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Published online 24 February 2006
Published in Crop Sci 46:774-780 (2006)
© 2006 Crop Science Society of America
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CROP BREEDING, GENETICS & CYTOLOGY

Virulence of Two Russian Wheat Aphid Biotypes to Eight Wheat Cultivars at Two Temperatures

J. L. Jyoti, J. A. Qureshi, J. P. Michaud* and T. J. Martin

Dep. of Entomology, Kansas State Univ., Agricultural Research Center-Hays, 1232 240th Ave., Hays, KS 67601

* Corresponding author (jpmi{at}ksu.edu)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Biotype 2 of the Russian wheat aphid, Diuraphis noxia (Mordvilko), is virulent to both sources of resistance presently available in commercial wheat, Triticum aestivum L. The performance of biotype 2 was compared with that of biotype 1 on eight wheat cultivars at two constant temperatures, and the plants were evaluated for overall damage and leaf rolling. Colonies of biotype 2 grew an average of 2.3 and 24.9 times faster in the first and second generation, respectively, than did their biotype 1 counterparts at 20°C, reaching 80 to 125 aphids per plant after 20 d, compared with 10 to 31. The no. of aphids per plant at 10 and 20 d after infestation displayed a significant biotype–temperature interaction. There was also a biotype–temperature interaction for plant damage at 10 d, and for damage and leaf rolling at 30 d. After 20 d at 24°C, damage ratings ranged from 7.3 to 8.6 on a scale of 1.0 to 9.0, and leaf rolling ranged from 2.4 to 2.9 on a scale of 1.0 to 3.0 for biotype 2, whereas values for biotype 1 ranged from 2.8 to 5.1 and 1.4 to 2.2, respectively. There were no differences among cultivars in plant damage or leaf rolling induced by biotype 2, and ratings of both were higher than for biotype 1 in all cultivar–temperature combinations. Biotype 2 D. noxia has overcome both Dn4- and Dny-based sources of resistance, was more virulent than biotype 1 to all the cultivars tested, and induced plant injury more rapidly than biotype 1, especially at higher temperatures.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
THE RUSSIAN WHEAT APHID is a relatively important pest of winter wheat and other small grains in the USA. Feeding by D. noxia on susceptible wheat leads ultimately to the death of the plant if infestation is uncontrolled (Walters et al., 1980; Gilchrist et al., 1984; Deol et al., 2001). In general, infested plants develop white, yellow, or purple longitudinal streaks on leaves and stems, exhibit rolled leaves, and often display a prostrate growth habit. In older plants, rolling of the flag leaf may trap the emerging awns, causing the heads to bend. Diuraphis noxia was first reported in the USA in 1986, and by 1993 had caused direct and indirect losses of more than $800 million in the western USA (Morrison and Peairs, 1998). Additional losses have been incurred since then, primarily in Colorado and parts of neighboring states including northeastern New Mexico, southwestern Nebraska, and western Kansas (Berzonsky et al., 2002). Various management approaches have proven effective in alleviating damage from D. noxia (Quisenberry and Peairs, 1998) and natural biological controls have continued to evolve (Noma et al., 2005). Considerable loss reduction has been attributed to the widespread adoption of D. noxia-resistant cultivars by producers of winter wheat in areas with frequent D. noxia infestations (Berzonsky et al., 2002). Approximately 25% of wheat acreage in Colorado has been planted with cultivars resistant to D. noxia over the past 5 yr (Colorado Agricultural Statistics Service, 2004).

Some minor biotypic variation was previously reported in D. noxia collections from the Great Plains, but it was not considered of practical significance as no differential host–plant reactions were observed (Bush et al., 1989; Shufran et al., 1997). However, various infestations of D. noxia reached economically damaging levels on resistant cultivars in eastern Colorado in spring 2003 and required pesticide applications (Haley et al., 2004). This apparent failure of resistant cultivars led to characterization of a novel strain of D. noxia since designated as biotype 2 that is distinguished from biotype 1 on the basis of its virulence to Dn4-based resistance in wheat. This is the first report of biotypic variation in D. noxia in the new world, although a number of biotypes are recognized in the Old World that vary in virulence to different resistance sources (Basky, 2003). Puterka et al. (1992) examined eight D. noxia isolates, including one from the USA, and seven unique virulence patterns were identified. One isolate from the former Soviet Union was virulent to PI 372129, the donor parent of the Dn4 resistance gene deployed in virtually all the resistant cultivars grown in Colorado. Basky (2003) demonstrated virulence of a Hungarian D. noxia isolate to wheat lines expressing Dn1, Dn2, and Dn4. More recently, Smith et al. (2004) reported an isolate of D. noxia in Chile that proved highly virulent to Dn4-expressing wheat lines, but avirulent to those expressing Dn2, Dn5, Dn6, Dnx, and Dny.

A previous study (Jyoti and Michaud, 2005) compared the performance of both D. noxia biotypes on three wheat cultivars, Trego, Halt, and Stanton, under standardized conditions, and characterized substantial differences in both aphid biology and plant responses. Subsequent observations (Jyoti, 2004, unpublished data) suggested additional disparity between biotypes with respect to their responses to temperature. A previous study (Qureshi et al., 2005) evaluated colonization of commercial wheat cultivars by the two biotypes and reported some differential responses. The present experiments were designed to evaluate the performance of both biotypes of D. noxia on a wider range of commercially available cultivars, particularly those that are most extensively grown in Colorado and Kansas. The objectives were to compare colony growth rates of the two D. noxia biotypes on eight cultivars at two constant temperatures and assess the progression of plant damage symptoms.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Aphid Colonies
A colony of D. noxia was established from a single apterous virginopara (wingless parthenogenetic female) collected from wheat in Ellis County, Hays, KS, in autumn 2002 and has been in continuous culture at Agricultural Research Center-Hays ever since. This colony was identified as biotype 1 D. noxia on the basis of its reduced survival and reproduction on the resistant cultivars Halt and Stanton (Jyoti and Michaud, 2005). A colony of biotype 2 D. noxia was initiated from material provided by USDA-ARS in Stillwater, OK, in fall of 2003. This colony had been cultured continuously in isolation at Stillwater since its collection from an infested field of ‘Prairie Red’ in eastern Colorado in the spring of 2003.

Colonies of biotype 1 D. noxia were maintained on Trego, and those of biotype 2 on Halt. The two biotypes were isolated in separate growth chambers (Percival Model I-37VL, Percival Scientific, Inc., Perry, IA) held in separate buildings at the Agricultural Research Center-Hays. Colonies of both biotypes were maintained at a temperature of 22 ± 1°C under cool-white fluorescent lights with a photoperiod of 16:8 (L/D) h. Fresh trays of 10-d-old wheat seedlings were introduced for each colony at intervals of approximately 2 wk. Then, each tray of plants was manually infested with 25 fourth instars of D. noxia using a camel's hair brush, and the old tray of plants removed, autoclaved, and discarded before the production of any alate (winged) aphids that could pose a hazard for cross-contamination.

Wheat Cultivars
The eight wheat cultivars tested in the experiments were Trego (PI 612576), Stanton (PI 617033), 2137 (PI 592444), Jagger (PI 593688), Yuma (PI 559720), Yumar (PI 605388), Akron (PI 632275), and TAM 110 (PI 495594). Trego and Stanton are both winter wheat cultivars released by Kansas State University in 1999 and in 2000, respectively (Martin et al., 2001). Trego is rated as susceptible to biotype 1 D. noxia, whereas Stanton expresses an uncharacterized source of resistance currently designated Dny (Smith et al., 2004). Yuma and Yumar are isogenic lines with the exception that the latter expresses the Dn4 resistance gene that is also expressed in the cultivars Prairie Red, Halt, and Ankor. The cultivars Jagger, 2137, Akron, and TAM 110 all lack any specific resistance to D. noxia, although the latter has resistance to greenbug, Schizaphis graminum (Rhondani). Seeds were obtained from the wheat breeding programs of Kansas State University, Agricultural Research Center-Hays (Trego, Stanton, 2137, Jagger, and TAM 110) and Colorado State University, Fort Collins, CO (Yuma, Yumar, and Akron).

Experimental plants were grown in plastic planting cones (2.4 x 16.5 cm) (Stuewe & Sons, Corvallis, OR) filled with a mixture of soil, peat moss, and vermiculite. Drainage holes in bottoms of the cones were first plugged with a small piece of tissue paper to retain the dry soil during the filling process and encourage retention of moisture during the course of the experiment. Three to four seeds of each cultivar were sown in each cone and then covered with the same soil mixture before being placed back in a plastic rack. Once completely planted, the entire rack was immersed in a water bath so that the moisture required for germination would be drawn up by soil in the cones. After 24 h, the rack of cones was removed from the water bath and held in a greenhouse at 20 to 25°C. Five days after germination, the seedlings were thinned to one per cone. Once plants were 10 d old, the rack of cones was placed in an air-tight cabinet for a 24-h period of fumigation with dichlorvos (2,2-dichloroethenol dimethyl phosphate) to kill any insects that might have colonized the plants while they were maintained in the greenhouse. Following fumigation, plants were removed from the chamber and ventilated in clean air for a period of 24 h before use in experiments.

Experimental Design
The study comprised four separate experiments, one for each D. noxia biotype conducted at each of two temperatures (20 and 24°C). Each experiment consisted of eight wheat cultivars arranged in a randomized complete block design with 12 replications, each containing 24 plants (three of each cultivar), for a total of 288 plants. One plant of each cultivar from each of the 12 replications was harvested destructively on each of three successive dates, at 10, 20, and 30 d after infestation.

Each experimental plant was infested with two fourth instar D. noxia by placing them in the primary leaf axil with a fine camel hair brush. Following infestation, each cone and plant was covered with a transparent ventilated plastic cylinder (3.5-cm diam. x 30.0 cm height) to isolate the aphids on their respective plants within the rack of cones. Thereafter, the rack holding the conetainers was transferred to a growth chamber that had been previously calibrated to maintain the desired temperature (20 or 24°C). Minimum and maximum temperatures were recorded daily within the chamber throughout the experiment using a digital thermal probe (Thermohygro, Oregon Scientific Int., Tualatin, OR) held in a conetainer in the same rack as the experimental replicates.

Data Collection
On each harvest date (10, 20, and 30 d postinfestation), a subsample of 12 plants of each cultivar was examined and rated for overall plant damage and leaf rolling. Overall plant damage was rated on a scale of 1 to 9, where 1 represented apparently healthy plants and 9 denoted plants that were either dead or expressing severe damage symptoms (streaking, chlorosis, and stunting) (Webster et al., 1987). Leaf rolling was rated on a scale of 1 to 3, where 1 represented a plant with flat leaves and no apparent rolling and 3 indicated plants with tightly rolled leaves (Burd et al., 1993). On these scales, plants with damage scores of 1 to 3 and leaf rolling scores of 1 are considered resistant, those with plant damage scores of 4 to 6 and leaf rolling scores of 2 are moderately resistant, and those with plant damage scores of 7 to 9 and leaf rolling scores of 3 are susceptible. Following assessment of its condition, each plant was harvested by cutting it at soil level and the no. of aphids were tallied.

Statistical Analysis
The experiment comprised a split-split-plot arrangement of a randomized complete block design. The first split corresponded to the two aphid biotypes that were reared and tested in separate buildings, and the second split corresponded to the two temperature regimes that were maintained in separate growth chambers. All data were analyzed by PROC GLM (SAS Institute, 1999) with cultivar, biotype, temperature, and block as independent variables and damage, leaf rolling, and no. aphids per plant as dependent variables. Main effects were separated by the LSD test ({alpha} = 0.05) and least square means were used for pairwise comparisons of biotype and temperature. Since the 10-d interval between harvests corresponded approximately to one D. noxia generation (Qureshi and Michaud, 2005), mean colony growth rates were estimated for first and second aphid generations separately for each biotype–cultivar combination at each temperature as the slope of the line joining the mean no. of aphids observed at the beginning and end of each 10-d period. Linear regression was employed to describe the relationships between no. of aphids per plant and overall plant damage and leaf rolling (SPSS, 1998).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Interactions
The three-way interaction between biotype, temperature, and cultivar was significant only for damage on the 10-d harvest (Table 1). There were significant interactions between biotype and temperature for plant damage ratings on the 10- and 30-d harvests, for leaf rolling scores on the 30-d harvest, and for no. of aphids per plant on the 20-d harvest. Interactions between cultivar and temperature were also significant for damage ratings on the 20-d harvest, and for damage ratings and leaf rolling on the 30-d harvest. Interactions between biotype and cultivar were not significant for any dependent variable on any harvest date.


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  		Table 1. Three-way ANOVA of cultivar (Trego/Stanton/2137/Jagger/Yuma/Yumar/Akron/TAM 110) and biotype (1/2) on plant damage ratings, leaf rolling scores, and no. of aphids per plant at 20 and 24°C.{dagger}

 
Effect of Biotype
The main effect of biotype was highly significant for overall plant damage, leaf rolling, and no. of aphids per plant on all three harvest dates (Table 1). At 20 d after infestation, all cultivars had significantly more damage and more leaf rolling when infested with biotype 2 D. noxia than when infested by biotype 1, and this was true at both temperatures (Table 2). At 30 d, there were no significant differences among cultivars in either damage or leaf rolling caused by biotype 2 aphids at either temperature, but biotype 1 aphids caused the most damage and leaf rolling on Trego, Akron, and TAM 110 at 20°C, and the most on Trego and TAM 110 at 24°C. Stanton and Yumar were least damaged by biotype 1 at both temperatures and also had the lowest levels of leaf rolling.


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  		Table 2. Cultivar ratings for overall damage (1–9) and leaf rolling (1–3) when infested with Diuraphis noxia biotypes 1 and 2 at 20 and 24°C. Ten-day-old plants were each infested with two fourth instar aphids on Day 0. Subsets of 12 plants from each treatment were harvested 10, 20, and 30 d after infestation.

 
Mean no. of aphids per plant on the 10- and 20-d harvest dates are reported in Table 3. Data for the 30-d harvest are not presented because many aphid colonies killed their plants and declined before this date, rendering comparisons meaningless. The relative growth rates of aphid colonies on the eight cultivars at both 20 and 24°C are depicted as the slopes of lines joining mean aphid numbers at the beginning and end of each generation (Fig. 1 ). Averaged across all cultivars, biotype 2 aphid colonies grew significantly faster at 20°C in both the first and second generations (P < 0.001 in both cases). At 24°C, biotype 2 colonies grew significantly faster in the first generation (P < 0.001), but not in the second (P = 0.074).


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  		Table 3. Mean no. of aphids per plant for eight wheat cultivars infested with Diuraphis noxia Biotypes 1 and 2 at 20 and 24°C. Ten-day-old plants were each infested with two fourth-instar aphids on Day 0. Subsets of 12 plants from each treatment were harvested 10 and 20 d after infestation.

 

Figure 1
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  		Fig. 1. Changes in mean colony size (±SEM) for two Diuraphis noxia biotypes during first and second generations at each of two constant temperatures. Values are mean colony sizes averaged across eight different wheat cultivars. Individual colonies were each initiated with two fourth instar apterae per plant on Day 0. Asterisks indicate significant differences between biotypes in mean colony size (***, P < 0.001).

 
After 10 d infestation at 20°C, all cultivars had significantly more biotype 2 D. noxia per plant than did their counterparts infested with biotype 1 aphids, with the exception of Stanton and TAM 110 that were not significantly different (Table 3). After 20 d at 20°C, all cultivars infested with biotype 2 had significantly more aphids per plant than did their counterparts infested with biotype 1. After 10 d at 24°C, all cultivars except Trego, Yuma, and Akron had significantly more biotype 2 aphids per plant than did their counterparts infested with biotype 1. After 20 d at 24°C, only Yumar had significantly more biotype 2 than biotype 1 aphids, whereas Trego and Jagger had more of the latter, with all the other cultivars not significantly different. Significant linear regressions of aphid numbers on plant damage and leaf rolling are reported in Table 4.


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  		Table 4. Significant linear regressions of Diuraphis noxia numbers on plant damage and leaf rolling.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Trego emerged as the cultivar most susceptible to damage and leaf rolling by biotype 1 D. noxia at both temperatures, with Jagger, Akron, and TAM 110 also yielding high values. To some degree, this might reflect acclimation of the biotype 1 colony to Trego, since it has been maintained on this cultivar for about 20 generations. Stanton and Yumar, expressing Dny and Dn4 resistance, respectively, emerged as the least suitable cultivars for biotype 1, a result consistent with expectation and with previous experiments that assessed the performance of biotype 1 on cultivars expressing these two sources of resistance (Jyoti and Michaud, 2005). However, Jyoti and Michaud (2005) observed diminished performance of biotype 2 on Trego compared with Stanton in one experiment, whereas the present observations suggest that it performs equally well on these two cultivars. Although the present experiments were performed with the same aphid clone, some 10 to 12 generations separated these experiments and it is possible that subtle changes have accumulated in the clone during this period, even though it was not propagated on either of these cultivars.

No cultivar tested demonstrated any significant resistance to biotype 2, and all cultivars suffered very high levels of plant damage. Our results are consistent with the findings of Haley et al. (2004), who reported no indication of resistance to biotype 2 in any of the commercial wheat cultivars they tested, but provide greater detail of the disparity between biotypes in life history parameters. However, Qureshi et al. (2005) reported differential colonization of biotype 2 apterae in choice tests in which Akron and Yumar were preferred over Stanton and Yuma, and more individuals abandoned plants of Yuma compared with Stanton, Trego, Yumar, and Halt. Our study also included some of the most popular commercial wheat cultivars currently grown in Kansas (Trego, 2137, Jagger, and TAM 110) in addition to popular Colorado cultivars. Despite the fact that biotype 2 D. noxia did not appear to be present in Kansas in 2004, and Russian wheat aphid infestations requiring insecticide treatment did not arise, our results suggest that most of the Kansas wheat crop is highly susceptible to biotype 2.

Colonies of biotype 2 aphids grew much faster than colonies of biotype 1 aphids on all cultivars at both temperatures. Previously, Jyoti and Michaud (2005) demonstrated that the major effect of both Dn4 and Dny resistance was a reduction in the reproductive rate of biotype 1 aphids, coupled with reduced survival of immature stages. On the cultivars Stanton and Yumar that express Dny and Dn4, respectively, biotype 2 aphid colonies grew 1.4 and 3.1 times faster, respectively, than biotype 1 colonies in the first generation at 20°C, and 104.4 and 38.6 times faster in the second generation. Excluding these two cultivars, biotype 2 colonies grew an average of 2.3 times faster than biotype 1 colonies in the first generation at 20°C (maximum difference = 3.6 times faster on 2137) and an average of 9.4 times faster in the second generation (maximum difference = 21.5 times faster on TAM 110), despite the fact that this temperature is reported as close to optimal for biotype 1 (Girma et al., 1990). Excluding Stanton and Yumar, biotype 2 colonies grew an average of 1.7 times faster than biotype 1 colonies in the first generation at 24°C, (maximum difference = 2.4 times faster on TAM 110), but 4.6 times slower in the second generation (maximum difference = 14.6 times slower on Jagger). Thus biotype 1 aphid colonies were still growing after 20 d at 24°C, while biotype 2 colonies were declining. The higher virulence of biotype 2 in comparison with biotype 1 appeared to result in more rapid deterioration of plant quality, especially at the higher temperature, such that biotype 2 colonies at 24°C never achieved the size they did at 20°C, despite experiencing initially higher growth rates.

No alatae were produced in any replication of these experiments. Since wing development in D. noxia is thought to be induced by declining plant quality (Baugh and Philips, 1991) and is also mediated through maternal effects (Messina, 1993), we infer that plant deterioration in all treatments occurred too precipitously for any alatae to complete development. Colonies failing to produce winged migrants would have zero fitness, so we would not expect selection to favor aphids that kill plants so fast that alate production cannot occur. This result would be less likely under field conditions where biotic and abiotic sources of mortality would likely reduce colony growth rates relative to those observed under controlled conditions, but it suggests that laboratory trials such as these might achieve better resolution of cultivars and treatments if conducted with somewhat older plants.

The biotype x temperature interaction for no. of aphids per plant was significant at the 20- and 30-d harvests, suggesting that the two temperature regimes did not affect the two aphid biotypes equally. However, the temperature x cultivar interaction was never significant for no. of aphids, plant damage, or leaf rolling, suggesting that temperature and cultivar affected these parameters independently. Differences between temperature regimes in both plant damage ratings and no. of aphids on particular cultivars were more pronounced with biotype 2 than with biotype 1. At 10 d after infestation, cultivars had higher damage ratings and more biotype 2 aphids per plant in the 24°C treatment than in the 20°C treatment. Biotype 1 aphids were also more abundant after 10 d in the 24°C treatment compared with the 20°C treatment, but plant damage ratings were not higher. At 20 d, both biotypes had produced higher levels of plant damage and leaf rolling at the higher temperature, but only biotype 1 aphids were more abundant than at the lower temperature. Interactions between biotype and temperature were significant for plant damage at 10 and 30 d, indicating that temperature did not influence the progression of plant damage similarly for both biotypes. We infer that damage symptoms in wheat induced by biotype 2 D. noxia increased more rapidly with temperature > 20°C than did those induced by biotype 1 feeding, with the result that biotype 2 aphid colonies declined much sooner at 24°C and never reached the size they did at 20°C. Regressions of aphid numbers on damage symptoms also suggested a closer relationship between aphid numbers and damage symptoms for biotype 1 compared with biotype 2.

We conclude that biotype 2 D. noxia is capable of faster colony growth rates than the original biotype 1 under both temperature regimes on all the commercial cultivars tested. Not only did biotype 2 D. noxia damage cultivars expressing Dny- and Dn4-based resistance, but it also demonstrated markedly higher virulence than biotype 1 to cultivars without specific resistance sources. Our quantitative estimates of aphid performance suggest that the higher virulence of biotype 2 is comprised of two components, one related to higher colony growth rates, the other related to more rapid development of damage symptoms, an effect that was more pronounced at the higher temperature. The higher growth rate of colonies compared with biotype 1, and the greater damage to wheat caused in earlier stages of colony development, can be expected to reduce the collective efficiency of biological control agents in suppressing populations of biotype 2 and mitigating yield losses where environmental conditions are favorable for the aphid.


   ACKNOWLEDGMENTS
 
We are thankful to K. Shufran for providing the source material of D. noxia, biotype 2; S. Haley for providing seed of the Colorado cultivars; and E. Boyko for reviewing the manuscript. This is contribution No. J-05-328 of the Kansas State Experiment Station.

Received for publication May 31, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 





This Article
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