Powdery Mildew Resistance Gene (Pm) Stability and Blumeria graminis f. sp. avenae Virulence Trends in Poland (2021–2023): Challenges to Durable Resistance in Oat

Abstract

Oat (Avena sativa L.) is a widely cultivated cereal crop valued for both its nutritional benefits and agricultural versatility. However, oat production is increasingly challenged by powdery mildew, which is caused by Blumeria graminis f. sp. avenae (Bga) and can lead to considerable yield losses. Genetic resistance remains the most sustainable and environmentally friendly method of disease control. This study aimed to evaluate the effectiveness of 14 oat genotypes carrying known resistance genes (Pm1–Pm12) and Avena strigosa accessions against Bga populations collected across four regions of Poland between 2021 and 2023. Host–pathogen assays were used to assess resistance levels, virulence frequency, and pathotype diversity. Resistance genes were categorized into three groups based on performance: highly effective (Pm2, Pm4, Pm5, Pm7 in APR122 and A. strigosa), variably effective (Pm7 in ‘Canyon’ and Pm9–Pm12), and moderately effective (Pm1, Pm3, Pm6 and Pm3+8). Pathogen populations exhibited decreasing virulence complexity and diversity over time, with substantial regional variation. There were few dominant pathotypes, but most were rare and transient. This study confirms the long-term effectiveness of several resistance genes and the necessity of continuous resistance monitoring. It supports the use of gene pyramiding to ensure durable, regionally adapted protection. These results highlight the importance of combining resistance breeding with integrated disease management to ensure sustainable oat production under changing environmental conditions.

1. Introduction

Oat (Avena sativa L.) is one of the most important cereal crops cultivated worldwide, ranking as the fifth most widely grown cereal globally according to the FAO [1]. In 2023, global oat production was geographically diverse, with Europe producing 59.1%, followed by the Americas (28%), Asia (6.5%), Oceania (5.3%), and Africa (1.1%). Oats are an annual grass species known for their unique, multifunctional characteristics and nutritional benefits [1]. Oats have primarily been cultivated to feed animals; however, due to their health-promoting properties and the increasing number of vegetarians, they have become more popular in human diets in the form of oat-based products such as oat milk [2,3]. They are also used extensively for medical purposes [4].

Despite these favorable characteristics, oat cultivation faces substantial challenges from various biotic and abiotic stresses, with fungal pathogens representing a major threat to crop productivity. Blumeria graminis f. sp. avenae (Bga), an obligate biotrophic fungus, is one of the most damaging agents affecting oat foliage [5,6]. Infection caused by this pathogen can result in significant economic losses, typical yield reductions are around 10% but severe outbreaks can result in losses of 39% [7,8,9]. In the United States alone, powdery mildew has been responsible for yield losses estimated between 20% and 33% [10].

The incidence fungal disease in cereal crops can be reduced through genetic resistance [11,12]. A sustainable and environmentally friendly plant protection system is of important economic and ecological importance. According to the principles of integrated pest management [13], the use of disease-resistant varieties is a key approach to limiting and controlling pathogen occurrence, offering an attractive alternative to chemical plant protection products [14,15,16]. Furthermore, sustainable management of powdery mildew and understanding pathogen structure aligns with contemporary agricultural paradigms, particularly Integrated Plant Management (IPM), which combines biological, mechanical, and agrotechnical strategies to maintain pathogen populations at economically acceptable levels [17,18]. This approach is particularly important in the context of modern agriculture’s excessive dependence on chemical pesticides [19], including the rapid development of pathogen resistance [19,20], degradation of biodiversity [21], ecosystem disruption [22], and negative impacts on human and animal health [23].

The dynamic nature of plant-pathogen interactions presents significant challenges to the durability of genetic resistance. Fungal pathogens can quickly adapt to environmental conditions and overcome resistance mechanisms [24]. Therefore, adopting a dual approach understanding to plant–pathogen interactions is critical. From the plant perspective, the identification of resistance genes, gene pyramiding, and continuous evaluation of their effectiveness are essential. Conversely, from the pathogen perspective, monitoring changes in population structure, evolutionary dynamics, and virulence frequency distribution is crucial. Comprehensive knowledge in these areas provides a foundation for developing novel and effective strategies for pathogen prevention, control, and potential eradication. Ultimately, such strategies contribute to minimizing yield losses due to plant diseases while supporting sustainable agricultural practices and reducing negative environmental and public health impacts. Monitoring evolutionary and demographic changes in pathogen populations is therefore indispensable for implementing timely and adequate protective measures [12,25,26,27].

The challenge of managing Bga is compounded by the pathogen’s highly dynamic population structure and continuous evolution through mutation, migration, and genetic recombination processes [28,29]. To date, 13 resistance genes against powdery mildew (Blumeria graminis f. sp. avenae) have been identified in oat [30,31,32,33,34,35]. However, previous studies demonstrated that only four of these genes (Pm2, Pm4, Pm5, and Pm7) provide effective resistance under natural pathogen pressure. Therefore, regular evaluations of the effectiveness of individual resistance genes, along with continuous monitoring of virulence levels in pathogen populations, are essential to ensuring durable resistance and effective disease control in oat cultivation. This study aims to assess the effectiveness of oat resistance genes against powdery mildew during the 2021–2023 period, which will facilitate the selection of the most suitable genes for use in breeding programs.

2. Materials and Methods

2.1. Differential Sets

The set of 14 genotypes was used as a differential reference set (Supplementary Table S1). This set included genotypes carrying the previously described powdery mildew resistance genes Pm1–Pm12, as well as A. strigosa genotypes [36] that are effective sources of resistance to Bga. Among the reference set, two genotypes carrying the Pm7 gene (line APR122 and the cultivar Canyon) were included, as previous studies demonstrated that these two genotypes exhibit different infection responses despite sharing the same resistance gene [37,38,39]. In the tested group, the cultivar Rollo was used as a representative of the Pm3+8 gene combination, since no genotype possessing the Pm8 gene alone was available. The reference set also included the Fuchs cultivar, which is susceptible to powdery mildew infection [39].

2.2. Pathogen Collection

Pathogen samples were collected in Poland over a three-year period (2021–2023) from four different locations (Figure 1) situated in areas with diverse environmental conditions, yet sharing the common feature of fertile soils that support intensive agricultural use: Polanowice, Lublin, Strzelce and Choryń. Polanowice (50°11′56″ N 20°04′33″ E), located within the Lesser Poland Upland, is characterized by gently rolling terrain with moderate slopes. Lublin (51°15′ N 22°34′ E), located in eastern Poland, lies on the Lublin Upland. It extends across a hilly loess plain. Strzelce (52°18′50″ N 19°24′24″ E), located within the Central Polish Lowland. It is set in predominantly flat to gently undulating terrain. Choryń (52°02′23″ N 16°46′01″ E), situated in the Greater Poland, features flat topography and fertile soils. Although the four sites differ in topography and regional setting—from loess uplands to central lowlands—they are unified by the presence of productive soils that underpin intensive and diversified agricultural practices.

The dataset comprised three temporal populations, each representing a different year. Within each population, four subpopulations were distinguished according to location, with 10 single-spore isolates per site, giving a total of 120 isolates.

Leaves of oat cultivars infected with Bga were randomly collected from fields belonging to both private farms and plant breeding companies. Under laboratory conditions, single-spore isolates were obtained from each sample, following the methodology previously described by Hsam et al. [40,41].

2.3. Host–Pathogen Tests

Seeds of each differential were sown in a pot filled with gardening peat substrate and placed in a mildew-proof growing chamber under natural daylight.

Three leaf segments of each differential were placed in 12-well culture plates with 6 g/L agar and 35 mg/L benzimidazole. The plates containing leaf segments were inoculated in a settling tower by spreading 500–700 powdery mildew spores per 1 cm². These plates were then incubated in a growing chamber at 17 °C and under approximately 4 kLx of illuminance.

2.4. Effectiveness of Pm Genes and Bga Population Diversity

The reaction type on each differential was determined 10 days after inoculation and scored according to a 0–4 modified scale described by Mains [42]; where 0 = no infection, no visible symptoms; 1 = highly resistant, fungal development limited, no sporulation; 2 = moderately resistant, moderate mycelium with some sporulation; 3 = moderately susceptible, extensive mycelium, more sporulation; 4 = highly susceptible, large colonies, and abundant sporulation. If disease symptoms were scored as 0 or 1, the resistance gene was classified as effective. A score of 2 indicated that the gene was moderately effective, while scores of 3 or 4 indicated that the resistance gene was ineffective or susceptible. The host–pathogen tests also enabled the assessment of Bga population virulence. Isolates with disease scores of 0, 1, or 2 were classified as avirulent toward the respective resistance genes, whereas scores of 3 or 4 indicated virulence.

The observed virulent and avirulent reactions were converted into a binary coding matrix for computational analysis. Based on this matrix, the analyzed Bga isolates were classified into appropriate pathotypes, following the methodology described by Okoń et al. [43].

The parameters used to compare all Bga populations were calculated based on the virulence patterns of isolates tested on a set of differential genotypes. The virulence frequency (p) was calculated for each year using the formula p = x/n, where x represents the number of times a virulent reaction was observed, and n is the total number of isolates tested in a given year. For each isolate, the total number of virulent reactions was determined and reported as its virulence complexity. The frequency distribution of virulence complexity was also calculated separately for each year.

Diversity within the pathogen populations was assessed using multiple parameters. Genetic diversity was estimated based on the pathotype structure of the populations using indices such as Simpson’s diversity index (Si), Shannon’s diversity index (Sh), and Rogers’ genetic distance (R). Gene diversity was evaluated based on virulence structure using Nei’s index (Hs), which corresponds to the average dissimilarity within a population (ADWm) derived from the simple mismatch coefficient (m), and Nei’s genetic distance (N). Additionally, Kosman’s indices were applied to assess both diversity (KWm) and genetic distance (KBm), incorporating information from both the pathotype and virulence structures of the populations [44,45,46]. All computations involving population parameters were performed with the HaGiS program [47] and VAT ver 4.6.1. software [46,48].

3. Results

3.1. Pm Gene Effectiveness

The powdery mildew resistance genes analyzed in this study exhibited varying levels of effectiveness depending on both the year of assessment and the origin of pathogen populations (Figure 2). To better visualize these differences, the genes were grouped according to their overall effectiveness across the observation period using the UPGMA clustering method. This approach allowed for the identification of general patterns in resistance performance, highlighting the temporal and spatial variability of gene effectiveness. Analyses performed separately for each location and year consistently grouped the genes into three major clusters. The first group includes genes that maintained consistently high resistance across locations and years. The second group comprises genes with variable effectiveness depending on specific locations and years. The third group contains genes showing low or initially low effectiveness, some of which increased in effectiveness over time. The detailed results for each group are presented below.

The first group includes genes that remained highly effective across all locations and years. The Pm2, Pm4, Pm5, and Pm7 (line APR122) genes showed very high resistance and were not overcome by any isolates in any of the studied locations. Although occasional mild infection symptoms were observed for Pm7, these were likely caused by particularly virulent isolates and did not substantially reduce its overall effectiveness. The resistance identified in A. strigosa also exhibited a high level of effectiveness in all locations and years, with isolates only occasionally able to infect lines carrying this source of resistance, even then, infection was at a high or moderate level.

The second group consists of genes whose effectiveness varied markedly by location and year of observation. The Pm9, Pm10, and Pm11 genes generally showed moderate to variable resistance, with Pm10 and Pm11 notably increasing in effectiveness in 2023 across all locations. In contrast, Pm12 demonstrated a clear and considerable improvement over the years: initially demonstrating moderate or low resistance in 2021 across all locations, its effectiveness changed, reaching complete resistance by 2023, when no isolates were able to overcome it. Throughout this study, the Pm7 gene present in the Canyon cultivar showed a consistently lower level of resistance compared to the Pm7 gene in the APR122 line, with only sporadic infection symptoms observed.

The third group consists of genes that initially showed low effectiveness but demonstrated some improvement over time. The Pm1, Pm3, Pm3+8 gene combination, and Pm6 genes demonstrated low overall effectiveness, with some variation depending on location and year. The Pm3 gene showed low effectiveness in Strzelce, Choryń, and Lublin during the entire study period, with only a few isolates unable to overcome its resistance. In Polanowice, complete resistance associated with Pm3 was observed in 2021, but isolates capable of breaking this resistance appeared in subsequent years. The combination of Pm3 and Pm8 in the cultivar Rollo also showed variable resistance depending on location and year. In Strzelce, Choryń, and Lublin, this combination had low effectiveness, with only a few isolates unable to overcome resistance. In Polanowice, these genes provided complete resistance in 2021, but this was overcome in 2022; in 2023, resistance remained effective against four out of ten isolates. The Pm6 gene exhibited complete susceptibility in Strzelce throughout the study period, showing only moderate effectiveness against a few isolates. In Lublin and Polanowice, single isolates failed to overcome Pm6, whereas in Choryń, this gene was highly effective; it showed high or moderate effectiveness against nearly all isolates in 2021, reached peak effectiveness in 2022 with no isolates overcoming it. In 2023, remained effective against half of the isolates from Choryń.

3.2. Bga Virulence Frequency

The Bga isolates belonging to the analyzed populations exhibited a high level of virulence against the Pm1, Pm3, Pm6, and Pm3+8 genes which persisted throughout all years of observation. Conversely, a low level of virulence was observed against the Pm7 gene in the Canyon cultivar and against Pm9, Pm10, and Pm12. For the Pm11 gene, virulence frequency was high in 2021 and 2022, exceeding about 0.85, but decreased sharply to 0.1 in 2023. A very low frequency of virulence against the resistance source derived from Avena strigosa was observed.

All tested isolates collected over the three consecutive years were avirulent to reference forms carrying the Pm2, Pm4, Pm5, and Pm7 (line APR122) genes. Detailed results of the virulence frequency analysis for each population are presented in

Table 1. Virulence frequencies of Blumeria graminis f. sp. avenae isolates sampled in 2021–2023 in four locations in Poland.

Reference Set	Year			Location
	2021	2022	2023	Lublin	Strzelce	Polanowice	Choryń
Pm1	1	1	0.95	1	0.933	1	1
Pm2	0	0	0	0	0	0	0
Pm3	0.725	0.725	0.825	0.867	0.867	0.367	0.967
Pm4	0	0	0	0	0	0	0
Pm5	0	0	0	0	0	0	0
Pm6	0.675	0.7	0.725	0.833	0.9	0.767	0.3
Pm7 in APR122	0	0	0	0	0	0	0
Pm7 (in Canyon)	0.45	0.075	0.175	0.267	0.2	0.267	0.2
Pm3+8	0.75	0.85	0.575	0.767	0.8	0.433	0.9
Pm9	0.25	0.375	0	0.2	0.233	0.233	0.167
Pm10	0.575	0.425	0.025	0.267	0.333	0.3	0.467
Pm11	0.875	0.85	0.1	0.6	0.633	0.567	0.633
Pm12	0.325	0.075	0	0.033	0.167	0.167	0.167
A. strigosa	0.025	0.05	0	0.067	0.033	0	0
Fuchs	1	1	1	1	1	1	1

.

3.3. Complexity

The pathogen populations analyzed exhibited variable virulence complexity depending on the year of collection (Figure 3). A general decline in complexity was observed over the years, reflecting a reduced ability of isolates to overcome multiple resistance genes simultaneously. The isolates most frequently overcame resistance conferred by five genes (33% of isolates in 2021 and 38% in 2022) and six genes (25% in 2021 and 30% 2022) out of the 14 genes included in the differential set. In 2021, isolates capable of overcoming resistance from seven, eight, or even nine genes simultaneously were identified. In 2022, isolate complexity reached up to seven genes. However, in 2023, a noticeable decrease in complexity was observed. Isolates from that year most commonly overcame resistance conferred by four genes (35%), two and three genes (20%), or five (15%) genes. Only one isolate capable of overcoming resistance to six genes was detected. Throughout the entire study period, no isolates were identified that could overcome resistance conferred by 10 or more genes simultaneously. The highest virulence complexity was observed in the population collected from Strzelce, where isolates capable of overcoming resistance to between two and nine genes were identified. The Lublin population showed isolates overcoming resistance to three to nine genes, while the Polanowice population included isolates overcoming resistance to one to seven genes. The population from Choryń exhibited the lowest complexity, with isolates capable of overcoming resistance to two to seven genes.

3.4. Pathotype Structure

The pathotype structure of the Bga populations showed considerable diversity, both in terms of frequency and temporal distribution (Figure 4). Among the 120 tested isolates, TBBB was the most frequently identified pathotype, accounting for the highest number of isolates across all three years. This pathotype was virulent towards the Pm1, Pm3, Pm4 genes and towards the Pm3+8 gene combination. It showed an avirulent reaction towards the remaining genes. Its consistent presence indicates a stable and widespread virulence profile.

The second most frequent pathotype was TBCB which was virulent towards the genes from the first code group (Pm1, Pm3, Pm4 Pm3+8) and the Pm11 gene, was avirulent towards the remaining genes. Although TBCB was detected in relatively few replicates per location, it was found in each year of the study and in all four locations. Its frequency, however, remained notably lower than that of TBBB.

The SBBB (breaking the resistance of Pm1, Pm3 and Pm6 genes) and TBMB (breaking the resistance of genes Pm1, Pm3, Pm6, Pm3+8, Pm7 (Canyon) and Pm11) pathotypes ranked third in terms of occurrence, but they were not detected in all years of observation. Less frequent pathotypes included RBBB (breaking the resistance of genes Pm1, Pm3, Pm3+8) and RBMB (breaking the resistance of genes Pm1, Pm3, Pm3+8, Pm7 (Canyon) and Pm11), which were found in multiple years, suggesting their persistence in the pathogen populations. These pathotypes typically occurred at moderate frequencies and were often shared between two or more locations.

In contrast, the majority of pathotypes were rare, each represented by only one or two isolates. These included NBFL, MBCB, LBFL, and RBKL, among others, many of which were recorded only in a single year, indicating transient appearances or localized emergence. Such pathotypes may represent either newly arising virulence combinations or remnants of past selective pressures.

The distribution over time showed a decline in pathotype diversity. While 2021 and 2022 each displayed a relatively broad spectrum of pathotypes, including several unique variants, 2023 was characterized by a narrower profile, dominated by a few frequent types and a noticeable reduction in single-occurrence pathotypes. This trend suggests either a shift in selection pressure or a potential bottleneck effect reducing diversity.

3.5. Diversity Within Populations

Various types of diversity parameters were calculated for individual populations and subpopulations. All obtained results are presented in

Table 2. Diversity parameters of the analyzed Bga populations.

Diversity Parameters	Year			Localization
	2021	2022	2023	Lublin	Strzelce	Polanowice	Choryń
Gene diversity (Nei index Hs) equivalent to ADWm diversity	0.219	0.176	0.119	0.176	0.186	0.217	0.167
Simpson index Si	0.956	0.943	0.85	0.927	0.944	0.94	0.922
Shannon normalized index Sh	0.884	0.824	0.624	0.829	0.881	0.873	0.789
Kosman index KWm	0.327	0.247	0.163	0.236	0.244	0.324	0.24

. These results indicate that the diversity of the Bga population in Poland varies between years. The highest coefficients were observed for the population collected in 2021, confirming its highest level of diversity. However, the population collected in 2023 is characterized by the lowest diversity. Considering the locations, isolates collected in Polanowice were the most diverse, while those from Lublin were the least diverse.

4. Discussion

Genetic resistance of plants to pathogens is a natural, heritable defense mechanism, which is encoded in the plant genome and based on complex interactions between resistance genes and pathogen genes. According to the gene-for-gene interaction model, a plant initiates a defense response when a resistance (R) gene in the plant is compatible with an avirulence (Avr) gene in the pathogen [49,50]. Resistance genes, therefore, play a central role in modern plant protection strategies, and the use of genetic resistance in crop breeding, as well as determining its level of effectiveness, allows for a significant reduction in fungicide applications. This supports the sustainable development of modern and environmentally friendly agriculture [14,15,24]. However, despite the identification of numerous R genes in plants, pathogens possess the ability to evolve rapidly, enabling them to evade recognition by the plant’s immune system. For this reason, continuous monitoring of the effectiveness of resistance genes and the adaptation of pathogen populations remains essential. The present study was designed to evaluate the effectiveness of selected resistance genes in common oat against powdery mildew, continuing the research initiated by Okoń [37]. At the same time, it addresses the analysis of changes in the virulence of Blumeria graminis f. sp. avenae populations, thereby extending the long-term studies started by Okoń and Ociepa [51]. Data from the literature concerning the effectiveness of specific resistance genes served as an important reference point for interpreting the obtained results. In oats, thirteen powdery mildew resistance genes, designated Pm genes, have been identified to date [32,34]. Research concerning these genes has primarily focused on analyzing their origin and genomic location in oat [30,32,33,34,35,40].

From the perspective of resistance breeding, it is essential to identify which resistance genes are effective at suppressing infection. Therefore, monitoring the effectiveness of these genes over time and across different environments is of considerable importance. A study conducted by Okoń [37] evaluated the effectiveness of six oat resistance genes against powdery mildew: Pm1, Pm3, Pm4, Pm6 and Pm7, as well as the cultivar ‘Canyon’, which also carries a variant of the Pm7 gene [52]. These analyses indicated that Pm1 and Pm3 did not provide high levels of resistance to powdery mildew, a finding supported by other studies [31,53], as well as our results. The Pm8 gene present in the Rollo cultivar also demonstrated a low level of resistance. This gene was identified in host–pathogen tests by Hsam et al. [41] who demonstrated that the Rollo cultivar, in addition to the Pm3 gene, possesses another gene that determines resistance. Its presence was confirmed by Hsam et al. [31], and in accordance with the nomenclature, it was assigned the symbol Pm8. There is no available line with a single Pm8 gene; however, due to its low effectiveness, it is not widely used in breeding programs, nor was it the subject of research work. Similarly, the Pm6 gene has been reported in the literature to offer limited protection against Bga [31,53,54]. Nonetheless, it is important to emphasize that, despite their long-standing use in breeding programs, these genes still confer a moderate level of resistance to Bga in many regions [39]. This suggests that they may be valuable components in the construction of gene pyramids, which provide partial but broad-spectrum resistance to multiple pathogen races.

Numerous publications have demonstrated the high effectiveness of Pm7 [31,40,41,53,54], which also showed a consistently high level of resistance in our study. Pm7 is found in many oat cultivars [52,53,55] and continues to be highly effective. Based on our results, as well as those in [38] and other studies [30,37,51], the Pm7 gene confers durable resistance that has remained stable over many years. However, the detection of isolates with minor virulence against the APR122 line suggests that the Bga population is variable and continues to evolve in terms of virulence, underscoring the need for ongoing monitoring of gene effectiveness. Additionally, the cultivar ‘Canyon’, which also contains the Pm7 gene, exhibited lower resistance to pathogen pressure. Both forms containing the Pm7 gene were used as reference genotypes due to differences in their effectiveness. As demonstrated by Okoń [37] and Cieplak et al. [38], the Pm7 gene in ‘Canyon’ is not as effective as the Pm7 gene present in APR122. Other studies have also reported differences in the effectiveness of this gene, suggesting the presence of distinct allelic variants. Research by Brodführer et al. [52] confirmed that the Pm7 genes in ‘Canyon’ and APR122 are located in the same genomic region, indicating that the two genotypes carry the same gene, albeit with differing effectiveness. Therefore, when introducing the Pm7 gene into a breeding program, attention should be paid to the source of the gene to achieve the intended effect of increased resistance.

It is worth emphasizing that not all resistance genes have been overcome by the pathogen. In an early study by Hsam et al. [41], the Pm4 gene was identified as a valuable source of resistance to powdery mildew, a finding corroborated by our present research. Other genes that have demonstrated high effectiveness include Pm2 and Pm5, which confer resistance that none of the tested isolates has yet managed to overcome. A study by Okoń and Ociepa [51] indicated that the resistance conferred by Pm2, Pm4, and Pm5 remained intact, with zero virulence observed among Bga isolates against the cultivars carrying these genes. Our analyses confirm that the high level of resistance associated with these genes has persisted in recent years. Unfortunately, these genes are not present in current commercial cultivars. Okoń et al. [54] found that Polish cultivated varieties do not contain Pm4 or Pm7, which would otherwise ensure resistance to the pathogen. As reported by Reilly et al. [55], the oat cultivar ‘Barra’, which had been cultivated for many years in Ireland, did not carry effective resistance genes. Since 2023, other cultivars such as ‘Husky’ have been recommended for cultivation. Although ‘Husky’ does not exhibit a high level of resistance to Bga infection, the presence of the Pm13 gene reduces the incidence of powdery mildew, enabling a reduction in the use of chemical crop protection products and contributing to improved yields.

In this study, the effectiveness of the Pm9, Pm10, Pm11, and Pm12 genes against isolates collected in Poland was evaluated for the first time. Their effectiveness increased over the study period, with Pm9, Pm10, and Pm12 showing a gradual improvement, whereas Pm11 displayed a sudden rise in effectiveness. These results highlight the considerable potential of these genes for incorporation into gene pyramids, particularly when combined with moderately effective resistance sources. Such combinations can broaden protection and substantially reduce disease incidence. Genotypes carrying these genes therefore represent promising resources for breeding powdery mildew-resistant oat cultivars. Nonetheless, given the limited duration of the present analysis, the effectiveness of these genes requires continued monitoring. The limited number of effective resistance genes currently used in breeding programs may enable pathogen populations to adapt to their presence and overcome plant defense mechanisms. Therefore, continuing to search for new sources of resistance is essential to support breeding efforts. One auspicious source is A. strigosa, whose genotype Pl51586, characterized by high effectiveness against powdery mildew, was identified by Okoń and Kowalczyk [36]. These authors demonstrated that this genotype exhibits a consistently high level of resistance, a finding later confirmed by additional studies [43]. Despite these promising results, it is necessary to continue monitoring the effectiveness of this resistance source and to focus on its genetic identification. Although, the A. strigosa genotype’s genetic background remains unidentified, it showed strong resistance to infection by Bga in this study. This broad-spectrum resistance, combined with its temporal stability, makes A. strigosa a valuable and promising donor of resistance genes for oat breeding programs.

To obtain comprehensive data, it is essential to not only systematically monitor the effectiveness of existing resistance genes and search for new sources of resistance but also characterize pathogen populations, estimate the dynamics of their changes, and assess their virulence levels [56,57]. The phenomenon of resistance breakdown may indicate a dynamic evolutionary process within pathogen populations, which results in the gradual overcoming of successive resistance genes. In contrast, only minor changes in virulence have been observed over time, suggesting low evolutionary potential and slow population dynamics, which reduces the likelihood of resistance breakdown in the coming years [58]. Given the observed variability and adaptability of the pathogen, continuous monitoring of its population is crucial for the effective implementation of breeding programs. Moreover, eco-evolutionary models and empirical studies highlight that the spatial structure, host diversity, and presence of non-host or cover crops can further slow pathogen evolution and reduce epidemic severity, thereby supporting the durability of resistance under field conditions. The interplay between host–pathogen coevolution and agricultural practices such as crop rotation creates selective pressures that hinder the fixation of aggressive pathogen strains and provide temporal breaks in disease cycles [59]. Recent advances in genetic resistance deployment strategies also contribute significantly to the durability of resistance. Approaches such as stacking multiple resistance genes and utilizing genome editing techniques (e.g., CRISPR/Cas) to target susceptibility genes enhance the breadth and longevity of plant resistance. These modern biotechnological tools complement traditional breeding and pathogen monitoring by generating cultivars with durable resistance profiles less prone to rapid resistance breakdown [60,61]. Given the observed variability and adaptability of the pathogen, continuous monitoring of its population remains crucial for effective breeding programs. As noted by Reilly et al. [55], virulence variation directly influences the recommendations for selecting cultivars suitable for cultivation, highlighting the importance of regularly assessing the durability of resistance genes under field conditions. Monitoring both evolutionary and demographic changes in pathogen populations is therefore indispensable for implementing timely and effective protective strategies.

This research revealed that the Bga population underwent significant changes over the years examined, with the dynamics of these shifts varying notably depending on the specific pathotype. The genetic diversity of the pathogen population was observed to be at its lowest in 2023 relative to previous years, indicating a potential reduction in genetic variability. Such fluctuations in pathogen population diversity are likely influenced by a complex interplay of environmental factors, particularly meteorological conditions. Weather phenomena such as temperature, humidity, and precipitation serve as crucial abiotic factors that can markedly impact pathogen development and proliferation. These conditions can exert selective pressures on different pathotypes, favoring those best adapted to prevailing environmental circumstances. Furthermore, meteorological variations can influence key reproductive processes and dispersal mechanisms of the pathogen, thereby shaping its population structure and genetic diversity. Understanding these interactions is essential for predicting pathogen evolution and devising effective disease management strategies. In their review, Velásquez et al. [62] compared infection levels in various crops, including barley, wheat, and maize, under differing weather conditions. From this comparison, they concluded that the most influential factors affecting disease development in plants are elevated atmospheric CO₂ concentrations [63,64], the optimal temperature range for a given pathogen [65], and water availability [66,67,68]. Based on these findings, it can be concluded that both the virulence levels of pathogen isolates and the dynamics of population changes are strongly dependent on climatic conditions. In our study, the most genetically diverse pathogen population was observed in 2021, which may suggest more favorable climatic conditions compared to those in 2023. Wyand and Brown [69] reported that Bga populations are characterized by a high level of local diversity and low global diversity. Our findings support this observation, revealing differences between isolates originating from distinct geographical regions of Poland, as represented by samples from Polanowice and Lublin.

Studies by Klocke et al. [70] demonstrated that the German population of Blumeria graminis f. sp. triticale exhibited a high level of diversity, with the six most common isolates accounting for only 5–14% of the total population. The pathotypes were characterized by complex virulence patterns, suggesting that the triticale powdery mildew population was highly diversified and evenly distributed. Similar findings were reported in the population of barley powdery mildew in the Czech Republic [12] and the leaf rust population of rye in Germany [71], reinforcing the idea that such diversity is a common feature among biotrophic fungal pathogens.

Our results are consistent with these previous observations. Within the analyzed populations of Bga, no dominant pathotype was identified. The most frequently observed pathotypes, TBBB, TBCB, SBBB, and TBMB, showed only moderate frequencies, ranging from 4% to 13%. This indicates a relatively even distribution of virulence types within the pathogen population, with no single variant gaining apparent prevalence.

These findings underscore the necessity of continuous assessment of both the genetic effectiveness of individual resistance genes and the virulence levels of Bga pathotypes. Only with ongoing monitoring can we gain insights into how the pathogen operates and under which conditions virulence is most likely to intensify. Moreover, B. graminis has been suggested as a suitable model organism for studying the impact of long-distance dispersal on population genetics [72,73], further highlighting its relevance in evolutionary and epidemiological research.

5. Conclusions

This study demonstrated that resistance genes against powdery mildew in oats exhibit varying levels of effectiveness, reflecting the complexity of host–pathogen interactions. Among the tested genes, only four demonstrated a high and durable level of protection over time, suggesting that the genetic changes occurring within the pathogen population are progressing at a relatively slow pace. This stability in resistance gene performance provides a promising outlook for their continued effectiveness in the near future, although ongoing monitoring remains essential to detect any emerging resistance-breaking pathogen strains. The observed variability in gene performance across different geographic regions underscores the importance of developing and deploying gene pyramids—combinations of multiple resistance genes—to enhance the durability of host resistance. Integrating genes with moderate effectiveness alongside highly durable ones can create a more comprehensive and resilient barrier against a wider spectrum of pathogen races, thereby reducing the risk of resistance breakdown. This strategic approach offers a robust means of ensuring long-term, regionally tailored protection against Bga infection, ultimately contributing to sustainable disease management and safeguarding oat production systems against evolving pathogen threats.