population diversity. Importantly, our work identifies genomic regions and genes that may be involved in local host adaptation which in the future may assist in the development of molecular markers and diagnosis of virulence.
Audience	Academic
Author	Figueroa, Melania Dos Santos Pereira, Danilo Henningsen, Eva C Dodds, Peter N Li, Feng Saunders, Diane G O Kianian, Shahryar F Nguyen-Phuc, Hoa Nazareno, Eric S Persoons, Antoine Stukenbrock, Eva Miller, Marisa E Riddle, Jakob Rottschaefer, Susan M
AuthorAffiliation	2 USDA-ARS Cereal Disease Laboratory, St. Paul, Minnesota, United States of America 1 Department of Plant Pathology, University of Minnesota, St. Paul, Minnesota, United States of America 5 INRA/Universite de Lorraine Interactions Abres/Microorganismes, Champenoux, France 7 Commonwealth Scientific and Industrial Research Organisation, Agriculture and Food, Canberra, Australia 3 Environmental Genomics Group, Max Planck Institute for Evolutionary Biology, Plon, Germany 4 Christian-Albrechts University of Kiel, Kiel Germany 6 John Innes Centre, Norwich, United Kingdom INRA, FRANCE
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Cites_doi	10.1534/genetics.118.301319 10.1139/b93-026 10.1093/bioinformatics/btn129 10.1038/s42003-018-0013-y 10.1006/tpbi.1996.0002 10.1017/CBO9780511525575 10.1139/g94-087 10.3389/fpls.2014.00759 10.21105/joss.00731 10.1038/nrg2812 10.1093/nar/gkq603 10.1126/science.aao4810 10.17221/17/2009-PPS 10.1094/PHYTO-95-0053 10.1111/1755-0998.12549 10.1186/gb-2012-13-8-r77 10.1093/bioinformatics/btu170 10.1371/journal.pone.0101271 10.1094/PDIS-09-10-0639 10.1101/gr.4252305 10.1094/PDIS-93-4-0347 10.1093/bioinformatics/btw313 10.1093/molbev/msj030 10.1126/science.aao7294 10.1080/07060661.2019.1577300 10.1101/gr.107524.110 10.1093/molbev/msp166 10.1023/A:1009652222382 10.1093/bioinformatics/btm069 10.1007/978-3-319-24277-4 10.1371/journal.pone.0024230 10.3389/fpls.2016.00205 10.1093/molbev/msu136 10.1094/PD-66-177 10.1093/bioinformatics/bts444 10.1093/genetics/123.3.585 10.1094/PDIS-92-3-0379 10.1038/s41467-019-12927-7 10.1186/s12915-019-0712-y 10.1007/BF00225163 10.7554/eLife.00731 10.1371/journal.pcbi.1005727 10.1146/annurev.phyto.40.120501.101443 10.1111/j.1365-294X.2011.05138.x 10.1094/PDIS.2000.84.5.580 10.1016/j.pbi.2020.02.007 10.1128/mBio.01650-17 10.1093/nar/gkz239 10.1080/07060661.2010.546957 10.1093/bioinformatics/btr521 10.1007/s11032-004-0148-z 10.1093/bioinformatics/btq033 10.1094/Phyto-78-342 10.7717/peerj.281 10.1093/bioinformatics/btp352 10.1046/j.1471-8278.2000.00014.x 10.1371/journal.pone.0209105 10.1109/TVCG.2014.2346248 10.1534/genetics.105.048975 10.1094/MPMI-10-17-0258-R 10.1111/j.1365-3059.2008.01836.x 10.3389/fpls.2014.00416 10.1111/mpp.12608 10.1016/0040-5809(75)90020-9 10.1038/ng.546 10.3835/plantgenome2015.10.0102 10.12688/f1000research.6924.1 10.1038/nrmicro.2017.76 10.1111/2041-210X.12628 10.7717/peerj.4958 10.1146/annurev.py.09.090171.001423
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Notes	new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Current address: Masonic Cancer Center, University of Minnesota, Minneapolis, Minnesota, United States of America Current address: Department of Ecology and Evolutionary Biology, Vietnam National University HCMC, Ho Chi Minh, Vietnam Current address: Pairwise Plants, LLC., Durham, North Carolina, United States of America The authors have declared that no competing interests exist.
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References	ML Carson (pgen.1009291.ref043) 2009; 93 A McKenna (pgen.1009291.ref069) 2010; 20 B Admassu-Yimer (pgen.1009291.ref024) 2018; 13 TC Bruen (pgen.1009291.ref033) 2006; 172 W. Stephan (pgen.1009291.ref058) 2019; 211 LG Barrett (pgen.1009291.ref005) 2009; 26 J Chong (pgen.1009291.ref023) 2000; 84 T Fetch (pgen.1009291.ref046) 2011; 4 M Möller (pgen.1009291.ref012) 2017; 15 KD Murray (pgen.1009291.ref030) 2017; 13 M Figueroa (pgen.1009291.ref013) 2016; 7 J Chong (pgen.1009291.ref017) 1993; 71 pgen.1009291.ref039 AP Roelfs (pgen.1009291.ref014) 1982; 66 PJ Maughan (pgen.1009291.ref052) 2019; 17 G. Simpson (pgen.1009291.ref090) 2015 PM Agapow (pgen.1009291.ref035) 2001; 1 G Yu (pgen.1009291.ref075) 2017; 8 E. Ortiz (pgen.1009291.ref079) 2019 J. Wakeley (pgen.1009291.ref083) 1996; 49 NM Upadhyaya (pgen.1009291.ref088) 2015; 5 H Klenová-Jiráková (pgen.1009291.ref019) 2010; 46 JG Menzies (pgen.1009291.ref044) 2019; 41 HH Flor (pgen.1009291.ref002) 1971; 9 U. NASS (pgen.1009291.ref038) 2019 ME Miller (pgen.1009291.ref022) 2018; 9 F Cabanettes (pgen.1009291.ref095) 2018; 6 F Kiehn (pgen.1009291.ref054) 1976; 18 ML Carson (pgen.1009291.ref059) 2008; 92 MR Crusoe (pgen.1009291.ref073) 2015; 4 AL Bush (pgen.1009291.ref026) 1998; 4 (pgen.1009291.ref068) 2018 K Wang (pgen.1009291.ref071) 2010; 38 T Jombart (pgen.1009291.ref032) 2011; 27 W Stacklies (pgen.1009291.ref063) 2007; 23 ES Nazareno (pgen.1009291.ref016) 2018; 19 ML Carson (pgen.1009291.ref018) 2011; 95 RC Team (pgen.1009291.ref061) 2013 AE Lipka (pgen.1009291.ref092) 2012; 28 I Letunic (pgen.1009291.ref078) 2019; 47 F. de Mendibru (pgen.1009291.ref082) 2016 S Bourras (pgen.1009291.ref049) 2015; 27 AS Chaffin (pgen.1009291.ref051) 2016; 9 H. Li (pgen.1009291.ref066) 2013; 1303 AR Quinlan (pgen.1009291.ref067) 2010; 26 CM Lewis (pgen.1009291.ref041) 2018; 1 B Pfeifer (pgen.1009291.ref076) 2014; 31 K. Slowikowski (pgen.1009291.ref064) 2018 A Lex (pgen.1009291.ref070) 2014; 20 C Xhaard (pgen.1009291.ref042) 2011; 20 H. Wickham (pgen.1009291.ref060) 2016 T Yin (pgen.1009291.ref086) 2012; 13 RR Hudson (pgen.1009291.ref034) 1992; 132 ZN Kamvar (pgen.1009291.ref081) 2014; 2 C Wright (pgen.1009291.ref055) 2004; 14 ZN Kamvar (pgen.1009291.ref080) 2015; 6 A Salcedo (pgen.1009291.ref010) 2017; 358 S Ali (pgen.1009291.ref047) 2014; 10 GN Agrios (pgen.1009291.ref007) 2005 AM Bolger (pgen.1009291.ref065) 2014; 30 NASS UNASS (pgen.1009291.ref021) 2010; 628 H Li (pgen.1009291.ref028) 2009; 25 JD Storey (pgen.1009291.ref094) 2019 KJ Leonard (pgen.1009291.ref050) 2005; 95 SD Turner (pgen.1009291.ref093) 2018; 3 B Schwessinger (pgen.1009291.ref087) 2019 R Nielsen (pgen.1009291.ref037) 2005; 15 Q Zhang (pgen.1009291.ref074) 2014; 9 M Figueroa (pgen.1009291.ref008) 2020; 50 K Yoshida (pgen.1009291.ref029) 2013; 2 K Rawlins (pgen.1009291.ref040) 2018 F. Tajima (pgen.1009291.ref085) 1989; 123 E Garrison (pgen.1009291.ref027) 2012; 1207 D. Jones (pgen.1009291.ref048) 1988; 78 J Chong (pgen.1009291.ref045) 2011; 33 E. Jongman (pgen.1009291.ref089) 1995 Z Gu (pgen.1009291.ref062) 2016; 32 R. Park (pgen.1009291.ref009) 2008; 57 BA McDonald (pgen.1009291.ref006) 2002; 40 D Harder (pgen.1009291.ref053) 1980; 22 F Li (pgen.1009291.ref015) 2019; 10 WL Rooney (pgen.1009291.ref020) 1994; 89 J Chen (pgen.1009291.ref011) 2017; 358 T. Jombart (pgen.1009291.ref031) 2008; 24 JF Tabima (pgen.1009291.ref036) 2018; 31 Z Zhang (pgen.1009291.ref091) 2010; 42 B Petre (pgen.1009291.ref003) 2014; 5 DH Huson (pgen.1009291.ref077) 2006; 23 S Sowa (pgen.1009291.ref056); 2020 BJ Knaus (pgen.1009291.ref072) 2017; 17 D Cantu (pgen.1009291.ref004) 2011; 6 KE Klos (pgen.1009291.ref025) 2017; 10 PN Dodds (pgen.1009291.ref001) 2010; 11 G. Watterson (pgen.1009291.ref084) 1975; 7 E Jellen (pgen.1009291.ref057) 1994; 37
References_xml	– volume: 211 start-page: 5 issue: 1 year: 2019 ident: pgen.1009291.ref058 article-title: Selective sweeps publication-title: Genetics doi: 10.1534/genetics.118.301319 contributor: fullname: W. Stephan – volume: 71 start-page: 248 issue: 2 year: 1993 ident: pgen.1009291.ref017 article-title: Virulence dynamics and phenotypic diversity of Puccinia coronata f. sp. avenae in Canada from 1974 to 1990 publication-title: Canadian Journal of Botany doi: 10.1139/b93-026 contributor: fullname: J Chong – volume: 24 start-page: 1403 issue: 11 year: 2008 ident: pgen.1009291.ref031 article-title: adegenet: a R package for the multivariate analysis of genetic markers publication-title: Bioinformatics doi: 10.1093/bioinformatics/btn129 contributor: fullname: T. Jombart – volume: 1 start-page: 13 year: 2018 ident: pgen.1009291.ref041 article-title: Potential for re-emergence of wheat stem rust in the United Kingdom publication-title: Communications Biology doi: 10.1038/s42003-018-0013-y contributor: fullname: CM Lewis – volume: 1303 start-page: 3997 year: 2013 ident: pgen.1009291.ref066 article-title: Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM publication-title: arXiv contributor: fullname: H. Li – volume: 49 start-page: 39 issue: 1 year: 1996 ident: pgen.1009291.ref083 article-title: The variance of pairwise nucleotide differences in two populations with migration publication-title: Theoretical population biology doi: 10.1006/tpbi.1996.0002 contributor: fullname: J. Wakeley – volume-title: Data analysis in community and landscape ecology: Ordination year: 1995 ident: pgen.1009291.ref089 doi: 10.1017/CBO9780511525575 contributor: fullname: E. Jongman – volume: 37 start-page: 613 issue: 4 year: 1994 ident: pgen.1009291.ref057 article-title: Genomic in situ hybridization differentiates between A/D-and C-genome chromatin and detects intergenomic translocations in polyploid oat species (genus Avena) publication-title: Genome research doi: 10.1139/g94-087 contributor: fullname: E Jellen – volume: 5 start-page: 759 year: 2015 ident: pgen.1009291.ref088 article-title: Comparative genomics of Australian isolates of the wheat stem rust pathogen Puccinia graminis f. sp. tritici reveals extensive polymorphism in candidate effector genes publication-title: Front Plant Sci doi: 10.3389/fpls.2014.00759 contributor: fullname: NM Upadhyaya – volume: 3 start-page: 731 issue: 25 year: 2018 ident: pgen.1009291.ref093 article-title: qqman: an R package for visualizing GWAS results using Q-Q and manhattan plots publication-title: Journal of Open Source Software doi: 10.21105/joss.00731 contributor: fullname: SD Turner – volume: 18 start-page: 717 issue: 4 year: 1976 ident: pgen.1009291.ref054 article-title: Cytology. Inheritance of resistance to Puccinia coronata avenae and its association with seed characteristics in four accessions of Avena sterilis publication-title: Canadian Journal of Genetics contributor: fullname: F Kiehn – volume: 11 start-page: 539 issue: 8 year: 2010 ident: pgen.1009291.ref001 article-title: Plant immunity: towards an integrated view of plant–pathogen interactions publication-title: Nature Reviews Genetics doi: 10.1038/nrg2812 contributor: fullname: PN Dodds – volume: 38 start-page: e164 issue: 16 year: 2010 ident: pgen.1009291.ref071 article-title: ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data publication-title: Nucleic acids research doi: 10.1093/nar/gkq603 contributor: fullname: K Wang – volume: 358 start-page: 1607 issue: 6370 year: 2017 ident: pgen.1009291.ref011 article-title: Loss of AvrSr50 by somatic exchange in stem rust leads to virulence for Sr50 resistance in wheat publication-title: Science doi: 10.1126/science.aao4810 contributor: fullname: J Chen – volume: 46 start-page: 98 issue: 3 year: 2010 ident: pgen.1009291.ref019 article-title: Diversity of oat crown rust (Puccinia coronata f. sp. avenae) isolates detected by virulence and AFLP analyses publication-title: Plant Protection Science doi: 10.17221/17/2009-PPS contributor: fullname: H Klenová-Jiráková – year: 2013 ident: pgen.1009291.ref061 contributor: fullname: RC Team – volume-title: EDD Maps–Early Detection & Distribution Mapping Systems year: 2018 ident: pgen.1009291.ref040 contributor: fullname: K Rawlins – year: 2019 ident: pgen.1009291.ref079 article-title: vcf2phylip v2.0: convert a VCF matrix into several matrix formats for phylogenetic analysis contributor: fullname: E. Ortiz – volume: 95 start-page: 53 issue: 1 year: 2005 ident: pgen.1009291.ref050 article-title: Virulence associations in oat crown rust publication-title: Phytopathology doi: 10.1094/PHYTO-95-0053 contributor: fullname: KJ Leonard – volume: 17 start-page: 44 issue: 1 year: 2017 ident: pgen.1009291.ref072 article-title: vcfr: a package to manipulate and visualize variant call format data publication-title: R. Molecular Ecology Resources doi: 10.1111/1755-0998.12549 contributor: fullname: BJ Knaus – volume: 13 start-page: R77 issue: 8 year: 2012 ident: pgen.1009291.ref086 article-title: ggbio: an R package for extending the grammar of graphics for genomic data publication-title: Genome biology doi: 10.1186/gb-2012-13-8-r77 contributor: fullname: T Yin – start-page: 859728 year: 2019 ident: pgen.1009291.ref087 article-title: Distinct life histories impact dikaryotic genome evolution in the rust fungus Puccinia striiformis causing stripe rust in wheat publication-title: BioRxiv contributor: fullname: B Schwessinger – volume: 30 start-page: 2114 issue: 15 year: 2014 ident: pgen.1009291.ref065 article-title: Trimmomatic: a flexible trimmer for Illumina sequence data publication-title: Bioinformatics doi: 10.1093/bioinformatics/btu170 contributor: fullname: AM Bolger – volume: 9 issue: 7 year: 2014 ident: pgen.1009291.ref074 article-title: These are not the k-mers you are looking for: efficient online k-mer counting using a probabilistic data structure publication-title: Plos One doi: 10.1371/journal.pone.0101271 contributor: fullname: Q Zhang – volume: 95 start-page: 1528 issue: 12 year: 2011 ident: pgen.1009291.ref018 article-title: Virulence in oat crown rust (Puccinia coronata f. sp. avenae) in the United States from 2006 through 2009 publication-title: Plant Disease doi: 10.1094/PDIS-09-10-0639 contributor: fullname: ML Carson – volume: 15 start-page: 1566 issue: 11 year: 2005 ident: pgen.1009291.ref037 article-title: Genomic scans for selective sweeps using SNP data publication-title: Genome research doi: 10.1101/gr.4252305 contributor: fullname: R Nielsen – volume: 93 start-page: 347 issue: 4 year: 2009 ident: pgen.1009291.ref043 article-title: Crown rust development and selection for virulence in Puccinia coronata f. sp. avenae in an oat multiline cultivar publication-title: Plant disease doi: 10.1094/PDIS-93-4-0347 contributor: fullname: ML Carson – volume: 32 start-page: 2847 issue: 18 year: 2016 ident: pgen.1009291.ref062 article-title: Complex heatmaps reveal patterns and correlations in multidimensional genomic data publication-title: Bioinformatics doi: 10.1093/bioinformatics/btw313 contributor: fullname: Z Gu – volume: 23 start-page: 254 issue: 2 year: 2006 ident: pgen.1009291.ref077 article-title: Application of phylogenetic networks in evolutionary studies publication-title: Mol Biol Evol doi: 10.1093/molbev/msj030 contributor: fullname: DH Huson – volume: 358 start-page: 1604 issue: 6370 year: 2017 ident: pgen.1009291.ref010 article-title: Variation in the AvrSr35 gene determines Sr35 resistance against wheat stem rust race Ug99 publication-title: Science doi: 10.1126/science.aao7294 contributor: fullname: A Salcedo – volume: 41 start-page: 379 issue: 3 year: 2019 ident: pgen.1009291.ref044 article-title: Virulence of Puccinia coronata var avenae f. sp. avenae (oat crown rust) in Canada during 2010 to 2015 publication-title: Canadian Journal of Plant Pathology doi: 10.1080/07060661.2019.1577300 contributor: fullname: JG Menzies – volume: 20 start-page: 1297 issue: 9 year: 2010 ident: pgen.1009291.ref069 article-title: The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data publication-title: Genome research doi: 10.1101/gr.107524.110 contributor: fullname: A McKenna – volume: 26 start-page: 2499 issue: 11 year: 2009 ident: pgen.1009291.ref005 article-title: Diversity and evolution of effector loci in natural populations of the plant pathogen Melampsora lini publication-title: Molecular Biology doi: 10.1093/molbev/msp166 contributor: fullname: LG Barrett – start-page: 1 year: 2018 ident: pgen.1009291.ref068 publication-title: Wilke COJRpv. Ggridges: Ridgeline plots in’ggplot2’ – volume: 4 start-page: 13 issue: 1 year: 1998 ident: pgen.1009291.ref026 article-title: High-resolution mapping adjacent to the Pc71 crown-rust resistance locus in hexaploid oat publication-title: Molecular breeding: new strategies in plant improvement doi: 10.1023/A:1009652222382 contributor: fullname: AL Bush – volume: 23 start-page: 1164 issue: 9 year: 2007 ident: pgen.1009291.ref063 article-title: pcaMethods—a bioconductor package providing PCA methods for incomplete data publication-title: Bioinformatics doi: 10.1093/bioinformatics/btm069 contributor: fullname: W Stacklies – volume: 4 start-page: 87 year: 2011 ident: pgen.1009291.ref046 article-title: Crops. Rust diseases in Canada publication-title: Prairie Soils contributor: fullname: T Fetch – volume-title: ggplot2: Elegant Graphics for Data Analysis year: 2016 ident: pgen.1009291.ref060 doi: 10.1007/978-3-319-24277-4 contributor: fullname: H. Wickham – year: 2018 ident: pgen.1009291.ref064 article-title: ggrepel: Automatically Position Non-Overlapping Text Labels with 'ggplot2' publication-title: R package version 0.8.0 contributor: fullname: K. Slowikowski – volume: 6 issue: 8 year: 2011 ident: pgen.1009291.ref004 article-title: Next Generation Sequencing Provides Rapid Access to the Genome of Puccinia striiformis f. sp tritici, the Causal Agent of Wheat Stripe Rust publication-title: Plos One doi: 10.1371/journal.pone.0024230 contributor: fullname: D Cantu – volume: 132 start-page: 583 issue: 2 year: 1992 ident: pgen.1009291.ref034 article-title: Estimation of levels of gene flow from DNA sequence data. contributor: fullname: RR Hudson – volume: 7 start-page: 205 year: 2016 ident: pgen.1009291.ref013 article-title: Changing the Game: Using Integrative Genomics to Probe Virulence Mechanisms of the Stem Rust Pathogen Puccinia graminis f. sp. tritici publication-title: Front Plant Sci doi: 10.3389/fpls.2016.00205 contributor: fullname: M Figueroa – volume: 31 start-page: 1929 issue: 7 year: 2014 ident: pgen.1009291.ref076 article-title: PopGenome: an efficient Swiss army knife for population genomic analyses in R publication-title: Molecular Biology Evolution doi: 10.1093/molbev/msu136 contributor: fullname: B Pfeifer – volume: 66 start-page: 177 issue: 2 year: 1982 ident: pgen.1009291.ref014 article-title: Effects of Barberry eradication publication-title: Plant Disease doi: 10.1094/PD-66-177 contributor: fullname: AP Roelfs – volume: 628 year: 2010 ident: pgen.1009291.ref021 publication-title: Field crops: Usual planting and harvesting dates contributor: fullname: NASS UNASS – volume: 28 start-page: 2397 issue: 18 year: 2012 ident: pgen.1009291.ref092 article-title: GAPIT: genome association and prediction integrated tool publication-title: Bioinformatics doi: 10.1093/bioinformatics/bts444 contributor: fullname: AE Lipka – year: 2019 ident: pgen.1009291.ref094 article-title: qvalue: Q-value estimation for false discovery rate control publication-title: R package version 2.18.0 contributor: fullname: JD Storey – volume: 123 start-page: 585 issue: 3 year: 1989 ident: pgen.1009291.ref085 article-title: Statistical method for testing the neutral mutation hypothesis by DNA polymorphism publication-title: Genetics doi: 10.1093/genetics/123.3.585 contributor: fullname: F. Tajima – volume: 92 start-page: 379 issue: 3 year: 2008 ident: pgen.1009291.ref059 article-title: Virulence Frequencies in Oat Crown Rust in the United States from 2001 Through 2005 publication-title: Plant Dis doi: 10.1094/PDIS-92-3-0379 contributor: fullname: ML Carson – volume: 10 start-page: 5068 year: 2019 ident: pgen.1009291.ref015 article-title: Emergence of the Ug99 lineage of the wheat stem rust pathogen through somatic hybridisation. publication-title: Nat Commun doi: 10.1038/s41467-019-12927-7 contributor: fullname: F Li – volume: 17 start-page: 92 issue: 1 year: 2019 ident: pgen.1009291.ref052 article-title: Genomic insights from the first chromosome-scale assemblies of oat (Avena spp.) diploid species publication-title: BMC Biol doi: 10.1186/s12915-019-0712-y contributor: fullname: PJ Maughan – volume: 89 start-page: 329 issue: 2–3 year: 1994 ident: pgen.1009291.ref020 article-title: Identification of homoeologous chromosomes in hexaploid oat (A. byzantina cv Kanota) using monosomics and RFLP analysis publication-title: Theor Appl Genet doi: 10.1007/BF00225163 contributor: fullname: WL Rooney – volume: 2 start-page: e00731 year: 2013 ident: pgen.1009291.ref029 article-title: The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine publication-title: Elife doi: 10.7554/eLife.00731 contributor: fullname: K Yoshida – volume: 13 start-page: e1005727 issue: 9 year: 2017 ident: pgen.1009291.ref030 article-title: kWIP: The k-mer weighted inner product, a de novo estimator of genetic similarity publication-title: PLoS computational biology doi: 10.1371/journal.pcbi.1005727 contributor: fullname: KD Murray – volume: 40 start-page: 349 issue: 1 year: 2002 ident: pgen.1009291.ref006 article-title: Pathogen population genetics, evolutionary potential, and durable resistance publication-title: Annual Review of Phytopathology doi: 10.1146/annurev.phyto.40.120501.101443 contributor: fullname: BA McDonald – volume: 20 start-page: 2739 issue: 13 year: 2011 ident: pgen.1009291.ref042 article-title: The genetic structure of the plant pathogenic fungus Melampsora larici-populina on its wild host is extensively impacted by host domestication publication-title: Molecular Ecology Notes doi: 10.1111/j.1365-294X.2011.05138.x contributor: fullname: C Xhaard – volume: 1207 start-page: 3907 year: 2012 ident: pgen.1009291.ref027 article-title: Haplotype-based variant detection from short-read sequencing publication-title: arXiv contributor: fullname: E Garrison – volume: 84 start-page: 580 issue: 5 year: 2000 ident: pgen.1009291.ref023 article-title: A North American system of nomenclature for Puccinia coronata f. sp. avenae publication-title: Plant Disease doi: 10.1094/PDIS.2000.84.5.580 contributor: fullname: J Chong – volume: 50 start-page: 20 year: 2020 ident: pgen.1009291.ref008 article-title: Evolution of virulence in rust fungi—multiple solutions to one problem publication-title: Current Opinion in Plant Biology doi: 10.1016/j.pbi.2020.02.007 contributor: fullname: M Figueroa – volume: 9 issue: 1 year: 2018 ident: pgen.1009291.ref022 article-title: De Novo Assembly and Phasing of Dikaryotic Genomes from Two Isolates of Puccinia coronata f. sp avenae, the Causal Agent of Oat Crown Rust publication-title: Mbio doi: 10.1128/mBio.01650-17 contributor: fullname: ME Miller – volume: 47 start-page: W256 issue: W1 year: 2019 ident: pgen.1009291.ref078 article-title: v4: recent updates and new developments publication-title: Nucleic Acids Res doi: 10.1093/nar/gkz239 contributor: fullname: I Letunic – volume: 33 start-page: 77 issue: 1 year: 2011 ident: pgen.1009291.ref045 article-title: Virulence of Puccinia coronata f. sp. avenae in the Eastern Prairie Region of Canada during 2007–2009 publication-title: Canadian Journal of Plant Pathology doi: 10.1080/07060661.2010.546957 contributor: fullname: J Chong – volume: 27 start-page: 3070 issue: 21 year: 2011 ident: pgen.1009291.ref032 article-title: adegenet 1.3–1: new tools for the analysis of genome-wide SNP data publication-title: Bioinformatics doi: 10.1093/bioinformatics/btr521 contributor: fullname: T Jombart – volume: 10 issue: 1 year: 2014 ident: pgen.1009291.ref047 article-title: Origin, Migration Routes and Worldwide Population Genetic Structure of the Wheat Yellow Rust Puccinia striiformis f. sp tritici publication-title: Plos Pathogens contributor: fullname: S Ali – volume: 14 start-page: 349 issue: 4 year: 2004 ident: pgen.1009291.ref055 article-title: Discovery, localization, and sequence characterization of molecular markers for the crown rust resistance genes Pc38, Pc39, and Pc48 in cultivated oat (Avena sativa L.) publication-title: Molecular breeding: new strategies in plant improvement doi: 10.1007/s11032-004-0148-z contributor: fullname: C Wright – volume: 26 start-page: 841 issue: 6 year: 2010 ident: pgen.1009291.ref067 article-title: BEDTools: a flexible suite of utilities for comparing genomic features publication-title: Bioinformatics doi: 10.1093/bioinformatics/btq033 contributor: fullname: AR Quinlan – volume-title: Chapter 11 Plant diseases caused by fungi year: 2005 ident: pgen.1009291.ref007 contributor: fullname: GN Agrios – volume: 78 start-page: 342 issue: 3 year: 1988 ident: pgen.1009291.ref048 article-title: Genetic properties of inhibitor genes in flax rust that alter avirulence to virulence on flax publication-title: Phytopathology doi: 10.1094/Phyto-78-342 contributor: fullname: D. Jones – year: 2016 ident: pgen.1009291.ref082 article-title: Statistical procedures for agricultural research publication-title: R package version 1.2–4 contributor: fullname: F. de Mendibru – volume: 2 start-page: e281 year: 2014 ident: pgen.1009291.ref081 article-title: Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction publication-title: PeerJ doi: 10.7717/peerj.281 contributor: fullname: ZN Kamvar – volume: 25 start-page: 2078 issue: 16 year: 2009 ident: pgen.1009291.ref028 article-title: The sequence alignment/map format and SAMtools publication-title: Bioinformatics doi: 10.1093/bioinformatics/btp352 contributor: fullname: H Li – volume: 1 start-page: 101 issue: 1–2 year: 2001 ident: pgen.1009291.ref035 article-title: Indices of multilocus linkage disequilibrium publication-title: Molecular Ecology Notes doi: 10.1046/j.1471-8278.2000.00014.x contributor: fullname: PM Agapow – ident: pgen.1009291.ref039 – volume: 13 issue: 12 year: 2018 ident: pgen.1009291.ref024 article-title: Mapping of crown rust resistance gene Pc53 in oat (Avena sativa) publication-title: Plos One doi: 10.1371/journal.pone.0209105 contributor: fullname: B Admassu-Yimer – volume: 20 start-page: 1983 issue: 12 year: 2014 ident: pgen.1009291.ref070 article-title: UpSet: visualization of intersecting sets publication-title: IEEE transactions on visualization computer graphics doi: 10.1109/TVCG.2014.2346248 contributor: fullname: A Lex – volume: 22 start-page: 27 issue: 1 year: 1980 ident: pgen.1009291.ref053 article-title: Cytology. Inheritance of crown rust resistance in three accessions of Avena sterilis publication-title: Canadian Journal of Genetics contributor: fullname: D Harder – volume: 10 issue: 2 year: 2017 ident: pgen.1009291.ref025 article-title: Genome-wide association mapping of crown rust resistance in oat elite germplasm publication-title: The plant genome contributor: fullname: KE Klos – volume: 172 start-page: 2665 issue: 4 year: 2006 ident: pgen.1009291.ref033 article-title: A simple and robust statistical test for detecting the presence of recombination publication-title: Genetics doi: 10.1534/genetics.105.048975 contributor: fullname: TC Bruen – volume: 31 start-page: 614 issue: 6 year: 2018 ident: pgen.1009291.ref036 article-title: Populations of Phytophthora rubi show little differentiation and high rates of migration among states in the western United States publication-title: Molecular plant-microbe interactions doi: 10.1094/MPMI-10-17-0258-R contributor: fullname: JF Tabima – year: 2019 ident: pgen.1009291.ref038 article-title: Census highlights contributor: fullname: U. NASS – volume: 6 start-page: 208 year: 2015 ident: pgen.1009291.ref080 article-title: Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality publication-title: Front Genet.PubMed Central PMCID contributor: fullname: ZN Kamvar – volume: 57 start-page: 591 issue: 4 year: 2008 ident: pgen.1009291.ref009 article-title: Breeding cereals for rust resistance in Australia publication-title: Plant Pathol doi: 10.1111/j.1365-3059.2008.01836.x contributor: fullname: R. Park – volume: 5 start-page: 416 year: 2014 ident: pgen.1009291.ref003 article-title: Effector proteins of rust fungi publication-title: Front Plant Sci doi: 10.3389/fpls.2014.00416 contributor: fullname: B Petre – volume: 27 start-page: 2991 issue: 10 year: 2015 ident: pgen.1009291.ref049 article-title: Multiple Avirulence Loci and Allele-Specific Effector Recognition Control the Pm3 Race-Specific Resistance of Wheat to Powdery Mildew publication-title: Plant Cell contributor: fullname: S Bourras – volume: 19 start-page: 1047 issue: 5 year: 2018 ident: pgen.1009291.ref016 article-title: Puccinia coronata f. sp. avenae: a threat to global oat production publication-title: Molecular plant pathology doi: 10.1111/mpp.12608 contributor: fullname: ES Nazareno – volume: 7 start-page: 256 issue: 2 year: 1975 ident: pgen.1009291.ref084 article-title: On the number of segregating sites in genetical models without recombination publication-title: Theoretical population biology doi: 10.1016/0040-5809(75)90020-9 contributor: fullname: G. Watterson – volume: 42 start-page: 355 issue: 4 year: 2010 ident: pgen.1009291.ref091 article-title: Mixed linear model approach adapted for genome-wide association studies publication-title: Nature Genetics doi: 10.1038/ng.546 contributor: fullname: Z Zhang – volume: 9 issue: 2 year: 2016 ident: pgen.1009291.ref051 article-title: A consensus map in cultivated hexaploid oat reveals conserved grass synteny with substantial subgenome rearrangement publication-title: The plant genome doi: 10.3835/plantgenome2015.10.0102 contributor: fullname: AS Chaffin – volume: 4 start-page: 900 year: 2015 ident: pgen.1009291.ref073 article-title: The khmer software package: enabling efficient nucleotide sequence analysis publication-title: F1000Res doi: 10.12688/f1000research.6924.1 contributor: fullname: MR Crusoe – volume: 15 start-page: 756 year: 2017 ident: pgen.1009291.ref012 article-title: Evolution and genome architecture in fungal plant pathogens publication-title: Nature Reviews Microbiology doi: 10.1038/nrmicro.2017.76 contributor: fullname: M Möller – volume: 2020 start-page: 1 ident: pgen.1009291.ref056 article-title: Identification of molecular markers for the Pc39 gene conferring resistance to crown rust in oat publication-title: Theoretical Applied Genetics contributor: fullname: S Sowa – volume: 8 start-page: 28 issue: 1 year: 2017 ident: pgen.1009291.ref075 article-title: ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data publication-title: Methods in Ecology Evolution doi: 10.1111/2041-210X.12628 contributor: fullname: G Yu – volume: 6 start-page: e4958 year: 2018 ident: pgen.1009291.ref095 article-title: D-GENIES: dot plot large genomes in an interactive, efficient and simple way publication-title: PeerJ doi: 10.7717/peerj.4958 contributor: fullname: F Cabanettes – year: 2015 ident: pgen.1009291.ref090 article-title: ggvegan:‘ggplot2’Plots for the ‘vegan’Package publication-title: R package version 00–3 contributor: fullname: G. Simpson – volume: 9 start-page: 275 issue: 1 year: 1971 ident: pgen.1009291.ref002 article-title: Current status of the gene-for-gene concept publication-title: Annual Review of Phytopathology doi: 10.1146/annurev.py.09.090171.001423 contributor: fullname: HH Flor
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Snippet	Pathogen populations are expected to evolve virulence traits in response to resistance deployed in agricultural settings. However, few temporal datasets have... R genes generally encode intracellular immune receptor proteins of the nucleotide binding leucine rich repeat (NB-LRR) class, which recognize pathogen...
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SubjectTerms	Asexuality Avena - microbiology Biology and Life Sciences Diseases and pests Epidemics Evolution Fungi Gene Frequency Genes Genes, Fungal Genetic aspects Genetic diversity Genomes Hybridization Infections Leucine Medicine and Health Sciences Mutation Oats Pathogens Physiological aspects Plant diseases Plant population genetics Polymorphism, Genetic Population Population genetics Principal components analysis Puccinia - genetics Puccinia - pathogenicity Puccinia coronata avenae Pucciniales Recombination Rust diseases Rust fungi Selection, Genetic Virulence Virulence (Microbiology) Virulence - genetics
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Title	Increased virulence of Puccinia coronata f. sp.avenae populations through allele frequency changes at multiple putative Avr loci
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