▪ Abstract We hypothesize that the evolutionary potential of a pathogen population is reflected in its population genetic structure. Pathogen populations with a high evolutionary potential are more likely to overcome genetic resistance than pathogen populations with a low evolutionary potential. We propose a flexible framework to predict the evolutionary potential of pathogen populations based on analysis of their genetic structure. According to this framework, pathogens that pose the greatest risk of breaking down resistance genes have a mixed reproduction system, a high potential for genotype flow, large effective population sizes, and high mutation rates. The lowest risk pathogens are those with strict asexual reproduction, low potential for gene flow, small effective population sizes, and low mutation rates. We present examples of high-risk and low-risk pathogens. We propose general guidelines for a rational approach to breed durable resistance according to the evolutionary potential of the pathogen.

Pathogen population genetics, evolutionary potential, and durable resistance

A vast number of plant pathogens from viroids of a few hundred nucleotides to higher plants cause diseases in our crops. Their effects range from mild symptoms to catastrophes in which large areas planted to food crops are destroyed. Catastrophic plant disease exacerbates the current deficit of food supply in which at least 800 million people are inadequately fed. Plant pathogens are difficult to control because their populations are variable in time, space, and genotype. Most insidiously, they evolve, often overcoming the resistance that may have been the hard-won achievement of the plant breeder. In order to combat the losses they cause, it is necessary to define the problem and seek remedies. At the biological level, the requirements are for the speedy and accurate identification of the causal organism, accurate estimates of the severity of disease and its effect on yield, and identification of its virulence mechanisms. Disease may then be minimized by the reduction of the pathogen's inoculum, inhibition of its virulence mechanisms, and promotion of genetic diversity in the crop. Conventional plant breeding for resistance has an important role to play that can now be facilitated by marker-assisted selection. There is also a role for transgenic modification with genes that confer resistance. At the political level, there is a need to acknowledge that plant diseases threaten our food supplies and to devote adequate resources to their control.

Plant Disease: A Threat to Global Food Security

Stripe rust of wheat, caused by Puccinia striiformis f. sp. tritici, is one of the most important diseases of wheat worldwide. This review presents basic and recent information on the epidemiology of stripe rust, changes in pathogen virulence and population structure, and movement of the pathogen in the United States and around the world. The impact and causes of recent epidemics in the United States and other countries are discussed. Research on plant resistance to disease, including types of resistance, genes, and molecular markers, and on the use of fungicides are summarized, and strategies for more effective control of the disease are discussed.

Epidemiology and control of stripe rust (Puccinia striiformis f. sp. tritici) on wheat

1: Wheat Rusts and the Genetic Bases on Disease Resistance. Introduction. Biology of Pathogen and Host. Host:Pathogen Genetics. Methodologies in Wheat Rust Disease. A Coordinated Strategy for Rust Control. Conclusion. Guide to Gene Descriptions and Illustrations. 2: The Genes for Resistance to Leaf Rust in Wheat and Triticale. Catalogued Leaf Rust Resistance Genes. Temporarily Designated and Miscellaneous Leaf Rust Resistance Genes. 3: The Genes for Resistance to Stem Rust in Wheat and Triticale. Catalogued Leaf Rust Resistance Genes. Temporarily Designated and Miscellaneous Stem Rust Resistance Genes. 4: The Genes for Resistance to Stripe Rust in Wheat and Triticale. Catalogued Stripe Rust Resistance Genes. Temporarily Designated and Miscellaneous Stripe Rust Resistance Genes. References. Appendix I: Species Names Used in the Text, Genomic Formulae and Synonyms. Appendix II: Pathotypes and Accessions (Cultures) Used in Photography.

Wheat Rusts: An Atlas of Resistance Genes

The durability of disease resistance is affected by the evolutionary potential of the pathogen population Pathogens with a high evolutionary potential are more likely to overcome genetic resistance than pathogens with a low evolutionary potential We will propose a set of guidelines to predict the evolutionary potential of pathogen populations based on analysis of their genetic structure Under our model of pathogen evolution, the two most important parameters to consider are reproduction/mating system and gene/genotype flow Pathogens that pose the greatest risk of breaking down resistance genes are those that possess a mixed reproduction system, with at least one sexual cycle per growing season and asexual reproduction during the epidemic phase, and a high potential for gene flow The lowest risk pathogens are those with strict asexual reproduction and low potential for gene flow We will present examples of high- and low-risk pathogens Knowledge of the population genetic structure of the pathogen may offer insight into the best breeding strategy for durable resistance We will present broad guidelines suggesting a rational method for breeding durable resistance according to the population genetics of the pathogen

The population genetics of plant pathogens and breeding strategies for durable resistance

Reflections of a plant pathologist on breeding for disease resistance, with emphasis on yellow rust and eyespot of wheat.

Crosses of a wheat line TP1295 with the cultivar Chinese Spring monosomic series were used to locate, on chromosome 1D, a major gene for resistance to isolate WYR 85-22 of race 6E0 of Puccinia striiformis The gene is designated as Yr25 and is probably present in several of the cultivars currently widely used for differentiating races of this pathogen The expression of the gene was modified by the environment and by at least one minor gene which may be located on chromosome 6A In F2 and F3 generations from a cross between TP1295 and euploid Chinese Spring, a wide range of variation in infection type (IT) was observed This precluded the classification of the plants as either resistant or susceptible, so they were assigned to 6 classes and analyzed by factorial correspondence analysis and non-hierarchical classification When all F3 plants in a family were fully resistant, like TP1295 itself (IT ;), both Yr25 and the modifying gene were assumed to be present and homozygous In environments favourable to expression of the gene, families thought to carry Yr25 alone had a distribution of ITs from fully resistant (IT ;) to intermediate (IT 2, rarely 3 or 3+) This F3 analysis indicated that use of IT data alone, in the monosomic analysis, would not reveal the chromosomal location of the genes and that chromosome counting of numerous plants was necessary As well as indicating the chromosomes carrying the genes for resistance to isolate WYR 85-22, the data showed that plants monosomic for chromosomes 5B and 5D were more resistant than the corresponding disomics, indicating that these chromosomes promote susceptibility and supporting other evidence of the effects of these chromosomes on yellow rust resistance

https://link.springer.com/content/pdf/10.1023/A:1008660904975.pdf

Chromosomal location of genes for resistance to Puccinia striiformis in the wheat line TP1295 selected from the cross of Soissonais-Desprez with Lemhi

One major gene for resistance to isolate WYR 85-22 of race 6E0 of Puccinia striiformis was identified by genetic analysis of the differential cultivars Heines Peko, Strubes Dickkopf and Heines VII. This gene was different from Yr2Yr6 already identified in Heines Peko (Yr2Yr6) and Heines VII (Yr2), was allelic in the three cultivars and also to a gene expressed in the other differentials Reichersberg 42 (Yr7) and Clement (Yr9). In Heines Peko, Strubes Dickkopf and Heines VII, a minor gene was also postulated, which, it is proposed, gave only a low level of resistance by itself but strengthened the expression of the major gene when the latter was homozygous or heterozygous. The genetics of the resistance was analysed using six resistance classes and applying multidimensional analyses. The number of resistance genes was hypothesized using data from F3 families from crosses between the three differentials and the cultivar Heines Kolben, which is susceptible to this race.

Genetic analysis of resistance to Puccinia striiformis in the wheat differential cultivars Heines VII, Heines Peko and Strubes Dickkopf

Genetic data showed that a common gene was present in the three differential wheat cultivars Heines VII (Yr2), Heines Peko (Yr2, Yr6) and Heines Kolben (Yr6) expressed against the race 109E9 of Puccinia striiformis which possesses virulence for Yr6 and avirulence for Yr2. This supported the hypothesis that Heines Kolben carries the gene Yr2 in addition to Yr6 for resistance to yellow rust in a genetic background in which Yr2 is weakly expressed in seedlings. F1, F2 and F3 progenies from the cross Heines Kolben × Peragis confirmed the monogenic segregation of Yr2 in Heines Kolben and demonstrated the variation of its expression with environmental conditions.

Identification and expression of the gene Yr2 for resistance to Puccinia striiformis in the wheat differential cultivars Heines Kolben, Heines Peko and Heines VII

Genetic analysis of resistance of wheat seedlings to two races of Puccinia striiformis was conducted on F1, F2 and F3 generations from crosses Carstens V (CV) × Lee, Spaldings Prolific (SPA) × Lee and CV × SPA. F2 generations from crosses of CV and SPA with Strubes Dickkopf (SD) were also studied. The plants were classified into six resistance classes and analysed by factorial correspondence analysis and nonhierarchical classification. The two P. striiformis isolates tested were a French isolate of race 43E138 and a Lebanese isolate of race 2E16, selected for the differences in their virulence spectra for the common differential cultivars Strubes Dickkopf and Nord Desprez. Resistance of CV and SPA was recessive and dominant to races 43E138 and 2E16, respectively. CV possessed three or four resistance genes, one of them being expressed with both races. Two genes of CV had a cumulative effect for resistance to 43E138 and two or three gave dominant resistance to 2E16. SPA had three resistance genes, all of which gave resistance to 2E16 and two of which also gave resistance to 43E138. SPA had one gene in common with CV for resistance to both races. Furthermore, the gene for resistance to race 2E16 in CV and SPA was allelic with a gene in SD, and was probably Yr25.

https://bsppjournals.onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-3059.2002.00788.x

R. Johnson

Papers

Reflections of a plant pathologist on breeding for disease resistance, with emphasis on yellow rust and eyespot of wheat.

Chromosomal location of genes for resistance to Puccinia striiformis in the wheat line TP1295 selected from the cross of Soissonais-Desprez with Lemhi

Genetic analysis of resistance to Puccinia striiformis in the wheat differential cultivars Heines VII, Heines Peko and Strubes Dickkopf

Identification and expression of the gene Yr2 for resistance to Puccinia striiformis in the wheat differential cultivars Heines Kolben, Heines Peko and Heines VII

Genetic analyses of resistance of the wheat differential cultivars Carstens V and Spaldings Prolific to two races of Puccinia striiformis