Abstract
Stripe rust (Puccinia striiformis f. sp. tritici, Pst) is an important disease of wheat in the United States and Pakistan. Genetic resistance in wheat is a cost-effective and convenient control measure. In the present study, resistance testing of 115 wheat landraces from Pakistan was carried out initially at the seedling stage with seven races of the pathogen, four from the USA and three from Pakistan. The germplasm showed a general lack of effective seedling resistance. Only two genotypes (PI 210916, PI 219752) were resistant against all races. Adult plants of the wheat genotypes were also tested at high temperatures under greenhouse conditions and at two field locations in Washington State. In the test with US Pst race PST-127, 28 (32%) of the landraces had seedling resistance and 41 (52%) had high-temperature adult-plant (HTAP) resistance. When tested with Pakistan isolate PK07-2, 14 (13%) of the wheat genotypes had seedling resistance and 61 (53%) had HTAP resistance. In the test with Pakistan isolate PK07-6, 32 (40%) had seedling resistance and 38 (48%) had HTAP resistance. In field tests, 94 (86%) genotypes were resistant and four (4%) were intermediate at Pullman, Washington; and 72 (89%) were resistant and none was intermediate at Mount Vernon, Washington. The greenhouse and field tests revealed that the majority of the wheat landraces possess HTAP resistance against stripe rust. These landraces should be useful genetic resources for developing stripe rust resistant cultivars in regions where climatic conditions are suitable for the expression of the durable type of resistance.
Résumé
La rouille jaune (Puccinia striifirmis f. sp. tritici, Pst) est une maladie importante du blé aux États-Unis et au Pakistan. Chez le blé, la résistance génétique est un moyen de lutte pratique et rentable. Dans cette étude, la résistance de 115 lignées pakistanaises a été testée, au départ, au stade de semis avec sept races d'agents pathogènes, 4 des États-Unis et 3 du Pakistan. Le plasma germinal a affiché un manque réel de résistance. Seulement deux génotypes (PI 210916 et PI 219752) étaient résistants à l'égard de toutes les races. Les plants adultes des génotypes de blé ont également été testés à haute température en serre ainsi que dans deux champs dans l'État de Washington. Au cours du test avec la race PST127, 28 lignées américaines (32 %) affichaient de la résistance au stade de semis et 41 (52 %) au stade adulte à haute température (RAHT). Dans les essais sur le terrain, à Pullman dans l'État de Washington, 94 (86 %) des génotypes étaient résistants et 4 (4 %) l'étaient moyennement, tandis qu'à Mount Vernon, dans le même État, 72 (89 %) étaient résistants et aucun ne l'était moyennement. Les essais en serre et au champ ont révélé que la majorité des lignées américaines de blé affichait la résistance RAHT contre la rouille jaune. Ces lignées devraient être utiles à titre de ressources génétiques pour développer des cultivars résistants à la rouille jaune dans des régions où les conditions climatiques se prêtent à l'expression de la résistance durable.
Introduction
Stripe rust (yellow rust), caused by Puccinia striiformis f. sp. tritici, is an important foliar disease of wheat. It occurs in temperate, moist and cool regions where wheat is grown (Boyd, Citation2005). All continents except Antarctica host this disease of wheat. In most of the wheat growing areas, stripe rust causes 10–70% grain losses depending on susceptibility of the cultivar, earliness of the initial infection and rate of disease development (Chen, Citation2005). Wheat growing regions in North America and Asia have been historically vulnerable to stripe rust. In the United States, stripe rust has been more destructive in the western U.S. (regions west of the Rocky Mountains) and has become increasingly important in the regions east of the Rocky Mountains (Chen et al., Citation2002; Chen & Penman, Citation2005, Citation2006). These wheat growing areas across the United States have suffered substantial yield losses and high cost of fungicides to reduce the damage (Chen et al., Citation2010). Similarly, the impact of the disease has been historically destructive in wheat growing areas across Pakistan. These areas span over 8 million ha of wheat, of which 70% remains prone to stripe rust (Singh et al., Citation2004; Chatrath et al., Citation2007). Epidemically, the disease has been a major production constraint in parts of Khyber Pakhtunkhwa (KPK), Punjab and Balochistan provinces (Khan et al., Citation2005). Its spread into hot areas of southern Punjab and Sindh province has also been recently observed. To control the disease, different measures such as fungicide use, agronomic practices and host genetic resistance are employed. Use of chemicals is expensive and not affordable in many developing countries. Whilst the cultural practices usually do not confer adequate control, host genetic resistance is a commonly preferred method being utilized worldwide.
Genetic resistances in wheat against rust diseases have been categorized as seedling resistance (also referred to as all-stage resistance) and adult-plant resistance (APR) (Chen, Citation2005). The former can be detected at the seedling stage and remains effective throughout all stages of plant growth. It is usually race-specific in nature and works according to the gene-for-gene hypothesis (Flor, Citation1971). Such type of resistance becomes ineffective when new races evolve through mutation, somatic or sexual recombination, or migration (Line & Qayoum, Citation1992; Line & Chen, Citation1995, Citation1996; Chen & Moore, Citation2002; Kolmer, Citation2005; Jin et al., Citation2010). In contrast, the APR can be race-non-specific and has the potential to be durable over time. High-temperature adult-plant (HTAP) resistance is a type of adult plant resistance. This type of resistance works under high temperature climates at later stages of plant growth (Chen & Line, Citation1995a , Citation1995b ). HTAP resistance is generally controlled by quantitative trait loci (Milus & Line, Citation1986; Chen & Line, Citation1995a , Citation1995b ).
Utilization of genetic resistance and its incorporation in wheat requires genetic resources with identified potential. These genetic resources have been categorized as wild relatives, elite cultivars and landraces. Wheat landraces are well recognized as important genetic resources offering resistance against biotic and abiotic stresses, including rusts. Landraces are also often considered a rich source of genetic diversity for resistance to pests, pathogens (Harlan, Citation1992), grain quality characteristics (Chaparzadeh et al., Citation2008), yield stability in conditions of traditionally low input agricultural systems, and morphological and agronomical traits (Strelchenko et al., Citation2008). In addition, landraces are abundant sources of alleles that can be used to improve gene pools of modern cultivars (Feldman & Sears, Citation1981; Nevo & Payne, Citation1987). The genetic diversity in wheat landraces also confers resistance to leaf rust (Van Ginkel & Rajaram, Citation1992), stem rust (Hare, Citation1997; McIntosh et al., Citation1998) and stripe rust (Van Dijk et al., Citation1988; Zhang, Citation1995). In Pakistan, many landraces have already completely disappeared and have been replaced by modern wheat varieties. The collection of wheat landraces in the last century has led to the need to characterize the collected germplasm to identify useful traits. Therefore, the present study was conducted to identify Pakistan wheat landraces with potential resistance against stripe rust to enhance wheat cultivar improvement efforts in the United States and Pakistan.
Materials and methods
Wheat germplasm and pathogen isolates
In total, 115 wheat landraces collected in Pakistan were obtained from USDA-Agriculture Research Service (ARS) National Small Grains Collections located at Aberdeen, ID, (USA). The experiment was conducted in the greenhouse located at USDA-ARS, Wheat Genetics, Quality, Physiology and Disease Research Unit, Pullman, WA (USA). A total of seven Pst isolates, four representing recently predominant races in the United States with wider virulence spectrum and three isolates from Pakistan, were used in the seedling tests. The Pakistani isolates represent the current virulence spectrum in the country (Rizwan et al., Citation2010).
Seedling testing
For the seedling test with each Pst isolate, five to seven seeds of each wheat genotype were planted in a plastic pot filled with a potting mixture of peat moss:perlite:sand:potting soil mix:vermiculite (6:2:3:3:4) with lime, Osmocote 14-14-14, and ammonium nitrate added at 1.7, 3.3 and 2.2 g L−1, respectively. The spring wheat ‘Lemhi’, susceptible to all tested races of Pst, was planted as a susceptible check along with a set of 20 US stripe rust wheat differentials (Chen et al., Citation2010) and 20 lines carrying single Yr genes for stripe rust resistance. The infection types displayed by differentials and single Yr gene lines were used as a basis for determining virulence and avirulence composition and identifying races. The seedlings were grown in a rust-free greenhouse (at diurnal temperature cycle gradually changing from 10 °C at 2:00 am to 25 °C at 2:00 pm with the 16 h light/8 h dark cycle). Seedlings at the two-leaf stage (about 10 days after planting) were uniformly dusted with a mixture of the urediniospores of a selected Pst isolate and talc (Sigma, St Louis, MO) at a ratio of approximately 1:20. After inoculation, the plants were placed in a dew chamber at 10 °C for 24 h and then transferred to a growth chamber operating at 16 h light and 8 h dark with diurnal temperature gradually changing from 4 °C at 2:00 am to 20 °C at 2:00 pm (Chen & Line, Citation1992a , Citation1992b ).
Evaluation of HTAP resistance
For the adult-plant testing, three seeds of each line were planted in plastic pots (14×14×15 cm) to obtain three plants of each line. ‘Lemhi’ was used as the susceptible check. Planting conditions were the same as those for the seedling test above. For high-temperature adult-plant (HTAP) test, three isolates were used (one from the United States (race PST-127) and two from Pakistan (PK07-2, PK07-6). These isolates carried broader virulence, representing all other isolates. One and half months after planting, plants at the boot to heading stage were inoculated with urediniospores mixed with talc (1:20) using a dusting pump. The inoculated plants were incubated at 10 °C for 24 h and then grown in a greenhouse section under controlled diurnal temperature cycles gradually changing between a minimum of 10 °C at 2:00 am during the 8-h dark period and a maximum of 30 °C at 2:00 pm during the 16-h light period. The test was repeated for each isolate. In the initial test, all 115 lines were tested against a Pakistan isolate PK07-2. Based on the infection type data of the given isolate, lines showing ITs 0 to 6 (with high to moderate resistance) were selected for further testing with additional isolates/races.
Field testing
The same set of the 115 Pakistan landraces were evaluated for stripe rust resistance at adult-plant stage in field tests. These lines were planted in experimental fields in late April 2010 on the Whitlow farm near Pullman in eastern Washington and Mt. Vernon in western Washington. The two locations are about 500 km apart and have very different environmental conditions and different virulent populations of the wheat stripe rust pathogen. Natural inoculum initiated epidemics at both locations. Each plot consisted of a 1-m row spaced 0.3 m, with a border of the stripe rust susceptible wheat cultivar (‘Lemhi’) as disease spreader rows. Stripe rust infection types (IT) and disease severity (percentage of leaf area infected) on plants were recorded at the jointing stage (Zadoks stage 31–32) and the flowering stage (Zadoks stage 60) in Mt. Vernon, and once at milk stage (Zadoks stage 70) at Whitlow farm near Pullman.
Disease evaluation
Disease evaluation of seedlings and adult plants under greenhouse and field conditions was carried out based on a 0–9 scale as described by Line and Qayoum (Citation1992). Infection types (ITs) 0–5 were recorded as avirulent and 6–9 as virulent on differential genotypes for Pst isolates (Chen et al., Citation2010). ITs 0–3 were considered resistant reactions, ITs 4–6 were considered intermediate, and ITs 7–9 were considered susceptible reactions.
Results
Seedling testing
The Pakistan landraces and a set of 40 wheat genotypes, consisting of 20 each of the US wheat stripe rust differentials and Yr single-gene lines for stripe rust resistant genes, were evaluated against the four isolates from the United States and the three isolates from Pakistan. Reactions of differential genotypes are given in . Thirty-seven of the 40 differential and single-gene genotypes were susceptible to all tested US races. The single-gene lines for resistance genes Yr5, Yr15 and YrSP were resistant to all of the seven Pst isolates. Virulence variation was also observed amongst the US races. Significantly, the near-isogenic line containing Yr10 was observed susceptible to PST-114 and PST-116 but resistant against all other races including PST-127, whereas the Yr17 near-isogenic line (AvSYr17NIL) was resistant to the isolate of PST-116 but susceptible to other three US isolates. Thirty-three of the 40 differential genotypes were classified as susceptible to one or more of the Pakistan Pst isolates. Isogenic lines with genes Yr5, Yr10, Yr15 and YrSP were found to be resistant. Virulence variation was also observed amongst the Pakistan races. The near-isogenic line containing Yr24 was observed susceptible to PK07-12 but resistant against isolates PK07-2 and PK07-6. Similarly, Yr25 was not effective against PK07-2, but effective against other tested isolates.
Table 1. Virulence/avirulence profile of wheat stripe rust pathotypes detected on the seedlings of US differentials and near-isogenic lines (NILs)
Pakistan wheat landraces were tested at seedling stage against stripe rust using seven isolates, four from the United States with each representing a different race and three from Pakistan with broad virulence patterns. Based on the seedling IT data, the genotypes were divided into three groups – resistant, intermediate and susceptible. Frequency distribution of the three groups is given in , while the raw data are presented in the supplementary material (Supplementary material is available via a multimedia link on the online article webpage). Test results indicated that the majority of landraces were susceptible at the seedling stage against races from both countries. When all isolates were considered, two (2%) of the genotypes (PI 210916, PI 219752) were resistant while 34 (14%) were susceptible to all seven isolates/races.
Table 2. Frequency distribution (%) of wheat landraces classified into different categories of resistance under greenhouse and field conditions
Evaluation of HTAP resistance
Adult plants of wheat landraces were tested in the greenhouse at high temperatures with three selected isolates; one from the United States and two from Pakistan. The genotypes were grouped into three classes – seedling resistant, HTAP resistant and susceptible. The first class of accessions designated as seedling resistant showed resistance at both seedling and adult-plant stages against the same isolate. Genotypes in the second class (i.e. HTAP resistant) were susceptible at the seedling stage and resistant to moderately resistant at adult-plant stage (IT 0–6). The susceptible category shows their susceptibility at both seedling and adult-plant stages. Frequency distribution of these groups is given in .
The initial testing of 115 wheat landraces with Pakistan isolate PK07-2, demonstrated that 14 (12%) of genotypes had seedling resistance, 61 (53%) had HTAP resistance and 40 (35%) were susceptible. Cultivars showing resistant (IT 0–3) and intermediate (IT 4–6) reaction types were selected for further testing with additional isolates. Among the 79 selected wheat genotypes tested with the US race PST-127, 28 (35%) cultivars had seedling resistance, 41 (52%) had HTAP resistance and 10 (13%) were susceptible. Testing of Pakistan isolate PK07-6 showed that 32 (41%) accessions had seedling resistance, 38 (48%) had HTAP resistance and nine (11%) were susceptible.
Field testing
The same set of 115 Pakistan wheat genotypes were evaluated in adult-plant stage against stripe rust under natural epidemics at two environmentally diverse locations, Pullman and Mt. Vernon in Washington State. Frequencies of accessions resistant, intermediate and susceptible are displayed in . Of the 115 genotypes, 94 (86%) and 72 (89%) cultivars were resistant, at Pullman and Mt. Vernon, respectively. Only four (4%) genotypes were classified as intermediate at Pullman. Field data from both locations revealed that the majority of the genotypes showed HTAP resistance. However, some different responses were recorded between the two locations. Four genotypes were either susceptible or intermediate at one and resistant (or intermediate) at another location. Furthermore, at the Mount Vernon location, data were recorded at two stages, jointing and flowering. Variation was also observed in the responses of the same cultivars at different stages. Two genotypes (PI 270000, PI 270002) were recorded as susceptible or intermediate at jointing stage and resistant at flowering stage. Conversely, a few landraces showed resistant or intermediate reactions at jointing stage and susceptibility at flowering stage.
Seedling and adult stage data in the greenhouse and field conditions displayed that two cultivars (PI 210916, PI 219752) were resistant in all tests. The majority of the genotypes were susceptible at seedling stage and resistant at adult-plant tests in greenhouse and field tests, which is consistent HTAP resistance.
Discussion
The present study revealed commonality in virulence of the tested isolates of P. striiformis f. sp. tritici races from Pakistan and the United States. This is because the isolates selected for evaluating resistance in the Pakistan landraces each have a broad virulence spectrum (Chen et al., Citation2010; Rizwan et al., Citation2010; Chen & associates, unpublished data). Among the tested resistance genes, only Yr5, Yr15 and YrSP were effective against the isolates from both countries. In addition, Yr10 was effective against the tested Pakistan isolates. The high level of virulence within P. striiformis f. sp. tritici populations from both countries has previously been documented (Bux, Citation2011). This commonality in virulence has multiple advantages to control the pathogen. Most importantly, the wheat germplasm with effective resistance in the United States can be introduced to Pakistan. Similarly, the germplasm with potential resistance against the stripe rust pathogen in Pakistan can be used in wheat breeding programmes in the United States.
The seedling test of wheat landraces displayed lack of seedling resistance as the majority of the landrace cultivars were susceptible at the seedling stage. However, two lines (PI 210916, PI 219752) were identified with seedling resistance, indicating that these genotypes may possess a combination of defeated resistance genes, one of the effective resistance genes (such as Yr5, Yr15 and YrSP) or new resistance genes. Genetic and molecular mapping studies should be conducted to identify the resistance genes in these genotypes.
Although the genotypes were largely susceptible at the seedling stage, the disease responses at the adult-plant stage tested under greenhouse and field conditions revealed enormous potential for adult-plant resistance against the stripe rust pathogen. Wheat researchers across the world are working to identify and develop wheat cultivars with durable resistance against stripe rust or other rust diseases to achieve sustainable control. The genotypes showing HTAP resistance in the present study could be valuable sources in breeding programmes to develop cultivars with durable resistance. Further studies are needed to identify resistance genes in these genotypes and develop molecular markers for the genes to make use of the resistance sources more efficiently.
HTAP resistance has been successfully adopted in the United States (Chen, Citation2005). The present study has identified Pakistan landraces with HTAP resistance. These resistant genotypes may also serve as a potential genetic resource to develop wheat cultivars with diverse genes conferring HTAP resistance. Currently, the use of HTAP resistance in Pakistan has not yet gained practical importance. The accessions identified with HTAP resistance will serve as novel germplasm for breeding resistant cultivars for wheat growing areas of Pakistan such as southern Punjab and Sindh, where high temperature climates are suitable for the expression of such kind of resistance against stripe rust. According to current observations, stripe rust is spreading to these areas with average high temperature conditions. To combat stripe rust epidemics in hot areas, the use of HTAP resistance will be valuable and could enhance wheat cultivar improvement efforts nationally.
tcjp_a_662998_sup_24225350.docx
Download MS Word (39.6 KB)Acknowledgements
We thank Higher Education Commission (HEC) Pakistan for financial support for the research conducted. We are grateful to USDA-Agriculture Research Service (ARS) National Small Grains Collections located at Aberdeen, ID, (USA) for providing germplasm.
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