Breeding cereals for rust resistance in Australia




Rust diseases have caused significant losses to Australian cereal crops, and continue to pose a serious threat. Because Australian cereal crop yields are generally low, genetic resistance remains the most economical means of rust control. Resistant cultivars also contribute significantly to reducing over-summer rust survival. A policy of releasing only rust resistant wheats in northern New South Wales and Queensland has resulted in industry-wide protection from rust in this region for the past 40 years. The Australian Cereal Rust Control Program conducts annual pathogenicity surveys for all cereal rust pathogens, undertakes genetic research to identify and characterize new sources of resistance, and provides a germplasm screening and enhancement service to all Australian cereal breeding groups. These three activities are interdependent, and are closely integrated with particular emphasis on linking pathology and genetics to ensure breeding outcomes. Recent changes in the wheat rust pathogens, including the development of virulences for Yr17, Lr24, Lr37 and Sr38 resistance genes, and the introduction of a new pathotype of the wheat stripe rust pathogen, have provided new and significant challenges for wheat rust resistance breeding. Similar challenges exist in breeding barley and oats for rust resistance. Examples are discussed to illustrate the ways in which rust isolates are providing information that can be used in breeding for rust resistance. In future, as more markers linked to durable rust resistance sources become available, it is likely that the use of marker-assisted selection will become more common-place in rust resistance breeding.


Rust diseases have caused significant economic losses to the Australian cereal industry, with estimated losses in wheat production due to stem rust of £400 000 in 1903, £2 million in 1916 (Waterhouse, 1929), £7 million in 1947 (Butler, 1948) and AUD $200 to 300 million in 1973 in south eastern Australia (Watson & Butler, 1984). More recently, epidemics of stem rust and leaf rust in wheat crops in Western Australia (WA) in 1999 were estimated to have cost the grains industry about AUD $50 million (Hills et al., 1999).

Yields of Australian cereal crops are typically low; the average yield of wheat in Australia in 2003–04, for example, was 1·9 t ha−1 (Anon, 2004). For this reason, the most economical way to control cereal rust diseases in Australia is to develop and grow genetically resistant cultivars. Although rusts continue to impact on Australian cereal production, this approach has been very successful in reducing losses, particularly in wheat crops in the rust-prone region of northern New South Wales and Queensland where rust resistant wheat cultivars have provided industry-wide protection from epidemics since the 1960s. Brennan & Murray (1988) estimated that wheat rust control in Australia, primarily by breeding efforts, represented an annual saving of AUD $289 million to the grains industry.

Australian cereal crops are affected by 10 rust pathogens (Table 1). Although some barley genotypes are affected by a form of stripe rust that infects wild barley grass (Wellings et al., 2000), the barley stripe rust pathogen (Puccinia striiformis f. sp. hordei) has not been detected in Australia to date. The leaf rust pathogen of durum wheat (Puccinia sp. Group II Type A; Anikster et al., 1997) and the crown rust pathogen of barley (P. coronata var. hordei; Jin & Steffenson, 1999) have also not been detected in Australia. Only one cereal rust pathogen, P. hordei, is known to undergo sexual recombination in Australia.

Table 1.  Cereal rust pathogens present in Australia; diseases and cereal host ranges
Major hostRust diseaseCausal agentOther cereals that may be affected
  • a

    Formerly P. recondita f. sp. tritici.

  • b

    Stem rust on barley can be caused by P. graminis f. sp. tritici, P. graminis f. sp. secalis (Pgs), or a form of P. graminis known colloquially as the ‘scabrum rust’, which is regarded to be the result of somatic hybridization between Pgt and Pgs.

  • c

    P. hordei is the only cereal rust pathogen known to undergo sexual recombination in Australia.

  • d

    Barley stripe rust, caused by Puccinia striiformis f. sp. hordei, has not been recorded in Australasia.

WheatStem rustPuccinia graminis f. sp. triticiBarley, rye, triticale
Leaf rustP. triticinaaTriticale
Stripe rustP. striiformis f. sp. triticiTriticale
BarleyStem rustP. graminisbWheat, rye, triticale
Leaf rustP. hordeic
Barley grass stripe rustdP. striiformis‘BGYR’ 
OatsStem rustP. graminis f. sp. avenae
Crown rustP. coronata f. sp. avenae
RyeRye stem rustP. graminis f. sp. secalisBarley
Rye leaf rustP. recondita

The Australian Cereal Rust Control Program (ACRCP)

Long-term pathogenicity surveys of the wheat stem rust pathogen (Puccinia graminis f. sp. tritici) have clearly established that cereal rust pathogens migrate freely and rapidly throughout the Australian and New Zealand region, and that this region is largely isolated from other major cereal growing regions of the world (Luig, 1985). This is strong justification for a centralized national approach to resistance breeding. The concept of a national program was formalized in the early 1970s following a disastrous stem rust epidemic in South Australia, Victoria, and southern New South Wales (Watson & Butler, 1984). Since then, the national program has evolved to become the Australian Cereal Rust Control Program (ACRCP), and during this time has provided a service to all Australian cereal breeding groups. The program has received long-term support from the University of Sydney as a hosting organisation and from the grains industry via the (currently) Grains Research and Development Corporation (GRDC). The GRDC is a national organisation that plans and invests in research and development for the Australian grains industry. It is a statutory corporation that is funded jointly by grain growers, via a levy on production, and by the Australian Government, who match half of the grower contributions up to a maximum of 0·5% of the gross value of production.

In addition to long term industry support, the ACRCP has also benefited from close links with regional breeding groups and cereal pathologists. The service activities of the program are underpinned by targeted research and the training of postgraduate students. The program encompasses all cereal rust diseases in Australia, and has three main activities.

  • 1Pathogenicity surveys of the cereal rust pathogens. These surveys involve greenhouse characterization of rust isolates in samples collected from all cereal growing regions using genotypes carrying different resistance genes (‘differentials’). Surveys provide advance warning to growers by identifying new pathotypes before they reach levels likely to cause significant economic damage. Efforts to identify new sources of resistance (activity 2), to screen breeders lines, and to incorporate effective resistance into advanced lines nominated by cereal breeders (activity 3) rely on the rust isolates identified and characterized by the surveys and maintained in liquid nitrogen. Surveys of the wheat stem rust (Puccinia graminis f. sp. tritici; Pgt) and leaf rust (P. triticina) pathogens have been conducted continuously since 1921, and of the stripe rust pathogen (P. striiformis f. sp. tritici; Pst) since it first appeared in Australia in 1979. The systems used to designate pathotypes of the three wheat rust pathogens are detailed in Tables 2–4. Surveys for the oat crown rust pathogen (P. coronata f. sp. avenae; P. c. avenae), oat stem rust pathogen (P. graminis f. sp. avenae; P. g. avenae) and barley leaf rust pathogen (P. hordei), while not continuous, date back to 1925 and have been conducted regularly for much of the past 20 years.
  • 2Identification of new rust resistance sources. The efficient and effective exploitation of rust resistance is dependent upon ongoing searches to identify new resistance sources and genetic studies aimed at determining the number of genes involved, their genetic relationships, and field assessments of the level of protection afforded by such new resistances. This includes the use of classical genetics, cytogenetics, molecular cytogenetics and molecular genetics. New and potentially useful resistance genes are directed into the germplasm enhancement program to evaluate the level of protection they provide and also so that they can be introduced into adapted germplasm (activity number 3).
  • 3Germplasm screening and enhancement. All Australian cereal breeders are encouraged to submit germplasm to screen for rust response in artificially inoculated greenhouse and field tests. In recent years, wheat rust screening has included routine tests (two greenhouse seedling tests and a single adult plant field test to all three rust pathogens) of at least 40 000 lines and detailed testing of about 500 lines (up to 18 greenhouse seedling tests and replicated field tests at two sites). The germplasm enhancement activities involve the incorporation of effective sources of resistance by backcrossing into advanced lines chosen in consultation with partner breeding programs. The backcrossing involves an initial cross, then backcrossing to produce either BC3F1 or BC5F1 lines with rust resistance selection taking place in each generation from BC1 onwards. Once the final backcross is completed, the derivatives are selfed, harvested, and then space planted in the field for a second cycle of selfing. The progeny are then either seedling greenhouse (major gene resistance) or adult plant field (adult plant resistance; APR) rust tested to identify non-segregating resistant BC3F3 or BC5F3 lines for further evaluation by breeders.
Table 2.  Differential genotypes used to characterize pathogenicity of isolates of Puccinia triticina in Australia
SeriesGenotypeResistance gene(s)
  1. Pathotype designations include an international standard race designation, as outlined by Johnston & Browder (1966), and a suffix indicting virulence on the Australian differential series. For example, pathotype 104-1,2,3,(6),(7),11 +Lr37 is standard race 104 according to Johnston & Browder (1966), and is virulent for the Australian differential numbers 1 (Thew; Lr20), 2 (Gaza; Lr23), 3 (Spica; Lr14a), 11 (Exchange; Lr16) and Trident (Lr37). Partial virulence on Australian differential numbers 6 (Gatcher; Lr27 + Lr31) and 7 (Songlen; Lr17a) is also designated by parentheses enclosing the respective numbers.

International seriesTarsaLr1
MediterraneanLr2a, Lr3a
Australian series1. ThewLr20
2. GazaLr23
3. SpicaLr14a
4. Kenya 1483Lr15
5. Klein TitanLr3ka
6. GatcherLr27 + Lr31
7. SonglenLr17a
8. CS 2A/2MLr28
9. MildressLr26
10. EgretLr13
11. ExchangeLr16
12. HarrierLr17b
13. AgentLr24
Additional genotypesNorkaLr1 + Lr20
Table 3.  Differential genotypes used to characterize pathogenicity of isolates of Puccinia graminis f. sp. tritici in Australia
SeriesGenotypeResistance gene(s)
  1. Pathotype designations include an international standard race designation, as outlined by Stakman et al. (1962), and a suffix indicting virulence on the Australian differential series. For example, pathotype 34-1,2,7 +Sr38 is standard race 34 according to Stakman et al. (1962), and is virulent for the Australian differential numbers 1 (McMurachy; Sr6), 2 (Yalta; Sr11), 7 (Norka; Sr15) and Trident (Sr38).

International seriesRelianceSr5
Line SSr13,Sr17
Australian series1. McMurachySr6
2. YaltaSr11
3. W2402Sr7b,Sr9b
4. W1656Sr36
5. RenownSr7b,Sr17
6. MentanaSr8a
7. NorkaSr15
8. FestiguaySr30
9. TAF 2SrAgi
10. Entrelago de MontijoSrEm
11. Barleta BenvenutoSr8b
12. Coorong triticaleSr27
13. Satu triticaleSrSatu
Additional genotypesAgentSr24
Norin 40SrNorin40
Table 4.  Differential genotypes used to characterize pathogenicity of isolates of Puccinia striiformis f. sp. tritici in Australia
SeriesGenotypeResistance gene(s)
  1. Pathotype designations include an international code and a European code, as proposed by Johnson et al. (1972), and with additional Australian differentials (Wellings, 2007). The international and European codes are determined by adding decanery values corresponding to each differential rendered susceptible. For example, pathotype 134 E16 A+ is virulent on Lee, Heines Kolben and Clement (21 + 22 + 27 = 134), Compair (24 = 16, preceded by E to indicate ‘European’), and Avocet R (A+).

International seriesChinese 166Yr1
Heines KolbenYr2, Yr6
Vilmorin 23Yr3
Strubes DickkopfYrStrubes Dickkopf
Suwon 92/OmarYrSuwon 92/Omar
ClementYr2, Yr9
Triticum spelta albumYr5
European seriesHybrid 46Yr4
Reichersberg 42Yr7
Heines PekoYr2, Yr6
Nord DesprezYrNord Desprez
Carstens VYr32
Spaldings ProlificYrSpaldings Prolific
Heines VIIYr2, Yr25
Australian seriesAvocet RYrA

Since 2002, the ACRCP has also included formal and informal collaborative links with research groups in CSIRO Plant Industry (fine mapping and cloning of resistance genes in wheat; Ellis et al., 2007), CIMMYT Mexico (polygenic resistance to stripe rust and leaf rust in wheat; Singh et al., 2000), and the University of Adelaide (improving and developing new sources of rust resistance from alien species; Dundas et al., 2007).

Recent challenges in breeding cereals for rust resistance

Leaf rust of wheat in Western Australia

Leaf rust of wheat was uncommon in Western Australia during the 1970s and 1980s, and was not reported in that state from 1984 to 1989. It was, however, located in several crops during September 1990 in the south eastern region of the Western Australia wheatbelt (Esperance to Ravensthorpe). The pathotype (pt) present was identified as pt 104-1,2,3,(6),(7),11, first detected in eastern Australia in 1988 and believed to be a single step mutational derivative of pt 104-2,3,(6),(7),11 with virulence for resistance gene Lr20 (Park et al., 1995). The latter pathotype was first detected in Victoria, and detailed comparative studies of differences in pathogenicity and isozyme characteristics with pathotypes of P. triticina that prevailed in Australia at that time concluded that it originated from outside Australia (Park et al., 1995). The derivative pt 104-1,2,3,(6),(7),11 presumably spread to Western Australia from eastern Australia. The eastern and western Australian cereal growing regions are separated by about 1300 km of desert, and long-term pathogenicity surveys of wheat rust pathogens have provided clear evidence of inoculum exchange between the two regions, and although this occurs predominantly from west to east in the direction of prevailing winds, there are examples where the reverse has occurred (Luig, 1985), including the spread of pt 104-1,2,3,(6),(7),11.

Following its initial detection in Western Australia in 1990, pt 104-1,2,3,(6),(7),11 rapidly increased in frequency throughout the WA wheatbelt and in 1992 reached epidemic levels and some 100 000 to 120 000 ha of wheat were sprayed with fungicide (Park et al., 1995). From 1991 to 2001, 1104 samples of leaf rusted wheat were received from Western Australia, and of the 969 isolates that were pathotyped, all except one (pt 104-1,2,3,5,(6),(7),11, believed to be a mutant with added virulence for Lr3ka) were identified as pt 104-1,2,3,(6),(7),11 (Park RF, unpublished). Leaf rust was common in Western Australia in most years during this time, and reached epidemic levels again in 1999 when estimates of production losses due to leaf rust and stem rust were in the order of AUD $50 million (Hills et al., 1999).

Virulence for the resistance genes Yr17, Sr38 and Lr37

The rust resistance genes Yr17, Sr38 and Lr37 occur together in common wheat on a translocated segment derived from Triticum ventricosum (the ‘VPM’ resistance; Bariana & McIntosh, 1993). This rust resistance source has been incorporated into several Australian wheat cultivars, the first of which was Sunbri, released in northern New South Wales in 1990. To date, some 22 cultivars carrying the VPM resistance have been released in Australia.

Virulence for Yr17 was detected for the first time in eastern Australia (Narrabri; Fig. 1) in 1999, and the pathotype responsible, pt 104 E137 A- Yr17+ was thought to have originated from an existing pathotype via mutation (Wellings, 2007). Although this pathotype was subsequently detected each year up to 2005 from various locations throughout eastern Australia, it remained at low levels (Wellings, 2007). Of potentially greater concern was the detection of another pathotype with virulence for Yr17, 134 E16 A+ Yr17+, in southern New South Wales in 2006. This pathotype poses a greater threat because it combines virulence for Yr17 with Yr6, Yr7 and YrA (Wellings, 2007).

Figure 1.

Map of Australia showing states, territories and towns referred to in text.

Virulence for Sr38 was first detected in Western Australia in stem rusted samples of cv. Camm collected from the Esperance district in early November 2001 (RF Park & RL Loughman, unpublished data). The pathotype responsible, pt 34-1,2,7 +Sr38, was thought to have arisen via a mutation to virulence for Sr38 in pt 34-1,2,7. Pt 34-1,2,7 +Sr38 became well established in Western Australia during the 2002 cropping cycle and was subsequently detected in eastern Australia at Arno Bay (South Australia) in November 2003 and then in a summer nursery at Horsham (Victoria) in March 2004, providing another example of rust inoculum exchange from Western Australia to eastern Australia, presumably on prevailing winds. Pt 34-1,2,7, +Sr38 was detected in Queensland and in Tasmania during 2006 (RF Park, unpublished data).

Virulence for Lr37 was first detected in Western Australia in 2002 (RF Park, unpublished data). Like the stem rust pathotype virulent for Sr38, the Lr37-virulent leaf rust pathotype (104-1,2,3,(6),(7),11 +Lr37) most likely arose via mutation and was subsequently detected in eastern Australia in 2002. By the end of the 2004 season, this pathotype had been isolated from throughout the Western Australian wheatbelt, and also through much of the eastern wheatbelt as far north as Willow Tree in northern New South Wales (Fig. 1), providing a graphic example of how quickly rust pathogens can spread throughout Australia.

Virulence for resistance gene Lr24

The wheat cultivar Torres, the first to be released in Australia carrying resistance gene Lr24, was released in 1983. Gene Lr24 remained effective in Australia until October 2000 when a virulent pathotype was detected in South Australia. The new pathotype, 104-1,2,3,(6),(7),11,13, most likely arose via mutation in an existing pathotype, and was subsequently detected in southern New South Wales (Nov 2000), Victoria (March 2001), and Queensland (March 2001) (Park et al., 2002). Greenhouse seedling tests revealed that the new pathotype rendered 24 of 28 Australian wheat cultivars carrying Lr24 susceptible. Additional seedling resistance in four cultivars was attributed to the gene Lr13 (cvs Giles, Petrie and Sunsoft 98), or genes Lr17b or Lr13 (cv. Dennis), both of which were effective to the Lr24-virulent pathotype. Adult plant field tests of 17 of the seedling susceptible cultivars with the Lr24-virulent pathotype indicated that all were either moderately resistant to moderately susceptible or susceptible. Subsequent studies have shown that the APR in at least some of these cultivars (Cunningham, Goroke, Janz, Perouse and Sunco) is due to the presence of Lr34 (Singh et al., 2007).

The gene Lr24 remains important in Australia because it is still effective to all known pathotypes of P. triticina in Australia when combined with Lr13 (e.g. cv. Giles) and Lr37 (e.g. cv. QAL 2000), and also because the Lr24-virulent pathotype has not been detected in Western Australia. This resistance gene is also completely associated with the stem rust resistance gene Sr24 (McIntosh et al., 1995), which remains effective against all Australian isolates of Pgt.

Detection of wheat stripe rust in Western Australia

The first recording of stripe rust of wheat in Australia was in 1979, when it was found in Victoria (O’Brien et al., 1980). The disease spread rapidly throughout most of the eastern Australian wheat belt, but was not recorded in Western Australia until August 2002 when it was detected in the Newdegate Shire (Wellings et al., 2003). Analyses demonstrated the presence of a single pathotype (pt 134 E16 A+) that was distinct from eastern Australian Pst pathotypes not only in pathogenicity but also in AFLP phenotype, indicating a likely exotic origin (Wellings et al., 2003). The new pathotype was subsequently detected in eastern Australia (southern New South Wales and South Australia) in September 2003, and has been the dominant Pst pathotype in all Australian wheat regions surveyed since then (Wellings, 2007). While estimates of the cost of fungicidal control in 2003 were about AUD $43 million, a more severe epidemic developed in 2004 and an estimated AUD $90 million was spent on chemical control (CR Wellings, unpublished data).

Detailed studies of pathotype 134 E16 A+ demonstrated its virulence profile on specific seedling or major resistance genes did not pose any greater threat to Australian wheat cultivars. Despite this, many cultivars were noticeably more affected by this pathotype at later adult plant growth stages (Wellings & Bariana, 2005). Whilst the reason for this is not known, it is possible that this pathotype carries virulence for an uncharacterized APR gene common in current Australian wheat cultivars. Genetic work is currently underway to clarify this. Several sources of resistance, including the durable minor APR genes Yr18 and Yr29, remain effective against pt 134 E6 A+ and contribute to the stripe rust resistance of some Australian wheat cultivars.

Stripe rust of wild Hordeum species and barley

Studies of the host range of the wheat stripe rust pathogen Pst in Australia demonstrated that a range of grasses, including wild Hordeum species, were susceptible (Holmes & Dennis, 1985). Isolates of P. striiformis established from infected barley grass (Hordeum leporinum and H. glaucum) in annual pathogenicity surveys prior to 1998 were all identified as pathotypes of Pst that had been previously characterized in collections of P. striiformis from wheat (CR Wellings, unpublished data). Samples of P. striiformis collected from wild Hordeum species in 1998, mostly from southern NSW but also from other regions in eastern Australia, included isolates that were pathogenically distinct from Australian pathotypes of Pst in being avirulent for many of the stripe rust differential genotypes (Wellings et al., 2000). Given the pathogenic distinctiveness of these isolates from Pst, it was concluded that they represented a new formae specialis of P. striiformis (colloquially, Barley Grass Stripe Rust; BGYR) that had been introduced into Australia (Wellings et al., 2000). Evidence from DNA-based studies using three marker systems further demonstrated the distinctiveness of BGYR from Australian isolates of Pst, and also revealed genetic variability among isolates of BGYR collected in 1999, suggesting that more than one pathogen genotype was introduced into Australia (Keiper et al., 2003).

Although pathogenically distinct from the true barley stripe rust pathogen P. striiformis f. sp. hordei, the BGYR pathogen can infect certain barley genotypes and has been found in commercial crops of the Australian barley cv. Skiff and in experimental plots of advanced breeding lines. Despite some initial concern, BGYR has not caused economic losses in commercial crops of barley or wheat. Given the possibility of increased pathogenicity on barley and/or wheat via mutation or even somatic hybridization with Pst, the pathogen continues to be monitored closely in annual pathogenicity surveys.

Leaf rust of barley

Leaf rust of barley, caused by Puccinia hordei, occurs in all barley growing regions of Australia and has reached epidemic levels and caused yield reductions in some regions since at least 1927 (Waterhouse, 1927). In Queensland, epidemics occur on average once every four years with yield losses of up to 26% in commercial crops (Cotterill & Rees, 1993). Epidemics have also occurred in South Australia and Tasmania (Cotterill et al., 1991), and Western Australia (RL Loughman, personal communication). A move towards more intensive barley production and early and extended crop planting coupled with cultivar susceptibility are believed to have contributed to increased levels of leaf rust in Australia (Cotterill et al., 1994).

Puccinia hordei is the only cereal rust pathogen in Australia that undergoes sexual recombination. The alternate host, Ornithogalum umbellatum, was reported as widespread on the Yorke Peninsula in South Australia by Wallwork et al. (1992). These authors also found aecial infections on many plants near the township of Warooka, and identified five pathotypes of P. hordei among seven uredinial isolates established from aecia, indicating the importance of this host in generating pathogenic variability. A study of pathogenic variability among isolates of P. hordei collected between 1966 and 1990 found evidence for an increase in the frequency of virulence for the resistance gene Rph4 in Queensland during the 1980s, and it was suggested that this may have been a consequence of the widespread use of the cv. Grimmett, which carries this gene (Cotterill et al., 1995). Regular annual pathogenicity surveys of P. hordei in Australia began in 1992, and from 1992–2001, a significant shift was observed in the composition of populations across Australia. Virulence for the resistance gene Rph12, first detected in a single pathotype in Tasmania in 1991 (pt 4610P+; Cotterill et al., 1991), was subsequently detected in 1993 in South Australia, Victoria and southern New South Wales. By the end of 2001, eight pathotypes with virulence for Rph12 had been isolated and virulence for this gene was present in all Australian barley growing regions (Park, 2003). Two pathotypes virulent for Rph12, 5610P+ and 5453P–, built up rapidly in WA following their initial detections in 1997 and 2001, respectively (RF Park, unpublished data). The origins of these pathotypes are unknown. Both reached epidemic levels in the years following detection in southern coastal areas, especially in early sown crops of cvs Franklin, Gairdner and Baudin (RL Loughman, personal communication).

The development and spread of virulence for Rph12 from 1992 to 2001 in Australia is most likely the consequence of the release and cultivation of barley cultivars with this resistance gene. The first Australian barley cultivar with Rph12 was Franklin, released in 1989 in Tasmania and later cultivated in several mainland states including South Australia and Victoria. Following the release of Franklin, three further cultivars with Rph12 were released: Tallon (1991, Queensland), Lindwall (1997, Queensland) and Fitzgerald (1997, Western Australia).

Virulence has not been detected for the resistance genes Rph3, Rph7, Rph11 or Rph14 in Australian pathogenicity surveys, and tests have further shown the potential value of genes such as Rph15, Rph18 and APR in a range of European barley cultivars including Vada, Pompadour and Baronesse (RF Park, unpublished data). Backcrossing of the genes Rph7, Rph15 and Rph18 plus APR into key Australian barley genotypes is currently underway and it is hoped that the seedling genes will be deployed in combinations to reduce the chance of matching virulence developing in the pathogen.

Crown rust and stem rust of oats

Oats are grown in Australia for human (grain) and livestock (grain, forage, green fodder and hay) consumption. Crown rust and stem rust of oats are widespread, not only on commercial hexaploid (Avena sativa) and diploid (A. strigosa) oat crops, but also in extensive wild oat populations that comprise the species A. barbata (tetraploid, 2n = 28), A. fatua (hexaploid, 2n = 42) and A. ludoviciana (hexaploid, 2n = 28).

Pathogenicity surveys of P.c. avenae were first conducted in 1935 (Waterhouse, 1952), and although not continuous, data from the past 70 years have clearly established that Australian populations of this pathogen are diverse (Luig, 1985). The large populations of P.c. avenae that are supported by the extensive wild oat communities presumably provide many opportunities for the development of new rust genotypes through random mutation. Previous studies have shown that the composition of isolates of P.c. avenae originating from cultivated and wild oats in Queensland and New South Wales do not differ (Oates et al., 1983; Park et al., 2000), indicating the importance of both host systems in the epidemiology and population dynamics of P. c. avenae.

The only current oat cultivar in Australia that is resistant to P.c. avenae is Volta, a forage oat released in Queensland in 2003. The genetic basis of the seedling resistance in this cultivar is currently unknown. Ten oat cultivars with known or unknown seedling resistance genes to P. c. avenae were developed and released in Australia from 1991–2003 (Barcoo, Bettong, Cleanleaf, Culgoa, Graza 68, Gwydir, Moola, Nugene, Taipan and Warrego). All were regarded as resistant at the time of release but virulence corresponding to each was detected soon after. Virulence for cv. Cleanleaf was first detected in two pathotypes in 1995, and by 1999 a further four had been detected (Park et al., 2000). Following the initial detection, virulence for Cleanleaf increased rapidly in Queensland and northern New South Wales, with at least 40% of the isolates identified from 1996 to 1998 being virulent on this cultivar (Park et al., 2000). Furthermore, from 1996 to 1999 the frequency of isolates virulent on Cleanleaf among isolates of P. c. avenae obtained from cultivated oats and wild oats were very similar, clearly illustrating the close relationship between populations of P. c. avenae on these two host groups (Park et al., 2000).

Stem rust of oats is common in all oat growing regions of Australia and can be damaging in commercial oat crops. An oat stem rust epidemic in NSW in 1973 caused an estimated 10 to 35% total yield loss with losses up to 80% in some regions (Anon., 1975). In 2001, a severe stem rust epidemic in South Australia and Victoria caused severe yield and quality losses (PK Zwer, personal communication). As with P. c. avenae, pathogenicity surveys of P. g. avenae have shown considerable pathogenic variability and this is presumably at least partly related to the widespread occurrence and susceptibility of wild oats. The rust also occurs on the grass species Amphibromus neesii, Dactylis glomerata, Lamarckia aurea, Phalaris minor and Vulpia bromoides (Waterhouse, 1952; Luig & Watson, 1977). A comprehensive study of Australian oat cultivars made in the mid 1990s found limited variability with respect to stem rust resistance, and while the genes Pg-1, Pg-2, Pg-3, Pg-4, Pg-13 and Pg-a were postulated in some cultivars, most cultivars likely carried Pg-2 and Pg-4 (Adhikari et al., 2000). With the exception of Pg-a, none of these genes were effective to pathotypes that prevailed at that time (Adhikari et al., 2000). Virulence for Pg-a was detected in 1996 in Queensland and northern NSW (S Meldrum & JD Oates, unpublished data), and in the following year, the frequency of virulence increased in this region (Meldrum et al., 1998). With the detection of virulence for Pg-a, virulence had been recorded in Australia for all known seedling stem rust resistance genes in oats. The development and increase in frequency of virulence for the resistance gene Pg-a is probably related to the deployment and cultivation of cultivars carrying this gene. The first Australian cultivars to be deployed with Pg-a were Culgoa II and Nobby, both released in Queensland in 1991, after which five additional cultivars were released (Amby II, Barcoo, Cleanleaf, Condamine and Quoll). No current Australian oat cultivar is resistant to stem rust.

Studies of rust pathogen populations in breeding for resistance

Because of the isolation of the Australian continent from other cereal growing regions of the world, the long term surveys of pathogenic variability in Pgt and P. triticina in particular have provided rare insight into rust population dynamics and the processes that generate variability in asexually reproducing populations. Combined, the survey data strongly implicate periodic introduction of exotic isolates, single-step mutation, and more rarely, somatic hybridization, as the major determinants of cereal rust population structure in Australia. All three processes were observed in pathogenicity surveys of P. triticina between 1980 and 2005.

Pathotype 104-2,3,(6),(7),11 was first detected in Victoria in 1984, and was concluded to be an exotic incursion on the basis of pathogenic and isozymic differences to isolates of P. triticina endemic at that time (Park et al., 1995). Since 1984, at least 16 pathotypes considered to have originated via single-step mutation from 104-2,3,(6),(7),11 have been detected, with additional partial or full virulence for one or more of the resistance genes Lr2a, Lr3ka, Lr15, Lr17a, Lr17b, Lr20, Lr24, Lr26 and Lr37. The most important mutational derivatives from pt 104-2,3,(6),(7),11 have been pathotypes with virulence for Lr24 and Lr37. By 1990, either pt 104-2,3,(6),(7),11 or 104-1,2,3,(6),(7),11, a derivative with virulence for Lr20, were present in all wheat growing regions of Australia, and both had been detected in New Zealand. In annual surveys from 1990 to 2005, one or more of the pathotypes derived from pt 104-2,3,(6),(7),11 have dominated in all wheat growing regions of Australia (Park et al., 1995; RF Park, unpublished data).

A second pathotype regarded as having an exotic origin, pt 53-1,(6),(7),10,11, was first detected in Australia in 1984 after being initially detected in New Zealand in January 1981 (Luig et al., 1985). This pathotype was virulent for Lr13, a trait not previously detected in Australasia, and was able to infect several important wheat cultivars with Lr13 such as Egret and Banks. It remained confined largely to northern New South Wales and Queensland, and reached epidemic levels in some regions of the latter state during 1988. Given this distribution, it is interesting that it was isolated from several samples collected in Tasmania in 1997. A year later, samples collected from Tasmania comprised a variant of this pathotype with added virulence for Lr17b (pt 53-1,(6),(7),10,11,12), and this pathotype was subsequently detected in Victoria and SA during the 1998 season. Pt 53-1,(6),(7),10,11,12 combined virulence for Lr13 and Lr17b and caused significant levels of leaf rust in crops of several winter wheat cultivars carrying this gene combination (e.g. cvs Muchmore & Paterson) in the Western District of Victoria and in Tasmania (Park et al., 2000).

Pathotype 64-(6),(7),(10),11, first detected in northern New South Wales in 1990, most likely arose from somatic hybridization between pts 53-1,(6),(7),10,11 and 104-2,3,(6),(7),11 (Park et al., 1999). Comparative studies demonstrated that pt 64-(6),(7),(10),11 combined several pathogenic and isozymic features that prior to its detection, were only known in pts 104-2,3,(6),(7),11 and 53-1,(6),(7),10,11. This strongly suggested that it had arisen via somatic hybridization between isolates from these two pathotypes, and RAPD fingerprinting provided further evidence in support of this hypothesis (Park et al., 1999). Greenhouse pathogenicity tests demonstrated that pt 64-(6),(7),(10),11 combined virulence for Lr1 with partial virulence for Lr13. These studies further demonstrated susceptibility of the hybrid wheat cultivars Meteor and Pulsar, with which it was associated in the wheat belt. It was concluded that the susceptibility of these cultivars to pt 64-(6),(7),(10),11 most likely related to partial virulence for Lr13 in the rust and heterozygosity for Lr13 in the hosts. Incomplete dominance of host resistance and pathogen avirulence have been demonstrated for several corresponding gene pairs in the P. triticina : Triticum aestivum pathosystem (Kolmer & Dyck, 1994).

What can rust pathogens tell us about breeding for resistance?

An important contribution to resistance breeding made by pathogenicity surveys that is often overlooked and not fully appreciated is the provision of characterized rust isolates for use in identifying resistance in germplasm. A comprehensive collection of well characterized rust isolates, coupled with a basic understanding of the genetics of host : pathogen interactions, are powerful tools to resolve the identities and relationships between resistance genes, and in assessing the potential value of new resistance sources.

Rust isolates as ‘near isogenic lines’ in understanding rust resistance in cereals

Valuable preliminary information on the genetic basis of rust resistance in cereal germplasm can be obtained using multipathotype tests in which an array of rust cultures with known pathogenicity are used for gene postulation (Loegering et al., 1971). Australian pathogenicity surveys of the wheat rust pathogens have identified groups of closely related pathotypes that are considered to represent clonal lineages comprising step-wise mutants of pathotypes that differ for virulence/avirulence for single resistance genes. These pathotypes are the pathogen equivalent of the near isogenic cereal series that carry individual rust resistance genes in a common genetic background, and they are invaluable in multipathotype testing to postulate the identities of resistance genes in recognising new resistance genes.

Because of the pathogenic variability in P. c. avenae in Australia, it has been difficult to identify clonal lineages in populations of this pathogen. This, plus reports of at least 96 Pc loci conferring resistance ( and a lack of single gene reference stocks for many of the genes at these loci, have made it very difficult to identify Pc genes in germplasm via multipathotype testing. Indeed, the seedling resistances of many Australian oat cultivars, all of which have been overcome by matching virulence in P. c. avenae, are unknown.

Detailed studies of the pathotypes virulent on the 10 oat cultivars that were regarded as seedling resistant to P.c. avenae when released between 1991–2003 (Barcoo, Bettong, Cleanleaf, Culgoa, Graza 68, Gwydir, Moola, Nugene, Taipan and Warrego) demonstrated that they are pathogenically very similar and were likely derived via single-step mutations. The pathotypes have been characterized extensively on host stocks and in turn have been used to resolve the identities of the resistances present in the cultivars. Whilst some of the 10 resistant oat cultivars were regarded as having ‘new’ uncharacterized seedling resistances, it is now clear from detailed comparative multipathotype studies that most possess combinations of previously characterized genes. For example, cv. Cleanleaf was previously reported to carry Pc38, Pc39 and an uncharacterized resistance gene (Bonnett, 1996) that on the basis of multipathotype testing is now considered likely to be Pc52 (RF Park, unpublished data).

The pathotypes virulent on the 10 oat cultivars have also been invaluable in identifying seedling resistance genes present in other oat germplasm. Detailed multipathotype tests of 166 lines from the 1998 and 1999 Quaker oat nurseries demonstrated the presence of a range of resistance genes, and it was clear that some lines carried the same resistance present in cvs Bettong (42 entries), Gwydir (six entries), Nugene (one entry) and Warrego (four entries) (S Haque & RF Park, unpublished data). These studies also permitted the field identification of 12 nursery entries that lacked effective seedling resistance genes but possessed very high levels of APR to crown rust (Haque, 2004).

It is hoped that these closely related pathotypes will also assist in resolving the confusion surrounding many of the Pc genes described so far. Recently, seedling tests of known genetic stocks using a pathotype virulent for Pc94 and a series of isolates that included the putative parent of this pathotype have implicated the presence of this resistance gene in Avena strigosa accession CI 3815. This line was originally reported to carry Pc19 and Pc30 (Simons et al., 1959; Marshall & Myers, 1961), and more recently was reported to carry five tightly linked genes, designated Pc81–85 (Yu & Wise, 2000). The genetic relationships between Pc19, Pc30 and the Pc8185 complex are not known. However, the evidence from tests suggests that one of these genes and Pc94 are synonymous. Gene Pc94 was introgressed into hexaploid oats by Aung et al. (1996) from A. strigosa accession RL1697. Tests of RL1697 with the Pc94 virulent and avirulent P. c. avenae pathotypes would be a simple means of further testing this hypothesis.

Sustained genetic control of cereal rusts

Industry acceptance and compliance

Long term national pathogenicity surveys have established that the Australasian region is largely isolated from other cereal growing regions and that it comprises a single rust epidemiological unit. These features have allowed the implementation of a national program for rust resistance breeding, which has developed strategies based on genetics and epidemiology that have greatly reduced the risk of rust epidemics in wheat and, to a lesser extent, other cereals. The greatest impact of this approach has been achieved in wheat rust control in wheat in northern NSW and QLD, where growers have enjoyed largely rust-free wheat cultivation since the early 1960s. This is the most rust prone region of Australia, because a summer-dominant rainfall pattern can favour the establishment and growth of self-sown cereals (the ‘green bridge’) and the rust pathogens during the non-cropping phase. Industry ‘pull’, whereby authorities in the region have insisted on adherence to a policy of releasing only cultivars with resistance to all three rust diseases and of rapid withdrawal of susceptible cultivars, has been a vital ingredient in the success of this process.

A significant change in the structure and funding of Australian wheat breeding began about 10 years ago, with a shift from non-profit publicly funded breeding programs to privately funded commercially focused programs. A major challenge for future genetic control of rust diseases will be whether or not the industry self regulation that occurred when wheat breeding was publicly funded will continue in a commercial environment. Concurrent with the privatization of wheat breeding has been the development of a National Variety Trials (NVT) system and the establishment of Minimum Disease Standards (MDS) for the three rust diseases of wheat, with strong support from the grains industry. The NVT system tests lines that are close to commercial release with the aim of generating independent information on new releases for growers ( An agreed set of MDS for the three rust diseases was established in the late 1990s, for three agroecological zones (Eastern region, Queensland and northern NSW and all winter cultivars; Southern region, southern NSW, Victoria and South Australia; Western region, Western Australia), which comprised well characterized cultivars carrying the minimum acceptable standard of resistance for each rust disease based on perceived risk in each zone (Wallwork, 2007). The objective of the standards is to protect the industry from cultivars that produce large amounts of inoculum, and in so doing, protect deployed resistance genes by reducing the number of mutant pathotypes that develop (Wallwork, 2007). While there is no legal mechanism to prevent the release of a cultivar that does not meet MDS, growers will be able to base cultivar choice on independent information on whether or not a cultivar meets MDS via the NVT system.

Future approaches to rust control

Fungicidal control of cereal rust diseases has increased in Australia in recent years as a result of increased yields, improved application technology and cheaper generic fungicides. Whilst an important tool in combating these diseases, fungicides do not necessarily provide complete protection and are less effective in reducing the overall size of rust populations (and hence reducing the number of mutant rust genotypes). The non-cropping summer period of December to March is important in cereal rust epidemiology in Australia because it is hot and often dry and the rust pathogens must survive on the ‘green bridge’. Resistant cultivars produce a resistant ‘green bridge’ and are therefore important in reducing the over-summering of rust inoculum.

Johnson (1981) defined durable resistance as ‘resistance that has remained effective in a cultivar during its widespread cultivation for a long sequence of generations or a period of time, in an environment favourable to the disease’. The concept of durability does not make any implications about the genetic control, mechanism, degree of expression or race-specificity of resistance. Johnson in Jacobs & Parlevliet (1993) further stated that ‘it seems reasonable to argue that genetic complexity, presented by combining many genes each of small effect is more likely to achieve durable resistance, but this should not lead to the neglect of the opportunities presented by the increasing number of major genes implicated as playing an important role in durable resistance’.

Both monogenic ‘major gene’ and polygenic ‘minor gene’ resistances have been used successfully to control cereal rust diseases in Australia in the past. Considerable value has been obtained from single major gene resistances such as Lr24/Sr24 and Sr26, made possible by their targeted deployment only in regions where inoculum load is low. In these cases, close monitoring of rust populations coupled with a willingness to dis-adopt cultivars if they are rendered susceptible to rust, are vital if losses are to be avoided. There are, however many examples from the past 60 years of resistance gene ‘breakdowns’, resulting from the deployment of a cultivar with single gene resistance in a region with moderate to high rust inoculum levels.

Recent genetic studies of minor gene resistance in a range of Australian wheat cultivars has shown the presence of two (e.g. cvs Cook, Dollarbird, Janz, Pelsart; Gosal, 2000) to 3–4 (e.g. cvs Batavia, Goldmark, Giles, Sunland; Nazari, 2006) additive genes controlling APR to stripe rust, and two genes conferring APR to leaf rust (e.g. cvs Harrier and Cranbrook; Singh et al., 2001a). Experience over the past 30 years has clearly demonstrated the important role of APR genes such as Sr2 and Lr34/Yr18 and Lr46/Yr29 in imparting durable rust resistance in wheat. All three resistance sources have been utilized in Australian wheat cultivars (McIntosh et al., 1995; Bariana et al., 2007; Park, 2007; Singh et al., 2007), and robust DNA markers are now available for Sr2 (Hayden et al., 2004) and Lr34/Yr18 (Lagudah et al., 2006). Genetic studies have demonstrated the presence of other sources of minor gene resistance to both leaf rust and stripe rust in wheat (e.g. William et al., 2006). It is anticipated that as other important loci conferring durable minor gene resistance are characterized and tagged, marker assisted selection (MAS) will become more commonplace. Kuchel et al. (2007) demonstrated the value of applying MAS within early generation segregating populations in a breeding program to achieve maximum genetic gain at the lowest cost, using markers for Lr34/Yr18 and Lr46/Yr29 initially, and then markers for semi-dwarfing genes and desirable glutenin alleles. The use of such technologies will allow the incorporation of important genes like Sr2, Lr34/Yr18 and Lr46/Yr29 as ‘background’ resistance, to which other resistances can be added, as proposed by McIntosh (1988). While many publications have reported the presence of APR to leaf rust and stripe rust in spring wheat (e.g. Singh et al., 2000; Bariana et al., 2001) and winter wheat (Singh et al., 2001b; Pathan & Park, 2006; Pathan et al., 2007), there are few well characterized sources of APR to stem rust and success in breeding for resistance to this disease in the past has utilized mainly combinations of major genes. The occurrence of a new pathotype of stem rust with virulence for many of the known major genes for resistance in eastern Africa (Singh et al., 2006) stresses the need to direct attention towards finding and characterizing new sources of minor gene resistance to this pathogen.


The Australian Cereal Rust Control Program is supported financially by the Grains Research and Development Corporation, Australia. The contribution of all staff engaged in cereal rust research at The University of Sydney, past and present, is gratefully acknowledged.