▪ 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

Agricultural crops benefit from resistance to pathogens that endures over years and generations of both pest and crop. Durable disease resistance, which may be partial or complete, can be controlled by several genes. Some of the most devastating fungal pathogens in wheat are leaf rust, stripe rust, and powdery mildew. The wheat gene Lr34 has supported resistance to these pathogens for more than 50 years. Lr34 is now shared by wheat cultivars around the world. Here, we show that the LR34 protein resembles adenosine triphosphate-binding cassette transporters of the pleiotropic drug resistance subfamily. Alleles of Lr34 conferring resistance or susceptibility differ by three genetic polymorphisms. The Lr34 gene, which functions in the adult plant, stimulates senescence-like processes in the flag leaf tips and edges.

https://science.sciencemag.org/content/sci/323/5919/1360.full.pdf

A Putative ABC Transporter Confers Durable Resistance to Multiple Fungal Pathogens in Wheat

Some of the most striking and extreme consequences of rapid, long-distance aerial dispersal involve pathogens of crop plants. Long-distance dispersal of fungal spores by the wind can spread plant diseases across and even between continents and reestablish diseases in areas where host plants are seasonally absent. For such epidemics to occur, hosts that are susceptible to the same pathogen genotypes must be grown over wide areas, as is the case with many modern crops. The strongly stochastic nature of long-distance dispersal causes founder effects in pathogen populations, such that the genotypes that cause epidemics in new territories or on cultivars with previously effective resistance genes may be atypical. Similar but less extreme population dynamics may arise from long-distance aerial dispersal of other organisms, including plants, viruses, and fungal pathogens of humans.

https://science.sciencemag.org/content/sci/297/5581/537.full.pdf

Aerial Dispersal of Pathogens on the Global and Continental Scales and Its Impact on Plant Disease

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

Stripe rust, caused by Puccinia striiformis, has been an important disease of wheat, barley, rye, triticale and certain graminaceous hosts for centuries. The significance of the disease on cultivated cereals has waxed and waned according to the vagaries of climate, inoculum levels and susceptible varieties. A progressive understanding of pathogen biology has revealed levels of specialisation between and within host groups, and these had varying impacts on the hosts concerned. The most economically important form is P. striiformis f. sp. tritici (Pst), the causal pathogen of stripe (yellow) rust of wheat, which is the major focus of this paper. The recent discovery of the perfect stage of Pst on Berberis spp. will encourage further work to uncover the potential importance of the sexual stage in pathogen biology in regions where Berberis spp. occur. A review of the evolution of pathotypes within Pst over the past 50 years reveals recurrent pandemics emanating from a combination of specific virulence in the pathogen population, wide scale cultivation of genetically similar varieties, and agronomic practices that led to high yield potential. When these factors operate in concert, regional stripe rust epidemics have proven to be dramatic, extensive and serious in terms of the magnitude of losses and the economic hardships endured. A review of these epidemics suggests that little progress has been made in containing the worst effects of epidemics. The current status of stripe rust was gauged from a survey of 25 pathologists and breeders directly associated with the disease. It was evident that Pst remains a significant threat in the majority of wheat growing regions of the world with potential to inflict regular regional crop losses ranging from 0.1 to 5%, with rare events giving losses of 5–25%. Regions with current vulnerability include the USA (particularly Pacific North West), East Asia (China north-west and south-west), South Asia (India, Pakistan, Nepal), Oceania (Australia, New Zealand), East Africa (Ethiopia, Kenya), the Arabian Peninsula (Yemen) and Western Europe (east England). The resources deployed to contain the worst effects of Pst will need to find a balance between training a new generation of breeders and pathologists in host-pathogen genetics, and an investment in infrastructure in IARCs and NARs.

Global status of stripe rust: a review of historical and current threats

SUMMARY Stripe (yellow) rust,caused by Puccinia striiformis f.sp.tritici (Pst), is a serious disease of wheat occurring in most wheat areas with cool and moist weather conditions during the growing season.The basidiomycete fungus is an obligate biotrophic parasite that is difficult to culture on artificial media. Pst is a macrocyclic, heteroecious fungus that requires both primary (wheat or grasses) and alternate (Berberis or Mahonia spp.) host plants to complete its life cycle. Urediniospores have the capacity for wind dispersal over long distances, which may, under high inoculum pressure, extend to thousands of kilometres from the initial infection sites. Stripe rust, which is considered to be the current major rust disease affecting winter cereal production across the world, has been studied intensively for over a century. This review summarizes the current knowledge of the Pst‐wheat pathosystem, with emphasis on the life cycle, uredinial infection process, population biology of the pathogen, genes for stripe rust resistance in wheat and molecular perspectives of wheat‐Pst interactions. Taxonomy: The stripe rust pathogen, Puccinia striiformis Westend. (Ps), is classified in kingdom Fungi, phylum Basidiomycota, class Urediniomycetes, order Uredinales, family Pucciniaceae, genus Puccinia. Ps is separated below the species level by host specialization on various grass genera,comprising up to nine formae speciales, of which P. striiformis f. sp. tritici Erikss. (Pst) causes stripe (or yellow) rust on wheat. Host range: Uredinial/telial hosts: Pst mainly infects common wheat (Triticum aestivum L.), durum wheat (T. turgidum var. durum L.), cultivated emmer wheat (T. dicoccum Schrank), wild emmer wheat (T. dicoccoidesKorn) and triticale (Triticosecale).Pst can infect certain cultivated barleys (Hordeum vulgare L.) and rye (Secale cereale L.),but generally does not cause severe epidemics. In addition,Pst may infect naturalized and improved pasture grass species, such as Elymus canadensis L., Leymus secalinus Hochst, Agropyron spp. Garetn, Hordeum spp. L., Phalaris spp. L and Bromus unioloides Kunth. Pycnial/aecial (alternative) hosts: Barberry (Berberis chinensis, B. koreana, B. holstii, B. vulgaris, B. shensiana, B. potaninii, B. dolichobotrys, B. heteropoda, etc.) and Oregon grape (Mahonia aquifolium). Disease symptoms: Stripe rust appears as a mass of yellow to orange urediniospores erupting from pustules arranged in long, narrow stripes on leaves (usually between veins), leaf sheaths, glumes and awns on susceptible plants. Resistant wheat cultivars are characterized by various infection types from no visual symptoms to small hypersensitive flecks to uredinia surrounded by chlorosis or necrosis with restricted urediniospore production. On seedlings, uredinia produced by the infection of a single urediniospore are not confined by leaf veins, but progressively emerge from the infection site in all directions, potentially covering the entire leaf surface. Individual uredinial pustules are oblong, 0.4‐0.7 mm in length and 0.1 mm in width. Urediniospores are broadly ellipsoidal to broadly obovoid, (16‐ )18‐30(‐32) × (15‐)17‐27(‐28) μm, with a mean of 24.5 × 21.6 μm, yellow to orange in colour, echinulate, and with 6‐18 scattered germ pores. Urediniospores can germinate rapidly when free moisture (rain or dew) occurs on leaf surfaces and when the temperatures range is between 7 and 12 °C. At higher temperatures or during the later growing stages of the host,black telia are often produced, which are pulvinate to oblong, 0.2‐0.7 mm in length and 0.1 mm in width. The teliospores are predominantly two-celled, dark brown with thick walls, mostly oblong-clavate, (24‐)31‐56(‐65) × (11‐)14‐25(‐29) μm in length and width,and rounded or flattened at the apex.

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Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici

Pathogenic attributes of the wheat stripe rust pathogen were monitored in annual surveys from the first recording of this disease in Australia in 1979. During the 10-year period to 1988,15 different pathotypes were detected in Australia and New Zealand. The pathotypes included some of economic importance to commercial wheat cultivars and others with no obvious selective advantage to aid their survival. Single-gene mutations were the most likely causes of variation. The implications of these results on pathogenicity surveys and breeding for resistance are discussed.

Puccinia striiformis f.sp. tritici in Australasia: pathogenic changes during the first 10 years

The wheat stripe rust pathogen (Puccinia striiformis f. sp. tritici; Pst) was first detected in Australia in 1979. The features of the initial pathotype suggested that it was of European origin, and later work provided evidence that it was most likely transmitted as adherent spores on travellers' clothing. Despite long-held views that this cool temperature pathogen would not adapt to Australian conditions, Pst became endemic and progressively adapted to commercial wheat production through step-wise mutation. Several of these mutant pathotypes became frequent in the Pst population, causing widespread infection and significant costs to production (yield and quality losses; chemical control expenditure) in certain cultivars and seasons. Pathotype evolution, including adaptation to native barley grass (Hordeum spp.) populations, is described. The occurrence of an exotic pathotype of Pst in Western Australia in 2002, and its subsequent spread to eastern Australia, represented a major shift in the pathogen population. This pathotype dominated pathogen populations throughout Australia from 2003, with chemical control expenditure estimated at AUS40-90 million annually. Another exotic introduction was detected in 1998. Initial data indicated that certain isolates collected from barley grass were highly avirulent to wheat differentials, with the exception of partial virulence to Chinese 166. Further seedling tests revealed that these isolates, tentatively designated barley grass stripe rust (BGYR), were virulent on several Australian barleys, notably those of Skiff parentage. Data, including molecular studies, suggest that BGYR is a new forma specialis of P. striiformis. Field nurseries indicate that BGYR is likely to have little impact on commercial barley, although this may change with further pathotype evolution or the release of susceptible cultivars.

Colin R. Wellings

Papers

Wheat Rusts: An Atlas of Resistance Genes

Global status of stripe rust: a review of historical and current threats

Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici

Puccinia striiformis f.sp. tritici in Australasia: pathogenic changes during the first 10 years

Puccinia striiformis in Australia: a review of the incursion, evolution, and adaptation of stripe rust in the period 1979–2006