THE DANIEL McALPINE MEMORIAL LECTURE 1985
Wheat Rust Resistance -- The Continuing Challenge
Introduction
Mr. Chairman, members of APPS. It is an honour to be invited to deliver the
fifth Daniel McAlpine Memorial Lecture at this first meeting of APPS to be held
in New Zealand.
We fail to be unmoved when we read of the many and varied achievements of
"the Father of Plant Pathology in Australia" and certain of his
contemporaries, including the wheat breeder, W.J. Farrer, with whom McAlpine had
close personal contact. Probably few are aware that McAlpine had a very
distinguished scientific (in Scotland) and teaching (Ormand College, Melbourne)
career before his appointment as Vegetable Pathologist with the Victorian
Department of Agriculture in 1890 "to attend to any disease that might form
the subject of enquiry". Fish (6) further stated "there is little
doubt that his appointment . . . was a result of the 1889 rust
epiphytotic". McAlpine participated in four of the five historic "Rust
in Wheat" Conferences held during the 1890's. Needless to say, the rusts of
Australia were an early challenge for him. By 1906, he had described 75 new
species of rust pathogens.
Today, we propose to discuss the development of current knowledge of
host-pathogen genetics in relation to the rust diseases of wheat. In the latter
part of the lecture, we will review a rust disease that is relatively new to our
geographic area, namely stripe rust of wheat.
Cereal rust problems are not new. The threat of rust was so important to the
Romans that they held a feast and made sacrifices on April 25 in order to
placate Rubigus, the Corn God. While we presume that similar events are no
longer commemorated, the threat of rust epidemics continues.
There are three rust diseases of wheat, viz., stem or black rust, leaf or brown
rust and stripe or yellow rust. Current methods of breeding rust resistant
wheats are largely dependent on a theoretical basis that has developed since the
mid-1800's. We propose to briefly discuss the various developments which
culminated in the gene-for-gene theory of host-pathogen genetics, and will
attempt to assess where this theory has taken us.
Landmarks of Wheat Rust Genetics
Our current knowledge of the biology of wheat rusts began with the formal
description of the heteroecious nature of cereal rust fungi by de Bary and
colleagues. However, French farmers had long recognised the benefits of barberry
eradication in reducing epidemics and yield losses due to stem rust in areas
where today rust incidence is low (12).
In the 1890's, Eriksson and colleagues - contemporaries of McAlpine and Farrer-
showed that the stem rust and stripe rust pathogens were specialized in ability
to attack different graminaceous species. About 25 years later, Stakman and
colleagues demonstrated a further dimension of pathogenic specialization within
formae speciales. Puccinia graminis triciti was divided into races, (or strains
or pathotypes) on the basis of ability to attack individual wheat genotypes
(17). In the 1920's, Craigie (4) discovered the role of pycnia in the sexual
cycle on barberry, the alternate host for P. graminis.
Thus the scene was set for the most significant development in host-pathogen
genetics when, in the 1940's and 1950's, Flor made concurrent studies of the
inheritance of reaction in the flax host and of the inheritance of pathogenicity
in the flax rust pathogen (5, 7s 13). He firstly showed that resistance in a
selected flax host was determined by a single dominant allele, and that
avirulence in Melampsora lini with respect to the particular flax resistance
gene was also inherited as a single dominant allele. Thus, incomparability
between host and pathogen occurred only in the presence of the host gene for
resistance and the pathogen gene for avirulence (Fig. 1). It should be noted
that this also established that resistance and susceptibility, and avirulence
and virulence, were allelic states. When two genes were studied jointly, it was
possible to demonstrate that each interacted only with its corresponding
counterpart (see Fig. 2). Moreover, the presence of only one corresponding host
resistance gene-pathogen avirulence gene pair was sufficient to produce an
incompatible interaction, irrespective of the genotypes at other corresponding
gene sites.
It should be remembered that the phenotypes (and often, genotypes) for both host
and pathogen are deduced from the disease phenotype. The interaction can be
compared to a lichen, a complex organism consisting of a fungus and an algae.
Hence the genetics of disease might be considered analogous to the genetics of a
lichen.
For genetics we must have words describing the character of interest and we must
have words describing the contrasting phenotypes we wish to examine (Fig. 3).
The gene-for-gene relationship has been demonstrated for various plant diseases
and pests (for examples, see (5)). Moreover, the types of data available allow
us to assume its application to other systems; for example, stripe rust of wheat
where there is no known sexual stage in the pathogen.
Allow us to restate the genetic rules that are comparable with Mendel's laws: 1
. Low infection type or incomparability is the consequence of interaction of a
host gene for low reaction (resistance) and the corresponding pathogen gene for
low pathogenicity (avirulence) i.e., LIT = LR:LP (Fig. 1). 2. When more than one
corresponding pair of low reaction and low pathogenicity genes are involved, the
low infection type that is expressed is as low as, or lower than, the lowest of
the single corresponding gene pair interactions, i.e., LIT 1 +2 @LIT 1 where LIT
1 <LIT 2 (Fig. 2). One example of a two-corresponding-gene-pair interaction
in wheat stem rust where increased incompatability occurs is Srl5Sr22:P15P22.
Experimentation
The above attributes of the gene-for-gene relationship are used in everyday
experimental designs (1). There are four main designs that vary with the extent
of knowledge of the genetics of host and pathogen (Table 1).
Design 1 applies to situations where no genetic information is available with
respect to either host or pathogen. A data matrix is generated from tests of an
array of host lines with an array of pathogen isolates. By inspection of rows
and columns, one can postulate hypothetical genotypes and can select
representative host lines and pathogen isolates for further study. Design 2 is
the basis for pathotype surveys. A set of genetically, or phenotypically,
distinct lines is chosen as testers for pathotyping unknown collections of the
pathogen. If the purpose of the survey is to relate pathogen variation to the
performance of commercial cultivars, then commercial cultivars, or stocks with
the genes possessed by commercial cultivars, must be used as the testers. Design
3 permits host materials to be tested with a selected group of distinctive
pathotypes. This permits postulation of host genotypes and, in a breeding
context, allows the selection of host lines most likely to extend the range of
host variation. Design 4 forms the basis for physiological and biochemical
experiments. Various workers have emphasised the significance of the quadratic
check (Fig. 1) in providing the essential experimental controls for fundamental
studies.
The genetics of host-pathogen interactions tell us that both the host allele for
resistance and the pathogen allele for avirulence produce active products. Only
a few days ago, I attended an Australian-U.S. Workshop on genetic engineering in
plants. I believe there was a consensus of opinion indicating that the time is
ripe for someone to clone a resistance gene (or a pathogen avirulence gene), to
establish its DNA base sequence, to isolate or synthesise the gene product, and
to transfer DNA possessing a resistance gene from a resistant host to a
susceptible host, either within a host species or between related host species.
It is most gratifying that the experimental systems being used by molecular
geneticists are precisely those predicted by the gene-for-gene relationship.
Rust Resistant Cultivare in Agriculture
Our laboratory at Castle Hill is committed to the development of rust resistant wheats for Australia. For this, a multidisciplinary approach is essential in order to combine rust resistance with the many other criteria needed in a modern wheat cultivar that is to be sold into a competitive international market. In order to achieve rust resistance, we must be the wearers of several hats: as geneticists we are interested in the inheritance of phenotypic contrasts; we often make special crosses for this, as pathologists we must ensure that resistance sources provide adequate protection at critical stages of epidemics, as breeders we require simple, fast and lowcost methods for screening and selection; we must be able to combine resistance with the other attributes required in a cultivar, as agronomists we must be able to introduce and recommend the resistant cultivar to agriculture, as extension workers we must provide information to farmers enabling them to assess risk and to take management decisions. The information must be relevant to current pathotypes and should provide an adequate
Fig. 1. Australasian Plant Pathology Vol. 15 (1) 1986
description of expected cultivar responses. Our laboratory has recently
adopted the principles of listing recommended cultivars in genetic diversity
groups and in one of four disease response groups. In rust terms, response
groups 1,2,3 and 4 equate with resistant, moderately resistant, moderately
susceptible and susceptible.
Table 1. Experimental designs for genotypes used in host-pathogen genetics.
Design Host Pathogen
1. Unknown Unknown
2. Known Unknown
3. Unknown Known
4. Known Known
It is not difficult to breed for resistance. The main problem in respect of
rust, and certain other diseases, is that pathogens acquire the ability to
neutralize the resistances with which they are challenged.
Australasia forms a geographic region with respect to variation in cereal rust
pathogens. New pathotypes arise (20) as a consequence of introduction of
inoculum to a particular area: Australasia forms a unique geographical area for
plant pathogens and insect pests. Nevertheless, distinctive new rust pathotypes
- indeed, new pathogens among which P. striiformis tritici must be included -
may be introduced from time to time (23). Within the geographical area,
air-borne re-distributions of pathotypes usually reflect the directions of
predominant weather patterns. For example, pathotypes occurring in Western
Australia are soon found in the east and in New Zealand. On the other hand,
those occurring in eastern Australia only slowly find their way to W.A., and the
occurrence in eastern Australia of pathotypes previously unique to New Zealand,
is rare.
Sexual hybridization: This is not important in Australasia.
Asexual hybridization: While this appears to be an infrequent event, it is
believed to have contributed to at least one important group of strains
attacking wheat (3v 21) and to putative hybrids between certain formae speciales
(2).
Mutation: Mutations are the most obvious events contributing to agriculturally
important variation in rust fungi in Australasia. Examples of recent mutational
changes in two groups of P. graminis tritici pathotypes are shown in Fig. 4. In
1984, there were two limited, but different, stem rust epidemics in Queensland.
The first involved Oxiey wheat and the high inoculum levels that developed on
that cultivar probably contributed to the occurrence of a new pathotype on
cuitivar Cook; the second epidemic involved Satu triticale which had been
recommended as a replacement for the previously susceptible cultivar Coorong
(15).
Progressive increases in virulence: Longterm studies at Castle Hill have
shown that differences between avirulent and virulent pathogen isolates with
respect to a particular host line carrying a single gene for resistance are not
always bimorphic and clear-cut (22). As many as five distinctive phenotypes have
been distinguished. Neither the genetic basis for this variation, nor its
significance in pathogen evolution is understood.
Disease Control
Plant disease control strategies are directed at: - reducing the probability
of epidemics - reducing the magnitude of losses There is no doubt that the
probability of epidemics can be reduced with resistant cultivars; this has been
clearly demonstrated in the northern wheat areas of Australia where there has
been no major stern rust epidemic for 30 years, an area where, previously, the
probability of a stem rust epidemic was about one year in four. The probability
of epidemics can also be reduced by adopting procedures that reduce carryover
inoculum, and this may be a community problem since both farms and public areas
such as roads and railway lines can be involved.
The magnitude of losses is reduced by resistant cultivars, but especially by the
use of genetically diverse resistances so that failure of one resistance source
does not have excessively large affects. Extreme levels of susceptibility
"rust suckers" - should be avoided, either as
Fig. 2. Australasian Plant Pathology Vol. 15 (1) 1986
cultivars or as genetic backgrounds for a breeding program based on backcrossing. Specified minimum disease standards before cultivar recommendation in some countries takes account of knowledge that some susceptible cultivars are far more susceptible than others.
Resistance
In broadest terms, two types of resistance have been contrasted, but there
are no genetic criteria that clearly distinguish them. Specific host resistance
is dependent on the concurrent presence of the corresponding gene(s) for
aviruience in the pathogen population. Several features are said to warn that
currently effective specific resistance genes will prove transient; these
include:
- Simple inheritance
- Seedling-stage effectiveness
- Hypersensitivity
On the other hand, non-specific resistance has the contrasting features. Most of
all, non-specific resistance will be durable, but to demonstrate durability, the
resistance source must be widely tested over area and time (g).
Hence our recipe for the prevention of widespread losses as a consequence of
rust epidemics is -
- Avoidance of ultra-susceptibility
- Genetic diversity of resistance, either between or within crops
- Use of geneticaily complex resistances
- Use of durable resistance
Stripe Rust
Wheat stripe rust was first found in southeastern Australia in October, 1979. When first reported, it was already widespread, but crop surveys indicated that the outbreak was centred around Chariton in north-central Victoria. The initial outbreak revealed certain significant features. Firstly, crop losses in susceptible cultivars such as Zenith - then the leading cultivar in Victoria - were as high as 50-60%. Losses in less susceptible wheats such as Egret, Halberd and Condor were considerably less. Secondly, uredospores moved over relatively long distances. This was evident not only in 1979, if we assume that as the year of introduction, but again in 1980, when stripe rust appeared in New Zealand, apparently having been windborne from Australia.
When it first appeared, experience and knowledge of this disease were
superficial. No suitable temperature-controlled facilities for infection and
incubation were available. Moreover, the possibility that the disease might not
survive the dry summers put a necessary constraint upon study, especially in
laboratories located in wheatgrowing areas. The first preparations for research
came with a recommendation by the National Wheat Rust Control Committee that the
University of Sydney make special application to Wheat Industry Research Council
for funds. Support for a greenhouse facility was provided from reserve funds,
and C.R. Wellings was seconded to the program from the N.S.W. Department of
Agriculture.
A further recommendation by the Committee was that it would be consistent with
the other wheat rust diseases to adopt the American name of stripe rust, rather
than the European name, yellow rust. Stripe rust was the adopted name throughout
Australia and New Zealand.
Pathotype Analysis
Using the International and European sets of host differentials (10) obtained
from R. Johnson, P.B.I., Cambridge, the initial P.striiformis tritici pathotype
in Australia was identified as 104 E137. During the late 1970's, pathotype 104
E137 was present in southern and central Europe. We therefore assume that the
pathogen was transported to Australia by man, either on his person or his goods.
During its short history in this region, four single-step mutational variants
have been identified in Australia, and another has been found in New Zealand
(Fig. 5). Clearly, the pathogen has maintained its reputation for variability,
despite the absence of a sexual reproductive phase. Although temperatures during
the Australian wheat-growing season, i.e., from May until November, are ideal
for infection and spread of stripe rust, its greatest barrier to survival is the
dry summers. However, experience has shown that the disease does survive at low
levels and apparently at more-or-less random locations. Unfortunately, it has
not been possible to find infections during summer. While several grasses, as
well as barley and triticale, may become infected, survival almost certainly
occurs on self-sown wheat.
Stripe Rust Control
John S. Brown and colleagues at Crops Research Institute, Horsham, have
studied crop loss and chemical control. They have produced a model suggesting
that crop losses are directly related to the amount of disease 2-3 weeks after
flowering.
Table 2. Responses of Australian wheat cultivars to P. striiformis tritici
pathotype 104 E137A+i based on results from Disease Progress Nurseries and field
reports.
Response
Group Cultivar
1 Banks, Bass, Bindawarral, Cook, Corelial, Cranbrook3, Hartog 1 2@ Jacupl,
Milingl, Miliewal, Oxiey', Quarrion, Sunkota 2 , Takaril,
Vascol.
2. Blade, Cocamba, Condor, Festiguay, Gatcher 2 4 , Gutha, Kite, Matong,
Meering, Osprey, Sundor, Suneca, Suneig, Sunstar, Torres, Vufcan.
3. Egret, Flinders, Gamenya, Dagger, Halberd, Harrier, Hyden, King, Katyil,
Kewell, Machete, Madden, Mokoan, Olympic, Songlen, Warimba, Warigal, Wialki,
Wyuna.
4. Aroona, Avocet, Bayonet, Bodailin, Eradu, lsis, Lance, Teal, Tincurrin,
Zenith.
1 Yr6.
2 Yr7.
3 Unknown seedling resistance.
4 Genetically heterogeneous for indicated gene.
While chemical control of stripe rust is very effective, the relatively low
wheat yields in Australia will usually limit applications to a single foliar
spray. In addition, seed dressings give several weeks of post-emergent
protection. The farmer must, therefore, have access to reliable information on
expected cultivar responses and anticipated losses. Furthermore, he must be
alerted as soon as possible in the event of pathotype changes, even though these
are not always easily confirmed.
The good news for breeders is the wealth of genetic resistance to stripe rust.
The first impression one gains from a stripe rust disease nursery is the
continuous range of host responses covering a wide array of germplasm. In
addition, many Australian wheats show some resistance. Part of this undoubtedly
reflects the widespread use of CIMMYT germplasm, especially in eastern
Australia. Interestingly, stripe rust has not become a problem in South
Australia and Western Australia, despite the significantly more susceptible
cultivars.
For convenience, the first subdivision of resistance types are those occurring
at the seedling stage and effective for the entire growth cycle. The second
subdivision includes the postseedling types which become effective at various
growth stages and may be influenced by temperature. However, under Australian
conditions, resistance may not occur early enough to prevent some damage.
Because of variable adult plant responses, we have directed considerable effort
at placing cultivars into response groups (Table 2).
Implications for Resistance Breeding
In New South Wales in particular, there are increasing demands for wheats
with stronger winter growth habit, permitting earlier and more flexible sowing,
and possibly higher yields as a consequence. The implications of this in
relation to rust are that the oversummer survival period for the pathogen will
be shortened and there will be a longer growing season for development of
epidemics. To compensate, it may be essential to have more effective resistance
in cultivars designated for early sowing.
How do we obtain that resistance? We can try seedling resistance either as
single genes, or as gene combinations, but be warned, these genes may have
short-term effectiveness.
we can use post-seedling resistances. Again, various sources of this kind of
resistance are highly specific whereas other sources have proved durable. The
problem is how to distinguish between them, especially in the short term.
In addition to the pragmatic approach of using whatever is currently available,
we at Castle Hill, are exploring two breeding approaches based on overseas
experience. Studies in the U.S. (8@l 1916) and U.K. (19) suggest that improved
levels of resistance can be obtained from intercrosses among moderately
resistant and moderately susceptible wheats. Since such transgressive
segregation to stripe rust occurs fairly frequently,
Australian wheats, established sources of durable resistance. Unfortunately,
most sources are poorly adapted to Australian wheat-growing conditions, and are
red seeded and stem rust susceptible.
For the future, there are three immediate areas requiring more information.
Firstly, we need to establish how and where oversummering occurs. Secondly, we
need to assess seed treatment as a
Fig. 4. Australasian Plant Pathology Vol. 15 (1) 1986
Fig. 5. Australasian Plant Pathology Vol. 15 (1) 1986
it seems reasonable to expect it to occur in intercrosses of adapted
Australian cultivars. If it occurs, such resistance should be determined by
additive gene effects, and therefore unlikely to be neutralized as a consequence
of a single mutational event in the pathogen. The second approach is to
transfer., by backcrossing to means of controlling early infection and to
develop firmer guidelines for foliar sprays. Thirdly, we need to refine our
pathotype surveys in order to more closely monitor adult resistances; currently,
only seedling resistances are being monitored.
Conclusion
Throughout this presentation, we have attempted to emphasise the
multi-disciplinary problems involved in the study of rust resistance, and in the
exploitation of resistance in agriculture. Whereas pathologists such as de Bary,
McAlpine, Cobb, Stakman and Flor laid the foundations for host-pathogen
genetics, many of the agriculturally significant contributions came from
breeder/pathologists including Farrer, Waterhouse, Watson, Caldwell and Borlaug.
Today, there is a more-than-ever need for a multi-disciplinary approach
involving genetics, pathology and breeding. We believe we are now at the
beginning of the most exciting stage in the history of plant pathology. The next
great advance will come with the DNA-base sequencing of resistance (and
avirulence) genes, with a consequent understanding of what they do and how they
do it. Most of all, we should have increased knowledge of how resistance genes
might be manipulated or engineered in our constant efforts to keep ahead of
rapidly evolving pathogens.
Finally, Mr. Chairman, allow us to express our gratitude to all members of the
Castle Hill group who have contributed in various ways to wheat rust research '
Our thanks go to John S. Brown for supplying data and reports from studies in
Victoria. In addition, we acknowledge the long-term support that has been
provided by Wheat Industry Research Council.
References