Identification of different types of resistance to stripe rust Puccinia striiformis f. sp. tritici, in some dryland wheat genotypes of Iran

Research Article

Identification of different types of resistance to stripe rust Puccinia striiformis f. sp. tritici, in some dryland wheat genotypes of Iran

Safarali Safavi^1*, Farzad Afshari², Naser Mohammadi³ and Maghsoud Hasanpour-hossni³

1. Crop and Horticultural Science Research Department, Ardabil Agricultural and Natural Resources Research and Education Center, Agricultural Research, Education and Extension Organization, Ardabil, Iran.

2. Department of Cereal Research, Seed and Plant Improvement Institute, Agricultural Research, Education and Extension Organization, Karaj, Iran.

3. Department of Cereal Research, Dryland Agricultural Research Institute, Agricultural Research, Education and Extension Organization, Maragheh, Iran.

Abstract: Stripe (yellow) rust, caused by Puccinia striiformis f. sp. tritici (Pst), is a globally devastating wheat disease and a critical yield-limiting factor in Iran, often resulting in severe production losses and necessitating costly chemical interventions. The deployment of host resistance remains the most economical and sustainable management strategy. This study aimed to identify different types of resistance to stripe rust among dryland wheat genotypes to support cultivar improvement programs. A collection of 233 dryland wheat genotypes (comprising 120 winter bread wheat, 64 spring bread wheat, and 49 durum wheat) was evaluated for adult plant resistance (APR) under field conditions at the Ardabil Agricultural Research Station, Iran. Parallel seedling resistance screenings against two prevalent Pst pathotypes (6E6A+, Yr27 and 142E158A+, Yr27) were conducted under controlled greenhouse conditions. The results revealed a spectrum of resistance responses. Forty-six genotypes (19.7%) exhibited all-stage resistance (ASR) at the seedling level against both pathotypes, suggesting the presence of known seedling resistance genes such as Yr3b, Yr4, Yr5, Yr10, Yr15, YrSP, YrCV, YrSD, or other unidentified genes. Fourteen genotypes were susceptible as seedlings to at least one pathotype but displayed a low relative area under the disease progress curve (rAUDPC) value (0-10) in the field, indicating effective APR. Another 10 genotypes, susceptible at the seedling stage, showed moderate rAUDPC values (11-30), characteristic of slow-rusting (SR) resistance. The remaining 163 genotypes were highly susceptible (high rAUDPC) in the field, regardless of their seedling response. The resistant genotypes identified in this study, particularly those with APR and SR characteristics, represent valuable genetic resources for breeding programs aimed at pyramiding multiple resistance genes to develop durable resistance and achieve long-term control of stripe rust in Iran.

Keywords: Dryland wheat, Race-specific resistance, Non-race specific resistance, Durable resistance

Introduction[1][2]

Wheat stripe (yellow) rust, caused by the fungus Puccinia striiformis Westend. f. sp. tritici Eriksson (Pst) is a major foliar disease affecting wheat in temperate, cool, and high-altitude regions worldwide (Boyd, 2005). Present on all continents except Antarctica, it is widespread and consistently threatens global wheat production, with documented yield losses ranging from 30 to 100% (Chen, 2005). The economic importance of wheat rusts is undeniable; however, stripe rust is often considered more devastating and widespread than leaf or stem rust due to its direct impact on photosynthetic tissue, leading to severe foliar damage and significant reductions in grain yield and quality (Line, 2002; Chen, 2005).

The high adaptability of the Pst pathogen, facilitated by mutation, migration, and both vegetative and sexual hybridization, allows it to overcome resistance and thrive in diverse climatic conditions (Kolmer, 2005; Jin et al., 2010). This adaptability has led to frequent and severe epidemics. Over recent decades, major outbreaks have been reported across most wheat-growing areas of the world, including Iran, where epidemics in 1992 and 1994 resulted in yield reductions of 1.5 and 1 million tons, respectively (Torabi et al., 1995). Significant epidemics have also been documented in Central and West Asia, China, Australia, the United States, and North Africa (Chen, 2005; Wellings, 2011; Ziyaev et al., 2011; Morgounov et al., 2012). Globally, annual damage from wheat rusts is estimated at up to 15.04 million tons, underscoring the persistent threat to food security (Huerta-Espino et al., 2020; Basnet et al., 2022).

While chemical and cultural control methods can reduce damage, they are often impractical for farmers in developing countries and are not aligned with long-term sustainable agriculture priorities (Chen, 2005). Consequently, the deployment of host genetic resistance remains the most economical, effective, and environmentally safe strategy for managing stripe rust (Chen, 2007). Two primary types of genetic resistance are recognized: race-specific (all-stage) resistance and non-race-specific (adult plant) resistance. Race-specific resistance, which operates on the gene-for-gene principle (Flor, 1942), is often effective but can be rapidly overcome by evolving pathogen races, typically within 3–5 years (Line and Qayoum, 1992). In contrast, non-race-specific resistance, often controlled by minor-effect genes, is generally more durable. The most effective strategy for achieving long-lasting control is the pyramiding of both race-specific and non-race-specific resistance genes within a single cultivar (Singh et al., 2004). This approach necessitates the identification and characterization of diverse genetic resistance resources (Bux et al., 2011).

The evaluation of resistance, particularly quantitative adult plant resistance (APR) and slow rusting (SR), is best conducted under field conditions. Key parameters for quantification include final disease severity (FDS), the area under the disease progress curve (AUDPC), the relative AUDPC (rAUDPC), the apparent infection rate (r), and the average coefficient of infection (ACI) (Safavi and Afshari, 2012; Hei et al., 2015; Mohammadi et al., 2023). The rAUDPC is a particularly valuable integrated measure as it correlates strongly with components of slow rusting (e.g., latent period) and, importantly, with reduced yield loss (Sandoval-Islas et al., 2007; Ochoa and Parlevliet, 2007; Safavi, 2015). Field-based assessment is crucial because the correlation between greenhouse seedling tests and the expression of APR components in the field is often low (Sandoval-Islas et al., 2007).

Previous studies, both globally and in Iran, have successfully employed these methods to identify resistant sources. For instance, evaluations of international wheat collections have identified genotypes possessing all-stage resistance (ASR) genes such as Yr5, Yr10, and Yr15, as well as those with effective APR and SR (Bux et al., 2012; Zeng et al., 2014; Zahravi et al., 2019). Safavi and Afshari (2017) further demonstrated the diversity of resistance responses in Iranian wheat cultivars over a multi-year study.

Given the constant threat of new Pst races, identifying new and diverse sources of resistance remains a cornerstone of breeding programs. This study was therefore conducted to identify and characterize different types of resistance (seedling and adult plant) to stripe rust in a diverse collection of dryland wheat genotypes from Iran. The objective was to identify promising genetic stocks possessing effective ASR, APR, and SR to support breeding programs aimed at developing cultivars with durable resistance for sustainable wheat production.

Materials and Methods

Plant materials

A total of 233 dryland wheat genotypes (120 winter bread wheat, 64 spring bread wheat, and 49 durum wheat) provided by the Dryland Agricultural Research Institute were evaluated in this study. The characteristics of 70 selected genotypes, representing different resistance types from the initial set, are presented in Table 1.

Seedling resistance tests

Seedling reactions were assessed under controlled greenhouse conditions at the Seed and Plant Improvement Institute (Karaj, Iran). For each genotype, 5-7 seeds were sown in individual pots (7x7 cm) containing a soil: peat moss: sand mixture (7:5:5). Ten-day-old seedlings were inoculated separately with two distinct Puccinia striiformis f. sp. tritici pathotypes: 142E158A+, Yr27 (possessing a broad virulence spectrum) and 6E6A+, Yr27 (possessing a narrow virulence spectrum). The virulence/avirulence formula for these pathotypes is detailed in Table 2.

Table 1 Characteristics and stripe rust resistance responses of the evaluated dryland wheat genotypes at seedling and adult plant stages.

¹Wheat type: BW, bread wheat; DW, durum wheat.                                                              ²Growth habit: W, winter; S, spring; F, facultative.

³Seedling infection types were assessed against two Puccinia striiformis f. sp. tritici pathotypes—6E6A+, Yr27 (Pathotype 1) and 6E158A+, Yr27 (Pathotype 2)—using the scale described by McIntosh et al. (1995).

⁴Adult plant responses were recorded as final rust severity (FRS, %) and infection type (IT) according to Roelfs et al. (1992). The relative area under the disease progress curve (rAUDPC) was calculated to quantify disease progression. Infection type classifications: R (resistant; no sporulation), MR (moderately resistant; small pustules with necrosis), M (moderately resistant to moderately susceptible), MS (moderately susceptible; medium pustules, possible chlorosis), S (susceptible; large pustules without chlorosis or necrosis).

⁵Resistance type: ASR, all-stage resistance; APR, adult plant resistance; SR, slow rusting resistance.

Table 2 Virulence/avirulence profiles of Puccinia striiformis f. sp. tritici pathotypes employed in seedling resistance screening.

Inoculation was performed by spraying seedlings with a suspension of fresh urediniospores mixed with talcum powder (1:4 ratio). Following inoculation, the pots were placed in a dew chamber at 10°C with 100% relative humidity for 24 hours to facilitate infection. They were subsequently transferred to a greenhouse maintained at 8-10 °C with a 16-hour light/8-hour dark cycle. Infection types (ITs) were recorded 15-17 days post-inoculation using a 0-4 scale (McIntosh et al., 1995).

Adult plant resistance tests

Field evaluations were conducted during the 2018-2019 cropping season at the Agricultural Research Station in Ardabil, Iran (38.1705°N, 48.3907°E; altitude 1350 m). The same genotypes screened at the seedling stage were planted in a disease nursery. Each genotype was sown in two-row, 1-meter-long plots with 30 cm row spacing, using 8 grams of seed per plot.

To ensure uniform disease pressure, the highly susceptible cultivar 'Morocco' was planted as a spreader after every ten test genotypes and along the entire periphery of the nursery. Standard agronomic practices were followed, including flood irrigation (once in the fall and six times in the spring), weeding, and fertilization. Artificial inoculation was performed twice during the season, between stem elongation and flag leaf emergence, using a bulk mixture of urediniospores (collected from the previous season) and talcum powder applied by dusting. The bulk inoculum was virulent on seedlings carrying the resistance genes Yr1, Yr2, Yr6, Yr7, Yr9, Yr17, Yr22, Yr23, Yr24, Yr25, Yr26, Yr27, YrA, Yr21, Yr31, Yr32, and YrSU, and avirulent against Yr3v, Yr3a, Yr4a, Yr4, Yr5, Yr10, Yr15, Yr16, YrCV, YrSD, and YrND (Safavi, 2019).

Disease assessment and data analysis

Adult plant reactions were assessed based on infection type (IT) (Roelfs et al., 1992) and disease severity (DS), recorded as the percentage of leaf area affected (0-100%) (Peterson et al., 1948). Assessments began when disease severity on the 'Morocco' spreader rows reached approximately 50% and were repeated at 7-8 day intervals for a total of three recordings.

The area under the disease progress curve (AUDPC) was calculated for each genotype using the following formula (Milus and Line, 1986):

AUDPC = [N1(X1 + X2)/2] + [N2(X2 + X3)/2]

Where X1, X2, X3 are the rust intensities recorded on the first, second and third recording dates. N1 is the interval day between X1, X2 and N2 is the interval day between X2, X3.

To enable comparison across genotypes, the relative AUDPC (rAUDPC) was calculated as:

rAUDPC = (AUDPC of genotype/AUDPC of susceptible control) × 100

Classification of resistance types

Genotypes were classified into resistance groups by integrating seedling ITs with adult plant rAUDPC values, adapting methodologies from Bux et al. (2012) and Zeng et al. (2014):

All-Stage Resistance (ASR): Resistant (low IT) to both pathotypes at the seedling stage.

Adult Plant Resistance (APR): Susceptible (high IT) to at least one pathotype at the seedling stage but with low rAUDPC values (0-10) in the field.

Slow Rusting (SR): Susceptible to at least one pathotype at the seedling stage but with moderate rAUDPC values (11-30) in the field.

Susceptible: High rAUDPC values (> 30) in the field, regardless of seedling reaction.

Comparative graphs illustrating the reactions of different genotypes at both growth stages were generated using Microsoft Excel (Version 2010).

Results

Evaluation of seedling resistance

Screening 233 wheat genotypes at the seedling stage revealed distinct resistance patterns against the two pathotypes. When inoculated with pathotype 6E6A+, Yr27, a total of 155 genotypes exhibited resistance. This resistant group comprised 68 winter bread wheat, 28 durum wheat, and 59 spring bread wheat genotypes. A more virulent pathotype, 142E158A+, Yr27, overcame the seedling resistance of many lines, with only 113 genotypes showing resistance. This group included 66 winter bread wheat, 16 durum wheat, and 31 spring bread wheat genotypes (Fig. 1).

Notably, 97 genotypes (41.6% of the total) demonstrated resistance to both pathotypes, suggesting the presence of effective all-stage resistance (ASR) genes. This robust group consisted of 55 winter bread wheat, 12 durum wheat, and 30 spring bread wheat genotypes. However, seedling resistance alone is not always indicative of field performance. Several genotypes resistant at the seedling stage exhibited high disease severity in the field. After integrating data from both growth stages, 46 genotypes (19.7%) that were resistant to both pathotypes as seedlings also maintained effective resistance in the field and were selected for further analysis (Table 1). Furthermore, 24 genotypes (10.3%) that were susceptible to at least one pathotype as seedlings displayed various forms of resistance in adult plants, highlighting the presence of non-seedling types of resistance.

Assessment of adult plant resistance

To mitigate the potential influence of environmental variability on disease severity, this study used artificial inoculation, maintained optimal humidity through frequent irrigation, and incorporated susceptible checks at 10-genotype intervals. Due to favourable weather conditions at the experimental site, stripe rust became well established and spread across the wheat genotypes, enabling a careful assessment. Under field conditions, 66 genotypes were susceptible while 167 (71.7%) exhibited resistance. Among the resistant genotypes, the responses of winter bread wheat, spring bread wheat, and durum wheat varieties differed according to relative area under the disease progress curve (rAUDPC) values. Specifically, within these categories, 30 (25%) winter bread wheat, 43 (67.2%) spring bread wheat, and 26 (53%) durum wheat genotypes showed low rAUDPC values (0–10) and were classified as resistant (Figure 2). Another set of genotypes demonstrated intermediate rAUDPC values (11–30), comprising 37 (30.8%) winter, 16 (25%) spring, and 15 (30.6%) durum wheat types. Finally, a group with high rAUDPC values (> 30) consisted of 53 (44.2%) winter, 5 (7.8%) spring, and 8 (16.4%) durum wheat genotypes, which were categorized as susceptible.

Figure 1 Seedling infection responses of dryland wheat germplasm to two prevalent Puccinia striiformis f. sp. tritici pathotypes (6E6A⁺, Yr27 and 142E158A⁺, Yr27).

Figure 2 Evaluation of adult plant resistance to stripe rust in dryland wheat germplasm using relative area under the disease progress curve (rAUDPC).

Classification of resistance types

Integrating seedling and adult plant responses is crucial for characterizing the nature of resistance. Based on a combination of seedling infection types (ITs) and adult plant rAUDPC values, the genotypes were classified into distinct groups.

1. Adult plant resistance (APR) Group: This group consists of genotypes that were susceptible (high IT) to at least one pathotype at the seedling stage but displayed a low rAUDPC value (0-10) in the field. This phenotype is indicative of race-nonspecific adult plant resistance, which is often considered more durable. Fourteen genotypes (6%) were identified in this highly valuable category (Table 1).

2. Slow rusting (SR) group: This category includes genotypes that were susceptible at the seedling stage but exhibited moderate rAUDPC values (11-30) in the field. This pattern is characteristic of slow rusting resistance, conferred by combinations of minor-effect genes that reduce the epidemic rate. Ten genotypes (4.2%) were classified into this group, which also represents an important source of potentially durable resistance (Table 1).

3. All-stage resistance (ASR) group: This group comprised genotypes that exhibited resistance to both pathotypes at the seedling stage, indicating the presence of race-specific or all-stage resistance (ASR) genes. Although these genotypes may also possess non-race-specific resistance genes, their effects are often masked by dominant ASR genes (Ali et al., 2007; Dadrezaei et al., 2013). Of the 233 genotypes evaluated, 96 (41%) belonged to this category. However, due to susceptibility observed in some genotypes at the adult plant stage, only 46 genotypes demonstrating consistent resistance (R) or moderate resistance (MR) to infection types under field conditions are listed in Table 2. While these genotypes show promise, their race-specific resistance necessitates further multi-year and multi-location evaluations—preferably within advanced breeding programs such as those at the Seed and Plant Improvement Institute (Karaj)—to assess their durability against emerging pathotypes before any cultivar release considerations.

4. Susceptible group: Genotypes in this category were susceptible to both pathotypes at the seedling stage and displayed high rAUDPC values (>30) along with moderately susceptible to susceptible (MSS) or fully susceptible (S) infection types in adult plants. This susceptibility indicates the absence of both effective race-specific resistance genes against the tested pathotypes and functional adult plant resistance genes. A considerable number of genotypes fell into this group; however, their listings are omitted from Table 1 due to their susceptible phenotypes.

5. Seedling-specific resistance group: A subset of genotypes displayed resistance at the seedling stage but high disease severity, with moderately susceptible (MS) or moderately susceptible to susceptible (MSS) infection types, at the adult plant stage. This suggests that although these genotypes possess race-specific resistance genes, those genes are ineffective against the pathotype(s) prevalent in the field. The discrepancy between seedling and adult responses may be attributed to several factors: the field pathotype(s) might be present at low frequencies under greenhouse conditions, or may not have been included in the seedling screening panel. Alternatively, pathogen populations may overcome race-specific resistance over time and under prolonged field exposure. This underscores the limitations of relying solely on seedling tests for predicting field performance and highlights the need to incorporate adult-plant resistance into breeding programs.

Discussion

The comprehensive classification of genotypes into five distinct groups offers valuable insights into the diversity of resistance mechanisms within dryland wheat germplasm. The identification of genotypes exhibiting adult plant resistance (APR) and slow-rusting (SR) characteristics is particularly promising for developing varieties with durable resistance (Singh et al., 2011), in contrast to those with only race-specific resistance, which require careful management to avoid rapid breakdown. A notable strength of this study is the concurrent evaluation of winter bread wheat, spring bread wheat, and durum wheat genotypes—a comprehensive approach not frequently employed in investigations of Iranian dryland wheat germplasm. Our resistance grouping framework aligns with established methodologies for studying wheat-rust pathosystems (Tariq-Khan and Irfan-Ul-Haque, 2011; Dadrezaei et al., 2013; Zeng et al., 2014; Shah et al., 2014).

This work is underpinned by the fundamental principle that resistance genes have distinct expression patterns; APR genes are typically not expressed at the seedling stage, whereas all-stage resistance (ASR) genes are functional throughout plant development (Chen, 2005). Consequently, reliance solely on seedling assays is inadequate (Sandoval-Islas et al., 2007), as it may misclassify valuable sources of quantitative, non-race-specific resistance as susceptible. Our results confirm that genotypes that are susceptible as seedlings can exhibit high levels of quantitative resistance as adult plants, demonstrating that this resistance is more durable than race-specific resistance conferred by major ASR genes (Roelfs et al., 1992; Nazari et al., 2000). The well-documented lack of durability in monogenic race-specific resistance has driven breeders to prioritize slow-rusting resistance (Ali et al., 2007; Shah et al., 2010; Safavi and Afshari, 2017).

This type of race-nonspecific and durable resistance has been extensively studied in wheat, and efforts to incorporate it into elite cultivars are longstanding (Singh et al., 2011; Alo et al., 2018; Huerta-Espino et al., 2020; Hatami-Maleki et al., 2024). Notably, several genotypes identified in our study with superior resistance features are renowned international cultivars in their pedigrees, such as Tukuru, Kukuna, and Attila. These source cultivars are known to confer durable, multi-pathogen resistance through combinations of non-race-specific genes, such as Yr18, Yr29, Yr30, Yr36, and Yr46, often pyramided with resistance from germplasm such as Chapio and Kingbird (Singh et al., 2005; Singh et al., 2011). The genetic complexity and value of these slow-rusting genes are further underscored by their frequent pleiotropic effects and linkages with other agronomically important traits, as exemplified by research from CIMMYT showing that Yr18 (linked with the genes Lr34/Pm38/Sr57 /Bdv1/Stb1) is associated with leaf tip necrosis (Ltn1) and confers broad-spectrum resistance (Singh, 1992; Kumar et al., 2019). Similarly, Yr29 is linked with Lr46 and Ltn2 (Singh et al., 2005; Kumar et al., 2019), and Yr46 (linked with Lr67/Sr55/Pm46) is associated with Ltn3 and multi-disease resistance (Herrera-Foessel et al., 2011; Singh et al., 2015; Kumar et al., 2019).

This expanded genetic spectrum is critically needed for Iranian dryland wheat improvement, as older cultivars were historically based on a narrow set of major ASR genes, rendering them highly vulnerable to new Pst pathotypes (Nazari et al., 2000; Safavi and Afshari, 2017; Bux et al., 2011; Safavi, 2019). This vulnerability underscores the urgent need to diversify the genetic foundation of resistance. A highly effective strategy is the pyramiding of both minor- and major-effect resistance genes within a single cultivar using molecular marker-assisted selection. The development of cultivars that combine both types of resistance is fundamental to sustainable management, as they reduce disease prevalence and slow down pathogen evolution (Randhawa et al., 2012).

The choice of resistance strategy may also be informed by regional disease epidemiology (Zeng et al., 2014). In regions of Iran with late disease onset, APR genes are highly recommended, whereas areas with fall or early-season infection require a combination of seedling (ASR) and adult-plant resistance genes for comprehensive protection.

The present study provides valuable resources for such a strategy. The identified seedling resistance sources are likely to carry genes such as Yr3b, Yr4, Yr5, Yr10, Yr15, or other unknown genes, which can be pyramided with the identified APR and SR sources. For immediate breeding applications, genotypes exhibiting APR/SR should be prioritized for advanced multi-location trials due to their non-race-specific nature and stability. Conversely, genotypes with all-stage resistance require further multi-year and multi-race validation to ensure they are not vulnerable to emerging pathotypes. Future work must include molecular validation of the putative resistance genes, and the most promising lines should enter rigorous multi-location, multi-year trials conducted by relevant national institutes (e.g., the Seed and Plant Improvement Institute; the Dryland Agricultural Research Institute) to assess their stability against Iran's evolving Pst population as a prerequisite for potential cultivar release.

Conclusion

This study identified numerous wheat genotypes possessing seedling or all-stage resistance (ASR). Those resistant to both pathotypes at the seedling stage most likely carry effective genes such as Yr3b, Yr4, Yr5, Yr10, Yr15, YrSP, YrCV, and YrSD. Furthermore, a significant number of genotypes were characterized by adult plant resistance (APR) or slow-rusting (SR) resistance. The frequency of genotypes with APR and SR was notably higher in spring bread wheat than in winter bread wheat and durum wheat. These genetic resources provide a critical foundation for gene pyramiding strategies to achieve durable resistance. The integration of both APR and ASR into Iranian breeding programs is essential for the sustainable management of stripe rust.

Acknowledgments

This research was funded by the Dryland Agricultural Research Institute (Project No. 0-15-15-93112). The authors extend their sincere gratitude to all colleagues at the Institute and the Ardabil Agricultural and Natural Resources Research and Education Center for their invaluable assistance in conducting this study.

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