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© 2011 Plant Management Network.
Accepted for publication 5 April 2011. Published 20 May 2011.


A New Pathogenic Race of Tilletia caries Possessing the Broadest Virulence Spectrum of Known Races


Janet B. Matanguihan and Stephen S. Jones, Mount Vernon Research and Extension Center, Washington State University, Mount Vernon, WA 98273


Corresponding author: Stephen S. Jones. joness@wsu.edu


Matanguihan, J. B., and Jones, S. S. 2011. A new pathogenic race of Tilletia caries possessing the broadest virulence spectrum of known races. Online. Plant Health Progress doi:10.1094/PHP-2010-0520-01-RS.


Abstract

Common bunt, caused by the fungi Tilletia caries and T. laevis, is one of the most destructive seedborne diseases of wheat. In conventional agriculture, common bunt is managed almost exclusively with chemical seed treatments. However, in organic farming, synthetic chemicals are prohibited. Because of this, there has been a resurgence of this disease in organic wheat. In order to maintain high yields and excellent seed quality, organic growers must rely heavily on resistant wheat cultivars. To breed cultivars with resistance against common bunt, and to effectively deploy resistance genes, it is necessary to identify and monitor the pathogenic races of the local pathogen population. Towards this goal, races of T. caries present in Washington, Oregon, California, and Idaho were identified by inoculating field collections of the pathogen on 13 differential wheat cultivars. Results of three years’ testing show that there is a new pathogenic race in Washington State, which possesses the broadest virulence spectrum to date compared with known bunt races. Furthermore, two-year data indicates the presence of other new races in Washington, California, and Oregon.


Introduction

The organic wheat sector in the United States and Canada is growing. In the United States, the organic wheat acreage grown has grown from 129,393 in 2001 to 415,902 in 2008 (47). In Canada, the acreage more than doubled from 75,816 acres in 2005 to 282,254 acres in 2008 (4). Despite this growth, there is a dearth of research on the management of seedborne diseases under organic systems. Indeed, this is a critical need of the organic wheat sector, especially in the production of disease-free organic seed.

Common bunt is the major seedborne disease posing a threat to organic wheat production. It is caused by two closely related fungi, Tilletia caries (D.C.) Tul. & C. Tul. [syn. T. tritici (Bjerk.) G. Winter] and T. laevis J.G. Kühn [syn. T. foetida (Wallr.) Liro]. The teliospore wall of T. caries is reticulated whereas that of T. laevis is smooth.

Though morphologically different, the two species are similar in germination requirements, life cycles, and disease symptoms produced (6). Historically, common bunt has been one of the most destructive diseases of wheat. The pathogen infects seedlings and grows systemically in the plant then multiplies in the spikes when ovaries begin to form. The kernels are eventually converted into bunt balls (sori) that are filled with dark masses of teliospores (Fig. 1). Typically, disease incidence approximates yield loss because the wheat kernels have been replaced with bunt balls (40). Yield losses up to 50% have occurred in years favorable to infection, but can be as high as high as 70 to 80% (5,7). Aside from causing huge yield losses, the disease can also cause severe reduction in grain quality due to the production of trimethylamine which gives the disease a distinct fishy odor. Grain with contamination levels as low as 5 to 14 bunt balls per 250 grams of seed will be graded “smutty” and docked. It could also be unfit for milling, depending on the level of contamination (34). The teliospores of T. caries can be mistaken for the spores of the dwarf bunt fungus, which is a quarantine organism in some countries (40).


 

Fig. 1. Dark masses of Tilletia caries teliospores released from bunt balls (sori).

 

In conventional agriculture, common bunt is controlled almost exclusively with fungicidal seed treatments, and is rarely seen when seed is properly treated. Whenever untreated or improperly treated seed is used, common bunt has been observed in the United States, Canada, and United Kingdom (10,32,38,49) and in low-input farms in western Asia and North Africa (21,34). In organic wheat, where chemical seed treatments are prohibited, the disease has re-emerged and has caused enormous yield losses, especially when susceptible cultivars have been grown (7). In Europe, the legal requirement that only organically produced seed can be used in organic farms has compounded the bunt problem (36). The spore contamination levels allowed for organic seed is extremely low and it remains a challenge to produce bunt-free seed.

At present, organic farmers must rely on host resistance, non-chemical seed treatments, and the use of clean seed in combination with cultural practices to manage common bunt, as reviewed by Matanguihan et al. (36). In organic wheat, host resistance is the most effective, economically feasible and environmentally sound way of managing the disease. However, resistance to common bunt is often short lived because it is race specific. Resistance is controlled by major genes that interact with the genes of specific pathogenic races. Pathogenic races are genetic variants of the same species and can be distinguished by their ability to attack host genotypes with different resistance genes. Thus, the expression of resistance or susceptibility of a wheat cultivar depends on the pathogenic race attacking it. The gene-for-gene interaction that exists between avirulence genes of the bunt pathogen and the individual host resistance genes accounts for the non-durable resistance of most cultivars. In the Pacific Northwest region of the United States, a series of resistant cultivars were overcome by new races or races that have become predominant in the bunt population in response to the resistance gene (30). Resistance genes served to select the virulent types from the pathogen population. Thus, it is essential for plant breeders to know the prevalent races in a given area (13), together with the non-prevalent races. It is the non-prevalent races in the pathogen population which later predominate in response to the release of new resistance genes or new combinations of resistance genes. In the past, this need has spurred periodic surveys of race distribution and identification of new races in the United States, particularly in the Pacific Northwest (11,13,14,15,16, 22,24,27,28,29,39,42,43,44,45). In other parts of the world where common bunt is still a major disease, surveys and identification of races have been reported more recently (1,2,817, ,20,26,34,46). In the United States, since common bunt occurs so rarely due to the use of chemical seed treatments, the last report on the status of bunt races was made in 1976 (23). With the growth of the organic wheat sector in the United States, there is a need once more to identify the races of the existing bunt population for effective deployment of resistance genes in organic wheat.


Collection of Common Bunt Samples

Bunt collections were made from experimental wheat nurseries in Washington, Oregon, California, and northern Idaho from 2007-2009 (Table 1). In fields with high disease incidence, at least 100 bunted heads were collected at random from as many plants as possible. All of the collections used in this study were identified as Tilletia caries, based on teliospore morphology and ability of teliospores to germinate on water agar at 15°C within 7 days (19).


Table 1. Date and location of Tilletia caries collections used in the study.

Collection Date Location Hostx
1 16 Aug '07 Spillman Agronomy Farm,
Pullman, WA
WW, WA 7821
2 16 Jul '07 USDA Central Ferry Research Stn.,
Pomeroy, WA
WW, RIL of ‘Centurk/Norstar’
3 16 Jul '07 USDA Central Ferry Research Stn.,
Pomeroy, WA
WW, ‘Madsen’
4 16 Aug '07 Spillman Agronomy Farm,
Pullman, WA
WW, breeding line X010259
5 16 Aug '07 Spillman Agronomy Farm,
Pullman, WA
WW, breeding line X010259
6 14 May '08 UC Davis, CA SW, ‘Laura’
7 1 Jul '08 Hermiston, OR WW, ‘Summit’
8 1 Jul '08 Walla Walla, WA WW, ‘Brundage 96’
9 1 Jul '08 Walla Walla, WA WW, ‘Jubillee’
10 10 Sep '08 Rust Nursery, Pullman, WA WW, ‘Ambassador’
11 10 Sep '08 Rust Nursery, Pullman,WA SW, ‘Taf 2’
12 18 Aug '09 Univ. of Idaho Plant Science Farms, Moscow, ID WW, F4 breeding lines

 x SW = spring wheat, WW = winter wheat.


Determination of Virulence Patterns

The pathogenic race of each T. caries collection was determined by analyzing its virulence pattern to a set of differential cultivars. Each of these cultivars possesses a single gene conferring resistance to common bunt. Due to the gene for gene interaction that exists between specific avirulence genes in the pathogen and bunt resistance genes in wheat, each race has its own unique virulence pattern. If a T. caries field collection has a virulence pattern that is consistently unlike those of the known races (19,23), this should be proposed as a new pathogenic race.

Race identification experiments were conducted from October 2007 to August 2010. Seed of 15 differential cultivars monogenic for the bunt (Bt) resistance genes 1 to 15 (Table 2) were obtained from Blair Goates (USDA-ARS, Aberdeen, ID). ‘Heines VII,’ since it has no known bunt resistance genes, was included as the susceptible host. All seeds were disinfested before inoculation, by immersing seed for 10 min in an aqueous solution of formaldehyde (3 parts/thousand solution of 37% formaldehyde) then rinsing thoroughly in running water for 30 min (19). Using sterile spatulas, bunt balls from one infected head were crushed to release the teliospores inside a sterile 50-ml Falcon conical centrifuge tube (Fisher Scientific Co., Pittsburgh, PA). Three grams of seed for each cultivar were added to the tube and mixed with the teliospores by shaking the tubes in a Vortex-Genie Touch Mixer (Scientific Industries Inc., New York, NY) until all the seeds were evenly coated with teliospores. The inoculated seed were sown by hand at a depth of 5 cm in 1.5 m rows replicated twice at the Spillman Agronomy Farm near Pullman, WA. Planting was done during mid-October for the winter wheat differential cultivars, when the soil temperatures were 5 to 10°C, and in early April for the spring wheat differentials ‘Doubbi’ (Bt14) and ‘Carleton’ (Bt15). Race identification experiments for collections 1 to 5 were repeated three times (2008-2010), twice for collections 6 to 11 (2009-2010), and once for collection 12 (2010). Different fields were used each year to avoid spore contamination of the soil from the previous year’s experiments. The differential cultivars were also inoculated with three known bunt races (T-16, T-27, and L-16, obtained from B. Goates) to ensure that the inoculation methods and environmental conditions were conducive for differentiating resistant or susceptible reactions among the differential cultivars. Non-inoculated susceptible hosts were also included in the study to check for the presence of soilborne spores of the pathogen.


Table 2. Wheat differential cultivars monogenic for bunt resistance
genes used in this study to determine pathogenic races of Tilletia
caries
.

Differential cultivar Bunt (Bt) resistance gene
Sel 2092 Bt1
Sel 1102 Bt2
Ridit Bt3
CI 1558 Bt4
Hohenheimer Bt5
Rio Bt6
Sel 50077 Bt7
M82-2161 (PI 173438 × Elgin) Bt8
M90-387 (Elgin × PI 178383) Bt9
M82-2102 (PI 178383 × Elgin) Bt10
M82-2123 (Elgin × PI 166910) Bt11
PI 119333 Bt12
Thule III Bt13
Doubbi Bt14
Carleton Bt15

 Source: Goates (19).


The percent bunt infection was determined during plant maturity by counting all bunted heads and dividing this by the total number of heads in the entire row. The mean percent bunt infection was obtained per year, and the standard deviation was obtained across the years. T. caries collections which produced infection percentages from 0 to 10 were classified as avirulent and those that produced 11 to 100% infections were classified as virulent.

The virulence patterns of the T. caries collections were analyzed and compared to that published by Hoffman and Metzger (23) and Goates (19). In this study, the spring wheat differentials possessing the genes Bt-14 and Bt-15 (Table 2) were included in all tests, but were later dropped from the analysis because of inconsistency of disease reactions attributed to environmental conditions. Other scientists, through several years of testing, have also made the same observation regarding the disease reactions of Bt-14 and Bt-15 (B. Goates, personal communication).


New Pathogenic Race

Three years’ testing showed that there is a new pathogenic race of T. caries in Washington State. Collection 1 from Spillman Agronomy Farm and collection 2 from the USDA Research Station in Central Ferry, Pomeroy, WA, have the same virulence patterns (Table 3) that are unlike any of the known common bunt races. The collections showed consistent virulence patterns through three years of testing, being virulent to resistance genes Bt1, Bt2, Bt3, Bt4, Bt6, Bt7, Bt9, and Bt10. The disease pressure was also high for the first two years of testing, making the results reliable. The non-inoculated susceptible hosts were also disease free, indicating the absence of soilborne inoculum. Moreover, the known races T-16, T-27, and L-16 showed the expected virulence patterns (data not shown), a confirmation that the inoculation methods and the environmental conditions were conducive for bunt infection. Thus, T. caries collections 1 and 2 can be classified as a new race.


Table 3. Percent common bunt infection in wheat differential cultivars inoculated with Tilletia caries field collections, at Spillman Agronomy Farm, Pullman, WA, 2008-2010.

R
gene
Collection 1 from Pullman, WA Collection 2 from Central Ferry, WA
2008x 2009 2010 SDy Virz 2008 2009 2010 SD Vir
none 93.6 80.9 39.0 23.3 + 80.6 74.8 36.9 19.4 +
Bt1 69.3 32.9 23.3 19.8 + 53.0 44.5 25.0 11.8 +
Bt2 72.7 61.9 31.2 17.6 + 66.3 59.3 19.3 20.7 +
Bt3 79.7 20.3 24.2 27.1 + 39.4 60.0 22.7 15.2 +
Bt4 89.2 11.3 49.2 31.8 + 76.0 73.6 72.7 1.4 +
Bt5 2.3 0.0 4.3 1.8 + 4.9 0.0 10.8 4.4
Bt6 75.8 48.8 30.6 18.6 + 90.4 63.0 49.8 16.9 +
Bt7 80.7 30.0 47.0 21.1 + 88.2 68.1 42.6 18.7 +
Bt8 4.4 0.0 6.4 2.7 0.0 0.0 2.0 1.0
Bt9 59.7 24.8 13.9 19.5 + 66.9 54.2 38.7 11.5 +
Bt10 64.7 38.9 34.6 13.3 + 54.0 50.2 30.8 10.2 +
Bt11 0.0 0.0 2.1 1.0 0.0 0.0 0.0 0.0
Bt12 6.7 3.8 1.3 2.2 6.1 9.3 0.0 3.8
Bt13 3.1 0.0 0.0 1.5 0.0 0.0 0.0 0.0

 x Mean of two replicates.

 y Standard deviation of mean bunt percentages from three years of testing (2008-2010).

 z Virulence: 0-10% smutted heads is considered an avirulent reaction (-) while 11-100% smutted heads is considered a virulent reaction (+).


Other T. caries collections from Washington State but from different locations had the same virulence patterns as those of collections 1 and 2. Collection 10 from the Rust Nursery in Pullman, WA, and collection 8 from Walla Walla, WA, were tested for 2 years (Table 4). Collection 12 from the University of Idaho Plant Science Farm, located in Moscow, ID, was tested for only 1 year as it was the last to be collected. All three collections had the same virulence patterns as collections 1 and 2 and could be the same race.


Table 4. Percent of common bunt infection on differential cultivars inoculated with field collections of Tilletia caries from Washington State and Idaho, 2009-2010.

R
gene
Collection 8
(Walla Walla, WA)
Collection 10
(Rust Nursery, Pullman, WA)
Collection 12
(Moscow, Id)
2009x 2010 SDy Virz 2009 2010 SD Vir 2010 Vir
none 82.1 28.6 26.7 + 83.2 26.4 28.4 + 63.4 +
Bt1 79.3 35.8 21.8 + 56.7 34.3 11.2 + 27.8 +
Bt2 82.0 31.6 25.2 + 84.8 13.2 35.8 + 13.5 +
Bt3 42.0 31.8 5.1 + 49.2 25.7 11.8 + 40.4 +
Bt4 75.2 65.7 4.8 + 62.5 27.7 17.4 + 52.2 +
Bt5 0.0 5.3 2.6 0.0 0.0 0.0 4.5
Bt6 72.2 16.9 27.7 + 62.5 73.7 5.7 + 63.2 +
Bt7 69.9 26.4 21.7 + 73.7 59.5 7.1 + 30.2 +
Bt8 5.6 2.9 1.4 0.8 0.0 0.4 3.5
Bt9 51.6 33.2 9.2 + 42.6 42.0 0.3 + 23.6 +
Bt10 61.2 38.9 11.2 + 48.2 41.7 3.2 + 32.7 +
Bt11 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Bt12 6.0 0.0 3.0 0.7 2.5 0.9 1.2
Bt13 1.5 0.0 0.7 6.0 0.0 3.0 0.0

 x Mean of two replicates.

 y Standard deviation of mean bunt percentages from two years of testing (2009-2010).

 z Virulence: 0-10% smutted heads is considered an avirulent reaction (-) while 11-100% smutted heads is considered a virulent reaction (+).


Discussion

Unlike the bunt collections from past race surveys, this collection of bunt samples was by no means systematic or representative of the bunt population in the western United States. Due to the scarcity of common bunt in commercial wheat fields, we were only able to collect from experimental wheat nurseries where the seed was untreated. Nevertheless, even with a limited area sampled, a new pathogenic race of Tilletia caries was identified in Washington.

This new pathogenic race has the broadest virulence spectrum reported so far, able to attack 8 of the 13 resistance genes used. It is virulent on Bt1, Bt2, Bt3, Bt4, Bt6, Bt7, Bt9, and Bt10, and avirulent on Bt5, Bt8, Bt11, Bt12, and Bt13. Of the known bunt races, T-30 has the broadest virulence spectrum, but can only attack 7 resistance genes. This new race differs from T-30 in that it is virulent on Bt3 while T-30 is not. The virulence pattern of this new race is also unlike those of the bunt populations in Europe (3,25,31,41,42,48). However, it has the same virulence pattern as R-55, an artificial race produced through hybridization of races by R. J. Metzger (B. Goates, personal communication). R-55 is not yet in the list of known races and has never been found in field populations in the United States. However, our identification of this new pathogenic race means that this virulence spectrum is now in field populations of Washington.

It is significant that aside from having the broadest virulence spectrum, this new race can also infect the differential cultivars with Bt9 and Bt10. These genes provide excellent resistance since each can only be attacked by five other races. In particular, Bt10 has been employed in breeding programs in several countries (18). After 1965, there had been a disproportionate number of cultivars in the United States possessing bunt resistance from PI 178383, a Turkish landrace resistant to many other diseases (35). This landrace is the source of the genes Bt9 and Bt10 in the differential cultivars (Table 2). The contributions of cultivars possessing the resistance genes Bt1, Bt3, Bt4, Bt6, and Bt7 are also significantly higher in the bunt resistant cultivars, since these have been used as sources of resistance for several decades in the United States (35). All of these genes can be attacked by the new race reported in this study. The only bunt resistance genes that cannot be attacked by this new race are Bt5, Bt8, Bt11, Bt12, and Bt13. Of these genes, only Bt8 has been heavily introgressed into adapted wheat cultivars. So far, there are no known races that attack Bt8 in the United States (B. Goates, personal communication) and Europe (36). The detection of this new race, and possibly four other races, shows the need for identifying bunt resistance genes in cultivars to be used in organic farming. It also highlights the necessity of knowing the distribution of this new race and other bunt races in areas grown with organic wheat in the Pacific Northwest.

Other T. caries collections from California, Oregon and Washington (collections 6, 7, 9 and 11) exhibited virulence patterns different from that of the Washington collections, and also different from those of known races (data not shown). These collections may represent unknown races, but more testing is needed since these have only been tested for two years. Screening of wheat germplam for bunt resistance has shown that bunt incidence could vary among replicates and over years of screening. To achieve a more precise assessment of bunt infection, workers have recommended at least three years’ testing under high disease pressure (9). Repeated testing would confirm that the avirulent reactions were not due to disease escape, a phenomenon where the host is susceptible but was not infected due to the absence of factors necessary for disease development, or because these factors did not coincide long enough for disease to develop. Additional tests would also eliminate the possibility of race mixtures in one teliospore collection.

In the United States, common bunt is still a minor disease in organic wheat because growers are allowed to use conventionally grown seed as long as it is not of transgenic origin and has not been treated with chemicals before sowing. This is no longer true in Europe and has contributed to the resurgence of the disease in organic wheat (36). When conventionally produced seed is no longer allowed on organic farms in the United States, the re-emergence of common bunt is inevitable.

According to McIntosh and Brown (37), there is a lapse of one to several years from the time a new pathogenic race is detected until severe losses are incurred. This time lapse can be used to select and increase resistant cultivars, in a process called “anticipatory plant breeding,” with the objective of averting future losses (37). This concept can be applied to the development of bunt resistant cultivars for organic and low-input farming systems, provided that the following exist: knowledge of pathogenic races and host genotypes, a pathogen surveillance system, and a germplasm enhancement program. This study contributes to the first requirement.


Acknowledgments

We thank Blair Goates for providing seed of the differential cultivars and isolates of the known bunt races, and for technical advice during the conduct of this study. We also thank Dr. Xianming Chen for supplying bunt collections obtained during his stripe rust monitoring trips. Funding from the USDA-Organic Agriculture Research and Extension Initiative (OREI) is gratefully acknowledged.


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