Genet Resour Crop Evol (2017) 64:913–926 DOI 10.1007/s10722-016-0411-2 RESEARCH ARTICLE Adult plant resistance to Puccinia triticina in a geographically diverse collection of Aegilops tauschii Bhanu Kalia . Duane L. Wilson . Robert L. Bowden . Ravi P. Singh . Bikram S. Gill Received: 2 December 2015 / Accepted: 18 May 2016 / Published online: 15 June 2016 Ó Springer Science+Business Media Dordrecht 2016 Abstract Despite extensive genetics and breeding research, effective control of leaf rust caused by Puccinia triticina Eriks. and an important foliar disease of wheat, has not been achieved. This is mainly due to the widespread use of race-specific seedling resistance genes, which are rapidly overcome by new virulent races. There is increased emphasis now on the use of race-nonspecific adult plant resistance (APR) genes for durable control of leaf rust. The objective of this study was the evaluation of Aegilops tauschii Coss. (the D-genome donor of bread wheat) for APR, previously known to be a rich source of seedling resistance genes to leaf rust. A geographically diverse collection of A. tauschii maintained by the Wheat Genetics Resource Center was evaluated for APR in the field with a leaf rust composite culture of predominant races. Out of a total of 371 A. tauschii B. Kalia
D. L. Wilson
B. S. Gill (&) Department of Plant Pathology, Wheat Genetics Resource Center, Kansas State University, Manhattan, KS 66506, USA e-mail: bsgill@ksu.edu R. L. Bowden Hard Winter Wheat Genetics Research Unit, USDA-ARS, Throckmorton Hall, Kansas State University, Manhattan, KS 66506, USA R. P. Singh International Maize and Wheat Improvement Center (CIMMYT), Apdo. Postal 6-641, 06600 Mexico, D.F., Mexico accessions, 50 with low to moderate levels of disease severity were subsequently tested at the seedling stage in the greenhouse with four races and one composite culture of leaf rust. Nine accessions displayed moderate resistance to one or more races of leaf rust at the seedling stage. The remaining 41 seedling-susceptible accessions are potential sources of new APR genes. Accessions from Afghanistan only displayed APR whereas both seedling resistance and APR were common in the Caspian Sea region (Iran and Azerbaijan). The APR in these newly identified A. tauschii accessions will be further characterized for novelty, effectiveness, and race-specificity. Keywords Adult plant resistance
Aegilops tauschii
Disease severity
Puccinia triticina
Seedling resistance
Wheat Introduction Leaf rust, caused by Puccinia triticina Eriks., is one of the most destructive foliar diseases of wheat worldwide (Chen et al. 2013). Historically, leaf rust is the most damaging disease of wheat in the Great Plains of the United States. Ability of the leaf rust pathogen to adapt to diverse climatic conditions has led to its widespread distribution, thus affecting wheat production worldwide (Kolmer 1996). Losses to leaf rust are primarily due to decreased number of kernels per head 123 914 and lower kernel weight. Manipulation of host genetic resistance is the most desirable, cost-effective, and environmentally safe method of controlling wheat rusts (Huerta-Espino et al. 2011). Genetic resistance to wheat rusts can be categorized as either adult plant resistance (APR) or seedling resistance. Adult plant resistance is defined by a susceptible reaction at the seedling stage, followed by increased resistance in post-seedling stages (Park and McIntosh 1994). APR is usually measured on the flag leaf. Seedling resistance, also known as race-specific, major gene or qualitative resistance, is effective throughout the life cycle of the plant, i.e. from seedling to adult plant stages. In many cases, seedling resistance genes confer high levels of resistance, generally accompanied by a hypersensitive response. Use and deployment of single, race-specific seedling resistance genes typically leads to evolution of new pathogen races and accumulation of new virulences (Dyck and Kerber 1985; McIntosh et al. 1995). Molecular cloning of seedling resistance genes Lr10 (Feuillet et al. 2003), Lr21 (Huang et al. 2003) and Lr1 (Cloutier et al. 2007) has demonstrated that they belong to the nucleotide-binding site leucine-rich repeat (NBS-LRR) type gene resistance family. APR can be either race-specific or race-nonspecific. Examples of race-specific APR genes include Lr12 and Lr13 (McIntosh et al. 1995). Examples of racenonspecific APR genes in wheat include Lr34/Yr18 mapped on chromosome 7DS (Dyck 1977; Singh et al. 2000), Lr46/Yr29 on 1BL (Singh et al. 1998; Martinez et al. 2001), Lr67/Yr46 on 4DL (Hiebert et al. 2010; Herrera-Foessel et al. 2010) and Lr68 on 7BL (Herrera-Foessel et al. 2012). Race-nonspecific APR is quantitatively inherited and associated with a slow rusting phenotype (Kolmer 1996; Singh et al. 2000; 2005). The slow rusting phenotype was first described by Caldwell (1968) and results from compatible host reaction accompanied by longer latent period, smaller pustule size and lower spore production. Incorporating slow rusting APR genes can achieve increased levels of durable resistance to leaf rust (Kolmer et al. 2008). The mechanism of slow rusting is not well understood but cloning of the Lr34/Yr18 locus has provided new insights and better understanding of the genetic nature of race-nonspecific genes (Krattinger et al. 2009). Unlike race-specific genes, which often encode proteins of the NBS-LRR family, Lr34 belongs to ATP-binding cassette (ABC) transporter of the ABCG 123 Genet Resour Crop Evol (2017) 64:913–926 subfamily (Krattinger et al. 2009). Lr34 is a single locus that not only confers partial resistance in a racenonspecific manner to leaf rust but also to stripe rust (Yr18), powdery mildew (Pm38) and barley yellow dwarf virus (Bdv1) (Singh 1992; McIntosh 1992; Spielmeyer et al. 2005). Effectiveness of Lr34/Yr18/ Pm38/Bdv1 resistance is highly enhanced when combined with other race-specific and/or race-nonspecific genes and is often associated with durability of resistance in some wheat cultivars (Singh et al. 2000; Kolmer 1996; Bariana et al. 2007). Similar to Lr34, other slow rusting genes have pleiotropic effects. Lr46 also confers resistance to stripe rust, Yr29 and powdery mildew, Pm39 (Lillemo et al. 2008). Lr67 is associated with stripe rust resistance gene Yr46 (Herrera-Foessel et al. 2010). To date, only a few slow rusting genes have been identified and characterized. Discovery of additional sources of slow rusting APR genes would be very useful for developing more durable resistance. Wild relatives of hexaploid wheat (Triticum aestivum L., 2n = 6x = 42, genome AABBDD) are an excellent reservoir of novel genetic variability that can be utilized for wheat improvement. Several agronomically important genes have been transferred from related wild species into wheat, including resistance genes to different pathogens like rusts (Gill et al. 1983, 1986; Dhaliwal et al. 1991, 2002), powdery mildew (Gill et al. 1985) and greenbug (Harvey et al. 1980). Aegilops tauschii Coss. (2n = 2x = 14, genome DD), the D genome donor of wheat, is an excellent source of novel genes to various biotic and abiotic stresses (Gill et al. 1986; Valkoun et al. 1985; Cox et al. 1992; Assefa and Fehrmann 2004). A. tauschii is widely distributed in the Caspian Sea region extending westwards to Turkey and eastwards to central Asia and Afghanistan, and thus has greater adaptation to diverse environmental conditions (Ogbonnaya et al. 2005). A. tauschii consists of two subspecies—A. tauschii Coss. subsp. strangulata (Eig) Tzvel. and A. tauschii subsp. tauschii. Subspecies strangulata is native to Transcaucasia (Armenia, Azerbaijan) and the southeastern Caspian Sea region in Iran. The subspecies tauschii grows naturally in northcentral Iran, the southwestern Caspian region in Iran and all of Afghanistan (Kihara et al. 1965; Ogbonnaya et al. 2005; Wang et al. 2013). High homology between the D genome of A. tauschii and D genome of wheat allows their chromosomes to Genet Resour Crop Evol (2017) 64:913–926 recombine freely. Transfer of genes can be achieved either through direct hybridization (Gill and Raupp 1987) or via the production of synthetic wheat (McFadden and Sears 1946, for recent review see Ogbonnaya et al. 2013). Most studies have reported identification of new leaf rust resistance genes expressed at the seedling stage in the A. tauschii gene pool, but only a few have explored genetic variation for APR genes in this species (Snyman et al. 2004). Since many APR genes have proved to be race-nonspecific and durable, it is important to find and characterize additional sources of APR. Therefore, the objective of this study was to evaluate genetic diversity for adult plant leaf rust resistance present in a collection of A. tauschii accessions from diverse geographic regions. Materials and methods Germplasm The panel of 371 accessions of A. tauschii was obtained from the Wheat Genetics Resource Center (WGRC) gene bank, at the Department of Plant Pathology, Kansas State University, Manhattan, Kansas, USA. This panel is of diverse geographic origin; out of 371 accessions: 104 came from Afghanistan, 94 from Iran, 40 from Azerbaijan, 12 from Turkmenistan, 16 from Uzbekistan, 27 from Turkey, 15 from Armenia, 14 from Georgia, 10 from Pakistan, 9 from the Russian Federation, 3 from China, 3 from Tajikistan and 1 from Kyrgyzstan (Fig. 1). Countries of origin of 23 accessions were unknown. 915 mineral oil (Chevron Phillips Chemical Company LLC, The Woodlands, TX). The oil was allowed to evaporate and the inoculated seedlings were incubated for 16–20 h in a dew chamber at 20 ± 2 °C. Infection types (ITs) were recorded 14 days post inoculation, using the 0–4 Stakman scale (Stakman et al. 1962; Roelfs et al. 1992), where 0 = no uredinia or other macroscopic sign of infection i.e. immune response,; = hypersensitive necrotic or chlorotic flecks without uredinia i.e. highly resistant, 1 = small uredinia surrounded by necrosis (resistant), 2 = small to medium sized uredinia surrounded by necrosis or chlorosis (moderately resistant), 3 = medium to large sized uredinia with or without chlorosis (susceptible) and 4 = large sized uredinia without chlorosis (highly susceptible). In case of heterogeneous accessions, the most frequent infection type was recorded first, followed by ‘‘/’’, followed by the next most frequent infection type. An initial screening of A. tauschii accessions was conducted at the seedling stage to leaf rust race PBD using 0–9 rating scale, where 0 = immune, 1–3 = highly resistant, 4–6 = intermediately resistant, and 7–9 = susceptible (Browder and Young 1975). Race nomenclature and the first three differential sets were described by Long and Kolmer (1989). Two additional differential sets are described in Kolmer and Hughes (2014). Advanced seedling tests included races MMKTN, PNMRL, TFGJG, and TNRJJ. Seedling tests were also done with a composite culture of eight diverse isolates plus bulk fieldcollected inoculum. The composite culture was designated as LR-COMP. Adult plant tests Seedling tests Accessions tested for resistance to leaf rust at the seedling stage in the greenhouse were grown in a 1:1 vermiculite:soil mixture in 4.5-cm-diameter pots. Five seeds per accession were planted in each of two pots and grown in a greenhouse with temperature maintained at 20 ± 3 °C. Thatcher and Thatcher ? Lr34 were included in the test as controls. Urediniospores of leaf rust cultures stored at -80 °C were heat shocked at 42 °C for 6 min before inoculation. 10 day old seedlings of A. tauschii accessions and controls were inoculated by spraying the seedlings with suspension of urediniospores in Soltrol 170 isoparaffin light All field tests were conducted at the Kansas State University Plant Pathology Rocky Ford Research Farm in Manhattan, Kansas. Seeds of each accession were planted in vermiculite:soil mixture in root trainers in October and were maintained in the greenhouse. At the four-leaf stage, the seedlings were transplanted in the field. Spreader rows of a leaf rust susceptible cultivar, ‘Jagger’, were planted parallel and perpendicular to the experimental entries. An artificial rust epidemic was initiated by inoculating spreader rows of Jagger with an atomized suspension of urediniospores of composite culture LR-COMP in Soltrol 170 at the flag leaf emergence stage. 123 916 Genet Resour Crop Evol (2017) 64:913–926 110 R accessions 100 S accessions 90 Number of Accessions Total accessions 80 70 60 50 40 30 20 10 0 F Country of Origin Fig. 1 Frequency distribution of 371 A. tauschii accessions based on seedling susceptible reaction to leaf rust race PBD in 2005 Leaf rust disease severity on the flag leaf was recorded using modified Cobb Scale (Peterson et al. 1948) three times at 7-day intervals and the final score was considered representative of each accession. Infection responses were estimated visually and were classified into five categories, which are based on size of the pustules and associated necrosis and/or chlorosis (Roelfs et al. 1992). The five categories were R = resistant, MR = moderately resistant, M = intermediate between MR and MS categories, MS = moderately susceptible, S = susceptible. Evaluation of A. tauschii accessions for adult plant resistance to leaf rust was carried out in two stages— initial and advanced. In 2005, for initial testing, 286 accessions were planted in single hill plots with winter wheat cultivar Jagger as control. A total of 10 plants per accession were tested for reaction to leaf rust. In 2006, 103 promising A. tauschii accessions were selected based on disease severity and infection responses for re-evaluation in two replicated hill plots with spring wheat cultivars, Thatcher and Thatcher ? Lr34 as control. Potentially resistant accessions, selected from the 2005 and 2006 initial screening, were evaluated as single rows with four replications in 2008 and 2009 for advanced testing. 123 Results Seedling tests To explore the potential of A. tauschii as a source of adult plant resistance to leaf rust, an initial screening was conducted at the seedling stage using leaf rust race PBD. Out of 371 accessions, 286 accessions that displayed intermediate resistance (5–6) to susceptible reaction (7–9) (Browder and Young 1975) to leaf rust at the seedling stage were selected for leaf rust screening at the adult plant stage in the field (Figs. 1, 2). Adult plants tests Evaluation of 286 seedling-susceptible accessions in 2005 resulted in identification of 103 accessions with low to moderate levels of disease severity as adult plants in the field (Table 1). Disease severity among the 103 accessions ranged from 1 to 40 %, with R and MR infection responses. Among the susceptible accessions, disease severity varied from 60 to 80 %, with MS to S infection type, similar to Thatcher. In 2006 field tests, most of these lines displayed similar Genet Resour Crop Evol (2017) 64:913–926 917 240 220 No. of accessions 200 180 160 140 120 100 80 60 40 20 0 0 1 2 3 4 5 6 7 8 9 NT 0-9 Rating scale Fig. 2 Frequency distribution of infection types (ITs) of 371 A. tauschii accessions to leaf rust at seedling stage based on 0–9 scale. In 0–9 scale, 0 = immune, no visible signs of infection; l–3 = highly resistant, increasing from no necrosis to large necrotic areas; 4–6 = intermediately resistant, necrotic areas changing to chlorotic areas and 7–9 = susceptible, NT = not tested levels of resistance, but 37 showed higher disease severity and were dropped from the panel (Table 1). Sixteen accessions showed resistance in both years, but they were not included in the panel for advanced evaluation in 2008 because of poor germination and plant growth. Fifty A. tauschii accessions with apparent APR were selected for advanced evaluation at seedling and adult plant stages. Comparison of disease severity data for 50 accessions across 4 years of field testing identified several accessions with effective adult plant resistance to leaf rust (Table 2). Disease severity and infection responses were relatively stable over the period of 4 years. Leaf rust disease severity ranging from 5 to 40 % was observed for 50 accessions in all 4 years of testing and most of the accessions were rated resistant (R) or moderately resistant (MR). Controls Thatcher and Thatcher ? Lr34 showed highest disease severity of 80 and 50 %, with infection response of S and MS, respectively. To further rule out the role of seedling resistance in APR, the 50 A. tauschii accessions were screened for seedling resistance to four leaf rust races TNRJJ, MMKTN, TFGJG, PNMRL and LRCOMP. Nine accessions were moderately resistant at seedling stage to one or more races, with intermediate ITs varying from; 2- to 2 and were eliminated from further testing (Table 2). Forty-one accessions with susceptible infection types of 3 or 4 at seedling stage exhibited moderate to high levels of resistance at adult plant stage in field tests. These results indicate that these accessions possess adult plant resistance. From this panel, we further identified 17 accessions that displayed moderate to high levels of adult plant resistance to Puccinia triticina in the field over 4 years of testing (Fig. 3). Geographical distribution of resistance The geographical distribution of analyzed accessions and their reaction to leaf rust infection at seedling and adult plant stages is shown in Fig. 4. Both seedling and adult plant resistance was found in accessions from the Caspian sea region whereas those from eastern region especially those collected from Afghanistan exclusively showed APR. Most of the seedling resistance was observed in accessions collected from Azerbaijan (60 %) and Iran (29 %) in the Caspian Sea region. Some seedling resistance was also present in accessions from Uzbekistan, Russian Federation, Turkey and Turkmenistan (Fig. 4). All accessions from Afghanistan, Armenia, Georgia, China and Pakistan showed susceptible reaction to leaf rust at the seedling stage. 123 918 Genet Resour Crop Evol (2017) 64:913–926 Table 1 Leaf rust responsea of 103 Aegilops tauschii accessions at adult plant stage: 2005–2006 Acc. Origin Subspecies 2005 2006 1578 Unknown tauschii 40MR 20MR 2435 Afghanistan tauschii 30MR 40MS 1581 Unknown tauschii 30MR 1MR 2436 Afghanistan tauschii 30MR 10MS 1586 1590 Turkey Turkey tauschii tauschii 1R 30MR 1R 70MS 2438 2442 Afghanistan Afghanistan tauschii tauschii 20MR 30MR 10MR 20MR 1591 Turkey tauschii 30MR 90S 2448 Iran tauschii 10MR 20M 1594 Turkey tauschii 40MR 15MR 2452 Iran strangulata 5R 1R 1600 Iran strangulata 1R 1MR 2455 Iran strangulata 5R 10MR 1604 Afghanistan tauschii 30M 60MS 2460 Iran tauschii 1R 15 M 1619 Iran tauschii 10MR 5M 2461 Iran tauschii 10R 30MS 1621 Georgia tauschii 20MR 70MS 2469 Iran tauschii 1R 30MS 1624 Azerbaijan strangulata 20MR 20MS 2474 Iran tauschii 10R 1R 1626 Turkmenistan strangulata 10MR 15 MR 2476 Iran tauschii 40R 20 MR 1631 Afghanistan tauschii 5MR 40MR 2485 Iran tauschii 20MR 5M 1632 Afghanistan tauschii 40MR 60M 2491 Iran tauschii 30M 80MS 1634 Turkey tauschii 40R 40MS 2492 Iran tauschii 30MR 50MS 1652 Tajikistan tauschii 40MR 60S 2493 Iran tauschii 40R 40MS 1656 Azerbaijan tauschii 10MR 5M 2496 Iran tauschii 5R 30MS 1658 Azerbaijan tauschii 1R 5R 2497 Iran tauschii 50 M 5MR 1671 1672 Azerbaijan Azerbaijan tauschii tauschii 5R 20MR 1R 50 M 2498 2504 Iran Turkey tauschii tauschii 10R 30MR 5MR 40MS 1678 Azerbaijan tauschii 1R 20MS 2519 Iran tauschii 40MR 70MS 1680 Azerbaijan tauschii 5R 5R 2520 Iran tauschii 30MR 70S 1681 Azerbaijan tauschii 40M 5MR 2521 Iran tauschii 30MR 80MS 1689 Unknown tauschii 10R 40M 2524 Iran tauschii 40MR 5M 1698 Russian Federation tauschii 40MR 20MR 2533 Afghanistan tauschii 30MR 20MS 1699 Russian Federation tauschii 30MR 30M 2536 Afghanistan tauschii 30R 40MR 1704 Tajikistan tauschii 30MR 50MS 2541 Afghanistan tauschii 20R 50MS 1707 Unknown tauschii 10R 5MR 2550 Afghanistan tauschii 30MR 80MS 1709 Unknown tauschii 30MR 70MS 2551 Afghanistan tauschii 20MR 80MS 1718 Iran tauschii 40MR 10MR 2554 Afghanistan tauschii 40MR 20M 2375 Iran tauschii 30M 30M 2556 Afghanistan tauschii 20MR 80M 2383 Pakistan tauschii 30MR 70M 2557 Afghanistan tauschii 40MR 60MS 2393 Afghanistan tauschii 30MR 80MS 2564 Azerbaijan tauschii 20MR 5M 2394 2395 Afghanistan Afghanistan tauschii tauschii 30MR 30R 15M 20MS 2565 2567 Azerbaijan Armenia tauschii tauschii 5MR 40MR 10R 80MS 2396 Afghanistan tauschii 20MR 60MS 2568 Armenia tauschii 20MR 10MR 2397 Afghanistan tauschii 30MR 15M 2571 Armenia tauschii 40MR 50MS 2402 Afghanistan tauschii 30MR 30 M 2574 Armenia tauschii 40MR 80S 2404 Afghanistan tauschii 20MR 60S 2578 Georgia tauschii 1R 1MR 2406 Afghanistan tauschii 20MR 40M 2581 Georgia tauschii 40MR 15MR 2410 Afghanistan tauschii 40MR 10M 2587 Afghanistan tauschii 40MR 50MS 2411 Afghanistan tauschii 30MR NT 10116 Turkmenistan tauschii 30MR 60MR 2414 Afghanistan tauschii 40MR 70M 10125 Uzbekistan tauschii 40R 70M 2418 Afghanistan tauschii 30R 5MR 10180 Turkmenistan tauschii 5R 15M 2422 Afghanistan tauschii 30MR 10MS 10186 Turkmenistan tauschii 30R 80MS 123 Acc. Origin Subspecies 2005 2006 Genet Resour Crop Evol (2017) 64:913–926 919 Table 1 continued Acc. Origin Subspecies 2005 2006 Acc. Origin Subspecies 2005 2006 2423 2426 Afghanistan Afghanistan tauschii tauschii 30R 30MR 40M 30MS 10191 10197 Uzbekistan Uzbekistan tauschii tauschii 40MR 40MR 20M 80MS 2427 Afghanistan tauschii 30MR 60MS 10199 Uzbekistan tauschii 5R 50MS 2429 Afghanistan tauschii 20MR 80S 10200 Uzbekistan tauschii 30MR 20M 2431 Afghanistan tauschii 40MR 50MS 10212 Uzbekistan tauschii 40MR 40M 2432 Afghanistan tauschii 40R 30MR Jagger 50MS 40M 2433 Afghanistan tauschii 30R 20MR Thatcher – 80S 2434 Afghanistan tauschii 30MR 50MS Thatcher ? Lr34 – 50MS R resistant, MR moderately resistant, M moderate, MS moderately susceptible, S susceptibility reaction types also indicated; missing data ‘–’ a Adult plant reaction types were scored on 0–100 scale For APR, the accessions collected from Afghanistan and Uzbekistan exhibited moderate disease severity, with infection response ranging from MR to MS, for all 4 years (Table 2). Nine out of twelve accessions from Iran displayed low disease severity throughout testing period. Seven of eight accessions from Azerbaijan showed high APR in all years of testing. TA1681 displayed low disease severity in all 3 years except 2005. Two accessions from Turkmenistan, one from Georgia and one of unknown origin displayed high APR during multiple years of testing. The highest frequency of adult plant resistance to leaf rust in all 4 years of testing was found in Azerbaijan (75 %) followed by Iran (67 %) and whereas moderate levels of resistance was prevalent in accessions from Afghanistan (53 %). Discussion Deployment of seedling resistance genes provides high levels of resistance but is often short lived in the field and overcome by emergence of new virulent races of the pathogen (Kolmer et al. 2007; McIntosh et al. 1995). Virulence to named seedling resistance genes mapped to the D genome of bread wheat tracing their origin to A. tauschii including Lr1 (McIntosh et al. 1965; Ling et al. 2004), Lr2 (Luig and McIntosh, 1968), Lr15 (Luig and McIntosh, 1968), Lr21 (Rowland and Kerber 1974), Lr32 (Kerber 1987), Lr39 (Cox et al. 1994,1997; Singh et al. 2004) and Lr42 (Cox et al. 1994) has been detected in several parts of the world where these genes were deployed. Increase in frequency of virulent isolates to genes Lr21 and Lr39 has been observed in past few years due to fact that genes are present in many hard red winter wheat cultivars grown in Great Plains (Kolmer and Hughes 2014). Lr22a is likely a race-specific APR gene and is mapped to chromosome 2DS (Dyck and Kerber 1970; Rowland and Kerber 1974; McIntosh et al. 1995). Lr22a is thought to be absent in U.S. cultivars, but it is deployed in cultivar AC Minto which was cultivated on small acreage in Canada from 1998 to 2006 (Hiebert et al. 2007). Absence of virulence for Lr22a in rust population might be due to relatively low exposure of Lr22a to leaf rust in Canada and U.S. (Huerta-Espino et al. 2011). Data is not available on deployment of another unnamed race-specific APR gene (Cox et al. 1991). On the other hand, resistance of race-nonspecific APR Lr34 has proven to be durable over a 50 year period (Dyck 1977; Lagudah et al. 2006). Previously, Snyman et al. (2004) provided preliminary data on APR in A. tauschii among a large sample of Triticeae species evaluated. In this study, we evaluated APR in a collection of 371 A. tauschii accessions representing the genetic and geographical diversity of this species, which is widely distributed in Transcaucasia and West Asia (Fig. 4). Following extensive evaluation, 41 accessions displayed APR. Further, we identified 17 accessions that displayed effective levels of adult plant resistance to Puccinia triticina in the field over 4 years of testing (Fig. 3). Each of these accessions is a potential source of new APR genes and can be utilized in wheat breeding programs. 123 920 Genet Resour Crop Evol (2017) 64:913–926 Table 2 Summary of reaction of 50 Aegilops tauschii accessions to Puccinia triticina tested at seedling and adult plant stage for 2008 to 2009 TA# Subspecies Origin Seedling datab Adult plant datac 2009 TNRJJ MMKTN TFGJG PNMRJ LR-COMP a 2008 2009 LR-COMP LR-COMP 1581 tauschii Unknown 3 3? 3 3 2? 40MS 30MR 1594 tauschii Turkey 3? 3 3 2 3 40MR 20MR 1600 strangulata Iran 3? 3 3 3 3 30MR 20MR 1619 tauschii Iran 3 3 3 3? 3 40M 20MR 1626 strangulata Turkmenistan 4 3 3? 3? 2?/3- 40M 30MR 1631 1634 tauschii tauschii Afghanistan Turkey 3 3? 3 3 3 3 3 3 3 3? 30MR 40M 30MR 30MR 1656 tauschii Azerbaijan 3 3? ;2? 3 ;2- 30MR 30MR 1658 tauschii Azerbaijan 3? 3 ;2 3? 2 30MR 20MR 1672 tauschii Azerbaijan 3 3 3- 3 3 30MS 30MS 1678 tauschii Azerbaijan 4 3? 3 3? 3? 20M 30MR 1680 tauschii Azerbaijan 3 3 3 3? 3 30MR 20MR 1681 tauschii Azerbaijan 3? 3? 3? 3 2? 20MR 30MR 1698 tauschii Russian Federation 3? 3 3 3 3 30MR 15MR 1699 tauschii Russian Federation 3 3 3 3 3 40MR 30MR 1707 tauschii Unknown 3 2? 3 3- 3 40MR 40MR 2375 tauschii Iran 3 3 3 3 3 15MR 20MR 2394 tauschii Afghanistan 2? 3- 3? 3 3 3? 10MR 30MR 2395 tauschii Afghanistan 3 3 3 3 3? 15MR 10MR 2397 tauschii Afghanistan 3 3 3 3? 3 10MR 15MR 2402 tauschii Afghanistan 3 3 3? 3 3 20MR 15R 2410 2422 tauschii tauschii Afghanistan Afghanistan 3 3 33 3 3 3 3 3 3 15MR 30MR 5MR 40MR 2426 tauschii Afghanistan 3 3 3 3 3 15MR 5R 2433 tauschii Afghanistan 3 3 3 3? 3 15MR 10MR 2435 tauschii Afghanistan 3 3 3 3? 3? 5RMR 5MR 2436 tauschii Afghanistan 3? 3 3 4 3 5MR 5R 2438 tauschii Afghanistan 3 3 3 3? 3? 20RMR 5R 15MR 2442 tauschii Afghanistan 3 3 3? 3? 4 30MR 2448 tauschii Iran 2? 3- 3 2? 3 3 3? 10MR 15MR 2452 strangulata Iran 3? 3 3? 3? 3 30M 10MR 2460 tauschii Iran 3 3? 3? 3 3 20MR 15MR 2474 tauschii Iran 3 3 3? 3 3? 20MR 20MR 2476 tauschii Iran 3? 4 3? 3? 3? 20MR 20MR 2485 tauschii Iran 3? 3 3 3 4 20MR 20MR 2497 tauschii Iran 3? 3? 3? 3 3 15MR 20MR 2498 2504 tauschii tauschii Iran Turkey 3? 3? 3 2? 3 2? 3 ;2?/2 3? 3 40MR 30MR 30MR 30MR 2524 tauschii Iran 2? 3 3 3? 3 3 40MR 10MR 2536 tauschii Afghanistan 3 3? 3 3 3 30MR 30MR 2554 tauschii Afghanistan 3 3 3 3 3 40MR 30MR 123 Genet Resour Crop Evol (2017) 64:913–926 921 Table 2 continued TA# Subspecies Origin Seedling datab Adult plant datac 2009 TNRJJ MMKTN TFGJG PNMRJ LR-COMP a 2008 2009 LR-COMP LR-COMP 2564 tauschii Azerbaijan 3 3 3 3? 3? 15MR 10MR 2565 tauschii Azerbaijan 3; 3 3; 3 3 20MR 15MR 30MR 2568 tauschii Armenia 3 3 3 3? 3? 20MR 2578 tauschii Georgia 3 3- 3 3 3 10MR 15MR 2581 tauschii Georgia 3 3 3? 3 3? 20MR 10MR 10180 tauschii Turkmenistan 2? 3 3 3- 3 20MR 10MR 10191 tauschii Uzbekistan 3 3 3 3 3 5RMR 5MR 10200 10212 tauschii tauschii Uzbekistan Uzbekistan 3 3 3 3? 3 3? 3 3? 3 3 50MS 40M 50M 30MR Thatcher 3? 3? 3 3? 3 70MS 70S Thatcher ? Lr34 3? 3 3 3 3 20M 30M a Leaf rust culture, LR-COMP consisted of mixture of common leaf rust races and natural field inoculum b Infection types at seedling stage were scored according to 0–4 scale where 0 = absence of any disease symptoms and 4 = high susceptibility; Flecks are shown by; and plus and minus signs indicate variation above and below established pustule sizes. Infection types;, 0, 1-, 1, 1? were classified as resistant (R); 2, 2? were classified as intermediate (I); 3-, 3, 3?, 4 were classified as susceptible (S) c Adult plant reaction types were scored on 0–100 scale. Resistant (R), moderately resistant (MR), moderate (M), moderately susceptible (MS) and susceptibility (S) reaction types also indicated; missing data ‘–’ As discussed earlier, APR may also be racenonspecific, controlled by a large number of genes with small effects and may be pleiotropic, imparting resistance to a number of pathogens. Slow rusting genes mapped to the D genome of wheat include Lr34/ Yr18/Pm38/Bdv1 mapped on chromosome 7DS (Dyck 1977; Singh et al. 2000; Singh 1993) and Lr67/Yr46 on 4DL (Hiebert et al. 2010; Herrera-Foessel et al. 2010). Despite widespread and prolonged use of Lr34 in wheat breeding programs around the world, virulence in the leaf rust pathogen population has yet to be reported (Kolmer 1996; Kolmer et al. 2008). Future work will reveal the nature of APR present in our collection of adult plant resistant A. tauschii accessions. However, preliminary work with APR transferred from one A. tauschii accession indicated that APR was quantitatively inherited (Kalia et al. 2014). The donor A. tauschii accessions is also resistant to stripe and stem rust as indicated by preliminary results (Kalia unpublished results) but it is not known if any of the APR genes is pleiotropic. Rusts are endemic to Middle East and have coevolved with wild wheat relatives for millions of years and with wheat crop since its domestication about 8000–12,000 years ago. The Caspian Sea region is the center of genetic diversity and origin of A. tauschii (Lubbers et al. 1991; Wang et al. 2013) and hot spot of defense related genes to different pathogens (Assefa and Fehrmann 2000). Our results confirm previous reports that southwestern Caspian Sea harbors high diversity for seedling resistance genes to rusts (Gill et al. 2008; Rouse et al. 2011). Our data indicate that it is one of the two centers of genetic diversity for APR. Humid and warm weather conditions in this region are ideal for occurrence of different foliar diseases and thus sustaining different pathogen populations. Co-existence and co-evolution of the host and rust pathogen (Vavilov 1939) have resulted in the huge genetic diversity for seedling and adult plant resistance of the A. tauschii populations from this region. Interestingly, the A. tauschii in central Asia and Afghanistan lacks seedling resistance but this region is a second center of genetic diversity for APR. Although both winter and spring wheat planting are practiced in Afghanistan, but wheat is usually planted in autumn and harvested in early summer. This region is arid with dry and cold winters during seedling stage in the 123 922 Genet Resour Crop Evol (2017) 64:913–926 100 2005 2006 2008 2009 90 80 Disease Severity (%) 70 60 50 40 30 20 10 0 Aegilops tauschii accessions Fig. 3 Phenotypic distribution of 17 A. tauschii accessions based on disease severity (%) to leaf rust during 4 years of testing from 2005 to 2009 Fig. 4 Geographical distribution of 371 A. tauschii accessions based on leaf rust reaction at seedling and adult plant stage (http://www.copypastemap.com) Color—Red color indicate accessions with susceptible reaction at seedling stage, green color indicates accessions with resistant reaction at seedling stage and yellow color indicates accessions with susceptible reaction at seedling stage and resistance at adult plant stage (APR). This category has 41 accessions autumn growing season and this may explain the lack of seedling resistance. A. tauschii is usually found as a weed in and around the edges of wheat fields. Less harsh climatic conditions in spring season may be more conducive to the development of the leaf rust during the heading stage of the wheat crop and hence 123 Genet Resour Crop Evol (2017) 64:913–926 the evolution of APR in A. tauschii populations from this region. Native agro-ecosystems have been implicated in the evolution of seedling resistance gene Lr21 (Huang et al. 2009) and similar mechanisms may have led to the evolution of APR genes. Additionally, contrary to seedling resistance, adult plant resistance to leaf rust was present in accessions collected from diverse geographic regions indicating APR is more widely distributed than seedling resistance (Fig. 4). Genetic diversity analysis has indicated incipient speciation of A. tauschii into two lineages L1 and L2, which appear to be reproductively isolated in nature although they produce fertile hybrids by artificial pollination (Kihara and Tanaka 1958). A. tauschii follows clear subdivision genetically but subdivision based on morphological traits and taxonomic classification is not precise (Lubbers et al. 1991; Wang et al. 2013). L1 lineage is usually restricted to elevations in the range of 400–3000 m above sea level whereas L2 lineage is adapted to 400–1500 m above sea level in Transcaucasia, and at elevations not higher than 25 m above sea level in Caspian Sea coast of Azerbaijan and Iran (Wang et al. 2013). There is also considerable morphological variation and several botanical varieties and subspecies have been described (Kihara and Tanaka 1958) and most of these belong to L2 lineage (Lubbers et al. 1991; Wang et al. 2013). A. tauschii Coss. subsp. strangulata (Eig) Tzvel. Broadly related to L2 lineage, is generally accepted as the D-genome donor of wheat. Vast majority of the accessions showing APR in this study belong to the L1 lineage, which is predominantly related to A. tauschii subsp. tauschii var. typica L. Thus introgression of APR will not only improve leaf rust resistance of wheat but would also enrich the genetic diversity of wheat’s D genome. Another implication of the data seems to be that agroecosystems associated with high altitudes are more conducive to the development of APR because almost all accessions showing APR belong to L1 lineage adapted to mid to high altitudes. Based on disease severity data collected in 4 years of field-testing, these 50 A. tauschii accessions can be roughly grouped into two categories—high and moderate APR, with few outliers. Wild relatives of wheat are known to carry several resistance genes to same pathogen. Accessions exhibiting high adult plant resistance are likely to carry either race-specific APR gene like Lr22a or combination of two or more minor genes (Hiebert et al. 2007). Adult plant resistance to 923 leaf rust followed a pattern across the range of geographic regions tested in this study. Adult plant resistance was high in A. tauschii accessions collected from Azerbaijan and southeastern Caspian Sea in Iran and somewhat intermediate in accessions from farther east growing in Uzbekistan and Afghanistan. It is likely that accessions from regions around Caspian Sea might carry more than one APR gene. Also, frequency of seedling resistance was high in accessions collected from Azerbaijan indicating that some of these adult plant resistant accessions might also carry additional genes that were effective to some races used in the study (Figs. 1, 4). Durability and effective levels of resistance can be achieved by either stacking up multiple race-specific resistance genes or by combining race-specific and race-nonspecific genes in a single cultivar (Kolmer et al. 2008). Ease in selection of resistance conferred by race-specific genes has made them popular with breeders. Although selection for seedling genes is relatively easier than that of APR, durability of resistance achieved by combining race-nonspecific APR gene Lr34/Yr18 with other genes has encouraged breeders to utilize race-nonspecific genes in breeding. Pyramiding two or more race-nonspecific resistance genes together to facilitate the development of durable resistance has become a well-known procedure in wheat breeding (Singh et al. 2011; Bariana et al. 2007). Our preliminary results indicate that a breeding strategy for introgression of APR genes to wheat will also need to be carefully worked out. The genes from A. tauschii to hexaploid wheat may be transferred either by synthetic crosses (McFadden and Sears 1944; Ogbonnaya et al. 2013) or by direct crosses (Gill and Raupp 1987). However, many instances of either dilution or suppression of resistance during transfers from lower ploidy to higher ploidy level have been reported (Kerber and Dyck 1979). Kerber (1964) used Triticum aestivum L. varieties, ‘Thatcher’ (2n = 42, AABBDD) and ‘Prelude’ to produce genetic stocks ‘tetraThatcher’ (2n = 28, AABB) (Thatcher/(TR.DR) Stewart-63//3*Thatcher) (http://www.wheatpedigree. net/sort/show/61051) and ‘tetraPrelude’ (2n = 28, AABB) (Prelude/(TR.DR)Stewart-63//5*Prelude) (http:// www.wheatpedigree.net/sort/show/61049). In ongoing research, we produced synthetic wheat (T. aestivum, 2n = 42, AABBDD) by crossing tetraThatcher and tetraPrelude with six A. tauschii accessions displaying 123 924 APR (Kalia et al. 2014; Kalia unpublished results). Unexpectedly, all synthetic hexaploids were susceptible to leaf rust. We crossed four synthetics with ‘Lal Bahadur’ lacking any known leaf rust gene and we did not recover any resistant progeny from all four progenies that were evaluated at El Batan, Mexico. However, we recovered effective APR from one cross of synthetic wheat with ‘WL711’, which seems to be controlled by at least three genes (Kalia et al. 2014). Although WL711 is known to carry Lr13, a defeated adult plant resistance gene, but it displayed high susceptibility in our field tests. (McIntosh et al. 1995). These brief results indicate the complexities of APR transfer from A. tauschii to wheat. In conclusion, we have identified seventeen A. tauschii accessions with effective levels of adult plant resistance and as potential donors of novel APR genes, which hold potential to enhance durability of wheat plant resistance to leaf rust. As preliminary results indicate, the transfer of A. tauschii APR genes to wheat will be a daunting task, however, it is feasible. Acknowledgments Contribution no. 15-039-J from the Kansas Agricultural Experiment Station. We thank Li Huang for her contributions to research during preliminary trials. Research was supported by a Monsanto Beachell-Borlaug International scholarship to Bhanu Kalia, Kansas Wheat commission, Kansas Agricultural Experiment Station and WGRC-I/UCRC NSF Grant (IIP-1338897). Compliance with ethical standards Conflict of interest The authors declare that they have no conflict of interest. References Assefa S, Fehrmann H (2000) Resistance to wheat leaf rust in Aegilops tauschii Coss. and inheritance of resistance genes in hexaploid wheat. Genet Resour Crop Evol 47:395–398 Assefa S, Fehrmann H (2004) Evaluation of Aegilops tauschii Coss. for resistance to wheat stem rust and inheritance of resistance genes in hexaploid wheat. Genet Resour Crop Evol 51:663–669 Bariana H, Brown G, Bansal U, Miah H, Staden G, Lu M (2007) Breeding triple resistant wheat cultivars for Australia using conventional and marker-assisted selection technologies. 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