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

Abstract

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. dicoccoides Korn) 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.

Keywords: genes for resistance; infection procedure; life cycle; molecular aspect; population biology.

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.

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 et al., 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.

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.

Figure 4

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

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.