© 2011 Plant Management Network.
Historical Durability of Resistance to Wheat Diseases in Kansas
William W. Bockus, Erick D. De Wolf, Bikram S. Gill, Douglas J. Jardine, and James P. Stack, Department of Plant Pathology, Kansas State University, Manhattan, KS 66506; Robert L. Bowden, Hard Winter Wheat Genetics Research Unit, USDA-ARS, Manhattan, KS 66506; Allan K. Fritz, Department of Agronomy, Kansas State University, Manhattan, KS 66506; and T. Joe Martin, Western Kansas Agricultural Research Center, Kansas State University, Hays, KS 67601
Bockus, W. W., De Wolf, E. D., Gill, B. S., Jardine, D. J., Stack, J. P., Bowden, R. L., Fritz, A. K., and Martin, T. J. 2011. Historical durability of resistance to wheat diseases in Kansas. Online. Plant Health Progress doi:10.1094/PHP-2011-0802-01-RV.
In Kansas, estimated annual losses from wheat diseases averaged 16% from 1976 through 1988; however, losses have declined to 10% in recent years. This decline is mainly due to emphasis on developing cultivars with resistance to important diseases. Data from annual KSU extension publications were used to track disease ratings over time for individual wheat cultivars to eight diseases to draw inferences on the durability of deployed resistance. The duration of durability of resistance to leaf rust has been short for some cultivars but moderate for others. Conversely, the duration of durability of resistance to stem and stripe rusts has been long, although a recent virulence shift in the stripe rust pathogen indicates only moderate duration. Duration of durability of resistance toward tan spot, Septoria tritici blotch, wheat soilborne mosaic, and wheat spindle streak mosaic has been long. Resistance to wheat streak mosaic has been of long duration in some cultivars but others have shown only moderate duration of durability. The effort by breeders to produce cultivars with resistance to diseases in Kansas has resulted in an annual savings of about $58 million. Just as important as the incorporation of resistance into those cultivars is the moderate to long duration of durability of the resistance contributing to effective management of these diseases.
There are about 20 wheat diseases that may be found in Kansas (3). Only 14 of those cause enough loss to warrant control methods including the development of resistant wheat cultivars. Planting resistant cultivars is arguably the best control method for plant diseases. Annual savings to wheat producers in Kansas from planting resistant wheat cultivars has been reported to be about $58 million (3).
Despite the deployment of resistant cultivars, serious losses can still occur. In 2007, for example, there was a severe epidemic of leaf rust in Kansas that caused an estimated 13.9% loss (1), the highest loss from a single wheat disease since estimates were begun in 1976. Contributing factors to this epidemic were virulence shifts that occurred in the leaf rust pathogen that rendered resistance in popular cultivars ineffective. Therefore, the duration of durability is of major importance with regard to the impact that host resistance will have on disease losses. Resistance durability is defined here as the length of time that a deployed resistant cultivar remains resistant to a particular disease; therefore, durability can be of relatively short, medium, or long duration.
The goal of this review was to document the durability of resistance in deployed Kansas wheat cultivars to important diseases. The reaction of cultivars that were resistant to a particular disease when they were released was tracked over time to draw inferences on how long the resistance had lasted. If there was a substantial increase in the disease rating of a previously resistant cultivar, it was assumed that a new race of the pathogen had become prevalent resulting in susceptibility of the cultivar. On the other hand, if the disease rating remained low for many years, it was assumed that the pathogen had not developed a new race with increased virulence toward that cultivar. The duration of durability of resistance was determined for leaf rust, stem rust, stripe rust, tan spot, Septoria tritici blotch, wheat soilborne mosaic, wheat spindle streak mosaic, and wheat streak mosaic. These diseases are among the most important that occur in Kansas and there is a long enough history of resistance being deployed against them to allow durability data to be collected.
Tracking Effectiveness of Resistance
Beginning in 1983, Kansas State University has published disease ratings for about 60 different wheat cultivars each year except for 1989 and 2005. Data for disease reactions were obtained by extension personnel as they toured breeding nurseries, producer fields, and replicated cultivar performance trials where there was sufficient disease to obtain accurate assessments of cultivar reaction to pathogens. Data from numerous disease phenotyping experiments (5,6) were also used in the assignment of scores. Notes on disease reaction were synthesized by the extension specialist into a score that was reported in the annual version of the publication [e.g., see (9)].
From 1983 through 1990, disease ratings were presented using a scale of R (resistant), MR (moderately resistant), I (intermediate), MS (moderately susceptible), and S (susceptible). Beginning in 1991, disease ratings were presented using a 1-to-9 scale where a value of 1 indicated the cultivar was highly resistant and a value of 9 indicated high susceptibility. To allow comparisons between the two rating scales, ratings of R were considered equal to 1, MR equaled 3, I equaled 5, MS equaled 7, and S equaled 9.
Data from the publications mentioned above were used to track disease ratings over time for individual wheat cultivars to specific diseases. Certain commercial cultivars were selected for presentation here because of their popularity and to show common trends. Coupled with these scores were data on the percentage hectares in Kansas that was planted to various cultivars (20). Using these data, charts were produced for cultivars of historical importance to Kansas: Arkan (Fig. 1), Karl (and a selection from Karl named Karl 92) (Fig. 2), and Jagger (Fig. 3). Disease reactions for these cultivars illustrate trends for durability of resistance to the foliar diseases leaf rust (caused by Puccinia triticina), Septoria tritici blotch (caused by Mycosphaerella graminicola), and tan spot (caused by Pyrenophora tritici-repentis). Data on reactions to stem rust (caused by Puccinia graminis f. sp. tritici) and stripe rust (caused by Puccinia striiformis f. sp. tritici) were collected but are not presented. Additionally, data for the reaction of cultivars to three virus diseases (wheat soilborne mosaic, wheat spindle streak mosaic, and wheat streak mosaic) are summarized in Table 1 and Table 2. Durability of resistance in a cultivar to a particular disease was considered of short duration if the disease rating rapidly went from low to high soon after the release of the cultivar. Durability was considered of moderate duration if the rating for a cultivar was low for a number of years after its release and then rose, or if the rise was gradual over several years. Durability was considered of long duration if the resistance rating was consistently low over many years or only showed an inconsequential increase. It should be noted that the amount of disease pressure during the time a cultivar was popular (Table 3) could have affected the duration of durability as defined here. However, the reason that a cultivar showed resistance durability of long duration is a separate issue and not necessarily known.
Resistance to Leaf Rust
Wheat cultivars in Kansas tended to follow the boom and bust
cycle for leaf rust that is evident for many other diseases when major
resistance genes are used (4). In the boom phase for the cultivar, it has
useful levels of resistance and losses are minimized, while in the bust phase,
it is susceptible and losses can be significant. Arkan (Fig. 1), Karl/Karl 92
(Fig. 2), and Jagger (Fig. 3) all showed good levels of resistance to leaf rust
when they were released (1982, 1988, and 1994, respectively). However, at the
end of their commercial popularity, all three cultivars were rated as
susceptible to leaf rust indicating that races of P. triticina with
virulence to them had become prevalent. Arkan is reported to contain resistance
gene Lr24 plus one unidentified gene (16), Karl has Lr1, Lr10,
and Lr14a (19), while Jagger has Lr17 (19) and Lr37
(R. L. Bowden, unpublished). It was reported that increases in the prevalence of races
of P. triticina with virulence to Lr17 in the central and southern
Great Plains occurred because of the increased planting of Jagger (13,15).
Although all three cultivars showed the typical boom and bust cycle toward leaf rust, each one had a somewhat different pattern to how long the boom phase lasted. Arkan had a gradual transition from resistant to fairly susceptible with susceptibility taking 10 years from the time of its release to be documented (Fig. 1). Additionally, during the time of its peak popularity (1985-1990), it was either highly resistant (rating of 1) or, at the most, intermediate (rating of 5) to leaf rust. Therefore, although the genes for resistance to leaf rust did not protect Arkan indefinitely, they did provide reasonable control while the cultivar was popular. Arkan showed a slow deterioration of resistance to leaf rust and what would be considered moderate duration of durability.
Karl/Karl 92 showed a different boom and bust cycle. The resistance in Karl/Karl 92 was ineffective about the same time as it began to become a popular commercial cultivar (Fig. 2). The curve showing the increase in the hectarage occupied by Karl/Karl 92 coincided with that for the decrease in its resistance to leaf rust (Fig. 2). Although it had a slightly higher initial rating than Arkan (3 compared to 1), it showed a more rapid shift to susceptibility. In fact, during all but the first year of the peak popularity for Karl/Karl 92 (1992-1998), it was rated a 7, 8, or 9. Therefore, the resistance in Karl/Karl 92 had very little effect on protecting those cultivars and would be classified as having short duration of durability in Kansas. It should be noted that Karl and Karl 92 were popular cultivars even though there were significant losses from leaf rust in Kansas, especially during the early years of their popularity (1991-1993, Table 3). Obviously, there were advantages to planting those cultivars that offset their susceptibility to leaf rust.
The resistance in Jagger was rendered ineffective even before it began to gain popularity (Fig. 3). Furthermore, during all but the first year of the peak years in the popularity of Jagger (1998-2008), it was rated 7, 8, or 9. Therefore, like Karl/Karl 92, the resistance in Jagger had little effect on protecting that cultivar from yield losses and would be classified as having durability of short duration. Many other common commercial cultivars have shown similar rapid shifts from resistance to susceptibility to leaf rust like those of Karl/Karl 92 and Jagger. During the peak years of Jaggerís popularity (1998-2006), there were only slight to moderate losses (0.1 to 3.4%) from leaf rust in Kansas (Table 3). This probably helped to prolong the usefulness of that cultivar.
Resistance to Stem Rust
Popular cultivars that possessed resistance to stem rust when they were released tended to have the same rating throughout the span of their popularity (data not shown). A few minor increases, such as going from a rating of 3 to 5, were seen but these occurred after changes in extension specialists and could reflect small differences in the way that rating values were obtained between different specialists. In no case was a low resistance rating for a cultivar observed to transition to a high rating such as was seen for leaf rust (Figs. 1, 2, and 3). Therefore, the resistance genes that have been used in Kansas have provided adequate protection from losses caused by stem rust. However, stem rust does not often occur in Kansas. Apparently, the selection pressure for virulence shifts in this pathogen is low or the appearance of new virulence is infrequent.
Durability of resistance to stem rust has been of much longer duration than that of leaf rust in North America. This could be attributable to the population structures of the pathogens. In North America, populations of P. graminis and P. triticina are thought to be asexual due to the absence or eradication of the alternate hosts. However, P. triticina has much higher race diversity than P. graminis. Surveys in the last decade have detected only 3 to 5 races of P. graminis, whereas annual surveys generally detected 40 to 60 races of P. triticina (12). In addition, leaf rust is common and widespread and has a larger population size than P. graminis, which has not been common since the last major epidemics in the 1950s (12). Therefore, perhaps the largest contributing factor to the stability in races of P. graminis f. sp. tritici is the small pathogen population (12) probably due to a combination of durable resistance in the northern, spring wheat region and early-maturing winter wheat cultivars in the central and southern United States. However, it is speculated that if stem rust was more of an annual problem, boom and bust cycles would be noticed for stem rust like they are for leaf rust.
Resistance to Stripe Rust
Prior to 2001, losses from stripe rust in Kansas were always less than 0.1% (Table 3). Clearly, stripe rust had not been a significant problem and disease ratings for cultivar reactions were not determined. In 2001, however, stripe rust was a major yield limiting factor and caused 7.3% loss statewide. In that year, extension specialists began to publish cultivar disease ratings for stripe rust. During the subsequent nine years, commercial cultivars that showed low disease ratings to stripe rust have, for the most part, kept the same low rating (data not shown). In no case was a rating of 1 to 3 seen to increase to a rating of 7 to 9. Therefore, the resistance genes (particularly Yr17) that have been used in Kansas from 1983 through 2009 provided adequate protection from losses caused by stripe rust. The large losses from stripe rust that occurred in 2001 (7.3%), 2003 (10.6%), and 2005 (8.0%) would have been much higher without these genes. Therefore, this resistance has shown a long duration of durability during that period. However, in 2010, there was evidence that there has been a virulence shift in the population of the stripe rust pathogen and cultivars that were resistant in the past now show susceptibility. Therefore, the Yr17 resistance to stripe rust that has been deployed in Kansas now appears to be ineffective.
Resistance to Tan Spot
Prior to 1988, popular commercial cultivars in Kansas were fairly susceptible to tan spot. With the release of Karl in 1988, there has been a history of cultivars with improved resistance to tan spot. From 1976 through 2000, the percentage hectares in Kansas that were planted to tan spot-resistant cultivars went from about 6% to over 60% (3). With this adoption of resistant cultivars, there was a 63% decline in losses from tan spot (3).
Despite the widespread planting of resistant cultivars for a long period of time, no resistant cultivar has become susceptible. One of the first popular resistant cultivars (Karl), which was released in 1988, and a selection from Karl (Karl92) remain resistant to this day (Fig. 2). Similarly, the cultivar Jagger has maintained its resistance from the year of release (1994) through the present despite being planted on over 40% of the hectares in Kansas during 2002, 2003, and 2004 (Fig. 3). Although there have been minor fluctuations in Jaggerís rating (Fig. 3), these coincided with a change in extension specialists and probably reflected small differences in the way that rating values were obtained. In spite of the minor fluctuations for Jagger, durability of resistance to tan spot in Kansas appears to be of long duration.
Resistance to Septoria Tritici Blotch
Similar to tan spot, there were few popular commercial cultivars in Kansas with resistance to Septoria tritici blotch prior to 1988. However, the release of Karl in 1988 began a long list of cultivars with improved levels of resistance to this disease. Early in the era of Karl/Karl 92 (1990-1995), they were rated 3, 2, or 4 before receiving a rating of 5 in 1996 (Fig. 2). Increases in susceptibility of cultivars that were previously resistant to Septoria tritici blotch have been reported in the Pacific states and in Europe (8). If such virulence changes have occurred in Kansas, that may explain the increase in rating for Karl/Karl 92. Other cultivars have also shown modest increases in their rating, such as 2137 which increased from a 3 to a 5 (data not shown). However, the rating of 5 for Karl/Karl 92 remained the same from 1996 through 2009 (Fig. 2). This indicates that high levels of virulence toward the gene(s) in Karl/Karl 92 have not occurred in Kansas. If an increase in virulence toward Septoria-resistant cultivars has occurred, it has been low to moderate.
Unlike what was observed for Karl/Karl 92, the rating for Jagger has remained a 3 since its release in 1994 through the present even though it occupied large percentages of the hectares in the state (Fig. 3). This indicates that the resistance in Jagger displayed long duration. Other popular resistant cultivars have also shown no indication of having become susceptible (data not shown). Therefore, the durability of resistance to Septoria tritici blotch deployed in Kansas cultivars appears to be of moderate to long duration. Although over 12 major genes for resistance to Septoria tritici blotch have been reported (14), it is not known which genes are deployed in Kansas. Consequently, no inferences can be made as to the genetic cause of the apparent moderate duration of resistance in cultivars such as Karl/Karl 92 as opposed to the long duration of resistance seen in cultivars such as Jagger.
Resistance to Wheat Soilborne Mosaic
Ratings for cultivars showing resistance to wheat soilborne mosaic remained stable throughout the life span of each cultivar (Table 1). Occasionally, small fluctuations in ratings were seen such as those for Jagger (Table 1); however, these were very minor and are not considered evidence for a virulence shift in the pathogen. Inheritance studies suggest that there are major genes conferring resistance to wheat soilborne mosaic (7,10,17). Therefore, it appears that single genes are providing high levels of resistance to wheat soilborne mosaic in Kansas and that these gene(s) have had a long duration of durability.
Resistance to Wheat Spindle Streak Mosaic
Compared with wheat soilborne mosaic, there have been fewer cultivars in Kansas with high levels of resistance to wheat spindle streak mosaic. Among these, two patterns of resistance were evident. The first pattern was like that shown by Jagger where the rating went from 1 to 4 (Table 1). Although virulence toward Jagger may have increased, spindle streak mosaic is difficult to rate because the symptoms occur earlier and are more fleeting than those for soilborne mosaic and they often occur together. Therefore, early ratings for Jagger may have been lower than they should have been until enough data over enough years were collected to give it a rating of 4.
A second pattern of ratings to spindle streak mosaic is like the one shown by Karl/Karl 92 (Table 1). Those cultivars have maintained the same rating from 1991 through the present. Therefore, it appears that resistance to spindle streak mosaic in Kansas has been of long duration although there is the possibility that a small shift in virulence has occurred for some cultivars.
Resistance to Wheat Streak Mosaic
There have not been many commercial cultivars in Kansas with high levels of resistance to wheat streak mosaic; however, a few have had ratings in the intermediate (4 to 6) range (Table 2). The cultivar 2137 had an initial rating of 5, dropped to 3, and then increased to 6. It is not known if these small fluctuations represent changes in virulence of the pathogen. Three other cultivars with intermediate ratings (2163, Jagger, and Triumph 64) had fairly constant ratings (5 to 4, 4 to 5, and 4, respectively). This consistency was in spite of the fact that Jagger was planted on over 40% of the hectares in Kansas for several years. Also, Triumph 64 had a constant, relatively low rating of 4 even though it had been planted in Kansas since 1964. Resistance in these cultivars appears to be of long duration.
A significant increase in susceptibility of a cultivar toward wheat streak mosaic was seen with TAM 107. That cultivar initially had a low rating but showed a jump from 3 to 6 between 1995 and 1996 (Table 2). It was determined that this was due to a shift toward susceptibility to the wheat curl mite vector of the virus (11). In spite of the increase in susceptibility for TAM 107, it had been a very popular cultivar in western Kansas for several years and its initial resistance helped to reduce the disease.
One other cultivar, RonL, should be mentioned with regard to resistance to wheat streak mosaic. The resistance in RonL comes from line CO960293 and is temperature-sensitive with resistance displayed at temperatures ≤ 18°C (18). Importantly, none of 51 different isolates of Wheat streak mosaic virus were able to defeat the resistance of CO960293 at 18°C (18). Despite only having four years of ratings, RonL has maintained a very low rating (Table 2). Thus, resistance to wheat streak mosaic in Kansas has shown moderate duration of durability in cultivars such as 2137 and TAM 107 but long duration of durability in other cultivars such as 2163, Jagger, and Triumph 64. It is too early to determine the durability of the newly deployed temperature-sensitive resistance in RonL.
Diseases are a major limiting factor in the production of wheat. In the state of Kansas for example, estimated annual losses from all wheat diseases averaged about 16% from 1976 through 1988 (3). With an average crop value of $1 billion, losses were about $160 million each year. Host resistance is one of the best methods to reduce losses and many cultivars have been developed in Kansas in recent years with high levels of resistance. Just as important is the durability of that resistance.
The durability of resistance in Kansas cultivars has been of short, moderate, or long duration depending upon the disease and the cultivar. Durability of resistance to leaf rust has been of short duration for most cultivars but of moderate duration for others. However, durability of resistance to stem and stripe rusts has been of long duration, although there is a recent virulence shift in the stripe rust pathogen, indicating durability of resistance to that disease has been of moderate duration. Durability of resistance toward the pathogens that cause tan spot and Septoria tritici blotch has been of long duration; most cultivars with improved levels of resistance to these diseases have maintained a low rating. Durability of resistance toward wheat soilborne mosaic and wheat spindle streak mosaic has also been of long duration. Finally, resistance to wheat streak mosaic has shown a long duration of durability in some cultivars but others have shown considerable increases in ratings over the years and resistance durability in those cultivars would be classified as of moderate duration.
Losses due to wheat diseases in Kansas have declined from about 16% prior to 1988 to only about 10% in recent years (2). This decline is mainly due to wheat breeders developing cultivars with resistance to important diseases. Prior to 1977, wheat cultivars were typically resistant to only one disease when they were released. In contrast, most cultivars released from 1988 through the present have been resistant to about eight different diseases (3). This effort has resulted in annual savings for wheat producers of about 6% ($58 million). However, just as important as the incorporation of resistance into those cultivars is the moderate to long duration of durability of resistance that has allowed for more effective management of many diseases. Commitment to incorporation of resistance with a long duration of durability to important Kansas wheat diseases should remain a high priority for breeders in order to maintain and build on this success story.
The authors gratefully acknowledge funding from the Kansas Wheat Commission and the Kansas Crop Improvement Association. Contribution no. 10-329-J from the Kansas Agricultural Experiment Station.
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