Plant disease epidemic regions are undergoing transformations because of shifting global climate patterns, including altering temperature, precipitation rate, and snowfall time (Skripnuk and Samylovskaya, 2018; Hossain et al., 2024). These changes stimulate disease epidemics and facilitate the emergence of new pathogen races and the migration and adaptation of exotic pathogen races in new regions. These new races may break down resistant genes in host plants (Newbery et al., 2016; Velasquez et al., 2018; Garrett et al., 2006). In the context of Puccinia striiformis f.sp. tritici (Pst), the causal agent of wheat stripe rust, environmental changes associated with climate variability directly impact overwintering survival, spore dispersal, and infection cycles (Awais et al., 2025; Zhang et al., 2025). Warmer winters and delayed snowfall may shorten the pathogen dormancy periods (Singh et al., 2023). It exemplified in higher snow blight (Phacidium infestans) infections in pine trees due to early snowmelt (Barbeito et al., 2013). Previous studies demonstrated that Puccinia striiformis f.sp. tritici (Pst) mycelia within living leaves can be killed by low temperatures independently of host senescence (Ma et al., 2015). However, the role of cold stress in shaping Pst populations and genetic diversity under natural conditions remains poorly understood. Temperature extremes in both summer and winter limit pathogen survival, as Pst cannot persist in extremely hot or extremely cold environments (Lyon and Broders, 2017). Generally, the optimal temperature for spore germination ranges from 8°C to 12°C, with an upper limit of approximately 20°C (de Vallavieille-Pope et al., 1995). In cold wheat-growing regions, snow exerts a dual influence on stripe rust epidemiology. While it provides protection and sustains the pathogen during harsh winters, facilitating early-season epidemics, it also acts as a selective filter, shaping the genetic structure of Pst overwintering populations. The severity of wheat stripe rust has significantly escalated in cold regions over the past few decades primarily due to global warming (Zhang et al., 2024), which was noticed in the Central Asian region, Uzbekistan, where the clonal lineage of Puccina striiformis causes a countrywide epidemic (Awais et al., 2025).

In China, the Xinjiang epidemic region is important because of several bordering countries with hot- and cold-adopted Pst epidemic regions, including Kazakhstan, Kyrgyzstan, Tajikistan, Afghanistan, Pakistan, India, Russia, and Mongolia. This geographic position makes the region highly vulnerable to incursions of foreign Pst races (Awais et al., 2025), thereby increasing the risk of wheat stripe rust epidemics. The region is also surrounded by major mountain ranges, the Tianshan mountains in the center, the Altai mountains to the north, and the Kunlun mountains to the south, which contribute to population subdivision by acting as natural barriers (Awais et al., 2023). In addition to these geographical factors, Xinjiang is characterized by a vast diversity of climatic conditions. Summers in the lowland basins can exceed 40°C, while winters in mountain valleys commonly reach –20°C to –30°C, creating strong ecological gradients that influence both host and pathogen dynamics. In recent years, Xinjiang has also been strongly affected by climatic change. Rising temperatures compared with those of previous decades have altered snowfall patterns and intervals, directly influencing both disease epidemiology and cropping schedules (Chaloner et al., 2021). These shifts not only affects wheat growth cycles but also modifies the conditions under which Pst survives and initiates infection, thereby increasing the risk of unexpected stripe rust epidemics.

Despite the climatic change, the emergence and evolution of Pst races pose a similar challenge. The high evolutionary potential of Pst, driven by mutations, recombination, and migration, enables the pathogen to rapidly overcome host resistance and adapt to changing environments (Schwessinger, 2017). Genetically uniform crop monocultures and high planting density in modern agriculture have accelerated the emergence of virulent Pst races capable of overcoming disease-resistant crop varieties and promote the pathogen’s population size and genetic diversity (Singh et al., 2023). This constant turnover of virulent races undermines the durability of resistant cultivars and complicates breeding programs aimed at long-term disease control. Consequently, monitoring race evolution and understanding the mechanisms underlying Pst adaptability remain critical for the sustainable management of stripe rust under present and future climatic conditions. In this context, investigating before snow and after snow populations in Xinjiang provides an opportunity to clarify how climatic variability shapes Pst diversity, lineage survival, and the timing of epidemics.

Snow covering wheat regions in Xinjiang is highly significant for the survival, evolution, and spread of Pst in China. Snow survival creates conditions for the long-term persistence of Pst lineages while, at the same time, immigration of exotic spores after snowmelt may introduce new diversity in this region. Given China’s vast climatic heterogeneity, from cold northern wheat-growing regions to mild southern environments, cold tolerance may represent a critical, yet overlooked, factor shaping the long-term persistence and spread of Pst. Investigating whether certain lineages exhibit enhanced cold tolerance will help clarify their evolutionary dynamics, regional adaptability, and implications for stripe rust epidemiology under both current and future climate scenarios.

The ability to predict pathogen survival potential may enable the timely implementation of integrated disease management strategies to reduce inoculum sources and prevent the formation of disease foci.

Puccinia striiformis, a fungal pathogen, causes stripe rust epidemic in various regions and poses a significant threat to global food security (Chen, 2005; Hovmøller et al., 2011). Generally, P. striiformis exhibits sensitivity to temperature. A study conducted by de Vallavieille-Pope (2018) using various isolates of the warrior race from Europe reported that none of the infected individuals exhibited any noticeable symptoms when the temperature exceeded 23°C. However, due to its high evolutionary potential (Riella et al, 2024), some genotypes of P. striiformis have emerged with adaptability against high temperatures (Zhang et al., 2024). Among different ecological factors, snowfall plays an important role in stripe rust disease epidemiology. However, due to climatic change, the snowfall pattern is also changed, which may affect the disease epidemic occurrence time and disease severity. As observed in the epidemic region of Xinjiang, China, this was due to late snowfall. The disease occurs early in December 2023 in the Yili region of Xinjiang. Based on previous population genetic studies, different epidemic zones have been reported worldwide. Some showed a distinct population genetic structure compared to others (Ali et al., 2014; Thach et al., 2016). Moreover, a migration pattern was observed among those epidemic regions, which have identical topography, similar environmental conditions, and an availability of susceptible host and exchange of winds flows. However, due to climate change, the population genetic structure may be reshaped in various epidemic regions, potentially favoring the migration of exotic lineages to establish their populations in new regions and causing early epidemics in some parts.

China hosts the world’s largest epidemic region of wheat stripe rust, characterized by a significant divergence in the Pst population structure. These epidemic zones exhibit distinct environmental characteristics, varying cropping patterns, and differing host availability (Ma et al., 2016). Among the different epidemic regions in China, Xinjiang stands out due to its geography, diverse ecological zones, and Pst epidemic characteristics. Based on the annual weather forecast of this region (Figure 6), it can be referred to as the cold Pst epidemic region. Typically, disease epidemics occur in this area during spring after snowmelt. Seedlings are primarily protected under snow, which occurs immediately after cultivation. However, recent climatic changes have disrupted this epidemic cycle. Disease has occurred earlier in the Xinjiang region of Yili in December 2023, while other regions have experienced delayed epidemics during spring when snow melts. However, the snow pattern has a bit changed, but the overall temperature in this region in winter is still freezing (below 0°C; Figure 6). Our results identified the cold-tolerant strains MLG_1 and MLG_2, which did not only exhibit cold tolerance but also survived under snow cover. Additionally, these genotypes demonstrated the ability to jump on summer and winter crops to survive the year-round cycle in Yili. As we have observed, this region’s summer is not even as hot compared to other parts of China, which may have helped these genotypes to survive even in summer. Li and Zeng (2002) reported that Pst could successfully survive in winter, even when the monthly mean temperature is below −10°C, as long as the wheat seedlings are covered with snow. We observed a low F_ST value among summer 2023 crops and the next early winter crop in December before snowfall occurred. Moreover, these two-crop season has high gene flow. In China, Pst can complete a year-round cycle in the northwest and southwest, significantly impacting the main wheat production region in the east (Awais et al., 2023; Chen et al., 2014). In the Yili region of Xinjiang, both spring and winter wheat crops are cultivated. During wheat stripe rust surveillance in this region, we noticed that this region has high disease severity compared to those in other parts of Xinjiang. As previous studies have reported, the regions where both spring and wheat crops are cultivated experience a more severe epidemic than those regions with either spring or winter wheat crop grown in the same season (Chen, 2005). Furthermore, in terms of adaptability to low temperatures, wheat stripe rust can emerge very early in the seedling stage, resulting in more severe damage in that area (Chen, 2005).

However, some genotypes did not survive during snow covers and low temperature, i.e., MLG_60, MLG_62, MLG_67, and MLG_83. As reported by Zhang et al. (2025), in winter, no stripe rust disease was reported in the east of Inner Magnolia and north of Heilongjiang, where the regions’ winter is too cold for Pst to cause infections. Interestingly, these genotypes did not survive during snow cover. They were also not found in the last summer crop 2023, suggesting that these genotypes may be migrant and may have come from neighboring regions as our recent work showed the potential of migration of the Pst population in this region from Central Asian countries (Awais et al., 2025) or of emerging through sexual reproduction on alternative host barberry, which was commonly found in this region to be with disease infection (Figure 7).

Monitoring cold-tolerant Pst strains is crucial for effective disease management. These strains survive harsh winters, initiating infections earlier, often at the seedling stage. Early epidemics accelerate the disease cycle and increase the risk of widespread infections throughout the cropping season. Seedling-stage outbreaks cause more severe wheat damage and yield loss, posing a greater threat to regional food security than late-season Pst epidemics. Understanding cold-tolerant populations and their spread is essential to develop timely monitoring systems, breeding-resistant cultivars, and sustainable management practices.

We investigated the impact of delayed snowfall due to climate change on the stripe rust epidemic and their population genetic diversity in Xinjiang epidemic region of China. We also explored genotype overlaps during summer and winter crop seasons. Recently, an unusual early stripe rust epidemic occurred in the Yili region of Xinjiang, where seedlings were generally protected by snow until spring in the previous years. However, delayed snowfall in the 2023 snow season led to the first earlier epidemic in the region. The region’s winter temperature dropped to -25°C, which was generally unfavorable to cause disease. However, in this study, we identified cold-tolerant strains of Pst, MLG_1 and MLG_2, that have the potential to cause infection in low temperatures and can survive under snow cover. We noticed pathogen population overlaps on summer and winter crop seasons, completing the disease cycle. However, genetic diversity decreased in the region. Some multilocus genotypes were observed in winter crops but not in summer crops, suggesting migration from other regions since this region has connectivity with central Asian countries and Pakistan, where both cold and hot Pst epidemics are present. Monitoring the migration of these cold-tolerant strains of Puccinia striiformis is crucial as they can infect wheat seedlings in winter, causing more crop damage than infection during the crop’s mature stage.