Races of Puccinia graminis f. sp. tritici with Combined Virulence to Sr13 and Sr9e in a Field Stem Rust Screening Nursery in Ethiopia P. D. Olivera, Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108; Y. Jin and M. Rouse, United States Department of Agriculture–Agricultural Research Service, Cereal Disease Laboratory, St. Paul, MN 55108; A. Badebo, Ethiopian Institute of Agricultural Research, Debre Zeit, Ethiopia; T. Fetch, Jr., Cereal Research Center, Agriculture and Agri-Food Canada, Winnipeg, MB R3T 2M9, Canada; and R. P. Singh and A. Yahyaoui, International Maize and Wheat Improvement Center, El Batan, Mexico, CP 56130 Abstract Olivera, P. D., Jin, Y., Rouse, M., Badebo, A., Fetch, T., Jr., Singh, R. P., and Yahyaoui, A. 2012. Races of Puccinia graminis f. sp. tritici with combined virulence to Sr13 and Sr9e in a field stem rust screening nursery in Ethiopia. Plant Dis. 96:623-628. North American durum lines, selected for resistance to TTKSK (Ug99) and related races of Puccinia graminis f. sp. tritici in Kenya, became susceptible in Debre Zeit, Ethiopia, suggesting the presence of stem rust races that were virulent to the TTKSK-effective genes in durum. The objective of this study was to characterize races of P. graminis f. sp. tritici present in the Debre Zeit, Ethiopia stem rust nursery. Three races of P. graminis f. sp. tritici were identified from 34 isolates: JRCQC, TRTTF, and TTKSK. Both races JRCQC and TRTTF possess virulence on stem rust resistance genes Sr13 and Sr9e, which may explain why many TTKSK-resistant durum lines tested in Kenya became susceptible in Debre Zeit. The Sr9e-Sr13 virulence combination is of particular concern because these two genes constitute major components of stem rust resistance in North American durum cultivars. In addition to Sr9e and Sr13 virulence, race TRTTF is virulent to at least three stem rust resistance genes that are effective to race TTKSK, including Sr36, SrTmp, and resistance conferred by the 1AL.1RS rye translocation. Race TRTTF is the first known race with virulence to the stem rust resistance carried by the 1AL.1RS translocation, which represents one of the few effective genes against TTKSK in winter wheat cultivars in the United States. Durum entries exhibiting resistant to moderately susceptible infection response at the Debre Zeit nursery in 2009 were evaluated for reaction to races JRCQC, TRTTF, and TTKSK at the seedling stage. In all, 47 entries were resistant to the three races evaluated at the seedling stage, whereas 26 entries exhibited a susceptible reaction. These results suggest the presence of both major and adult plant resistance genes, which would be useful in durumwheat-breeding programs. A thorough survey of virulence in the population of P. graminis f. sp. tritici in Ethiopia will allow characterization of the geographic distribution of the races identified in the Debre Zeit field nursery. Stem rust, caused by Puccinia graminis f. sp. tritici, is one of the most destructive diseases of bread wheat (Triticum aestivum), durum wheat (T. turgidum subsp. durum), and barley (Hordeum vulgare). Races that recently emerged in eastern Africa (TTKSK [Ug99] and its variants) possess broad virulence to wheat cultivars worldwide, and only a few genes in adapted cultivars are effective against these races (7,8,21). Durum wheat in North America generally has a higher frequency of resistance to race TTKSK than common wheat based on field evaluations conducted in Njoro, Kenya in 2005 and 2006 (R. Singh and Y. Jin, unpublished). Pozniak et al. (14) described that over 80% of the durum varieties and breeding lines from breeding programs in the United States and Canada evaluated in a field trial in Njoro exhibited a moderately resistant or resistant response to stem rust. Singh et al. (18) also reported that durum lines from Egypt and the International Maize and Wheat Improvement Center (CIMMYT) exhibited a high level of resistance to races TTKSK and TTKST in the Njoro’s field nursery. However, when durum lines from the United States and CIMMYT were selected for resistance in Kenya and subsequently were evaluated in Debre Zeit, Ethiopia, many became susceptible to stem rust (R. Singh and Y. Jin, unpublished). Thus, we hypothesized that races of P. graminis f. sp. tritici in the Debre Zeit nursery possess virulence that overcomes the TTKSK resistance in North American durum germplasm. The objective of this study was to identify the race or races of P. graminis f. sp. tritici present in the Debre Zeit, Ethiopia nursery that are virulent on durum lines with TTKSK resistance. Corresponding author: Y. Jin, E-mail: yue.jin@ars.usda.gov Accepted for publication 10 November 2011. http://dx.doi.org/10.1094 / PDIS-09-11-0793 This article is in the public domain and not copyrightable. It may be freely reprinted with customary crediting of the source. The American Phytopathological Society, 2012. Materials and Methods Stem rust nursery. The 2009 durum stem rust field nursery was established by the Ethiopian Institute of Agricultural Research at the Debre Zeit Research Center in Ethiopia. The nursery site was located at 08°46′N, 39°00′E, and 1,900 m in elevation. Entries were planted in double 1-m-row plots on 15 July 2009. Wheat ‘Red Bobs’ (CItr 6255) was included at an interval of 50 lines as a susceptible control. Continuous rows of stem rust spreader (mixture of susceptible cultivars) were planted perpendicular to all entries to facilitate inoculum build-up and uniform dissemination. The spreader rows were planted the same day as the wheat entries and were artificially inoculated by needle injection three times at a weekly interval, starting at stem elongation (stage = Zadoks 31) (23). Urediniospores were suspended in distilled water plus one drop of Tween 20 per 0.5 liters of suspension, and delivered with a hypodermic syringe into the stem tissue. Inoculum was composed of race TTKSK and a bulk of Ethiopian isolates (with unknown race identities) at a ratio of 50/50. Race TTKSK was originally collected from wheat ‘PBW343’ (carrying Sr31) at Debre Zeit, and the bulk of Ethiopian isolates was collected from durum lines at the Debre Zeit Research Center. Sample collection and storage. Forty-one samples of infected stems were collected from durum and common wheat lines with known Sr genes in the stem rust field nursery in 2009. Each sample consisted of 10 to 15 pieces of stem tissue of about 10 cm in length bearing moderately susceptible to susceptible pustules. Stem and leaf sheath tissue were kept in glassine bags and air dried for 2 days at room temperature in the dark. Dried samples were mailed Plant Disease / May 2012 623 to the United States using an international express courier service with a transit time of 5 days. Shipping protocol was followed according to United States Department of Agriculture (USDA) Animal and Plant Health Inspection Service permit conditions for handling international cultures of P. graminis f. sp. tritici. Upon arrival at the Cereal Disease Laboratory, samples were stored in a – 80°C freezer. In December, urediniospores from each stem sample were collected into three to four gelatin capsules (size 00) and stored at –80°C. Race identification. The North American stem rust differential set (15,16) that was modified to further delineate races in the TTKS race group (9) was used for race identification. One capsule per sample was removed from the –80°C freezer and exposed to a heat-shock treatment (water bath at 45°C for 15 min), then placed in a rehydration chamber (80% relative humidity maintained by a KOH solution) for a period of 4 h (9). Five seedlings from each of the 20 differential lines were inoculated with a bulk collection of spores on fully expanded primary leaves at 8 to 9 days after planting. Experimental procedures for inoculation, incubation, and disease assessment were done as described by Jin et al. (8). Singlepustule isolates were derived from individual plants after preliminary evaluation on the differential lines. Six to eight pustules were isolated from each original collection. Incubation and collection of urediniospores from each single pustule was done as described by Jin et al. (9). The pure cultures derived from single-pustule inoculation were increased on ‘McNair 701’ wheat (CItr 15288) and stored at –80°C. Each single-pustule isolate was evaluated two to three times on differential lines before a race was designated. Race designation was done based on the letter code proposed by Roelfs and Martens (16). Representative isolates from each race were further characterized on 17 additional monogenic lines carrying the following genes: Sr22, Sr25, Sr26, Sr27, Sr32, Sr33, Sr35, Sr37, Sr39, Sr40, Sr42, Sr44, Sr46, Sr47, Sr50, SrSatu, and the 1A.1R rye translocation. Cultivars and lines carrying Sr13 and Sr9e alone or in combination and both resistant (Iumillo [PI 210973]) and susceptible (Rusty [PI 639869]) checks were also included in the evaluation of each isolate. Seedling evaluation of wheat germplasm. One thousand durum entries deposited at the USDA Agricultural Research Service, National Small Grain Collection (Aberdeen, ID) were evaluated for resistance in field test at the 2009 durum stem rust field nursery in Debre Zeit. Disease assessment was done at the soft-dough stage of plant growth. Plants were evaluated for their infection response (pustule type and size) (17) and stem rust severity following the modified Cobb scale (13). In all, 137 durum wheat lines character- ized as resistant with a maximum 30% stem rust severity and maximum moderately susceptible infection response were evaluated at the seedling stage with P. graminis f. sp. tritici races identified from this nursery following procedures described above. Seedling evaluation was repeated once. Results and Discussion We obtained 34 single-pustule isolates from the 41 samples collected in 2009 from the Debre Zeit nursery. Three races of P. graminis f. sp. tritici were identified: JRCQC, TRTTF, and TTKSK (Table 1). The race most frequently observed was TTKSK (18 isolates), followed by JRCQC (12 isolates) and TRTTF (4 isolates). The high frequency of race TTKSK was likely due to artificial inoculation of P. graminis f. sp. tritici collected from PBW 343 in the 2009 Debre Zeit field nursery. The virulence profile of race TTKSK from Debre Zeit was identical to that of race TTKSK isolates found in Kenya (9,10). Race JRCQC produced high infection types (ITs) on differential lines carrying Sr6, Sr9a, Sr9d, Sr9e, Sr9g, Sr11, Sr13/17, Sr21, and SrMcN (Table 1). Race JRCQC produced a high IT on differential line Combination VII, which carries Sr13 in addition to Sr17 and was virulent on other Sr13-lines (Table 2). Thus, this race possesses relatively rare virulence to both Sr9e and Sr13, a combination believed to be the main component of stem rust resistance in contemporary North American durum cultivars (11). Race JRCQC produced an IT = X- on W2691Sr10 (tester for Sr10). W2691Sr10 generally produces IT = 0; to ;1 when inoculated with avirulent North American stem rust isolates, and IT = X is infrequent except for a few isolates from the Pacific Northwest (Y. Jin, unpublished). It is not known, however, whether the “X” type was due to Sr10 or a different gene in the W2691Sr10 background. Race JRCQC was avirulent to additional stem rust resistance genes tested in this study, except presumably Sr42 in Norin 40 (Table 2). Race TRTTF was first identified from a stem rust collection from Yemen in 2006 (Y. Jin and A. Yahyaoui, unpublished), and was further isolated from stem rust collections in Ethiopia and Yemen in subsequent years (T. Fetch, unpublished). Race TRTTF is virulent on most of the stem rust resistance genes in the differential set, including Sr9e (Table 1). Virulence on Sr13 was determined based on high IT (IT 3+) on Combination VII, which carries Sr13 in addition to Sr17 (Table 1). Virulence on Sr9e and Sr13 was also confirmed in monogenic lines Vernal (Sr9e) and Khapstein/9*LMPG (Sr13), respectively (Table 2). However, the low ITs observed on K253/3*Steinwedel/8*LMPG (Sr9e) and Leeds (Sr9e + Sr13) (Table 2) indicate that these lines may carry an additional Table 1. Infection types (ITs) observed on stem rust differentials using races JRCQC, TRTTF, and TTKSK of Puccinia graminis f. sp. tritici collected from the 2009 Debre Zeit (Ethiopia) field nurserya Gene Line Sr5 Sr21 Sr9e Sr7b Sr11 Sr6 Sr8a Sr9g Sr36 Sr9b Sr30 Sr17 (+Sr13) Sr9a Sr9d Sr10 SrTmp Sr24 Sr31 Sr38 McN a ISr5-Ra CnS_T_mono_deriv Vernstein ISr7b-Ra ISr11-Ra ISr6-Ra ISr8a-Ra CnSr9g W2691SrTt-1 W2691Sr9b BtSr30Wst Combination VII ISr9a-Ra ISr9d-Ra W2691Sr10 CnsSrTmp LcSr24Ag Sr31/6*LMPG Trident McNair 701 JRCQC (09ETH08-3) ;1 4 4 2 4 3+ 22+ 4 0 2+ 223 3+ 4 1+3; 222;1 4 TRTTF (09ETH06-1) 4 4 3+ 3+ 4 3+ 2 4 3+ 4 4 3+ 4 4 4 4 2 24 4 TTKSK (09ETH05-3) 4 3+ 4 4 3+ 4 4 4 0 4 4 22+ 3+ 4 4 2+ 24 4 4 ITs were accessed on seedlings at 14 days post inoculation using a 0-to-4 scale according to Stakman et al. (19), where ITs of 0, ;, 1, 2, or combinations are considered to be low ITs and ITs of 3 or higher are considered to be high. “N” or “C” denotes excessive necrosis or chlorosis, respectively. 624 Plant Disease / Vol. 96 No. 5 resistance gene or genes that are effective against race TRTTF. Race TRTTF has a virulence profile similar to race RRTTF (avirulent on Sr9e), identified from stem rust collections in Ethiopia and Yemen in 2007 (4) and Pakistan in 2009 (6). Interestingly, both races have a uredinial morphology that is distinct from other common stem rust isolates in that the epidermal tissue over the uredinia has a delayed breakage and the color of uredinia is darker than normal (Fig. 1). In addition to virulence to Sr13 and Sr9e, race TRTTF exhibited a high IT (IT 3) to stem rust resistance conferred by the 1AL.1RS translocation (Table 2). This is the first known race with virulence to the stem rust resistance gene carried by this rye translocation, which represents one of the few effective genes to Ug99 in winter wheat cultivars in the United States (7). Race TRTTF, in combination with TTKSK, differentiates the stem rust resistance gene on 1AL.1RS from other stem rust resistance genes present on 1RS; namely, Sr31 and Sr50 (3,12). Additional data are needed to determine the genetic relationship between 1A.1R resistance and both Sr31 and Sr50. In the United States, current bread wheat breeding lines and cultivars with resistance to race TTKSK possess resistance genes including Sr24, Sr36, SrTmp, and resistance on the 1A.1R translocation (7). Though race TRTTF is avirulent to Sr31, Table 2. Infection types (ITs) observed on additional resistant lines using races JRCQC and TRTTF of Puccinia graminis f. sp. tritici identified from the 2009 Debre Zeit (Ethiopia) field nurserya Gene Resistant check Susceptible check Sr13 Sr9e Sr9e Sr13 + Sr9e Sr22 Sr25 Sr26 Sr27 Sr32 Sr33 Sr35 Sr37 Sr39 Sr40 Sr42 Sr44 Sr46 Sr47 SrSatu 1A.1R Sr50 a Line Iumillo Rusty Khapstein/9*LMPG Vernal K253/3*Steinwedel/8*LMPG Leeds SwSr22T.B. LcSr25Ars Eagle WRT 238-5 ER 5155 Tetra Canthatch/Ae. Squarrosa Mq(2)5*G2919 W3563 RL6082 RL6088 Norin 40 TAF 2 AUS 18913 DAS15 Satu TAM 107 Fed*3/Gabo*51BL.1RS-1-1 JRCQC (09ETH08-3) ;N 3+ 3 3+ 4 4 22+ 2 ; 2 ;2= 0 31; 0; 233+ ;N1 ;1 ;2= 0; 22-; TRTTF (09ETH06-1) 11+;N 4 3+ 3 2+ ; 22+3222+ 2 0 13+; 22 4 3+;N1 2-; 20; 3 ;1- ITs observed on seedlings at 14 days post inoculation using a 0-to-4 scale according to Stakman et al. (19), where ITs of 0, ;, 1, 2, or combinations are considered to be low ITs and ITs of 3 or higher are considered to be high. “N” or “C” denotes excessive necrosis or chlorosis, respectively. Fig. 1. Infection types produced by races JRCQC, TRTTF, and TTKSK of Puccinia graminis f. sp. tritici on Combination VII (Sr13) and Vernstein (Sr9e). Plant Disease / May 2012 625 Table 3. Disease reaction of durum wheat (Triticum turgidum subsp. durum) selected for resistant to moderately resistant to Puccinia graminis f. sp. tritici at the adult stage in field evaluations in Debre Zeit (Ethiopia) and at the seedling stage against races JRCQC, TRTTF, and TTKSK Seedlingb Adulta Line ID CItr 6519 CItr 7287 CItr 8123 CItr 8214 CItr 8634 CItr 11477 CItr 11541 CItr 13245 CItr 13247 CItr 13333 CItr 13335 CItr 13338 CItr 13768 CItr 14091 CItr 14434 CItr 14965 CItr 15326 CItr 15769 CItr 15814 CItr 15892 CItr 17282 CItr 17283 CItr 17284 CItr 17337 CItr 17637 CItr 17748 CItr 17789 PI 45441 PI 56251 PI 61111 PI 61123 PI 61127 PI 61176 PI 61351 PI 61873 PI 70718 PI 94694 PI 94726 PI 94761 PI 113395 PI 113398 PI 166336 PI 167270 PI 168916 PI 168922 PI 178048 PI 178156 PI 182668 PI 184540 PI 184641 PI 185300 PI 191183 PI 191645 PI 192051 PI 192399 PI 192711 PI 193920 PI 208910 PI 210944 PI 234386 PI 253801 PI 264947 PI 272476 PI 272545 Typec Origin Debre Zeit 2009 Cultivar Cultivar Landrace Cultivar Landrace Cultivar Cultivar Cultivar Cultivar Cultivar Cultivar Breeding Cultivar Cultivated Landrace Cultivated Cultivar Breeding Breeding Cultivar Cultivar Cultivar Cultivar Cultivar Landrace Cultivar Cultivar Cultivated Landrace Landrace Landrace Cultivar Landrace Cultivated Cultivated Landrace Landrace Landrace Wild Landrace Landrace Landrace Landrace Breeding Breeding Landrace Landrace Cultivated Cultivated Landrace Breeding Landrace Cultivated Landrace Landrace Cultivated Landrace Landrace Landrace Landrace Landrace Cultivated Breeding Breeding North Dakota North Dakota Ethiopia North Dakota Ethiopia North Dakota North Dakota North Dakota North Dakota North Dakota North Dakota Manitoba North Dakota Unknown Ethiopia Unknown North Dakota North Dakota North Dakota North Dakota North Dakota North Dakota North Dakota Saskatchewan Ethiopia North Dakota North Dakota South Africa Portugal Georgia Kazakhstan Kyrgyzstan Russian Fed. Hokkaido Morocco Iraq Egypt Italy Georgia Egypt Egypt Turkey Turkey Mexico Mexico Turkey Turkey Lebanon Portugal Portugal Santa Fe Spain Sao Paulo Portugal Italy Gotland Portugal Iraq Cyprus Jordan Iraq Italy Hungary Hungary 10 R 20 MS 40 MR-MS 10 MS-MR 20 MR 20 MS 20 MS 10 R-MR 15 MS 5 R-MR 5R 10 MR-MS 20 MS-MR 5 MR-MS 20 R-MR 10 MR 20 MR 15 MR-MS T MR-MS 15 MR-MS 5 R-MR 15 MR-R 5 MR 15 MR 30 MS 10 MR 10 R-MR 15 MR-MS 20 MS 20 MS 10 MS 15 MS 15 MS 15 MS 50 MS-MR 20 MS 15 MS 0 / 20 R TR 10 MR 10 R-MR 15 MR-MS 5 MR 5R 5 MS-MR 5 MS 10 MS 5 MS 10 MS-MR 15 MS 25 MS 15 MS 20 MR-MS 5R 15 MS 5 MS / 40 S 30 MS-MR 30 MS 15 MS-MR 30 MS 30 MS 10 MS 30 MR-MS 30 MS a JRCQC (09ETH08-3) 0; 32 13+; 3+ / 3+;N 3+;1 ;13 4 ; 3+; 2+ 2 0; / 2+ 3+ 3 4;N / ;N ;N3+ ;N ;N ;3 ;N ;1+ ;N / 3 ;12 33+ / 2 ;1;1+N 32+; 2+ 3+3; 2+ 34 3+1+; 23+ 3-2+ 233+ 2+;N3 0; 3+ / 0 3+;N 4 2+ / ;N / 0 2+; 3+ / ; ;1+ 2+1; 2+ 2++ ;N3+ 2= 2=; 1-; 1;3 23+ 2-; / 33+ 3-2 / 4 ;13+ 2+2 2-; 3+1 TRTTF (09ETH061) 4 4 ;2-N 2+ 4 3 4 22+ ;1 2 2-; 0; 2+3- / 22+ 4 3+ 0; ;2;N ; ; ;2;N ;1N 22; ;N 2+33- / 2 3+ 4 4 3 3+ 2 3-; 3+ 2 4 22+; 3+ 3+ 3+ 22+ / 3 4 3+ 3+ 2+33+ / 3;N 4 4 3+ 2 4 2-; ;1 3+ / 2 3 4 4 2+33-2; 2 4 TTKSK (04KEN156-4) ;CN / 3+ 3 2- / 2+2 3+ 3+ 2 3+ 3+ 3+ 2- / 3+ 2;CN / 22-N X / 3+ 333+ 22-2 3+ 23 / 222222+ / 33+ 3+ 22 2 / 3+ 3+ 3+ 3+ 3+ 3+ 2 / 3+ 3+ 22- / 2+32;CN 3-; 3 3 ; 2 2 ; ;CN 324 2-2 22 2-;N 2+3;CN 2-; / 33 3+ 3+ 3+ 4 23+ (continued on next page) Plants evaluated for infection response (17) and severity following the modified Cobb scale (13). R = resistant, MR = moderately resistant, MS = moderately susceptible, S = susceptible, and T = traces. b Infection types (ITs) observed on seedlings at 14 days post inoculation using a 0-to-4 scale according to Stakman et al. (19), where ITs of 0, ;, 1, 2, or combinations are considered to be low ITs and ITs of 3 or higher are considered to be high. “N” or “C” denotes excessive necrosis or chlorosis, respectively; / indicates that an accession was heterogeneous (the predominant type was given first); and – denotes missing data, frequently caused by poor viability of seed. c Classification according to the United States Department of Agriculture–Agricultural Research Service, National Small Grain Collection (Aberdeen, ID). Cultivated = uncertainty about the improvement status. 626 Plant Disease / Vol. 96 No. 5 Table 3. (continued from preceding page) Seedlingb Adulta Line ID PI 272553 PI 274681 PI 278352 PI 278380 PI278503 PI 283854 PI 286539 PI 295967 PI 298547 PI 316092 PI 316096 PI 320128 PI 324928 PI 326315 PI 347217 PI 352317 PI 352463 PI 352512 PI 361149 PI 366110 PI 367224 PI 383416 PI 384111 PI 422412 PI 428539 PI 428541 PI 428549 PI 430747 PI 434919 PI 434952 PI 477881 PI 478298 PI 478304 PI 478306 PI 479916 PI 479921 PI 479923 PI 479956 PI 479959 PI 480006 PI 480401 PI 487290 PI 497927 PI 506469 PI 506470 PI 510694 PI 510696 PI 519170 PI 519171 PI 519445 PI 519559 PI 519619 PI 519639 PI 519642 PI 519811 PI 519832 PI 520299 PI 520300 PI 520392 PI 520413 PI 520518 PI 525395 PI 537310 PI 572862 PI 573005 PI 576787 PI 585010 PI 585020 PI 601250 PI 614658 PI 623997 PI 624854 PI 636501 Typec Cultivated Cultivated Cultivated Cultivated Cultivated Cultivated Cultivar Cultivar Landrace Breeding Cultivar Landrace Breeding Cultivar Landrace Breeding Cultivar Wild Landrace Landrace Breeding Breeding Landrace Cultivar Cultivar Cultivar Cultivar Landrace Landrace Landrace Landrace Cultivar Breeding Cultivar Landrace Landrace Landrace Landrace Landrace Landrace Landrace Landrace Breeding Cultivar Cultivar Breeding Cultivar Breeding Breeding Breeding Breeding Breeding Breeding Breeding Cultivar Cultivar Breeding Cultivar Breeding Breeding Breeding Cultivated Cultivar Landrace Cultivar Landrace Landrace Cultivated Cultivar Cultivar Landrace Landrace Breeding Origin Debre Zeit 2009 Hungary Poland Italy Malta Spain India Ecuador Israel Ethiopia Australia Australia Ethiopia Argentina Azerbaijan Iran Switzerland Switzerland Switzerland India Egypt Italy France Ethiopia Australia France France France Yemen Egypt Egypt Peru North Dakota North Dakota Washington Ethiopia Ethiopia Ethiopia Ethiopia Ethiopia Ethiopia Ethiopia Jordan North Dakota Colorado Colorado North Dakota North Dakota La Araucania La Araucania North Dakota Syria Syria Syria Kenya Italy Lebanon North Dakota California Mexico Syria North Dakota Morocco Saskatchewan Azerbaijan Arizona Algeria Ethiopia Saudi Arabia Arizona United States Iran Iran North Dakota 40 MS-MR TS TR 15 MS 10 MS 10 MS 5 MR 15 MS-MR 15 MR 20 MS 15 MS 20 MR-MS 15 MR TS 60 MS-MR 15 MR 20 MR 5R 10 MR 20 MR 10 R-MR 5 R-MR 15 MR 30 MS TR 10 MS-MR TR 40 MS-MR 30 MS 30 MS-MR 10 MR 15 MR-MS 5 MR-MS 5 MS 20 MR-MS 15 MR 20 MR-R 15 MR-R 40 MR-MS 20 R-MR 10 MS-MR 15 MS 5 MR TR 5 MR-MS 10 MR-MS 5 MR-MS 10 MS 5 MR TR 5 MS 5 MS 5 MS 5 MS 10 MS 15 MR 5 MS 5 MR-MS 15 MS 10 MR-R 5 R-MR 15 MS 10 MR 20 MR-MS 10 MR-MS 25 MS 50 MS-MR 20 MS 15 R-MR 30 MS 20 MS 15 MS-MR 15 MS-MR JRCQC (09ETH08-3) ;N / 3 ; 1+13;N4 31 4; ;1 3+ ;N 23 ;2= 1; 31; 2;1 3+ 3 3+ 1 0; 3-2+ ;1 0; 0; 2-; 3-3 2-; / 3 3+ 33+ ;N 3+/ 22+ /;N 2+ 2-; ;N ;2= / 22- / 3 2=; ;N1 ;1 3+ 31 ;3+1 ;11+ ;N 3; ;1+ 22+ ;N1+ 4 3+ 4 3+; ;N 23+ 2 3+2 ;N1 3+3 2+ 32 2+2 3+ 3+;N 3-2+ 1;N 3+ 3+ 4 1+; TRTTF (09ETH061) X 2 ;1 1+ 4 2 23-; ;1 23+ ; 2+33+ 4 22 2+ ;N1 4 2; 2 22 ; 3-2; ;1 22+ 3+ 3+ 3-2+ ;N ;N ;N 2-N 2-N 2-;N ;N2;N2;N234 0; ; 0; ;N ;N X2 ;N1 2-; 22223+ / 23;N ;N 22+ ; 3+ ;1 2 2 4 222+ 2 ; 3+ X; TTKSK (04KEN156-4) 23-c 2+33 23+ 22+ 3 2= 23 2- / 2 3 3+ 2 / 3+ 2332+ 233+ 3-2+ 2++ 222-; 3-3 223 3+ 3+3 2- / 3+ 222- / 3 22-2 2-2 2-N 222+ / 23+ 2-; 23+ / 2-; 22;33-2+ 22-; 22-;N 23 222-; 22+ 3 3 23-2+ 2-N 22+ 22-N; / 2+ 3 3 3- / 2- Plant Disease / May 2012 627 it is virulent to Sr36, SrTmp and the 1A.1R translocation that are effective against race TTKSK (Tables 1 and 2). Additional studies are needed to determine the percentage of bread wheat cultivars and breeding lines resistant to race TRTTF. Stem rust isolates with virulence to Sr9e and Sr13 were first reported in Ethiopia in 1988 and 1989, respectively (5). They appear to be widespread, because Admassu et al. (2) described races with virulence to these two genes in the major wheat-growing regions in Ethiopia. Races JRCQC and TRTTF, described in this report, possess combined virulence on Sr13 and Sr9e. This virulence combination may explain why the TTKSK-resistant durum entries in Njoro (Kenya) were susceptible in Debre Zeit (Ethiopia). Lines with Sr13 conferred a moderately resistant to moderately susceptible response when tested against race TTKSK in the Njoro nursery (8). However, lines and cultivars carrying Sr9e (Vernal, K253/3*Steinwedel/8*LMPG, Vernstein) and Sr13 (Khapstein/9*LMPG) exhibited a susceptible response in the Debre Zeit field (data not shown). The virulence combination to Sr9e and Sr13 is of particular concern because these two genes constitute major components of stem rust resistance in North American durum cultivars (11). Identification of novel resistance genes effective against races JRCQC, TRTTF, and TTKS is required to broaden the pool of resistance genes in durum wheat. The description of race TRTTF with virulence to several TTKSK-effective resistance genes should remind breeders and pathologists of the danger of deploying race-specific genes alone. Resistance gene combinations are necessary to provide long-lasting resistance to wheat stem rust. A set of durum germplasm (137 entries) selected for resistant to moderately susceptible responses from the 2009 field nursery in Debre Zeit was evaluated for reaction to races JRCQC, TRTTF, and TTKSK at the seedling stage (Table 3). The numbers of accessions exhibiting low ITs to race JRCQC, TRTTF, and TTKSK were 96 (70%), 89 (65%), and 84 (61%), respectively. Many of these lines appear to have race-specific genes and only 47 (34%) accessions were resistant to all three races used in this study. These resistant lines could serve as sources of stem rust resistance for wheat-breeding programs. The genetics of resistance to races JRCQC and TRTTF in selected lines are being investigated. Twenty-six lines (19%) that were resistant to moderately resistant in the field were susceptible to the three races at the seedling stage, suggesting that adult plant resistance might be present in these accessions. Most of the accessions (66%) susceptible at the seedling stage were landraces and other cultivated materials (with uncertainty about the improvement status) from the Middle East and Caucasus regions, and landraces from North and East Africa (Table 3). Race-typing experiments of isolates collected from Kenyan fields in recent years yielded only races belonging to the TTKS lineage (9,10,22). However, surveys conducted in Ethiopia in the last 20 years had more diversity of P. graminis f. sp. tritici races (1,2,20). Continuous and thorough race surveys in Ethiopia are required to have a clear picture of the virulence dynamics in the population of P. graminis f. sp. tritici in the country. Identifying and monitoring movement of races with virulence to effective and widely used resistance genes is critical for defining breeding strategies for stem rust resistance in durum and bread wheat. Our results highlight the relevance of evaluating durum wheat lines for stem rust resistance in Ethiopia due to the presence of combined virulence to genes Sr9e and Sr13 in the P. graminis f. sp. tritici population. Acknowledgments This research is funded by the United States Department of Agriculture–Agricultural Research Service and the Durable Rust Resistance of Wheat, Cornell. 628 Plant Disease / Vol. 96 No. 5 We thank L. Wanschura, S. Gale, C. Kebede, and B. 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