Summary

Introduction

Stripe (yellow) rust, caused by Puccinia striiformis Westend. (Ps), is one of the most widely destructive plant diseases in modern winter cereal production (Wellings, 2011). The specialized form infecting wheat is referred to as P.striiformis f. sp. tritici (Pst). The sexual stage on Berberis spp. and Mahonia spp. has only been described recently (Jin etal., 2010; Wang and Chen, 2013; Zhao etal., 2011, 2013). Mutation, somatic recombination, parasexuality, selection and probably sexual recombination are considered to be the mechanisms that drive pathogen variability (Duan etal., 2010a; Hovmøller etal., 2011; Mboup etal., 2009; Stubbs, 1985). The centre of origin for P.striiformis was earlier assumed to be Transcaucasia, where grasses were the primary host (Hassebrauk, 1965), and from there the pathogen dispersed in all directions, including eastward to East Asia and North America in the 1910s (Carleton, 1915; Fraser and Conners, 1925; Humphrey etal., 1924), and southward into West Asia and East Africa. Geographically isolated wheat‐producing regions were invaded by long‐distance pathogen migration: Australia from Europe in 1979 (O'Brien etal., 1980); Republic of South Africa from the Middle East in 1996 (Boshoff etal., 2002); Western Australia from North America in 2002 (Wellings, 2007). Western China and Central Asia are also speculated as a centre of origin based on a high degree of telial production for isolates sampled in those areas and a high genetic diversity consistent with frequent recombination signatures (Ali etal., 2010b; Mboup etal., 2009).

Stripe rust is considered to be a low‐temperature disease and frequently occurs in temperate areas with cool and moist weather conditions. Recent devastating epidemics have occurred in warmer areas where the disease was previously infrequent or absent (Hovmøller etal., 2010; Mboup etal., 2009). This led to the proposal that populations of Pst had developed adaptation to higher temperature, and supporting evidence was published by Milus etal. (2008). The minimum, optimum and maximum temperatures for urediniospore germination are 0°C, 7–12°C and 20–26°C, respectively (Schröder and Hassebrauk, 1964). Of the three wheat rusts (stripe rust, leaf rust and stem rust), stripe rust appears to be the most sensitive to environmental factors, such as air pollution and UV light, which reduce the germination of urediniospores (Sharp, 1967). Resistance of the host is also influenced by temperature and light, which, in turn, influences disease assessment of the infected plant (Sharp and Volin, 1970). Increasing day length or light intensity lowers the infection type (Bever, 1934; Stubbs, 1967; Wellings etal., 1988).

Yield losses in wheat from Pst infections are usually the result of reduced kernel number per spike, low test weight and reduced kernel quality (Prescott etal., 1986). Evidence from historical epidemics and crop losses, and a contemporary analysis of the incidence and crop loss magnitude experienced in current major world wheat‐growing regions, concluded that Pst was the most serious biotic threat to sustainable international wheat production (Wellings, 2011).

In this review, we summarize the current understanding of Pst biology, including studies of host–pathogen interactions, to develop strategies for resistance breeding which may form the basis for the development of practical control strategies in this economically significant pathosystem.

Life Cycle

In the asexual urediniospore stage, Ps infects a range of grasses within the Pooideae subfamily of the Poaceae. Collections of Ps from certain grasses showed evidence of host specialization, and this led Eriksson (1894) to propose five special forms (Latin: ‘formae speciales’) based on the originating host genus, namely P.striiformis f. sp. tritici (Pst) specialized on wheat, P.striiformis f. sp. hordei (Psh) on barley, P.striiformis f. sp. secalis on rye, P.striiformis f. sp. elymi on Elymus spp. and P.striiformis f. sp. agropyri on Agropyron spp. Additional formae speciales were reported: P.striiformis f. sp. dactylidis (Psd) on orchard grass (Dactylis glomerata L.) (Manners, 1960; Tollenaar, 1967), P.striiformis f. sp. poae (Psp) on Kentucky blue grass (Poa pratensis L.) (Britton and Cummins, 1956; Tollenaar, 1967), P.striiformis f. sp. leymi on Leymus secalinus (Georgi) Tzvel. (Niu etal., 1991) and P.striiformis f. sp. pseudo‐hordei (Psp‐h) on Hordeum spp. in Australia (Wellings, 2007).

Liu and Hambleton (2010) presented molecular [internal transcribed spacer (ITS) and β‐tubulin sequences] and morphological data from a set of 31 isolates to redefine several issues in the biology and taxonomy of Ps. Puccinia series striiformis was proposed to include P.striiformis sensu stricto (host range Aegilops, Elymus, Hordeum, Triticum), P.striiformoides (formerly Psd) infecting D.glomerata, P.pseudostriiformis (formerly Psp) infecting Poa spp. and P.gansensis in a single isolate from Achnatherum inebrians in China. The descriptions of the last three species agree well with the biology of these collections, including very close host affinity and distinct temperature optima for infection. However, the major formae speciales within Ps sensu stricto (i.e. Pst, Psh, Psp‐h) will remain as important taxa that assist in understanding the host biology and comparative potential threat of these forms in commercial agriculture.

Ps was long regarded as an autoecious microcyclic rust pathogen (urediniospores and teliospores forming on grass hosts) until Jin etal. (2010) identified Berberis spp. (B.chinensis, B.holstii, B.koreana, B.vulgaris) as alternative hosts supporting pycniospores and aeciospores of Pst and P.pseudostriiformis. Wang and Chen (2013) demonstrated that Oregon grape (Mahonia aquifolium) is also a host for the sexual phase of Pst.

Ps and P.pseudostriiformis are now classified as heteroecious macrocyclic rust pathogens (Fig.1). Urediniospores are primarily dikaryotic (n + n) and maintain the dominant asexual stage of the pathogen population on the primary hosts. This phase is responsible for wide‐scale stripe rust epidemics reported on cereal crops.

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Figure 1

Life cycle of Puccinia striiformis. (A) Uredinia on wheat leaf containing single‐celled dikaryotic urediniospores (n + n) originating from aeciospores (n + n) or urediniospores. Top inset: echinulate surface of a urediniospore under a scanning electron microscope (SEM) (×4000). Bottom inset: broadly obovoid urediniospores (×1000). (B) Telia typically form beneath the leaf epidermis near the end of the growing season. Top inset: the two‐celled, oblong‐clavate teliospores (2n) (×1000). Bottom inset: the elliptoid basidiospores (n) from the germination of teliospores (×2500). (C) Pycnia produced by basidiospore infection on Berberis chinensis on upper leaf surfaces via inoculation with germinating teliospores of P.striiformis. Top inset: a magnified flask‐shaped pycnia (×400). Middle inset: the oblong‐shaped pycniospores (×4000). Bottom inset: magnified receptive hyphae (×900). (D) Cluster of sunflower‐shaped aecia produced on the lower leaf surface of Berberis shensiana. Top inset: a campanulate aecium (×200). Middle inset: flat spherical‐shaped aeciospores (×3300). Bottom inset: cluster of aeciospores (×250). (E) A wheat seedling that can be infected by aeciospores produced on barberry plants and can produce urediniospores.

As temperatures rise late in the epidemic phase, Pst typically produces thick‐walled, predominantly two‐celled teliospores. Each cell of a mature teliospore contains a diploid (2n) nucleus formed by karyogamy. Pst isolates vary in their ability to produce telia even under similar environmental conditions (Chen XM etal., 2012). Unlike those of P.graminis f. sp. tritici, teliospores of Pst do not have dormancy and readily germinate. Wang and Chen (unpublished Washington State University) have determined that, under free water conditions at 12°C, teliospores germinate (24h) to produce a promycelium of four cells. Meiosis then produces a single haploid nucleus that forms a basidiospore (48h) ready to be ejected from the sterigma (60h). Basidiospores germinate and infect Berberis spp. or Mahonia spp. (72h). The authors also determined that a minimum 40‐h dew period was required for the infection of barberry leaves from basidiospores, with the highest infection achieved by keeping inoculated barberry plants in a dew chamber at 10°C for 93h. The absence of dormancy in teliospores and the consequent short period of available basidiospores led Rapilly (1979) to conclude that a sexual host, should it ever be discovered, would probably have a small role in pathogen survival. In view of this comment and the prolonged dew periods required for infection, it is perhaps unsurprising that there has been limited confirmation of Pst on Berberis spp. in nature, with just two reports from China (Zhao etal., 2011, 2013). It has been concluded that Berberis spp. do not play a role in stripe rust epidemics under the natural conditions in the US Pacific Northwest (Chen XM etal., 2012).

Uredinial Infection Process

Almost all biochemical and molecular studies have been based on urediniospores and their derived infection structures (Hahn, 2000; Hahn etal., 1997; Ling etal., 2007; Mendgen etal., 2000; Struck etal., 2004; Voegele, 2006; Voegele and Mendgen, 2003; Yin etal., 2009; Zhang etal., 2008). As an obligate biotrophic plant parasite, Pst infects the main hosts (cereal crops, grasses) from urediniospore deposition by wind or raindrops onto the leaf surface. Germination initiates within 3h of contact with free moisture at a range of temperatures. The cytoplasm of a urediniospore moves into the growing germ tube as it orientates perpendicular to the long axis of epidermal cells during its growth across the leaf surface (Kang, 1996; Kang etal., 1997, 2002) until it reaches a stoma (Fig.2C,D) (Moldenhauer etal., 2006; Wang etal., 2009). Within 6–8h post‐inoculation (hpi), an appressorium is formed on the stoma, and at 8–12 hpi, a substomatal vesicle is formed within the stomatal cavity, the penetration hyphae are delimited by a septum (Kapooria and Mendgen, 1985) and the primary infection hypha emerges at 12–18hpi. On contacting the mesophyll cell, a haustorial mother cell containing two to six nuclei develops (Kang etal., 1994, 2002) and most of the cytoplasm then moves into the haustorial mother cell, leaving earlier structures to become more or less vacuolated. Haustorial mother cells have a thick, multilayered wall that attaches firmly to the host cell wall. A slender neck forms from the haustorial mother cell, which then invaginates the host cell plasma membrane (Heath and Skalamera, 1997) to form a balloon‐shaped feeding structure, known as the haustorium (Fig.2E; Hovmøller etal., 2011; Kang etal., 1997, 2003). Haustoria draw nutrients from host cells (Hahn and Mendgen, 2001; Mendgen, 1981; Staples, 2001; Voegele and Mendgen, 2003) and have also been shown to be involved in vitamin synthesis (Sohn etal., 2000). Haustoria are typically located in host mesophyll cells and up to 15% of epidermal cells (Hovmøller etal., 2011). Unlike stem rust and leaf rust fungi, multinucleate conditions in hyphae, haustorial mother cells and haustoria are very common (Kang etal., 1994). From 48 to 120hpi, the primary infection hypha will give rise to many branched hyphae that develop between host mesophyll cells and produce multiple haustorial mother cells and haustoria, resulting in a branching network of fungal mycelium developing inter‐ and intracellularly within the host tissue. As the mycelium develops, a pustule bed becomes established from which a uredinium develops. Symptoms of chlorosis can be observed from 6 to 8 days after infection, whereas sporulation (uredinia appearing on the surface of leaves, leaf sheaths, glumes or awns) commences approximately from 12 to 14 days under favourable conditions. Symptoms of wheat stripe rust in the field and a range of seedling infection types in glasshouse tests are shown in Figs3 and ​and4,4, respectively.

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Figure 2

Uredinial infection process. (A) Schematic representation of early infection structures by Puccinia striiformis (Ps). (B) Urediniospore under a scanning electron microscope (SEM) (×4000). (C) A urediniospore germ tube (GT) enters the leaf through a stoma (ST). (D) A substomatal vesicle (SSV) is formed, from which an infection hypha (IH) emerges. On contacting with a mesophyll cell, a haustorial mother cell (HMC) is differentiated. (E) A haustorium develops from the haustorial mother cell with a slender neck (Kang, 1996). (F) Ps hyphae spread and form colonies in infected leaf tissue. (G) A uredinium under a SEM (Kang etal., 1997). AP, appressorium; EHM, extrahaustorial matrix; GT, germ tube; HB, haustorial body; HMC, haustorial mother cell; HN, haustorial neck; IH, infection hypha; PP, penetration peg; SSV, substomatal vesicle; U, urediniospore.

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Figure 3

Wheat stripe rust symptoms in the field. (A–C) Yellow to orange uredinial pustules on susceptible adult plant leaves. (D) Uredinial pustules on the glumes and awns. (E, F) Yellow to orange uredinial pustules on the seedling wheat leaves. (G) Telial and uredinial pustules together on an adult plant leaf.

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Figure 4

Range of stripe rust seedling infection types. From the left, leaves show infection types ranging from immune to completely susceptible reaction (McIntosh etal., 1995).

Pst is noted for enhanced sensitivity to environmental conditions in comparison with other cereal rust pathogens. The most important factors are temperature, moisture, light and air pollution. Temperature is critical for successful germination and infection. In the presence of adequate moisture, invitro germination studies showed a temperature range of 2–15°C with an optimum at 7°C (Sharp, 1965). Similar conclusions were drawn by Rapilly (1979) and Zhang etal. (2008). Newton and Johnson (1936) determined that the optimal temperature range for the latent period (time from infection to the beginning of sporulation) was 13–16°C. These temperatures are, on average, about 10–15°C lower in each category than those for P.triticina and P.graminis.

Moisture affects spore deposition, germination, infection and survival. Rapilly and Foucault (1976) observed that the adhesive force between urediniospore and receptive surfaces was significantly greater with high relative humidity, thus increasing the efficiency of spore attachment. Urediniospores require at least 3h of available moisture on plant surfaces to germinate and infect (Hermansen and Veterinary, 1968; Tu and Hendrix, 1967). Any period of desiccation will irreversibly abort urediniospore germination (Vallavieille‐Pope etal., 1995). Zadoks (1961) and Rapilly and Fournet (1968) concluded that relative humidity must exceed 50% for sporulation to occur, and that urediniospore production increased exponentially with rising relative humidity.

Light intensity influences the host–pathogen interaction (Stubbs, 1967). Low light intensities in the first 4 days post‐infection caused infection type to increase and effectively mask a resistant response (Wellings etal., 1988). Seedling tests should always be conducted at light intensities above 10000lx in order to ensure consistent infection types (Stubbs, 1985). Ps has been shown to be more sensitive to air pollution, relative to other cereal rust pathogens, during urediniospore germination (Sharp, 1967). Later work showed that isolates from various regions varied in sensitivity to air pollutants (Melching etal., 1974; Stubbs, 1985).

Population biology of P.striiformis

Like the other cereal rust fungi, Pst has nearly a century of research history investigating detailed aspects of host–pathogen specialization that was fundamental to devising strategies to control the disease in commercial cropping.

Long‐distance dispersal

Pst is capable of long‐distance dispersal by wind movement and human‐assisted transport (Brown and Hovmøller, 2002). Urediniospores of Pst can be efficiently air dispersed over hundreds and perhaps thousands of kilometres despite their vulnerability to environmental factors, such as ultraviolet light (Zadoks, 1961).

In North America, Pst gradually covered a distance of about 2400km from northern Mexico and southern Texas to North Dakota within 6months (Chen etal., 2010; Line and Qayoum, 1992).

In Europe, urediniospores can be transported 800km and even more than 1200km from north France to Algeria by wind (Stubbs, 1985). The wheat stripe rust pathogen entered New Zealand in 1982, probably as the result of 2000km of airborne transport from Australia (Wellings and McIntosh, 1990).

In China, evidence suggests that urediniospores are annually dispersed hundreds or even thousands of kilometres from western over‐summering areas to the main wheat belt in the east and north (Fig.5; Chen and Xie, 1999; Chen etal., 2007; Xie etal., 1992, 1993; Zeng and Luo, 2006). Upland areas 1500–1800m and 1900–2500m above sea level in northwestern and southwestern China, respectively, provide environments for year‐round pathogen survival and development, and hence these regions are major reservoirs of inoculum and pathogenic diversity (Brown and Hovmøller, 2002; Chen etal., 2007, 2009). The pathogen must re‐establish each autumn in northern and eastern China, the main winter wheat‐growing areas, because the pathogen cannot survive the hot dry summers. Ecological management of wheat stripe rust in the areas of inoculum sources has been considered the major strategy for the sustainable control of wheat stripe rust nationwide, resulting in effective containment of wheat yield losses that potentially amount to more than two million tonnes annually (Chen WQ etal., 2012, 2013).

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Figure 5

Ecological zones of wheat stripe rust and aerial dispersal of urediniospores in China. 1, The Guanzhong and Huabei winter wheat region is the main area of winter wheat cultivation and the over‐wintering area of Puccinia striiformis f. sp. tritici (Pst) in China. 2, The Chengdu Plain and Jianghan River Basin facultative wheat region is the winter‐increasing area and the major spring inoculum source of Pst. 3, The Northwest winter and spring wheat region is the most important over‐summering area of Pst and the major source of inoculum for wheat infection in autumn. 4, The Yunnan and Guizhou wheat region is one of the over‐summering areas of Pst. 5, The Xinjiang winter and spring wheat region is a relatively independent epidemic zone of Pst. 6, The Tibet highland barley and wheat region is a separate epidemic zone of Pst. 7, The South late‐sowing wheat region does not grow much wheat and stripe rust seldom occurs. 8, The Inner Mongolia and Northeast spring wheat region where wheat stripe rust epidemics occur occasionally. The full black arrows show dispersal of urediniospores from the over‐summering areas to the main wheat‐growing areas in autumn annually. The broken black arrows indicate the main pathway of urediniospore dispersal in spring. The red line indicates the boundary of Pst over‐wintering areas and the red circles show provincial capitals.

In the US Pacific Northwest, where both winter and spring wheat are grown, Pst urediniospores spread readily from winter wheat to spring wheat in the summer and from spring wheat to winter wheat in autumn, in addition to survival on volunteer wheat plants and wild grass species (Chen, 2005; Hendrix etal., 1965; Line, 2002).

In Australia, Pst was first detected in 1979 and the pathogenic features of the initial isolates predicted that it was of European origin. Wellings etal. (1987) provided evidence to support the survival of urediniospores on contaminated travellers’ clothing, and predicted that this was the most likely means of entry of Pst into Australia. The first detection of Pst in remote wheat‐growing regions previously free of the disease in South Africa in 1996 and in Western Australia in 2002 has similarly implicated long‐distance transport assisted by adherent urediniospores on travellers’ clothing (Wellings, 2007).

Molecular Perspectives

Genes for Stripe Rust Resistance in Wheat

The genetic characterization of resistance has been an active focus of research since the seminal work of Biffen (1905), who first described the Mendelian nature of resistance to stripe rust in wheat cultivar Rivet. The major types of resistance to Pst in wheat are seedling (or all‐stage) resistance and adult plant resistance (APR). The former is conveniently detected in seedling tests and remains effective throughout all growth stages provided that the same Pst pathotype is used in all assessments. APR, which expresses susceptible infection types in seedling tests, develops varying levels of resistance in post‐seedling stages in either field or glasshouse studies. Major reviews of the genetic basis for resistance to Pst can be found in Chen (2005, 2013), Röbbelen and Sharp (1978) and Wellings etal. (2012).

Seedling resistances are frequently conferred by single genes, or simple combinations of single genes, and have generally become vulnerable to single‐gene changes to increased virulence in Pst populations. APR has been considered to be more robust in terms of resistance in that it has not been as readily overcome by changing Pst populations, although there have been notable severe epidemics arising from the failure of single‐gene APR, for example, the sudden susceptibility of Joss Cambier in the UK in 1969 (Johnson and Taylor, 1972). A major conceptual development in searching for strategies to contain stripe rust epidemics was the description of durable resistance, which was defined as wheat cultivars that remained resistant when cultivated over large areas, for many years and in environments conducive to Pst epidemics (Johnson and Law, 1975).

Conclusions

The wide distribution and frequent occurrence of Pst epidemics in world wheat production zones will continue to yield focused effort in the development and deployment of economic control strategies. The increasing use of fungicide management for Pst control over the past decade has been driven by the availability of off‐patent generic products that have reduced chemical costs and thereby increased commercial economic benefit, even in production systems that have relatively low yield expectations. In addition, the emergence of new Pst pathotype lineages across large production regions, either through exotic incursion events or through local evolution to increased virulence, has evidently thwarted the capacity for breeding programmes to quickly respond with varieties that meet grower's demands for resistance, high yield and market quality. Although resistant varieties remain the goal, commercial industry imperatives will mean that alternative approaches, such as integrating fungicides and cultivation measures (including the regulation of plant date, crop nutrition, interplanting of crops and eradication of volunteer seedlings), may assume greater importance in the short to medium term. Specific management strategies in areas which function as pathogen inoculum sources and center of pathogenic diversity are considered to be the highest priority for sustainable stripe rust control.

In order to advance the development and distribution of resistant wheat cultivars to provide cost‐effective and environmentally acceptable disease control, research on Pst will continue to build on the large body of information already assembled for this important cereal pathogen. Molecular studies have assisted the identification of certain resistance genes that are likely to provide durable resistance. Efficient marker systems are available for these genes and should enable breeders to incorporate and select several durable genes in populations to build genetic foundations that stabilize and secure their germplasm against the uncertainties of Pst dynamics. Although gains in durable resistance are being made, it is essential that genetic diversity is encouraged through the identification and characterization of further durable sources for use in practical plant breeding. Seedling resistances will continue to be described and catalogued, but the application of these genes will centre around debates of stewardship that arise from concerns about the potential evolution and selection of new races and the means to minimize these effects using strategies ranging from the development of gene combinations to regional resistance gene deployment. The annotation and functional analysis of genes involved in the biology and pathogenicity of Pst by means of bioinformatics will provide new opportunities to understand the virulence variation in the pathogen and the mechanism of resistance in the host.

In parallel to host resistance, population studies in Pst will continue to focus on mechanisms underpinning pathogenic variability within and between hosts. An important area will be to evaluate the significance of apparent restricted sexual populations of Pst in certain regions and the role that the alternative Berberis hosts may play in generating variability and providing the opportunity for pathogen survival between cereal cropping seasons. Features of pathogen epidemiology, including mechanisms of survival between seasons, and interactions of disease onset and development in relation to variety and environment, remain relevant issues to disease control.

Acknowledgements

References