Biotype 2 Russian Wheat Aphid Resistance among Wheat Germplasm ...

Published online August 1, 2005

Biotype 2 Russian Wheat Aphid Resistance among Wheat Germplasm Accessions Meghan B. Collins, Scott D. Haley,* Frank B. Peairs, and Jeffrey B. Rudolph

Reproduced from Crop Science. Published by Crop Science Society of America. All copyrights reserved.

ABSTRACT

released cultivars, breeding and genetics programs have also focused attention on other resistance sources in efforts to broaden the resistance base. These efforts have resulted in several germplasm releases (Baker et al., 1994; Haley et al., 2002; Martin and Harvey, 1995, 1997) that have been used extensively in breeding. Biotypic variation in RWA has been known from other areas of the world since the early 1990s (Puterka et al., 1992). In North America, however, biotypic variation had not been detected until 2003 when a new biotype of RWA was identified in southeastern Colorado (Haley et al., 2004a). Since this initial identification, this new biotype (provisionally denoted as Biotype 2; D.R. Porter, USDA-ARS, 2004, personal communication) has spread to other areas of Colorado (unpublished data, 2004) and has been identified in collections from neighboring states (e.g., Kansas and Nebraska; J. Burd, USDAARS, 2004, personal communication). The identification and rapid spread of this new biotype is of great concern because no Biotype 2 resistant cultivars or germplasm sources are currently available for resistance breeding (Haley et al., 2004a), with the exception of the 94M370 germplasm accession that carries the Dn7 gene. However, Dn7 is located on a 1BL.1RS wheat-rye translocation (Marais et al., 1994, 1998) which is associated with poor bread-making quality (Graybosch et al., 1990). Therefore, the objective of this study was to identify additional wheat germplasm accessions that confer resistance to the new biotype of RWA present in the western and southern Great Plains region.

The Russian wheat aphid [Diuraphis noxia (Mordvilko), RWA] is an important pest of wheat (Triticum aestivum L.) in the western Great Plains region of the United States. The recent identification of a RWA biotype (provisionally denoted as Biotype 2) that is virulent on currently deployed RWA-resistant cultivars necessitates the rapid identification of resistance to the new biotype. The objective of this study was to identify Biotype 2 RWA resistance among a collection of germplasm accessions previously determined to be resistant to the original North American biotype of RWA (provisionally denoted as Biotype 1). A collection of 761 germplasm accessions was evaluated in standard seedling screening tests with Biotype 2 RWA. ‘TAM 107’ (carries no RWA resistance genes) and ‘Halt’ (Dn4 resistance gene) were used as susceptible checks while the germplasm line 94M370 (Dn7 resistance gene) was used as a resistant check. Evaluation of accessions showing at least a moderate level of resistance in unreplicated tests was repeated with three replications in a randomized complete block design. Forty-four germplasm accessions were identified as having high to moderate levels of resistance to Biotype 2 RWA. Most of these accessions originated from areas of the world where RWA is endemic or were derived from germplasm accessions that originated from these areas. Ten accessions showed a level of resistance comparable with the 94M370 check. These accessions should prove useful in future genetic studies and for breeding for resistance to Biotype 2 RWA.

T

he Russian wheat aphid is an important pest of wheat in several production areas of the world. Since its introduction to the United States in 1986, the RWA has caused economic losses of more than $1 billion from yield reduction and insecticide inputs alone (Morrison and Peairs, 1998). More than 65% of these losses have occurred in the hard winter wheat production area of the western Great Plains of the United States (Elliott et al., 1998). In the western Great Plains, host plant resistance has proven to be an effective means of control for RWA. Most of the resistant cultivar releases made to date have been based on the Dn4 resistance gene from PI 372129 (Haley et al., 2004b; Quick et al., 1996a, 2001a, 2001b, 2001c, 2001d), although a resistant cultivar derived from a different plant introduction (PI 220350) also has been released (‘Stanton’, PI 617033). While the Dn4 gene and the resistance in Stanton have predominated in

MATERIALS AND METHODS Germplasm Sources A collection of 761 germplasm accessions was obtained from the USDA-ARS National Small Grains Collection (NSGC) in Aberdeen, ID. The 761 accessions were chosen on the basis that they showed the same level of resistance as PI 372139 in previous screening studies with RWA Biotype 1 reported on the National Plant Germplasm System internet site (NPGS, 2004). Of the 761 accessions, 94% originated from the Middle East and Asia: 326 were from Afghanistan, 148 from Iran, 116 from Pakistan, 49 from Russian Federation states, 42 from China, and 35 from Turkey. Forty-five of the remaining accessions originated from other areas of the world.

M.B. Collins and S.D. Haley, Soil and Crop Sciences Dep., Colorado State Univ., Fort Collins, CO 80523; F.B. Peairs and J.B. Rudolph, Bioagricultural Sciences and Pest Management Dep., Colorado State Univ., Fort Collins, CO 80523. Research supported through funding from Colorado Agric. Exp. Stn. Projects 795 and 646 and the Colorado Wheat Administrative Committee. Received 15 Dec. 2004. *Corresponding author ([email protected]).

Russian Wheat Aphid Evaluation Standard seedling screening procedures (as described by Nkongolo et al., 1989) were employed for an initial, unreplicated evaluation of the entire germplasm set. Eleven to 26 seeds of each accession were planted in flats in a controlledenvironment growth room under a 16-h photoperiod with 24⬚C daytime temperature and 18⬚C nighttime temperature. The soil mix was composed of six parts Metro Mix (Scotts-Sierra

Published in Crop Sci. 45:1877–1880 (2005). Plant Genetic Resources doi:10.2135/cropsci2004.0730 © Crop Science Society of America 677 S. Segoe Rd., Madison, WI 53711 USA

Abbreviations: RWA, Russian wheat aphid.

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Table 1. Descriptors and ratings scales used for evaluation of wheat germplasm accessions for resistance to Biotype 2 Russian wheat aphid.


Descriptor/scale† Chlorosis 1 2 3 4 5 6 7 8 9 Leaf rolling† Flat Rolled

Description Plants appear healthy, may have small isolated chlorotic spots. Chlorotic spots become more noticeable, up to 5% of total leaf area. Chlorotic spots are larger and more numerous, up to 15% of total leaf area. Chlorosis covers up to 25% of the total leaf area. Some streaking may become apparent, especially along midrib. Chlorotic spots may begin to coalesce or definite streaking may occur. Chlorosis covers up to 40% of the leaf area. Larger chlorotic areas form coalesced spots; leaves start to die back from tips. Chlorosis covers up to 55% of the leaf area. Further symptom development, chlorosis covers up to 70% of the leaf area. Extensive chlorosis and necrosis, up to 85% of the leaf area affected. Plant death or no recovery possible. Leaves are flat with no apparent rolling. Leaves are folded, loosely rolled, or tightly rolled.

† Chlorosis scale from Webster et al. (1987) and leaf rolling scale from Burd et al. (1993).

Horticulture Products Company, Marysville, OH), three parts perlite, 1 part sphagnum peat moss, and three parts sieved field soil. Each flat included 22 germplasm accessions and three checks: TAM 107 (Porter et al., 1987; PI 495594) and Halt (Quick et al., 1996a; PI 584585), both susceptible to Biotype 2; and 94M370, identified as resistant to Biotype 2 RWA by Haley et al. (2004a). Because of the limited size of the growth room, screening was done in five separate sets, approximately 2 to 5 wk apart, with eight to 12 flats evaluated in each set. A repeat planting was required for some accessions that showed poor germination and fewer than five plants available for data collection. Seedlings were infested with RWAs from a greenhouse colony purified from a collection of Biotype 2 RWAs made in southeast Colorado in 2003. Infestation was done at the one-leaf stage, approximately 6 d after planting, by placing leaf segments containing four to seven RWAs at the base of each seedling. Plants were trimmed every 2 d to keep them from becoming too tall and becoming entangled with other accessions. Chlorosis and leaf rolling scores were recorded for each accession using the same scales used for the RWA Biotype 1 evaluations reported on the NPGS (2004) internet site (Table 1). A preliminary rating was recorded approximately 9 to 13 d after infestation when TAM 107 showed a chlorosis score of about 6 and Halt showed a chlorosis score of about 4. A second rating was recorded approximately 15 to 22 d after infestation when TAM 107 showed a chlorosis score of about 8 or 9 and Halt showed a chlorosis score of about 7 or 8. Only the second rating will be discussed hereafter. The number of total plants for each accession and the presence of heterogeneity of reaction types within the accessions were also recorded. Where heterogeneity was observed, the predominant reaction type of the accession was recorded to represent the overall reaction for that accession. A replicated evaluation, conducted as a randomized complete block design with three replications, was conducted with 59 germplasm accessions showing a chlorosis score ⱕ 4 or a flat leaf rolling score in the unreplicated test. Test procedures were similar to those with the unreplicated evaluation, except that the replicated evaluation was done in a greenhouse with a 16-h photoperiod with daytime temperatures approximately 23 to 26⬚C and nighttime temperatures approximately 18 to 20⬚C.

RESULTS AND DISCUSSION Unreplicated Russian Wheat Aphid Evaluation The unreplicated resistance evaluation in the growth room revealed clear symptom differences among the

check entries, appearing within 1 wk after infestation. As with previous evaluations with Biotype 2 RWA, both TAM 107 (which lacks genes for RWA resistance) and Halt (which carries the Dn4 resistance gene), showed characteristic leaf rolling, trapping, and white streaking along the leaf midribs. While these symptoms appeared slightly faster with TAM 107 than with Halt, both were consistently rated as highly susceptible with an 8 or 9 score for chlorosis and a rolled score for leaf rolling at the second rating. The resistant check 94M370, which carries the Dn7 RWA resistance gene, showed very little symptom expression from RWA infestation and was consistently rated as 1 or 2 for chlorosis and flat for leaf rolling. From the collection of 761 accessions, 52 accessions failed to germinate adequately to provide at least five plants for evaluation, despite repeated plantings. Among the group of 709 accessions for which data were obtained, 124 accessions (17.5%) showed heterogeneity of reaction for RWA resistance (Table 2). These were observed both as mostly resistant accessions containing one or more susceptible plants and mostly susceptible accessions containing one or more resistant plants. The observation of such a high number of heterogeneous accessions in this study is not surprising, given previous studies with RWA-resistant germplasm accessions (e.g., Zhang et al., 1998) and that many of them are categorized as landraces on the NPGS internet site (2004). While some of these accessions may contain promising resistance genes, use of these in future breeding or genetic studies would require careful purification. Clear differences were observed among the germplasm accessions for their response to Biotype 2 RWA. Among the group of 709 accessions for which data were collected, reactions spanned the entire spectrum from very resistant to very susceptible (Table 2). Approximately 10% of the accessions showed chlorosis scores considered to be resistant to moderately resistant (ⱕ3 score), while a slightly lower proportion (8.2%) showed a flat leaf rolling score considered to be resistant. Accessions that combined these two resistance criteria, however, were much less frequent (38 accessions, 5.3%). The frequency of accessions categorized as resistant in the unreplicated screening is markedly greater than previous reports of large-scale germplasm screening with Biotype 1 following the introduction of RWA to the

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Table 2. Summary of chlorosis and leaf rolling scores and occurrence of heterogeneity among 709 wheat germplasm accessions evaluated for resistance to Biotype 2 Russian wheat aphid.


Descriptor/category Chlorosis 1 2 3 4 5 6 7 8 9 Leaf rolling Flat Rolled Heterogeneous reaction

Number of accessions

Table 3. Mean chlorosis and leaf rolling ratings and country of origin of 40 germplasm accessions and check entries evaluated in replicated seedling screening tests with Biotype 2 Russian wheat aphid.

Percentage Accession

1 21 49 99 155 162 93 54 75

0.1 3.0 6.9 14.0 21.9 22.8 13.1 7.6 10.7

58 651 124

8.2 91.8 17.5

United States (Harvey and Martin, 1990; Porter et al., 1993). As the set of accessions in this study was selected from those that had shown resistance to Biotype 1, originating mostly from areas where RWA is endemic, it is not surprising that a larger number of accessions with at least a moderate level of resistance was identified in this study.

Replicated Russian Wheat Aphid Evaluation From the original set of 709 accessions, a subset of 59 accessions showing at least a moderate level of resistance were reevaluated in replicated tests in the greenhouse. In general, there was good agreement between the chlorosis scores, with about 73% of the accessions showing a replicated chlorosis score within one unit of the unreplicated chlorosis score. Of the 16 accessions that showed a difference greater than one unit between the two evaluations, 14 had a lower chlorosis score (e.g., were more resistant) in the unreplicated evaluation in the growth room than in the replicated evaluation in the greenhouse. With regard to leaf rolling scores, a greater degree of dissimilarity between the replicated and unreplicated evaluations was observed. Of the 21 accessions (36%) that showed different leaf rolling scores between the two evaluations, all but one showed a flat rolling score in the growth room and a rolled score in the greenhouse. These observations suggest that the conditions in the growth room, most likely related to temperature and light quality, used in this study may have been less favorable for RWA symptom development and expression than those in the greenhouse. In the replicated greenhouse evaluations, 40 of 59 germplasm accessions evaluated were identified as having moderate to high levels of resistance to Biotype 2 RWA (Table 3). Of this group, only 10 accessions showed a level of resistance that was comparable with that expressed by the 94M370 resistant check (e.g., chlorosis score ⱕ 2 and flat leaf rolling score). Most of these accessions originated from areas of the world where RWA is endemic, most notably Afghanistan and Iran, with PI 572289 from the United States being the lone exception. This accession, which is a germplasm release denoted as STARS-9302W (Baker et al., 1994), carries resistance from PI 149898 from Russia and interestingly

PI 366589 CItr 2401 PI 135064 PI 140204 PI 347006 PI 572652 PI 243659 PI 352008 PI 366572 PI 572289 CItr 11349 PI 243677 PI 361836 CItr 9355 PI 243648 PI 347019 PI 366566 PI 367053 PI 140213 PI 283886 CItr 15018 PI 243679 PI 243730 PI 243786 PI 245583 PI 347003 PI 366518 PI 429398 PI 220131 PI 269408 PI 221482 PI 366103 PI 137741 PI 245434 PI 366985 PI 220133 PI 366823 PI 134134 PI 245462 PI 250903 ‘Halt’ ‘TAM 107’ 94M370 Mean† LSD (0.05)†

Chlorosis 1.0 1.3 1.3 1.3 1.3 1.7 2.0 2.0 2.0 2.0 2.0 2.0 2.0 2.3 2.3 2.3 2.3 2.3 2.7 2.7 2.7 2.7 2.7 2.7 2.7 2.7 2.7 2.7 3.0 3.0 3.3 3.3 3.3 3.3 3.3 3.7 3.7 3.7 3.7 3.7 8.4 8.4 1.0 3.3 1.9

Leaf rolling

Country of origin

flat flat flat flat flat flat flat flat flat flat rolled rolled rolled rolled rolled rolled rolled rolled flat flat rolled rolled rolled rolled rolled rolled rolled rolled flat rolled flat flat rolled rolled rolled flat flat rolled rolled rolled rolled rolled flat

Afghanistan Tajikistan Afghanistan Iran Afghanistan Kazakhstan Iran Kazakhstan Afghanistan United States Bulgaria Iran Afghanistan Sweden Iran Afghanistan Afghanistan Afghanistan Iran Afghanistan Afghanistan Iran Iran Iran Afghanistan Afghanistan Afghanistan Iran Afghanistan Afghanistan Afghanistan Egypt Iran Afghanistan Afghanistan Afghanistan Afghanistan Afghanistan Afghanistan Iran

† Mean and LSD are from the ANOVA with 59 accessions identified in the unreplicated evaluation.

showed a moderately susceptible reaction in previous replicated greenhouse evaluations with Biotype 2 (Haley et al., 2004a). Little information is currently available on the other nine highly-resistant entries identified in this study. Dong et al. (1997) reported that the resistance to Biotype 1 RWA in CItr 2401 was controlled by two dominant genes, one of which being the Dn4 gene from PI 372129 and the second being an unidentified gene other than Dn5 or Dn6. It is unknown whether the Biotype 2 resistance in CItr 2401 is due to this unidentified resistance gene or an epistatic interaction between Dn4 (which itself is ineffective against Biotype 2) and another resistance gene. There is also evidence that another accession that was susceptible in both the unreplicated and replicated tests, PI 366515, may carry multiple genes for resistance to RWA. A USDA-ARS germplasm line with RWA resistance derived from PI 366515, denoted as 2414-11 (C.


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Baker, USDA-ARS, personal communication, 2003) has shown a similar level of resistance as the 94M370 check in Biotype 2 screening tests in our laboratory (data not shown). Assuming that the pedigree of 2414-11 (‘Custer’*3/3/‘Karl92’//‘Chisholm’/PI 366515) is correct, and given that it was selected based on screening with Biotype 1, it is possible that PI 366515 contains different genes for resistance to both Biotypes 1 and 2 or perhaps genes that act epistatically to confer resistance to Biotype 2. The identification of effective sources of resistance to Biotype 2 RWA in this study is encouraging for resistance breeding efforts. Although the Dn7 gene from the 94M370 germplasm line confers a very high level of resistance to Biotype 2, adverse bread making quality effects of the 1BL.1RS wheat–rye translocation (Graybosch et al., 1990) hinder its use in bread wheat breeding. As each of the most resistant accessions identified are landraces, it is unlikely that any of them carry the Dn7 gene on the 1BL.1RS translocation. Studies are currently underway to characterize inheritance and allelism and mechanisms of resistance of Biotype 2 RWA resistance among purified selections from these germplasm accessions. ACKNOWLEDGMENTS We are grateful to Dr. Harold Bockelman (USDA-ARSNational Small Grains Collection, Aberdeen, ID) for providing samples of the wheat germplasm accessions used in this study. We also thank Dr. G.F. Marais (Department of Genetics, University of Stellenbosch, South Africa) for providing the original seed of 94M370 to Dr. Nora Lapitan (Colorado State University). We thank Dr. Lapitan for providing purified seed used in this study.

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