Oat stem rust occurs worldwide and understanding the dynamics of the pathogen’s diversity is crucial to developing methods for its control. The diversity of Pg populations in oats has been documented for many authors (Harder, 1994; Mariscal et al., 2011; Gnocato, 2017; Fetch et al., 2020;). Recently, Sowa et al. (2021) reported 57 Pg races among 157 isolates collected from 2017 to 2020 in Poland, showing a great diversity in the population; while Li et al. (2022) conducting a virulence survey in China found 8 races among 159 isolates collected during 2018 and 2019, indicating limited diversity.
This study documents for the first time the structure and complexity of Pg populations and their evolution over a period of 17 years, based on 70 isolates collected in different sites in Argentina during 2005, 2021, 2022 and 2023. We identified 22 different races among the 70 single-uredinial isolates collected during the period, showing a greater diversity than in the China population but lower than in the Poland population. Although, there is limited information available on Pg in South America, Campos & Giménez (2011) characterizing 83 isolates collected between 2007 and 2009 in Argentina, reported high variability in the Pg population. Likewise, Gnocato (2017) found 9 Pg races among 16 isolates collected during two epidemic years in southern Brazil and suggests that the high virulence variation identified can be explained by a high genetic diversity on the host with respect to the resistance genes (samples collected on different Brazilian cultivars). It is unclear what causes the high level of virulence polymorphism observed in Argentinian Pg as there is no evidence of sexual reproduction in the region for Pg. Different authors studying the South American Pc populations (Martinelli, 2000; Leonard & Martinelli, 2005; Dietz et al., 2023) suggest that the high mutation rate would be the main factor for variation in these populations. Additionally, the existence of a large region established in southern Brazil, Argentina and Uruguay, where oats are cultivated most of the year and during the interval between successive oat crops; and the presence of volunteer oat plants contribute to the maintenance of these polymorphisms (Leonard & Martinelli, 2005; Vieira et al., 2007).
It is important to mention that while in the present study we used 11 differential lines carrying individual genes (Harder, 1994), the inclusion of Pg6 and Pg12, would allow for the utilization of the letter code nomenclature system presented by Fetch et al. (2007). This system will be beneficial in enabling us to uniformly characterize Pg isolates, facilitating discussions on virulence dynamics and population studies.
We reported that most of the races identified in 2021, and all the races identified in 2022 and 2023, were different from those found in 2005. This allows us to affirm that the populations from 2005 and the current ones are markedly distinct. "Race 1", virulent on Pg1-Pg2-Pg3-Pg4-Pg9-Pg13-Pg15-Pg16, was the most frequent in 2005 and was not identified in 2022 and 2023. Meanwhile, "race 11", virulent on all 11 Pg genes, was first identified in 2021 and has been the most prevalent every year since then.
The change in population dynamics detected here suggests that the use of a few genes as a basis for resistance to stem rust in the Argentinian germplasm has resulted in the continuous selection of Pg phenotypes with virulence to these resistance genes, similar to what Dietz et al. (2023) mentioned for the Pc population. The introduction of certain genotypes carrying Pg genotypes (materials from the Quaker International Oat Nursery, either as cultivars or parentals in Argentinian germplasm), and their widespread adoption for larger areas, has led to cycles of selection and displacement of specific virulences like Person's conceptual model (Person, 1966). This phenomenon, known as directional selection, occurs when advantageous isolates increase due to variations in survival and reproduction among different phenotypes. This pressure results in an increase in the proportion of races virulent on these genes and/or the emergence of new virulent races (Carson, 2011; Chong et al., 2011; Dietz et al., 2023).
Descriptive parameters, such as virulence frequency and virulence complexity (Kosman,1996; 2003), were calculated for all isolate populations, providing us with a deeper comprehension of the population's dynamics. These parameters enable us to gain insight into how virulence manifests within the population and how it evolves over time. Our findings indicate that the current population (2021, 2022, and 2023) exhibits greater virulence compared to that of 2005; in other words, it possesses the ability to overcome a larger number of genes than in the past. The virulence complexity reached its highest level in 2022 and 2023; where most of the isolates (50 and 53%, respectively) were able to overcome the 11 Pg reference oat lines used in this work.
Moreover, the Kruskal–Wallis one-way variance analysis revealed that Pg isolates from 2005 were less virulent than those collected in 2021, 2022, and 2023, indicating an increase in virulence frequency within the populations over the past three years. By 2021, there was a substantial rise in the average virulence level to 87%, compared to 59% in 2005. However, no significant difference was observed compared to 2022 (91%) and 2023 (92%). Therefore, current populations are more virulent and complex, and the predominant race is virulent over all the reference genes used in this study. This suggests that the widespread use of genotypes containing only a few resistance genes in large areas of Argentina creates strong selection pressure (Harder & Haber, 1992; Dietz et al., 2023), which is the driving force behind the increase in virulence in the Argentinean Pg population. There are no studies in South America that describe the complexity of the virulence of Pg populations, although studies carried out on crown rust mention the presence of super-races (Leonard & Martinelli, 2005; Vieira et al., 2007), high complexity in populations (Leonard & Martinelli, 2005; Dietz et al., 2023), and an increase in the virulence of current populations as a result of the use of a few genes as the basis of resistance in oat cultivars.
An additional goal of the study was a preliminary evaluation of Pg genes and their potential for use in practical breeding in Argentinian growing conditions. In 2021–2023, Pg1, Pg2, Pg3, Pg4, Pg8, Pg13, and Pg16 presented low levels of effectiveness. Likewise, Pga was the most effective gene in 2021 and 2023 (53% and 73%, respectively), while Pg9 was the most effective in 2022 (75%). The Pga gene has shown its utility in some areas of Canada (Fetch et al., 2020), as well as in the south of Brazil (Gnocato, 2017). However, the high values reported here indicate its limited effectiveness in Argentinian conditions, even when both genes are used in combination.
Our results demonstrated that the frequency of virulence of Pg isolates increase on most of the resistance genes compared to the 2005 population. Genes such as Pg1, Pg2, Pg4, Pg8, and Pg13 showed significant increases, while others like Pg3, Pg9 and Pg15 showed smaller ones.
These findings confirmed changes in the race dynamics of the population as a consequence of the use of a few resistance genes, an increment in the virulence frequency and the existence of complex Pg races in Argentina. This emphasizes the dynamic nature of plant (genes)-pathogen interactions and underscores the importance of ongoing surveys and surveillance efforts to monitor these changes. Moreover, our findings highlight the necessity to broaden the search for new resistance genes and deepen our understanding of the genetic mechanisms underlying resistance to stem rust in oats.