Part I New pathotypes of wheat leaf rust and Part II Adult plant resistance

Take home messages

• Rust pathogens spread freely and rapidly through the Australasian region. While this is predominantly in a west-to east direction, recent years have seen two examples of east-to-west transport.
• Monitor for the presence of the green bridge, and if present, make sure it is destroyed at least 4 weeks before crops are sown, either by heavy grazing or herbicides.
• Warm, moist autumn conditions favour the development of leaf rust.
• Monitor crops of vulnerable varieties for leaf rust in 2016 and send samples for pathotype analysis to the Australian Rust Survey. This service is free to all, and is funded by the grower levy paid to the Grains Research and Development Corporation. 
• The identification of rust pathotypes involves greenhouse tests in which seedlings of indicator varieties are infected, and takes about 3 weeks. These tests are increasingly being supplemented with DNA-tests that are much quicker (less than 48 hours). The DNA tests provide useful basic information but are nowhere near powerful enough to identify pathotypes. 
• Genetic resistance to rust in cereals delivers significant benefit to Australian grain growers, estimated at $1.1 billion annually with wheat alone, and remains the basis of rust control.
• Minimum disease standards remain important for industry-wide benefit from genetic resistance.

New pathotypes of wheat leaf rust:  potential impacts and what to look for 

Australian wheat crops are infected by 3 different rust pathogens: stem rust (caused by Puccinia graminis f. sp. tritici), stripe rust (caused by Puccinia striiforimis f. sp. tritici), and leaf rust (caused by Puccinia triticina).

What is a rust pathotype?

Many people who have an interest in cereal production would have heard the term “pathotype” (pt., aka “races” or “strains”). Pathotypes are variants within a pathogen that differ in their ability to overcome rust resistance genes in cultivars. A good recent example of this concerns stripe rust and the wheat cultivar Mace. Like many current wheat varieties grown in WA, Mace carries the stripe rust resistance gene Yr17, a gene that is expressed at all growth stages (often referred to as seedling resistance genes, major resistance genes, all stage resistance genes; see below). While Mace is resistant to the “WA stripe rust pathotype”, first detected in 2002, the resistance provided by Yr17 was overcome in eastern Australia by a new pathotype, 134 E16 A+ Yr17+, first detected in 2006. To date, the latter Mace-virulent pathotype has not been detected in WA. For this reason Mace is regarded as susceptible to stripe rust in eastern Australia, and resistant to stripe rust in WA.

Thirteen pathotypes of wheat leaf rust have been detected in north eastern Australia since 2000, of which six have been common in recent years (Table 1).

Rust pathotype surveillance

The existence of rust pathotypes was first shown in the early 1900s in the USA. Not long after, Australian annual rust surveys were initiated at the University of Sydney, and continue to this day at the University’s Plant Breeding Institute (PBI). The identification of rust pathotypes at the PBI is a free service that is open to anyone who would like to submit a sample for analysis. Directions on how to do so are provided at the end of this paper. Following this procedure is vital if the viability of a rust isolate is to be ensured.

Pathotype identification involves infecting seedlings of a set of cereal varieties, each carrying a different rust resistance gene, with a field collected sample of rust. The ability or inability of the rust isolate to overcome the resistance gene in each variety allows the pathotype or pathotypes present to be identified. These tests take about 3 to 4 weeks to complete, and if a new pathotype is suspected, often a longer time is needed to confirm this. The pathotype identification work at PBI is increasingly being supplemented by DNA profiling, which is comparatively quicker and may only take several days. However, while providing important information and a means by which exotic rust incursions can be recognised rapidly, as yet, DNA profiling is nowhere near powerful enough to identify individual pathotypes.

The long-term studies of pathogenic variability of rust pathogens conducted at PBI have clearly established that Australia and New Zealand comprise a single rust epidemiological unit, within which rusts migrate freely and rapidly. This is why a nationally coordinated approach to the genetic control of cereal rusts (i.e. the Australian Cereal Rust Control Program) is fundamental to success.

The annual surveys of rust variability carried out at PBI have and continue to form the basis of all gene-based rust control efforts. They monitor the effectiveness of rust resistance genes in commercial cultivars; determine the implications of new rust pathotypes in the rust responses of current cereal cultivars; facilitate the discovery and introduction of new resistance genes into locally adapted germplasm; and allow pre-emptive resistance breeding.

Table 1. Current common wheat leaf rust pathotypes detected in north eastern Australia

Recent changes in the wheat leaf rust pathogen in eastern Australia

A new pathotype of the wheat leaf rust pathogen, Puccinia triticina, was detected in a sample of leaf rust collected from a crop of the wheat cultivar SQP Revenue at South Bool Lagoon (South Australia) in mid-August 2014. The new pathotype, 104-1,3,4,6,7,8,10,12 +Lr37, was considered to be an exotic incursion based on its unique virulence profile and SSR fingerprint. This pathotype is the 12^th documented incursion of an exotic wheat rust pathogen since Australia-wide cereal rust surveys conducted by University of Sydney staff began in 1922.

Following its initial detection in SA, pt. 104-1,3,4,6,7,8,10,12 +Lr37 spread rapidly throughout much of the eastern Australian wheat belt and in late September 2015 it was identified in samples of leaf rusted wheat collected from four separate locations in the northern region of the WA wheat belt.

Pt. 104-1,3,4,6,7,8,10,12 +Lr37 carries virulence for the resistance genes Lr27+Lr31, and the adult plant resistance (APR) gene Lr12, and combines this with virulence for Lr13 and Lr37. All four resistances occur in Australian wheat varieties, and consequently this pathotype has resulted in increased leaf rust susceptibility in some varieties.

Of the 37 varieties for which detailed information is available, the leaf rust responses of 31 are not expected to change (Table 2). The remaining six carry resistance genes either singly or in combination that prior to the detection of the new pathotype would have provided some protection against leaf rust. While all of these varieties are now more susceptible to leaf rust, it is very fortunate that all except Mitch and Wallup carry a level of residual resistance due to the presence of uncharacterised APR. Growers of these varieties are nonetheless advised to monitor crops for the presence of leaf rust.

The leaf rust responses of the newer varieties B53, Buchanan, Flanker, Kiora and Mansfield are currently not well known, and further data will be collected during the 2016 cropping cycle.

If any rust is found on any cereal crop, it can be sent to the Australian Rust Survey (see below), where it will be analysed and the sender will be notified of the results. This is a free service, and its success in establishing the distribution and occurrence of known rust pathotypes, and in detecting new rust pathotypes, depends entirely on the collection and submission of samples. 

Table 2. Leaf rust response and genotype for wheat varieties grown in north-eastern Australia^a

^aFor full genotypes (i.e. stem rust, stripe rust and leaf rust), see Cereal Rust Report 2016 14(4) [http://sydney.edu.au/agriculture/plant_breeding_institute/cereal_rust/reports_forms.shtml] 

^bGenes in bold font are effective against common pathotypes of the leaf rust pathogen

Pathotype surveys and rust control

To have maximum impact in disease control, surveys of pathogenic variability in rust pathogens must be closely integrated with the development and management of new wheat cultivars. Where this has been practiced, surveys have provided both information and pathogen isolates that have underpinned rust control efforts, from gene discovery to post-release management of resistance resources. Information generated by pathotype surveys has been used to devise breeding strategies, inform selection of the most relevant isolates for use in screening and breeding, define the distribution of virulence and virulence combinations, allow predictions of the effectiveness/ineffectiveness of resistance genes, and issue advance warning to growers by identifying new pathotypes that overcome the resistance of cultivars before they reach levels likely to cause significant economic damage.

Maintaining and improving current levels of rust control

It has been estimated that 50% of the cost of plant improvement involves breeding to maintain current yield and quality levels to meet the challenges of degrading growing environments and evolving pathotypes of major pathogens (“maintenance breeding”). Protecting the ca. $1 billion savings to the Australian wheat industry from resistance breeding and reducing the current impact of rust diseases will only be possible if resistance remains a priority in breeding programs, and if the wheat industry as a whole continues to support genetic approaches to rust control. 

Adult plant resistance and rust management decision making

Many people in the cereals industry would be familiar with the expression that a variety’s disease resistance has ‘broken down’. This expression can be misleading because it suggests that the variety itself has changed in some way. However, the shift in a variety’s response to rust is actually caused by a change in the pathogen that causes the disease. This is why monitoring rust populations for new pathotypes is critical to informing knowledge of how a variety’s resistance stacks up.

The emergence of a new rust pathotype can result in a resistant variety becoming more susceptible to rust. Because this shift is often subtle, describing the change in a variety to a new rust pathotype accurately can be difficult.

Changes in a variety’s response to new pathotypes are influenced by the nature and number of genes that confer resistance to the disease. Such resistance genes protect against the disease either at all growth stages, which is called all stage resistance (ASR; also referred to as ‘seedling’ or ‘major’ resistance), or at adult plant growth stages only, which is called adult plant resistance (APR; also referred to as minor gene resistance).  

Genes that confer ASR usually provide very high levels of protection against rust, while those conferring APR usually provide moderate levels of protection. A variety may carry one or both gene types, resulting in different effects on resistance levels.

Where a variety only carries an ASR gene, and this is overcome by a new rust pathotype, its resistance rating may change from highly resistant to highly susceptible.

There are many examples of such changes in a variety’s resistance levels – known as the ‘bust’ part of what is known as the ‘boom and bust cycle’. One of the first examples of this shift was recorded in the Eureka wheat variety’s resistance to stem rust. Eureka was highly resistant to stem rust when it was released in 1938. However, because this variety only has one ASR gene (Sr6) to protect it against stem rust, it became highly susceptible to the disease when this single gene was overcome by a new rust pathotype in 1942. Similarly, the stripe rust resistance rating of Mace  was downgraded from highly resistant to very susceptible because it only has one ASR gene (Yr17), which was overcome by a new pathotype in eastern Australia. However, in other grain growing regions such as Western Australia, Mace remains highly resistant to stripe rust because its single ASR gene has not been overcome.

Adding another dimension of complexity are the many wheat varieties that carry a combination of ASR and APR genes. Having both these genes means a pathotypic change can result in a slight increase in susceptibility that occurs when the ASR gene is overcome by a new pathotype, but the APR gene is still effective in providing ‘back-up’ resistance .

Field testing is the only reliable way to determine the levels of back-up resistance provided by the APR gene. For example, the full impact of the new wheat leaf rust pt. 104-1,3,4,6,7,8,10,12 +Lr37 will not be known until further field tests are completed this year.

While many years of painstaking genetic research has led to a sound understanding of ASR genes, intensive genetic analyses of APR genes began only about 20 years ago. Consequently, information about the APR genes in Australian wheat varieties is incomplete, and varietal information on rust response such as that which appears in the University of Sydney’s Cereal Rust Update reports (see:  http://sydney.edu.au/agriculture/plant_breeding_institute/cereal_rust/reports_forms.shtml) has partial information only. The rust response and rust genotype (i.e. which rust resistance genes are present) of varieties that are currently grown in north eastern Australia are provided in Table 2. Where a variety is rated as having useful resistance (i.e. either: R, MR, MR-MS), and does not carry an effective ASR gene, the resistance present must be due to APR. For example, from Table 2:

• Sentinel carries the ASR gene Lr26, which is not effective to currently prevailing leaf rust pathotypes (in the table, the ineffectiveness of Lr26 is indicated by “Lr26” not being in bold font). It does however carry the APR gene Lr34. This variety is rated as highly resistant to leaf rust (R), which is due to the APR.
• Gazelle carries the ASR genes Lr24 and Lr37, which again are not effective against currently prevailing pathotypes. This variety is rated as Moderately Resistant (MR), which must be due to APR. The genetic basis of this APR is, however, unknown (‘uncharacterised’).
• Note that although the variety Dart  carries the APR gene Lr34, it is rated as being highly susceptible to leaf rust (S-VS). This is because some APR genes on their own do not provide strong levels of resistance (and is why they are sometimes referred to as ‘minor genes’, or ‘genes of minor effect’).

Acknowledgements

The research undertaken as part of this project is made possible by the significant contributions of growers through both trial cooperation and the support of the GRDC, the author would like to thank them for their continued support.

Contact details

Robert F. Park
The University of Sydney
Mob: 0414 430 341
Email: robert.park@sydney.edu.au