Rates of evolution of avirulence phenotypes and DNA markers in a northwest European population of Puccinia striiformis f. sp. tritici

The effects of evolutionary processes in fungal pathogen populations may occur more rapidly and display larger effects in agricultural systems than in wild ecosystems because of human involvement by plant breeding and crop management. In this study, we analysed the rate of evolution in three lineage...

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Bibliographic Details
Published inMolecular ecology Vol. 16; no. 21; pp. 4637 - 4647
Main Authors HOVMØLLER, MOGENS S, JUSTESEN, ANNEMARIE F
Format Journal Article
LanguageEnglish
Published Oxford, UK Oxford, UK : Blackwell Publishing Ltd 01.11.2007
Blackwell Publishing Ltd
Subjects
AFLP
Agriculture
alleles
amplified fragment length polymorphism
Amplified Fragment Length Polymorphism Analysis
Basidiomycota - genetics
Basidiomycota - isolation & purification
Basidiomycota - pathogenicity
clonal evolution
Crop diseases
Crop management
Denmark
Deoxyribonucleic acid
DNA
Ecology
ecosystems
Europe
Evolution, Molecular
Evolutionary biology
Farming systems
Fungal infections
fungi
Genetic Markers
humans
loci
Molecular biology
Mutation
mutation rate
Pathogens
Phenotype
Phenotypes
Phylogeny
Plant breeding
Plant Diseases - microbiology
Polymorphism, Genetic
Puccinia striiformis
Puccinia striiformis f. tritici
stripe rust
Triticum aestivum
United Kingdom
virulence
Virulence - genetics
Wheat
wheat stripe rust
Europe
United Kingdom > UK
Denmark
United Kingdom
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Abstract The effects of evolutionary processes in fungal pathogen populations may occur more rapidly and display larger effects in agricultural systems than in wild ecosystems because of human involvement by plant breeding and crop management. In this study, we analysed the rate of evolution in three lineages of a northwest European population of a biotrophic and asexual reproduced fungal pathogen, Puccinia striiformis f. sp. tritici, causing yellow rust on wheat. Pathogen samples were collected between 1975 and 2002 in the UK and Denmark, and assayed for 14 individual avirulence/virulence alleles and up to 234 amplified fragment length polymorphism (AFLP) primer pairs producing approximately 17 000 AFLP fragments. The large number of fragments and a targeted sampling of isolates allowed a reconstruction of phylogenies in great detail, i.e. no homoplasy and a representation of sequential, evolutionary steps by pathogen samples. A recent, phenotypic loss of avirulence was observed at least once for loci corresponding to P. striiformis f. sp. tritici resistance Yr2, Yr3, Yr4, Yr7, Yr9, and Yr15, whereas Avr6 and Avr17 were lost independently in all three lineages, corresponding to 16 events of loss of avirulence (emergence of virulence). The opposite process, restoration of avirulence, was observed for Yr9 and Yr32. An interpretation of phenotypic changes within lineages as independent mutation events resulted in mutation frequencies from 1.4 x 10⁻⁶ to 4.1 x 10⁻⁶ per AFLP fragment (locus) per generation, whereas the effective rate by which a mutation from avirulence to virulence was established in the pathogen population, when subject to selection by host resistance genes, was approximately three orders of magnitude faster.
AbstractList The effects of evolutionary processes in fungal pathogen populations may occur more rapidly and display larger effects in agricultural systems than in wild ecosystems because of human involvement by plant breeding and crop management. In this study, we analysed the rate of evolution in three lineages of a northwest European population of a biotrophic and asexual reproduced fungal pathogen, Puccinia striiformis f. sp. tritici, causing yellow rust on wheat. Pathogen samples were collected between 1975 and 2002 in the UK and Denmark, and assayed for 14 individual avirulence/virulence alleles and up to 234 amplified fragment length polymorphism (AFLP) primer pairs producing approximately 17,000 AFLP fragments. The large number of fragments and a targeted sampling of isolates allowed a reconstruction of phylogenies in great detail, i.e. no homoplasy and a representation of sequential, evolutionary steps by pathogen samples. A recent, phenotypic loss of avirulence was observed at least once for loci corresponding to P. striiformis f. sp. tritici resistance Yr2, Yr3, Yr4, Yr7, Yr9, and Yr15, whereas Avr6 and Avr17 were lost independently in all three lineages, corresponding to 16 events of loss of avirulence (emergence of virulence). The opposite process, restoration of avirulence, was observed for Yr9 and Yr32. An interpretation of phenotypic changes within lineages as independent mutation events resulted in mutation frequencies from 1.4x10(-6) to 4.1x10(-6) per AFLP fragment (locus) per generation, whereas the effective rate by which a mutation from avirulence to virulence was established in the pathogen population, when subject to selection by host resistance genes, was approximately three orders of magnitude faster.
The effects of evolutionary processes in fungal pathogen populations may occur more rapidly and display larger effects in agricultural systems than in wild ecosystems because of human involvement by plant breeding and crop management. In this study, we analysed the rate of evolution in three lineages of a northwest European population of a biotrophic and asexual reproduced fungal pathogen, Puccinia striiformis f. sp. tritici, causing yellow rust on wheat. Pathogen samples were collected between 1975 and 2002 in the UK and Denmark, and assayed for 14 individual avirulence/virulence alleles and up to 234 amplified fragment length polymorphism (AFLP) primer pairs producing approximately 17,000 AFLP fragments. The large number of fragments and a targeted sampling of isolates allowed a reconstruction of phylogenies in great detail, i.e. no homoplasy and a representation of sequential, evolutionary steps by pathogen samples. A recent, phenotypic loss of avirulence was observed at least once for loci corresponding to P. striiformis f. sp. tritici resistance Yr2, Yr3, Yr4, Yr7, Yr9, and Yr15, whereas Avr6 and Avr17 were lost independently in all three lineages, corresponding to 16 events of loss of avirulence (emergence of virulence). The opposite process, restoration of avirulence, was observed for Yr9 and Yr32. An interpretation of phenotypic changes within lineages as independent mutation events resulted in mutation frequencies from 1.4 x 10-6 to 4.1 x 10-6 per AFLP fragment (locus) per generation, whereas the effective rate by which a mutation from avirulence to virulence was established in the pathogen population, when subject to selection by host resistance genes, was approximately three orders of magnitude faster. [PUBLICATION ABSTRACT]
The effects of evolutionary processes in fungal pathogen populations may occur more rapidly and display larger effects in agricultural systems than in wild ecosystems because of human involvement by plant breeding and crop management. In this study, we analysed the rate of evolution in three lineages of a northwest European population of a biotrophic and asexual reproduced fungal pathogen, Puccinia striiformis f. sp. tritici, causing yellow rust on wheat. Pathogen samples were collected between 1975 and 2002 in the UK and Denmark, and assayed for 14 individual avirulence/virulence alleles and up to 234 amplified fragment length polymorphism (AFLP) primer pairs producing approximately 17 000 AFLP fragments. The large number of fragments and a targeted sampling of isolates allowed a reconstruction of phylogenies in great detail, i.e. no homoplasy and a representation of sequential, evolutionary steps by pathogen samples. A recent, phenotypic loss of avirulence was observed at least once for loci corresponding to P. striiformis f. sp. tritici resistance Yr2, Yr3, Yr4, Yr7, Yr9, and Yr15, whereas Avr6 and Avr17 were lost independently in all three lineages, corresponding to 16 events of loss of avirulence (emergence of virulence). The opposite process, restoration of avirulence, was observed for Yr9 and Yr32. An interpretation of phenotypic changes within lineages as independent mutation events resulted in mutation frequencies from 1.4 × 10−6 to 4.1 × 10−6 per AFLP fragment (locus) per generation, whereas the effective rate by which a mutation from avirulence to virulence was established in the pathogen population, when subject to selection by host resistance genes, was approximately three orders of magnitude faster.
The effects of evolutionary processes in fungal pathogen populations may occur more rapidly and display larger effects in agricultural systems than in wild ecosystems because of human involvement by plant breeding and crop management. In this study, we analysed the rate of evolution in three lineages of a northwest European population of a biotrophic and asexual reproduced fungal pathogen, Puccinia striiformis f. sp. tritici, causing yellow rust on wheat. Pathogen samples were collected between 1975 and 2002 in the UK and Denmark, and assayed for 14 individual avirulence/virulence alleles and up to 234 amplified fragment length polymorphism (AFLP) primer pairs producing approximately 17 000 AFLP fragments. The large number of fragments and a targeted sampling of isolates allowed a reconstruction of phylogenies in great detail, i.e. no homoplasy and a representation of sequential, evolutionary steps by pathogen samples. A recent, phenotypic loss of avirulence was observed at least once for loci corresponding to P. striiformis f. sp. tritici resistance Yr2, Yr3, Yr4, Yr7, Yr9, and Yr15, whereas Avr6 and Avr17 were lost independently in all three lineages, corresponding to 16 events of loss of avirulence (emergence of virulence). The opposite process, restoration of avirulence, was observed for Yr9 and Yr32. An interpretation of phenotypic changes within lineages as independent mutation events resulted in mutation frequencies from 1.4 x 10 super(-6) to 4.1 x 10 super(-6) per AFLP fragment (locus) per generation, whereas the effective rate by which a mutation from avirulence to virulence was established in the pathogen population, when subject to selection by host resistance genes, was approximately three orders of magnitude faster.
The effects of evolutionary processes in fungal pathogen populations may occur more rapidly and display larger effects in agricultural systems than in wild ecosystems because of human involvement by plant breeding and crop management. In this study, we analysed the rate of evolution in three lineages of a northwest European population of a biotrophic and asexual reproduced fungal pathogen, Puccinia striiformis f. sp. tritici, causing yellow rust on wheat. Pathogen samples were collected between 1975 and 2002 in the UK and Denmark, and assayed for 14 individual avirulence/virulence alleles and up to 234 amplified fragment length polymorphism (AFLP) primer pairs producing approximately 17 000 AFLP fragments. The large number of fragments and a targeted sampling of isolates allowed a reconstruction of phylogenies in great detail, i.e. no homoplasy and a representation of sequential, evolutionary steps by pathogen samples. A recent, phenotypic loss of avirulence was observed at least once for loci corresponding to P. striiformis f. sp. tritici resistance Yr2, Yr3, Yr4, Yr7, Yr9, and Yr15, whereas Avr6 and Avr17 were lost independently in all three lineages, corresponding to 16 events of loss of avirulence (emergence of virulence). The opposite process, restoration of avirulence, was observed for Yr9 and Yr32. An interpretation of phenotypic changes within lineages as independent mutation events resulted in mutation frequencies from 1.4 × 10⁻⁶ to 4.1 × 10⁻⁶ per AFLP fragment (locus) per generation, whereas the effective rate by which a mutation from avirulence to virulence was established in the pathogen population, when subject to selection by host resistance genes, was approximately three orders of magnitude faster.
The effects of evolutionary processes in fungal pathogen populations may occur more rapidly and display larger effects in agricultural systems than in wild ecosystems because of human involvement by plant breeding and crop management. In this study, we analysed the rate of evolution in three lineages of a northwest European population of a biotrophic and asexual reproduced fungal pathogen, Puccinia striiformis f. sp. tritici , causing yellow rust on wheat. Pathogen samples were collected between 1975 and 2002 in the UK and Denmark, and assayed for 14 individual avirulence/virulence alleles and up to 234 amplified fragment length polymorphism (AFLP) primer pairs producing approximately 17 000 AFLP fragments. The large number of fragments and a targeted sampling of isolates allowed a reconstruction of phylogenies in great detail, i.e. no homoplasy and a representation of sequential, evolutionary steps by pathogen samples. A recent, phenotypic loss of avirulence was observed at least once for loci corresponding to P. striiformis f. sp. tritici resistance Yr2, Yr3, Yr4, Yr7, Yr9 , and Yr15 , whereas Avr6 and Avr17 were lost independently in all three lineages, corresponding to 16 events of loss of avirulence (emergence of virulence). The opposite process, restoration of avirulence, was observed for Yr9 and Yr32 . An interpretation of phenotypic changes within lineages as independent mutation events resulted in mutation frequencies from 1.4 × 10 −6 to 4.1 × 10 −6 per AFLP fragment (locus) per generation, whereas the effective rate by which a mutation from avirulence to virulence was established in the pathogen population, when subject to selection by host resistance genes, was approximately three orders of magnitude faster.
The effects of evolutionary processes in fungal pathogen populations may occur more rapidly and display larger effects in agricultural systems than in wild ecosystems because of human involvement by plant breeding and crop management. In this study, we analysed the rate of evolution in three lineages of a northwest European population of a biotrophic and asexual reproduced fungal pathogen, Puccinia striiformis f. sp. tritici, causing yellow rust on wheat. Pathogen samples were collected between 1975 and 2002 in the UK and Denmark, and assayed for 14 individual avirulence/virulence alleles and up to 234 amplified fragment length polymorphism (AFLP) primer pairs producing approximately 17,000 AFLP fragments. The large number of fragments and a targeted sampling of isolates allowed a reconstruction of phylogenies in great detail, i.e. no homoplasy and a representation of sequential, evolutionary steps by pathogen samples. A recent, phenotypic loss of avirulence was observed at least once for loci corresponding to P. striiformis f. sp. tritici resistance Yr2, Yr3, Yr4, Yr7, Yr9, and Yr15, whereas Avr6 and Avr17 were lost independently in all three lineages, corresponding to 16 events of loss of avirulence (emergence of virulence). The opposite process, restoration of avirulence, was observed for Yr9 and Yr32. An interpretation of phenotypic changes within lineages as independent mutation events resulted in mutation frequencies from 1.4x10(-6) to 4.1x10(-6) per AFLP fragment (locus) per generation, whereas the effective rate by which a mutation from avirulence to virulence was established in the pathogen population, when subject to selection by host resistance genes, was approximately three orders of magnitude faster.The effects of evolutionary processes in fungal pathogen populations may occur more rapidly and display larger effects in agricultural systems than in wild ecosystems because of human involvement by plant breeding and crop management. In this study, we analysed the rate of evolution in three lineages of a northwest European population of a biotrophic and asexual reproduced fungal pathogen, Puccinia striiformis f. sp. tritici, causing yellow rust on wheat. Pathogen samples were collected between 1975 and 2002 in the UK and Denmark, and assayed for 14 individual avirulence/virulence alleles and up to 234 amplified fragment length polymorphism (AFLP) primer pairs producing approximately 17,000 AFLP fragments. The large number of fragments and a targeted sampling of isolates allowed a reconstruction of phylogenies in great detail, i.e. no homoplasy and a representation of sequential, evolutionary steps by pathogen samples. A recent, phenotypic loss of avirulence was observed at least once for loci corresponding to P. striiformis f. sp. tritici resistance Yr2, Yr3, Yr4, Yr7, Yr9, and Yr15, whereas Avr6 and Avr17 were lost independently in all three lineages, corresponding to 16 events of loss of avirulence (emergence of virulence). The opposite process, restoration of avirulence, was observed for Yr9 and Yr32. An interpretation of phenotypic changes within lineages as independent mutation events resulted in mutation frequencies from 1.4x10(-6) to 4.1x10(-6) per AFLP fragment (locus) per generation, whereas the effective rate by which a mutation from avirulence to virulence was established in the pathogen population, when subject to selection by host resistance genes, was approximately three orders of magnitude faster.
The effects of evolutionary processes in fungal pathogen populations may occur more rapidly and display larger effects in agricultural systems than in wild ecosystems because of human involvement by plant breeding and crop management. In this study, we analysed the rate of evolution in three lineages of a northwest European population of a biotrophic and asexual reproduced fungal pathogen, Puccinia striiformis f. sp. tritici, causing yellow rust on wheat. Pathogen samples were collected between 1975 and 2002 in the UK and Denmark, and assayed for 14 individual avirulence/virulence alleles and up to 234 amplified fragment length polymorphism (AFLP) primer pairs producing approximately 17 000 AFLP fragments. The large number of fragments and a targeted sampling of isolates allowed a reconstruction of phylogenies in great detail, i.e. no homoplasy and a representation of sequential, evolutionary steps by pathogen samples. A recent, phenotypic loss of avirulence was observed at least once for loci corresponding to P. striiformis f. sp. tritici resistance Yr2, Yr3, Yr4, Yr7, Yr9, and Yr15, whereas Avr6 and Avr17 were lost independently in all three lineages, corresponding to 16 events of loss of avirulence (emergence of virulence). The opposite process, restoration of avirulence, was observed for Yr9 and Yr32. An interpretation of phenotypic changes within lineages as independent mutation events resulted in mutation frequencies from 1.4 x 10⁻⁶ to 4.1 x 10⁻⁶ per AFLP fragment (locus) per generation, whereas the effective rate by which a mutation from avirulence to virulence was established in the pathogen population, when subject to selection by host resistance genes, was approximately three orders of magnitude faster.
Author HOVMØLLER, MOGENS S.
JUSTESEN, ANNEMARIE F.
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/17887968$$D View this record in MEDLINE/PubMed
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References Orbach MJ , Farrall L , Sweigard JA , Chumley FG , Valent B ( 2000 ) A telomeric avirulence gene determines efficacy for rice blast resistance gene Pi-ta . Plant Cell , 12 , 2019 - 2032 .
Calonnec A , Johnson R , de Vallavieille-Pope C ( 1997 ) Genetic analysis of resistance to Puccinia striiformis in the wheat differential cultivars Heines VII, Heines Peko and Strubes Dickkopf . Plant Pathology , 46 , 373 - 386 .
Burdon JJ , Silk J ( 1997 ) Sources and patterns of diversity in plant-pathogenic fungi . Phytopathology , 87 , 664 - 669 .
Duan X , Enjalberrt J , Vautrin D , Solignac M , Giraud T ( 2003 ) Isolation of 12 microsatellite loci, using an enrichment protocol, in the phytopathogenic fungus Puccinia triticina . Molecular Ecology Notes , 3 , 65 - 67 .
Zambino PJ , Kubelik AR , Szabo LJ ( 2000 ) Gene action and linkage of avirulence genes to DNA markers in the rust fungus Puccinia graminis . Phytopathology , 90 , 819 - 826 .
Justesen AF , Ridout CJ , Hovmøller MS ( 2002 ) The recent history of Puccinia striiformis f. sp. tritici in Denmark as revealed by disease incidence and AFLP markers . Plant Pathology , 51 , 13 - 23 .
Vera Cruz CM , Bai JF , Ona I et al . ( 2000 ) Predicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutation . Proceedings of the National Academy of Sciences, USA , 97 , 13500 - 13505 .
Hovmøller MS , Munk L , Østergård H ( 1993 ) Observed and predicted changes in virulence gene-frequencies at 11 loci in a local barley powdery mildew population . Phytopathology , 83 , 253 - 260 .
Ridout CJ , Skamnioti P , Porritt O , Sacristan S , Jones JDG , Brown JKM ( 2006 ) Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance . The Plant Cell , 18 , 2402 - 2414 .
Wellings CR , McIntosh RA ( 1990 ) Puccinia striiformis f. sp. tritici in Australia: pathogenic changes during the first 10 years . Plant Pathology , 39 , 316 - 325 .
Zhan J , McDonald BA ( 2004 ) The interaction among evolutionary forces in the pathogenic fungus Mycosphaerella graminicola . Fungal Genetics and Biology , 41 , 590 - 599 .
Hovmøller MS , Justesen AF ( 2007 ) Appearance and interpretation of atypical phenotypes of Puccinia striiformis f. sp. tritici in NW-Europe . Australian Journal of Agricultural Research , 58 , 518 - 524 .
Flor H ( 1971 ) Current status of the gene-for-gene concept . Annual Review of Phytopathology , 9 , 275 - 296 .
Keiper FJ , Hayden MJ , Park RF , Wellings CR ( 2003 ) Molecular genetic variability of Australian isolates of five cereal rust pathogens . Mycological Research , 107 , 545 - 556 .
Felsenstein J ( 1989 ) phylip, Phylogeny Inference Package , Version 3.2 . Cladistics , 5 , 164 - 166 .
Taylor JW , Jacobson DJ , Fisher MC ( 1999 ) The evolution of asexual fungi: reproduction, speciation and classification . Annual Review of Phytopathology , 37 , 197 - 246 .
Parnell S , van den Bosch F , Gilligan CA ( 2006 ) Large-scale fungicide spray heterogeneity and the regional spread of resistant pathogen strains . Phytopathology , 96 , 549 - 555 .
Luderer R , Takken FLW , de Wit PJGM , Joosten HAJ ( 2002 ) Cladosporium fulvum overcomes Cf-2-mediated resistance by producing truncated AVR2 elicitor proteins . Molecular Microbiology , 45 , 875 - 884 .
Hovmøller MS , Justesen AF , Brown JKM ( 2002 ) Clonality and long-distance migration of Puccinia striiformis f. sp. tritici in north-west Europe . Plant Pathology , 51 , 24 - 32 .
Steele KA , Humphreys E , Wellings CR , Dickinson MJ ( 2001 ) Support for a stepwise mutation model for pathogen evolution in Australasian Puccinia striiformis f. sp. tritici by use of molecular markers . Plant Pathology , 50 , 174 - 180 .
Catanzariti A , Dodds PN , Lawrence GJ , Ayliffe MA , Ellis JG ( 2006 ) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors . The Plant Cell , 18 , 243 - 256 .
Drake JW , Charlesworth B , Charlesworth D , Crow JF ( 1998 ) Rates of spontaneous mutation . Genetics , 148 , 1667 - 1686 .
Stubbs RW ( 1967 ) Influence of light intensity on the reactions of wheat and barley seedlings to Puccinia striiforms . Phytopathology , 57 , 615 - 617 .
Bürger R , Willensdorfer M , Nowak MA ( 2006 ) Why are phenotypic mutation rates much higher than genotypic mutation rates? Genetics , 172 , 197 - 206 .
Hovmøller MS ( 2001 ) Disease severity and pathotype dynamics of Puccinia striiformis f. sp. tritici in Denmark . Plant Pathology , 50 , 181 - 189 .
Hovmøller MS ( 2007 ) Sources of seedling and adult plant resistance to P. striiformis f. sp. tritici in European wheats . Plant Breeding , 126 , 225 - 233 .
Maynard Smith J , Smith NH , O'Rourke M , Spratt BG ( 1993 ) How clonal are bacteria? Proceedings of the National Academy of Sciences, USA , 90 , 4384 - 4388 .
Clark TA , Anderson JB ( 2004 ) Dikaryons of the basidiomycete fungus Schizophyllum commune: evolution in long-term culture . Genetics , 167 , 1663 - 1675 .
Schürch S , Linde CC , Knogge W , Jackson LF , McDonald BA ( 2004 ) Molecular population genetic analysis differentiates two virulence mechanisms of the fungal avirulence gene NIP1 . Molecular Plant-Microbe Interactions , 17 , 1114 - 1125 .
Wellings CR ( 2007 ) Puccinia striiformis in Australia: a review of the incursion, evolution, and adaption of stripe rust in the period 1979-2006 . Australian Journal of Agricultural Research , 58 , 567 - 575 .
Johnson R ( 1992 ) Reflections of a plant pathologist on breeding for disease resistance, with emphasis on yellow rust and eyespot of wheat . Plant Pathology , 41 , 239 - 254 .
Lawrence GJ , Mayo GME , Shepherd KW ( 1981 ) Interactions between genes controlling pathogenicity in the flax rust fungus . Phytopathology , 71 , 12 - 19 .
Manners JG ( 1988 ) Puccinia striiformis, yellow rust (stripe rust) of cereals and grasses . Advanced Plant Pathology , 6 , 373 - 387 .
Skamnioti P , Ridout CJ ( 2005 ) Microbial avirulence determinants: guided missiles or antigenic flak? Molecular Plant Pathology , 6 , 551 - 559 .
Bayles RA , Flath K , Hovmøller MS , de Vallavieille-Pope C ( 2000 ) Breakdown of the Yr17 resistance to yellow rust of wheat in northern Europe - a case study by the yellow rust sub-group of COST 817 . Agronomie , 20 , 805 - 811 .
Leonard KJ , Szabo LJ ( 2005 ) Stem rust of small grains and grasses caused by Puccinia graminis . Molecular Plant Pathology , 6 , 99 - 111 .
Huang Y-J , Li Z-Q , Evans N , Rouxel T , Fitt BDL , Balesdent M-H ( 2006 ) Fitness cost associated with loss of the AvrLm4 avirulence function in Leptosphaeria maculans (phoma stem canker o foilseed rape) . European Journal of Plant Pathology , 114 , 77 - 89 .
de Vallavieille-Pope C , Huber L , Leconte M , Goyeau H ( 1995 ) Comparative effects of temperature and interrupted wet periods on germination, penetration, and infection of Puccinia recondita f. sp. tritici and P. striiformis on wheat seedlings . Phytopathology , 85 , 409 - 415 .
Enjalbert J , Duan M , Leconte M , Hovmøller MS , de Vallavieille-Pope ( 2005 ) Genetic evidence of local adaptation of wheat yellow rust (Puccinia striiformis f. sp. tritici) within France . Molecular Ecology , 14 , 2065 - 2073 .
Johnson R ( 1984 ) A critical analysis of durable resistance . Annual Review of Phytopathology , 22 , 309 - 330 .
Vos P , Hogers R , Bleeker M et al . ( 1995 ) AFLP: a new technique for DNA fingerprinting . Nucleic Acids Research , 23 , 4407 - 4414 .
Newton AC , Caten CE , Johnson R ( 1985 ) Variation for isozymes and double-stranded RNA among isolates of Puccinia striiformis and two other cereal rusts . Plant Pathology , 34 , 235 - 247 .
de Vallavieille-Pope C , Picard-Formery H , Radulovic S , Johnson R ( 1990 ) Specific resistance factors to yellow rust in seedlings of some French wheat varieties and races of Puccinia striiformis Westend. in France . Agronomie , 10 , 103 - 113 .
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References_xml – reference: Johnson R ( 1992 ) Reflections of a plant pathologist on breeding for disease resistance, with emphasis on yellow rust and eyespot of wheat . Plant Pathology , 41 , 239 - 254 .
– reference: Keiper FJ , Hayden MJ , Park RF , Wellings CR ( 2003 ) Molecular genetic variability of Australian isolates of five cereal rust pathogens . Mycological Research , 107 , 545 - 556 .
– reference: Orbach MJ , Farrall L , Sweigard JA , Chumley FG , Valent B ( 2000 ) A telomeric avirulence gene determines efficacy for rice blast resistance gene Pi-ta . Plant Cell , 12 , 2019 - 2032 .
– reference: Steele KA , Humphreys E , Wellings CR , Dickinson MJ ( 2001 ) Support for a stepwise mutation model for pathogen evolution in Australasian Puccinia striiformis f. sp. tritici by use of molecular markers . Plant Pathology , 50 , 174 - 180 .
– reference: Felsenstein J ( 1989 ) phylip, Phylogeny Inference Package , Version 3.2 . Cladistics , 5 , 164 - 166 .
– reference: de Vallavieille-Pope C , Picard-Formery H , Radulovic S , Johnson R ( 1990 ) Specific resistance factors to yellow rust in seedlings of some French wheat varieties and races of Puccinia striiformis Westend. in France . Agronomie , 10 , 103 - 113 .
– reference: Calonnec A , Johnson R , de Vallavieille-Pope C ( 1997 ) Genetic analysis of resistance to Puccinia striiformis in the wheat differential cultivars Heines VII, Heines Peko and Strubes Dickkopf . Plant Pathology , 46 , 373 - 386 .
– reference: Manners JG ( 1988 ) Puccinia striiformis, yellow rust (stripe rust) of cereals and grasses . Advanced Plant Pathology , 6 , 373 - 387 .
– reference: de Vallavieille-Pope C , Huber L , Leconte M , Goyeau H ( 1995 ) Comparative effects of temperature and interrupted wet periods on germination, penetration, and infection of Puccinia recondita f. sp. tritici and P. striiformis on wheat seedlings . Phytopathology , 85 , 409 - 415 .
– reference: Stubbs RW ( 1967 ) Influence of light intensity on the reactions of wheat and barley seedlings to Puccinia striiforms . Phytopathology , 57 , 615 - 617 .
– reference: Zhan J , McDonald BA ( 2004 ) The interaction among evolutionary forces in the pathogenic fungus Mycosphaerella graminicola . Fungal Genetics and Biology , 41 , 590 - 599 .
– reference: Taylor JW , Jacobson DJ , Fisher MC ( 1999 ) The evolution of asexual fungi: reproduction, speciation and classification . Annual Review of Phytopathology , 37 , 197 - 246 .
– reference: Hovmøller MS , Justesen AF ( 2007 ) Appearance and interpretation of atypical phenotypes of Puccinia striiformis f. sp. tritici in NW-Europe . Australian Journal of Agricultural Research , 58 , 518 - 524 .
– reference: Hovmøller MS , Munk L , Østergård H ( 1993 ) Observed and predicted changes in virulence gene-frequencies at 11 loci in a local barley powdery mildew population . Phytopathology , 83 , 253 - 260 .
– reference: Vos P , Hogers R , Bleeker M et al . ( 1995 ) AFLP: a new technique for DNA fingerprinting . Nucleic Acids Research , 23 , 4407 - 4414 .
– reference: Duan X , Enjalberrt J , Vautrin D , Solignac M , Giraud T ( 2003 ) Isolation of 12 microsatellite loci, using an enrichment protocol, in the phytopathogenic fungus Puccinia triticina . Molecular Ecology Notes , 3 , 65 - 67 .
– reference: Schürch S , Linde CC , Knogge W , Jackson LF , McDonald BA ( 2004 ) Molecular population genetic analysis differentiates two virulence mechanisms of the fungal avirulence gene NIP1 . Molecular Plant-Microbe Interactions , 17 , 1114 - 1125 .
– reference: Skamnioti P , Ridout CJ ( 2005 ) Microbial avirulence determinants: guided missiles or antigenic flak? Molecular Plant Pathology , 6 , 551 - 559 .
– reference: Hovmøller MS ( 2001 ) Disease severity and pathotype dynamics of Puccinia striiformis f. sp. tritici in Denmark . Plant Pathology , 50 , 181 - 189 .
– reference: Wellings CR , McIntosh RA ( 1990 ) Puccinia striiformis f. sp. tritici in Australia: pathogenic changes during the first 10 years . Plant Pathology , 39 , 316 - 325 .
– reference: Zambino PJ , Kubelik AR , Szabo LJ ( 2000 ) Gene action and linkage of avirulence genes to DNA markers in the rust fungus Puccinia graminis . Phytopathology , 90 , 819 - 826 .
– reference: Hovmøller MS , Justesen AF , Brown JKM ( 2002 ) Clonality and long-distance migration of Puccinia striiformis f. sp. tritici in north-west Europe . Plant Pathology , 51 , 24 - 32 .
– reference: Johnson R ( 1984 ) A critical analysis of durable resistance . Annual Review of Phytopathology , 22 , 309 - 330 .
– reference: Clark TA , Anderson JB ( 2004 ) Dikaryons of the basidiomycete fungus Schizophyllum commune: evolution in long-term culture . Genetics , 167 , 1663 - 1675 .
– reference: Huang Y-J , Li Z-Q , Evans N , Rouxel T , Fitt BDL , Balesdent M-H ( 2006 ) Fitness cost associated with loss of the AvrLm4 avirulence function in Leptosphaeria maculans (phoma stem canker o foilseed rape) . European Journal of Plant Pathology , 114 , 77 - 89 .
– reference: Leonard KJ , Szabo LJ ( 2005 ) Stem rust of small grains and grasses caused by Puccinia graminis . Molecular Plant Pathology , 6 , 99 - 111 .
– reference: Flor H ( 1971 ) Current status of the gene-for-gene concept . Annual Review of Phytopathology , 9 , 275 - 296 .
– reference: Ridout CJ , Skamnioti P , Porritt O , Sacristan S , Jones JDG , Brown JKM ( 2006 ) Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance . The Plant Cell , 18 , 2402 - 2414 .
– reference: Hovmøller MS ( 2007 ) Sources of seedling and adult plant resistance to P. striiformis f. sp. tritici in European wheats . Plant Breeding , 126 , 225 - 233 .
– reference: Maynard Smith J , Smith NH , O'Rourke M , Spratt BG ( 1993 ) How clonal are bacteria? Proceedings of the National Academy of Sciences, USA , 90 , 4384 - 4388 .
– reference: Catanzariti A , Dodds PN , Lawrence GJ , Ayliffe MA , Ellis JG ( 2006 ) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors . The Plant Cell , 18 , 243 - 256 .
– reference: Wellings CR ( 2007 ) Puccinia striiformis in Australia: a review of the incursion, evolution, and adaption of stripe rust in the period 1979-2006 . Australian Journal of Agricultural Research , 58 , 567 - 575 .
– reference: Vera Cruz CM , Bai JF , Ona I et al . ( 2000 ) Predicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutation . Proceedings of the National Academy of Sciences, USA , 97 , 13500 - 13505 .
– reference: Bürger R , Willensdorfer M , Nowak MA ( 2006 ) Why are phenotypic mutation rates much higher than genotypic mutation rates? Genetics , 172 , 197 - 206 .
– reference: Justesen AF , Ridout CJ , Hovmøller MS ( 2002 ) The recent history of Puccinia striiformis f. sp. tritici in Denmark as revealed by disease incidence and AFLP markers . Plant Pathology , 51 , 13 - 23 .
– reference: Lawrence GJ , Mayo GME , Shepherd KW ( 1981 ) Interactions between genes controlling pathogenicity in the flax rust fungus . Phytopathology , 71 , 12 - 19 .
– reference: Bayles RA , Flath K , Hovmøller MS , de Vallavieille-Pope C ( 2000 ) Breakdown of the Yr17 resistance to yellow rust of wheat in northern Europe - a case study by the yellow rust sub-group of COST 817 . Agronomie , 20 , 805 - 811 .
– reference: Enjalbert J , Duan M , Leconte M , Hovmøller MS , de Vallavieille-Pope ( 2005 ) Genetic evidence of local adaptation of wheat yellow rust (Puccinia striiformis f. sp. tritici) within France . Molecular Ecology , 14 , 2065 - 2073 .
– reference: Drake JW , Charlesworth B , Charlesworth D , Crow JF ( 1998 ) Rates of spontaneous mutation . Genetics , 148 , 1667 - 1686 .
– reference: Burdon JJ , Silk J ( 1997 ) Sources and patterns of diversity in plant-pathogenic fungi . Phytopathology , 87 , 664 - 669 .
– reference: Newton AC , Caten CE , Johnson R ( 1985 ) Variation for isozymes and double-stranded RNA among isolates of Puccinia striiformis and two other cereal rusts . Plant Pathology , 34 , 235 - 247 .
– reference: Parnell S , van den Bosch F , Gilligan CA ( 2006 ) Large-scale fungicide spray heterogeneity and the regional spread of resistant pathogen strains . Phytopathology , 96 , 549 - 555 .
– reference: Luderer R , Takken FLW , de Wit PJGM , Joosten HAJ ( 2002 ) Cladosporium fulvum overcomes Cf-2-mediated resistance by producing truncated AVR2 elicitor proteins . Molecular Microbiology , 45 , 875 - 884 .
– volume: 34
  start-page: 235
  year: 1985
  end-page: 247
  article-title: Variation for isozymes and double‐stranded RNA among isolates of and two other cereal rusts
  publication-title: Plant Pathology
– volume: 83
  start-page: 253
  year: 1993
  end-page: 260
  article-title: Observed and predicted changes in virulence gene‐frequencies at 11 loci in a local barley powdery mildew population
  publication-title: Phytopathology
– volume: 114
  start-page: 77
  year: 2006
  end-page: 89
  article-title: Fitness cost associated with loss of the AvrLm4 avirulence function in Leptosphaeria maculans (phoma stem canker o foilseed rape)
  publication-title: European Journal of Plant Pathology
– volume: 107
  start-page: 545
  year: 2003
  end-page: 556
  article-title: Molecular genetic variability of Australian isolates of five cereal rust pathogens
  publication-title: Mycological Research
– start-page: 163
  year: 1987
  end-page: 179
– volume: 5
  start-page: 164
  year: 1989
  end-page: 166
  publication-title: phylip, Phylogeny Inference Package
– volume: 58
  start-page: 518
  year: 2007
  end-page: 524
  article-title: Appearance and interpretation of atypical phenotypes of f. sp. in NW‐Europe
  publication-title: Australian Journal of Agricultural Research
– volume: 12
  start-page: 2019
  year: 2000
  end-page: 2032
  article-title: A telomeric avirulence gene determines efficacy for rice blast resistance gene Pi‐ta
  publication-title: Plant Cell
– volume: 85
  start-page: 409
  year: 1995
  end-page: 415
  article-title: Comparative effects of temperature and interrupted wet periods on germination, penetration, and infection of f. sp. and on wheat seedlings
  publication-title: Phytopathology
– start-page: 27
  year: 1983
  end-page: 35
– volume: 6
  start-page: 373
  year: 1988
  end-page: 387
  article-title: , yellow rust (stripe rust) of cereals and grasses
  publication-title: Advanced Plant Pathology
– volume: 14
  start-page: 2065
  year: 2005
  end-page: 2073
  article-title: Genetic evidence of local adaptation of wheat yellow rust ( f. sp. ) within France
  publication-title: Molecular Ecology
– volume: 41
  start-page: 239
  year: 1992
  end-page: 254
  article-title: Reflections of a plant pathologist on breeding for disease resistance, with emphasis on yellow rust and eyespot of wheat
  publication-title: Plant Pathology
– volume: 18
  start-page: 243
  year: 2006
  end-page: 256
  article-title: Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors
  publication-title: The Plant Cell
– volume: 57
  start-page: 615
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Snippet The effects of evolutionary processes in fungal pathogen populations may occur more rapidly and display larger effects in agricultural systems than in wild...
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SubjectTerms AFLP
Agriculture
alleles
amplified fragment length polymorphism
Amplified Fragment Length Polymorphism Analysis
Basidiomycota - genetics
Basidiomycota - isolation & purification
Basidiomycota - pathogenicity
clonal evolution
Crop diseases
Crop management
Denmark
Deoxyribonucleic acid
DNA
Ecology
ecosystems
Europe
Evolution, Molecular
Evolutionary biology
Farming systems
Fungal infections
fungi
Genetic Markers
humans
loci
Molecular biology
Mutation
mutation rate
Pathogens
Phenotype
Phenotypes
Phylogeny
Plant breeding
Plant Diseases - microbiology
Polymorphism, Genetic
Puccinia striiformis
Puccinia striiformis f. tritici
stripe rust
Triticum aestivum
United Kingdom
virulence
Virulence - genetics
Wheat
wheat stripe rust
Title Rates of evolution of avirulence phenotypes and DNA markers in a northwest European population of Puccinia striiformis f. sp. tritici
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https://www.ncbi.nlm.nih.gov/pubmed/17887968
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https://www.proquest.com/docview/1999920702
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Volume 16
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