Tilletia laevis Kühn is a threatening pathogen of wheat crops, which causes huge damage worldwide, and mostly sporulation occurs in the plant ovary with host tissues in the kernel slowly replaced by masses of black teliospores (Nguyen et al., 2019). Losses in wheat crops reached 75–80% in many wheat-growing areas of the world (Qin et al., 2020). The relationship between plant pathogens and soil microbes can be either commensalistic, symbiotic, antagonistic, or parasitic (Ruby, 2008; Haegeman et al., 2009). For Tilletia, the characterization of the microbial communities in wheat tissues and rhizosphere soil (Din et al., 2021; Xu et al., 2021), characterization of rhizosphere microbial communities for disease incidence and optimized concentration of difenoconazole fungicide for controlling of wheat dwarf bunt (Jia et al., 2022), and microbiome signature of endophytes in wheat seed response to wheat dwarf bunt caused by Tilletia controversa Kühn were explored (Ren et al., 2020). The T. laevis, with a fishy smell, leads to the decreased quality and quantity of wheat crops (Lu et al., 2005). Some plants can alter soil biochemical properties (Hussain et al., 2011; Tang et al., 2015), and some plant pathogens can change rhizosphere microbial communities (Zhou and Wu, 2012; She et al., 2017) and alter the relative abundance of other soil-borne pathogens (Din et al., 2021). Soil microbial diversity is not only important for the soil life but also important for soil nutrient cycling (Berendsen et al., 2012). This microbial diversity plays an important role in the health of plants, increasing the soil fertility, and cycling of N, C, and many other nutrients (Berendsen et al., 2012; Miransari, 2013). Previous studies revealed that plant pathogens, such as T. laevis (Din et al., 2021), root know nematode (Zhou et al., 2019), and Erwinia spp. (She et al., 2017), changed rhizosphere microbial communities. Similarly Mendes et al. (2013) demonstrated that rhizosphere soil microbiome can alter the composition and structure of plant pathogenic and beneficial microorganisms (Mendes et al., 2013). Several studies have shown that soil microbial diversity is influenced by plant pathogens (Zhou et al., 2019; Din et al., 2021). Additionally, environmental factors, like pH, influence soil microbial diversity (Kim et al., 2016; Zhang et al., 2016). Therefore, it is very important to analyze the relationship between environmental factors and soil microbial diversity. However, limited studies have concerns about fungal and bacterial communities under different conditions with different plants after pathogen infection.

Wheat crops is a staple food crop in many countries of the world. Owing to its high amino acid contents, high protein, deliciousness, and use in many products, wheat is used as a food crop throughout the world (Chen et al., 2021). Alfalfa (Medicago sativa L.) is a Fabaceae perennial herb and is an important legume crop used for forage worldwide. Moreover, alfalfa is a key source of pollen and nectar throughout the world (Taha, 2015). Oats (Avena sativa L.) is an important crop for their high content of functional substances such as phytochemicals, dietary fibers, and several other substances with high nutritional value (Havrlentová et al., 2020). Because of the plant pathogens, the soil microbial community is influenced, which may increase or decrease the relative abundance of soil microorganisms (Din et al., 2021). Additionally, long-term continuous cropping alters the soil microbial community by increasing the relative abundance of soil-borne pathogens in the soil (Yang et al., 2012; Liu et al., 2014; Tang et al., 2015; She et al., 2017). Therefore, there is a need to investigate the effect of a plant pathogen on microbial diversity in different crops that have been growing continuously for a long period. It is known that plant species or soil environment influence the soil microbial diversity composition (Harrison and Bardgett, 2010; Huang et al., 2014). The plants adapt to biotic stresses by modifying the chemistry of their root exudates to assemble a health-promoting microbiome, such as the “cry for help” hypothesis, which provides a mechanistic explanation for previously described soil feedback responses to plant diseases, such as the development of disease-suppressive soils following continuous cultivation of take all-infected wheat (Rolfe et al., 2019). Din et al. (2021) revealed that the diversity and composition of the rhizosphere microbiome associated with wheat crops changed after T. laevis infection. However, issues associated with wheat, alfalfa, and oat crops are caused by alterations in the rhizosphere in response to diseases, the cultivation area of these crops has decreased sharply in recent years in Gansu province.

Here, to obtain an inclusive understanding of the rhizosphere soil microorganisms in wheat, alfalfa, and oat crops in Gansu province, China, after T. laevis infection, for comparatively exploring fungal and bacterial communities, we subjected fungal and bacterial communities from wheat, alfalfa, and oat cropping fields in Gansu province, China, to high-throughput sequencing, and we used redundancy analysis (RDA) to analyze relationships between soil microbial communities and soil properties with enzyme activities.

In this study, using high-throughput sequencing, we analyzed bacterial and fungal communities in wheat, alfalfa, and oat crop fields in Gansu Province, China. According to the α-diversity analysis, the overall diversity of bacterial and fungal community compositions differed among the soil samples. The Chao1 α-diversity and Shannon analysis revealed that the diversity of microbial communities is different in different crops (Figure 1). This may be due to different soil characters and crops in different periods. For bacteria, the Proteobacteria, Acidobacteria, Actinobacteria, Chloroflexi, Gemmatimonadetes, and Bacteroidetes, while for fungus, the Ascomycota, Basidiomycota, and Mortierellomycota were the dominant phyla (Figure 3), which was by the findings of previous studies (Zhou et al., 2019; Wang et al., 2020; Din et al., 2021). These phyla were also dominant in fields of soybean (Li et al., 2010), peanut (Li et al., 2014), and tobacco (She et al., 2017), as well as in T. laevis (Din et al., 2021) and root-knot nematode-infected (15)fields. The members of Proteobacteria play an important role in S, N, and C in soil (Nosheen et al., 2016). Previous studies revealed that there is greater abundance of Proteobacteria in fertile soil as compared to diseased soil (Wang et al., 2017). However, in our results, the percentage of Proteobacteria was the highest in TFL2 (alfalfa rhizosphere soil infected with T. laevis) from different crops after T. laevis infection. The Acidobacteria and Actinobacteria are key players in the suppression of fungal pathogen F. oxysporum (Trivedi et al., 2017). The Bacillus is a genus of Firmicutes, which has the role of controlling soil-borne pathogens and can stimulate plant growth activities as a beneficial microbe (Jos et al., 2008). For instance, Bacillus spp. inhibits R. solanacearum infection, which causes bacterial wilt (Guo et al., 2004; Tan et al., 2010; Muhae-ud-Din et al., 2018). Additionally, application of Bacillus spp. as a fertilizer can increase the soil microbial diversity (Huang et al., 2012). Therefore, Firmicutes are the best options to improve the soil microbial community and are influenced by soil-borne pathogens (Wang et al., 2020; Din et al., 2021). In our study, the relative abundance of fungal and bacterial rhizosphere microorganisms significantly changed in T. laevis-inoculated samples as compared to control samples with the increased abundance of Ascomycota, Basidiomycota, Proteobacteria, and Acidobacteria. These changes could be attributed to a change in the root exudation patterns in the presence of soil-borne pathogens, a higher prevalence of dead roots, and microbial competition (Jones et al., 2009; Berendsen et al., 2012; Zahar et al., 2014; Dudenhöffer et al., 2016; Gu et al., 2016). These rhizosphere soil microorganisms have a role in changing redox conditions, C flow, soil pH, and the production of rhizodeposits, including the release of root exudates of various natures (Hinsinger et al., 2003; Jones et al., 2009; Dennis et al., 2010). In our results, Ascomycota, Basidiomycota, and Mortierellomycota were the dominant phyla, which were consistent with the findings of previous studies (Xu et al., 2018; Din et al., 2021). The Basidiomycota and Ascomycota are important groups of fungi in most types of soils (Wallenstein et al., 2007; Unterseher et al., 2013), and species of these phyla are involved in crop cycling by degrading organic substances (Unterseher et al., 2013; Purahong et al., 2016). We observed significant changes in the relative abundance of Basidiomycota and Ascomycota in our samples, especially in CK-4, the relative abundance of Ascomycota was the highest compared to other soil samples.

The soil properties, including available N and soil pH, are influenced directly or indirectly by plant pathogens (Lazcano et al., 2021). Soil properties play an important role in plant nutrient acquisition and resistance to biotic and abiotic stresses (Eaton et al., 2012; Yu et al., 2022; Tiecher et al., 2023), such as adequate total nitrogen (TN) levels, vigorous plant growth, and higher yields. Phosphorus (TP) and total kalium deficiency can limit crop growth and yield, and low levels of NO₃(−)-N can limit plant growth. NH₄(+)-N can be influenced by soil pH and temperature, Adequate phosphorus (AP) levels are crucial for early root development and flowering. Available kalium (potassium) deficiency can increase susceptibility to diseases and stress. High organic carbon (OC) content, moisture content (MC), and pH can influence nutrient availability, microbial activity, and plant growth, excessive and low levels both will hinder nutrient uptake. Hence, we used RDA analysis for the relationship between environmental factors (including soil T, available K, soil pH, TN, and urease activity) and soil microbial composition. RDA results showed that environmental factors differentially affected the fungal and bacterial communities, which were proven by various previous studies (Zhang et al., 2005; DeAngelis et al., 2015; Zhou et al., 2017). Urease catalyzes the breakdown of urea into NH₃ and CO₂, which may be good for soil quality (Jezierska-Tys and Rutkowska, 2014). The plants and rhizosphere soil microorganisms release urease enzymes (Follmer, 2008).

The plant pathogens cause a decline in the urease activity, and positive correlations between soil micro-organisms and urease have been previously found (Lazcano et al., 2021).

Soil microbial communities were altered in response to pathogen infection, leading to changes in soil enzymatic activities and nutrient availability (Mendes et al., 2013). Pathogen-infected plants may exhibit altered nutrient uptake and cycling dynamics. For example, Phytophthora infestans infection in potato plants can lead to changes in phosphorus cycling and availability in the soil; pathogen infections can decrease crop yield globally, with significant variation depending on the pathogen and crop species (Garrett et al., 2018). Pathogen infections can alter the composition and function of soil microbial communities, which play crucial roles in nutrient cycling, disease suppression, and plant health. For example, Fusarium oxysporum infection in different common beans has been shown to reduce microbial diversity and alter soil bacterial community composition (Hollander, 2018). Similarly, in our results, the urease activity changed after T. laevis inoculation in different crops (Table 2). Previous studies revealed that N has a role in regulating the rhizosphere soil microbial community (Cleveland et al., 2007; Högberg et al., 2014), and urease activity increased by the N application from 247 to 433 mg/kg (Liang et al., 2016; Lei et al., 2018). Therefore, N provides a good means to increase the urease activity to increase the soil micro-biota. However, a high concentration of ammonia can reduce the activity of the urease enzyme (Piotrowska and Wilczewski, 2012). Additionally, TN has a major role in influencing the fungal and bacterial community (Wang et al., 2020).

In conclusion, according to the RDA analysis of rhizosphere microorganisms and environmental factors in Gansu province, a positive correlation was noted in the chemical properties and enzyme activity of rhizosphere and top-layer soil. We explored some dominant fungi and bacterial phyla in the rhizosphere and top soil in infected wheat by T. laevis, such as Proteobacteria, Acidobacteria, Actinobacteria, Chloroflexi, Ascomycota, Basidiomycota and Mortierellomycota, which were related to T. laevis, we may reduce the content of this may contribute to the control of T. laevis shortly, and we may isolate these to explore the interaction with T. laevis (Jin et al., 2023; Zhou et al., 2023). Even though some taxa belong to the same genus, they can have different functions in the control of different pathogens. Additionally, nitrogen, total kalium, ammonium nitrogen, available kalium, and organic carbon were increased after T. laevis infection, so, reducing these elements may also contribute to controlling wheat’s common bunt disease which is caused by T. laevis. Hope shortly, we can control the wheat’s common bunt disease with efficient and friendly microbiology and the elements mentioned above.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article/Supplementary material.

YS: Data curation, Writing – original draft. CD: Data curation, Writing – original draft. TL: Formal analysis, Writing – review & editing. WC: Formal analysis, Writing – review & editing. HG: Formal analysis, Writing – review & editing. LG: Conceptualization, Data curation, Funding acquisition, Investigation, Resources, Supervision, Writing – original draft, Writing – review & editing. GL: Formal analysis, data curation, Writing – review & editing.