Ten-Year Comparison of Fungicide Sensitivity and Mycotoxin Production of Fusarium Head Blight Isolates from Korea

Article information

Plant Pathol J. 2025;41(4):518-531

Publication date (electronic) : 2025 August 1

doi : https://doi.org/10.5423/PPJ.OA.05.2025.0068

Parthiban Subramanian ¹^,^†

, Jung-Hye Choi ¹^,²^,^†

, So-Soo Kim ¹

, Bo-Eun Kim ¹

, Ja-Yeong Jang ¹

, Ji-Seon Baek ¹

, Theresa Lee ¹^,

¹Plant Disease Control Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju 55365, Korea

²Allium Vegetable Research Center, National Institute of Horticultural and Herbal Science, Rural Development Administration, Muan 58545, Korea

^*Corresponding author. Phone) +82-63-238-3401, FAX) +82-63-238-3840, E-mail) tessyl1@korea.kr

†These authors contributed equally to this work.Handling Editor : Kyunghun Min

Received 2025 May 26; Revised 2025 July 8; Accepted 2025 July 9.

Abstract

Fusarium head blight (FHB) is an important disease reducing yield and quality of wheat and barley. To study changes in fungicide efficacy over time, 161 FHB isolates (F. asiaticum and F. graminearum) were obtained from infected wheat and barley in the Jeolla provinces of the Republic of Korea from 2010–2013 and 2020–2023. Over 10 years, FHB fungi developed resistance to demethylation inhibitors (DMIs), methyl benzimidazole carbamates (MBCs), and phthalimides, with few exceptions. Also, no significant resistance against succinate dehydrogenase inhibitors (SDHI) and quinone-outside inhibitors (QoI) was observed, but sensitivity to phenylpyrrole (PP) increased. Mycotoxin production by four representative isolates of both species indicated that higher doses of DMI, DMI + DMI, MBC, MBC + DMI, and PP controlled trichothecenes, whereas zearalenone was controlled only by SDHI. QoI, QoI + DMI, and phthalimide did not control mycotoxin production in either species. Despite resistance development, DMI, MBC, and PP can still be used to control FHB and mycotoxins in wheat and barley in Korea with close monitoring of resistance.

Keywords: cereals; effective concentration 50%; scab; toxin

Fusarium head blight (FHB) is a common disease that affects barley and wheat–staple crops for more than 2.5 billion people. As of 2023, more than 220 million hectares of land was used to cultivate wheat globally, producing nearly 800 million tons of crop (Food and Agriculture Organization of the United Nations, 2024). Meanwhile, estimates from the Food and Agriculture Organization of the United Nations (FAO) indicate that every year, up to 40% of global agricultural production is lost to pests (Food and Agriculture Organization of the United Nations, 2021). In wheat, microbial pathogens, including fungi, viruses, and bacteria, contribute to mean global loss of 21.5% of the total production (Savary et al., 2019). This makes fungal diseases, such as FHB, a major barrier to improving overall wheat yield and grain quality. Among the FHB-causing fungi, Fusarium graminearum and F. asiaticum have been reported to be the major pathogenic species (Jang et al., 2019; Wegulo et al., 2015). In addition to being detrimental to agricultural productivity, FHB remains a public health concern because of associated mycotoxins, such as deoxynivalenol and zearalenone (ZEA), which frequently contaminate wheat and other cereal crops (Goswami and Kistler, 2004; Johns et al., 2022; Tini et al., 2020). The most commonly reported FHB mycotoxins are deoxynivalenol (DON), nivalenol (NIV), acetyl derivatives of DON and NIV, and ZEA (Cervini et al., 2024; Jang et al., 2019; Lee et al., 2012; Savary et al., 2019). Exposure to these mycotoxins can cause several immunological, digestive, dermatic, and reproductive problems in humans as well as in animals (Cervini et al., 2024; Ganesan et al., 2022; Rai et al., 2020).

The most common strategies used to manage FHB include crop rotation with non-hosts, tillage, irrigation regulation, use of moderately resistant cultivars, and the application of foliar fungicides (McMullen et al., 2012; Paul et al., 2018; Wegulo et al., 2015). Among these, fungicides remain the most effective, as they are reported to control disease incidence by as much as 77% (de Chaves et al., 2022; Gaurilčikienė et al., 2011). The most common classes of fungicides currently used against FHB include demethylation inhibitors (DMIs), methylbenzimidazole carbamates (MBCs), quinone-outside inhibitors (QoIs), succinate dehydrogenase inhibitors (SDHIs), and phenylpyrroles (PP). Among these, DMI fungicides are the most effective and are widely used to combat FHB (Paul et al., 2018). Such DMI fungicides include hexaconazole, metconazole, propiconazole, prothioconazole, tebuconazole, and so on, which control fungal growth by disrupting the biosynthesis of ergosterol, a crucial sterol for fungal cell membrane integrity (McMullen et al., 2012; Wegulo et al., 2015; Yin et al., 2009). Other fungicides used to treat FHB include carbendazim, thiophanate-methyl (MBC), azoxystrobin, trifloxystrobin (QoI), fenpiclonil, fludioxonil (PP), fluopyram, and fluxapyroxad (SDHI) (Chen et al., 2019; Jiang et al., 2025; Oliver, 2024; Zhang et al., 2009, 2023a; Zhou et al., 2020). However, over time, the efficacy of these fungicides has been challenged by development of resistance in FHB-causing fungi (Andrade et al., 2022; Baek et al., 2022; Chen et al., 2019; de Chaves et al., 2022; Dubos et al., 2011; Gaurilčikienė et al., 2011; McMullen et al., 2012; Oliver, 2024; Wegulo et al., 2015; Yin et al., 2009). Recent genomic studies of 140 isolates of F. asiaticum and F. graminearum identified genetic alterations that could potentially increase the risk of developing resistance against several fungicides in the future (Zhang et al., 2023b). In addition to disease control, the reduction of mycotoxins in wheat grains is equally important. Previous studies on the effects of fungicides on mycotoxin synthesis have been equivocal. While time-dependent application of fungicides has been reported to control the disease as well as mycotoxin levels in laboratory and field conditions (Chen et al., 2025; D’Angelo et al., 2014; Limay-Rios and Schaafsma, 2018), contrasting results have also been obtained where fungicide treatments controlled disease but had no control over mycotoxin levels or led to increased mycotoxin concentration (Caldwell et al., 2017; Ellner, 2005; Ramirez et al., 2004).

As the use of fungicides has been practiced for almost a century now (Oliver, 2024), monitoring their resistance to plant pathogens is critical for sustaining agricultural productivity. Our objective was to study the changes in fungicide efficacy in controlling growth and mycotoxin production in FHB-causing isolates from wheat and barley fields in the Republic of Korea over a period of 10 years. In the present study, we isolated FHB fungi from wheat and barley fields at two different time periods 2010 and 2020, and studied their sensitivity to 15 different fungicide treatments. For mycotoxin production, four representative isolates (two each of F. asiaticum and F. graminearum) were treated with varying concentrations of fungicides or combinations.

Materials and Methods

Isolation, identification and chemotyping of fungi

F. asiaticum and F. graminearum were isolated from infected heads of wheat and barley at two time periods about ten years apart, 2010–2013 and 2020–2023, as described previously (Lee et al., 2016). For comparison, the isolates obtained from 2010–2013 were combined into the 2010 group and the isolates obtained from 2020–2023 were combined into the 2020 group. The fields were located in Jeollabuk-do and Jeollanam-do provinces, which are the primary wheat- and barley-cultivating regions in the Republic of Korea (Jeon et al., 2024, 2025). Identification was performed based on morphological traits and multi-locus sequence analysis of Tef-1α, Mat1-1-3, and Tri101 (Lee et al., 2016). Trichothecene genotypes were determined based on PCR assays targeting Tri12 genes (Jang et al., 2019).

Analysis of growth and half-maximal effective concentration (EC₅₀) of fungi

The susceptibility of FHB isolates to different fungicidal compounds or combinations was compared by examining the degree of mycelial growth inhibition in media supplemented with various concentrations of fungicides (Baek et al., 2022). Fungicide treatments and concentration ranges were determined to assess the EC₅₀ of each fungicide for all FHB isolates and were based on the recommended field application rates for each fungicide (Table 1). The fungicides were grouped according to DMI, MBC, PP, QoI, or SDHI. The isolates were initially grown on potato dextrose agar plates at 25°C for five days. The tips of the actively growing mycelia were cut using a cork borer (diameter, 5 mm). Plates containing varying concentrations of the tested fungicides were prepared by adding appropriate volumes of the dissolved fungicides to the medium, and the cut mycelia were placed at the center of the medium. After incubation at 25°C for 5 days, diameter of the fungal colonies were measured horizontally and vertically followed by calculation of average diameter after subtracting the initial inoculum diameter. The mycelial growth inhibition rate (%) was calculated by comparing the measured diameter with that of the corresponding fungal colony on the control medium that did not contain any fungicide. The EC₅₀ was calculated using the Quest Graph EC₅₀ calculator (AAT-Bioquest-Inc., Pleasanton, CA, USA). Two F. asiaticum (R17 and R50) and two F. graminearum (R05 and R51) isolates were selected to compare mycotoxin production under varying levels of different fungicides (Table 2).

Table 1

List of fungicides and fungicide combinations tested

Table 2

List of FHB causative Fusarium asiaticum and F. graminearum isolates tested for mycotoxin production

Mycotoxin production

Mycotoxins were analyzed using a liquid chromatography-tandem mass spectrometry system (Shimadzu Nexera UHPLC coupled with QTRAP 5500+System-QTRAP activated, AB SCIEX, Singapore). Mycotoxins were extracted from fungal colonies grown at different fungicide concentrations as described earlier and measured in triplicate (Jang et al., 2019; Lee et al., 2016). The fungal extracts were obtained using the protocol of Jeon et al. (2025) and cleaned using 0.22 μm syringe filters (Korea Ace Scientific, Seoul, Korea). From the filtered extracts, 2 μL of each sample was passed through a UPLC BEH C18 1.7 μM column (Waters ACQUITY, Waters Corporation, Milford, MA, USA) maintained at 40°C with a flow rate of 0.3 mL/min. The mobile phase consisted of (A) 5 mM ammonium formate, 0.1% formic acid in water, and (B) 5 mM ammonium formate, 0.1% formic acid in methanol. The gradient elution program was as follows: 0–1 min = 95% (A), 1–5.5 min = 70% (A), 5.5–13 min = 0% (A), and 13.1–18 min = 95% (A). Standard mycotoxin solutions were purchased from Biopure (Tulln, Austria).

Statistical analyses

Preliminary statistical analyses, including t-tests to compare EC₅₀ values between the two species, as well as between the two time groups (2010 and 2020), were performed in Microsoft Excel. Principal component analysis (PCA) was performed on SIMCA 18 (Sartorius, Umeå, Sweden). Further statistical analysis of mycotoxin synthesis was performed using the R statistical software v4.4.2 (The R Foundation for Statistical Computing, Vienna, Austria), with the packages car, GGally, multcomp, and tidyverse. The Shapiro-Wilk test was used to check the normality of the data, and Pairwise Spearman’s correlation values were computed and visualized using the ggpairs function from the GGally v2.2.1R package.

Results

A total of 161 isolates, comprising F. asiaticum (149) and F. graminearum (12), were obtained from FHB-infected wheat and barley heads in the 2010 group and 2020 group. The distribution and composition of isolates were almost equal between the two sampled provinces, with F. asiaticum-NIV being the most common chemotype (77.02%) (Fig. 1). Over 10 years, F. asiaticum showed a significant increase (P < 0.05) in the EC₅₀ values against DMI fungicides and combinations that included DMI (propiconazole, difenoconazole + propiconazole, propiconazole + tebuconazole, and propiconazole + thiophanate-methyl) (Fig. 2). An increase in the EC₅₀ values against QoI + DMI (azoxystrobin + hexoconazole) was also observed, but the difference was not statistically significant. Similarly, F. graminearum isolates showed non-significant increases in resistance to DMI-containing fungicide combinations (difenoconazole + propiconazole, propiconazole + tebuconazole, propiconazole + thiophanate-methyl, and azoxystrobin + hexaconazole). In contrast, the FHB isolates developed sensitivity to other DMI fungicides. F. asiaticum isolates developed significant sensitivity to the DMI fungicides metconazole and tebuconazole, whereas F. graminearum developed non-significant sensitivity to difenoconazole, hexoconazole, metconazole, propiconazole, and tebuconazole (Fig. 2).

Fig. 1

(A) A map of the Republic of Korea indicating two provinces where the sampling was done. Parenthesized percentages represent distribution of isolates from the respective regions. (B) Distribution of Fusarium asiaticum and F. graminearum isolates by chemotypes at two time periods. Number of isolates obtained in respective chemotype are given above bars. NIV, nivalenol; 3AD, 3-acetyl deoxynivalenol; 15AD, 15-acetyl deoxynivalenol.

Fig. 2

Comparison of sensitivity of Fusarium asiaticum and F. graminearum isolates to 15 fungicide treatments between 2010 and 2020. Asterisk (*) in red indicates significant difference (P ≤ 0.05) in EC₅₀ values between compared time periods within a species. Hash sign (#) followed by year indicate significant difference (P ≤ 0.05) in EC₅₀ values between F. asiaticum and F. graminearum at respective time period. Arrows within each chart represent intuitive comparison of the changes in the slope. The less-than sign “<“ between the species in charts indicate the fungicide treatments for which F. asiaticum isolates showed less mean EC₅₀ values compared to F. graminearum isolates. DMI, demethylation inhibitor; MBC, methyl benzimidazole carbamate; PP, phenylpyrrole; QoI, quinone-outside inhibitor; SDHI, succinate dehydrogenase inhibitors.

Against the MBC fungicides (thiophanate-methyl), the range of EC₅₀ values of F. asiaticum isolates in the 2020 group remained similar to 2010, whereas significant resistance (P < 0.05) was observed in F. graminearum. For captan (phthalimides), both species showed increased resistance, and the difference was significant for F. graminearum. In the case of the PP fungicide fludioxonil, F. asiaticum isolates developed significant sensitivity in the 2020 group compared to those in the 2010 group. The distribution of EC₅₀ values against QoI fungicides (azoxystrobin and trifloxystrobin) in both F. graminearum and F. asiaticum was very widespread, with several isolates showing intrinsically high EC₅₀ values. In 2010 group, while the majority of the F. asiaticum isolates (86%) exhibited an EC₅₀ < 1 mg/L against trifloxystrobin, the remaining 14% of isolates showed high EC₅₀ values ranging from 1–99.5 mg/L. Similarly, in the 2020 group, 74.7% of F. asiaticum isolates expressed an EC₅₀ < 1 mg/L against azoxystrobin but 25.3% of the isolates showed EC₅₀ values in the range of 1–8.9 mg/L. No significant changes in the EC₅₀ values were observed against fluxapyroxad (SDHI) in both species. Therefore, between the two periods, the FHB fungi developed resistance to DMI (especially those containing propiconazole), MBC fungicides, and phthalimides. No significant changes were observed against the SDHI and QoI fungicides, whereas significant sensitivity was observed for the PP fungicide fludioxonil.

PCA was performed to identify the influence of fungicide treatment, species, host, location, and year of isolation on EC₅₀ values. PCA could explain 30% variation in the dataset (Fig. 3). Primarily, the two species were clearly separated by PC1. As observed earlier, the NIV chemotype was found along with F. asiaticum and the 15-acetyl deoxynivalenol (15-ADON) chemotype was found alongside F. graminearum. Close clustering of F. asiaticum isolates (brown points in Fig. 3) was observed, whereas isolates of F. graminearum (black triangles in Fig. 3) were relatively loosely distributed in the lower left quadrant, indicating an inverse relationship with both principal components. The close proximity of the F. asiaticum isolates and their positioning near zero (0) in the chart indicate that they express similar or uniform responses against the tested fungicides, thereby exhibiting no significant influence over the variance in the data. In contrast, F. graminearum isolates were found to spread and were positioned in the vicinity of the fungicide treatments with high EC₅₀ values. The F. asiaticum isolates were grouped according to their respective isolation periods and hosts (wheat and barley). However, none of these factors significantly influenced either principal components, indicating that the EC50 values of the isolates were not influenced by the period of isolation or the host. Although no significant grouping of isolates based on geographical region was observed, we found that Jeollanam-do (JN), fludioxonil, and metconazole negatively contributed to PC2, indicating their impact on the total variance. This result indicates that fungal isolates from Jeollanam-do exhibited similar EC₅₀ values for both fludioxonil and metconazole (Fig. 3).

Fig. 3

Principal component analysis based on EC₅₀ values of 161 Fusarium asiaticum and F. graminearum isolates against 15 fungicide treatments. Proportion of total variance that can be explained by the first and second principal components are given by RX2 values. Labels in color represent: brown points for F. asiaticum isolates, black triangle points for F. graminearum isolates, and green points for factors including fungicide treatments, plant hosts, year of isolation, province, chemotypes and species.

Generally, for most fungicides, mycotoxin production was reduced with an increase in fungicide concentration. DMI, DMI + DMI, MBC, DMI + MBC, and PP fungicides were found to control mycotoxin production at high doses (≥25 μg/mL) in both F. asiaticum and F. graminearum with few exceptions. However, in F. graminearum, the DMI fungicide hexaconazole could not control DON and 15-ADON production even at the highest dose (25 μg/mL), and propiconazole was found to increase mycotoxin levels in the isolate R51. We also observed that the DMI fungicides difenoconazole and hexaconazole, and the MBC fungicide thiophanate-methyl increased 4-acetyl nivalenol (4-ANIV) at lower doses (≤1 μg/mL for D and Th; ≤5 μg/mL for H) (Fig. 4A and B), but then suppressed the mycotoxins at high doses (25 μg/mL). A similar trend was observed in the F. graminearum isolates where difenoconazole (DMI) and difenoconazole + propiconazole (DMI + DMI), increased mycotoxins at lower doses (<1 μg/mL), followed by suppression at high doses (25 μg/mL).

Fig. 4

Growth (colony diameter) and mycotoxin production by Fusarium asiaticum (R17 & R50), F. graminearum (R05 & R51) at different fungicide concentrations. Alphabetical labels inside each chart represent respective fungicides. (A) Demethylation inhibitor (DMI) and DMI combination fungicides. D, difenoconazole; H, hexaconazole; M, metconazole; P, propiconazole; T, tebuconazole; DP, difenoconazole + propiconazole; PT, propiconazole + tebuconazole; DMI + MBC: PTh, propiconazole + thiophanate-methyl; AH, azoxystrobin + hexaconazole. (B) Non-DMI fungicides. PP fungicide: F, fludioxonil; MBC: Th, thiophanate-methyl; QoI: A, azoxystrobin; Tr, trifloxystrobin; SDHI: Fl, fluxapyroxad; Phthalimides: C, captan. Columns in charts represent growth in terms of colony diameter. Continuous lines across charts represent mycotoxins; 4-ANIV (red), nivalenol (green), 15-ADON (grey), deoxynivalenol (orange), 3-ADON (yellow), and zearalenone (blue). MBC, methyl benzimidazole carbamate; PP, phenylpyrrole; QoI, quinone-outside inhibitor; SDHI, succinate dehydrogenase inhibitors.

QoI, QoI + DMI, SDHI, and phthalimide fungicides could not control mycotoxin levels even at higher doses (>25 μg/mL). Incremental doses of the QoI fungicide trifloxystrobin resulted in a stepwise increase in the 4-ANIV concentration in F. asiaticum (Fig. 4B). Similarly, QoI + DMI, SDHI, and phthalimide fungicides increased the 15-ADON levels in F. graminearum. In addition to the species-specific mycotoxins, ZEA was produced by both Fusarium species. However, its production was inconsistent, and could not be controlled by almost any of the fungicides. High doses of DMI and MBC fungicides lead to increased ZEA production. However, ZEA production was controlled only by the SDHI fungicide fluxapyroxad. Within each species, we observed isolate-specific variations in mycotoxin production in both the FHB fungi (Fig. 4B). Major differences observed included mycotoxin production pattern against specific fungicides and amount of mycotoxins produced in response to different fungicide concentrations. Correlation analyses using Spearman’s rank correlation between fungicide concentrations, fungal growth, and mycotoxin levels indicated that in both species, significantly negative correlation was observed between fungicide concentrations, growth, and mycotoxin production. Mycotoxin production by both species was positively correlated with fungal growth (Fig. 5).

Fig. 5

Correlation analyses between fungicide concentration, growth (colony diameter) and mycotoxin production in Fusarium asiaticum (A) and F. graminearum (B). The upper triangle of the plot shows the Spearman’s correlation coefficients for pairs of variables, the diagonal displays density plots, which help understand the distribution of each variable and the lower triangle shows scatterplots to visualize the relationship between variables. Asterisks (*) indicate statistical significance. ***Highly significant (P < 0.001), **Moderate significance (P < 0.01), *Significant (P < 0.05), no asterisk indicate non-significant. DON, deoxynivalenol; NIV, nivalenol; PP, phenylpyrrole; ZEA, zearalenone; 4-ANIV, 4-acetyl nivalenol; 3-ADON, 3-acetyl deoxynivalenol; 15-ADON, 15-acetyl deoxynivalenol.

Discussion

In this study, we observed that FHB isolates developed resistance to DMI fungicide treatment, especially to those containing propiconazole. The EC₅₀ values of F. asiaticum isolates against propiconazole, difenoconazole + propiconazole, propiconazole + tebuconazole, and propiconazole + thiophanate-methyl significantly increased from 2010 to 2020. Previously, we reported the development of propiconazole resistance in F. asiaticum isolates obtained between 2010–2016 and 2020–2021 (Baek et al., 2022). The changes in EC₅₀ values reported against propiconazole in the earlier study (3.87–5.96 μg/mL) were similar to the current results (4.34–5.22 μg/mL). This reaffirms the increase in propiconazole resistance among FHB-causing F. asiaticum in the southern wheat-growing regions of Korea. Compared with other DMI fungicides, propiconazole has been reported to be less effective in controlling FHB disease severity (McMullen et al., 2012; Mengesha et al., 2021). In addition, as propiconazole was one of the early DMI fungicides, being introduced in 1979 (Morton and Staub, 2008), its long-time usage may be a reason for the development of resistance among FHB fungi. In addition to propiconazole, the current data included resistance development against additional DMI and other fungicide classes (difenoconazole + propiconazole, propiconazole + tebuconazole, propiconazole + thiophanate-methyl, captan, and thiophanate-methyl) not included in an earlier study, thereby allowing for a more comprehensive evaluation of fungicidal effects on the growth of FHB fungi.

Most previous reports on FHB resistance describe an increase in resistance to DMI fungicides over time (Becher et al., 2010; Chen et al., 2021; de Chaves et al., 2022; Lux et al., 2023; Oliver, 2024; Yin et al., 2009; Zhou et al., 2024). However, no significant resistance was observed toward difenoconazole or hexaconazole, and a significant increase in sensitivity was observed toward metconazole and tebuconazole. Previous reports indicate that EC₅₀ values against DMI fungicides, such as tebuconazole, in some cases, can be sustained for longer periods of time (15–80 years) (Hellin et al., 2017; Pasquali et al., 2020). Moreover, the development of resistance against particular fungicides depends on several factors, including the frequency and intensity of fungicide use, genetic diversity within the population, development of unfavorable fitness cost traits, and changing climatic conditions (Cervini et al., 2024; Hellin et al., 2017; Miedaner and Juroszek, 2021).

Among other fungicides, an increase in resistance was observed against MBC and phthalimide, particularly among F. graminearum isolates. Resistance to thiophanate-methyl (MBC) and phthalimides (captan) among Fusarium isolates has been previously documented (Broders et al., 2007; Munkvold and O’Mara, 2002; Rekanović et al., 2010). The development of resistance against MBC fungicides occurs over shorter periods of time (three growing seasons), and continued use has led to complete failure in controlling disease progress (Oliver, 2024). Here, we also report resistance to thiophanate-methyl and captan among FHB fungi in the southern regions of Korea; however, as it was confined only for F. graminearum, it can still be used to combat FHB, albeit with close monitoring of resistance in F. asiaticum. We also observed that the F. asiaticum isolates developed significant sensitivity to the PP fungicide fludioxonil in 2020. Earlier studies have shown that fludioxonil strongly inhibits FHB fungi with very low frequency of resistant isolates (Qiu et al., 2018; Zhou et al., 2020). In another study, among 2910 F. graminearum isolates, only six fludioxonil-resistant isolates were obtained (Wen et al., 2022). All of these studies indicate that more than 99% of the isolates are sensitive to fludioxonil, with EC50 values < 0.2 mg/L. In the present study, the range of EC₅₀ values in F. asiaticum against fludioxonil was 0.001–0.113 mg/L (2010) and 0.002–0.071 mg/L (2020), confirming previous results which indicate that the difference in EC₅₀ between the time periods is very low (<0.02 mg/L). Moreover, the sensitivity to fludioxonil has been reported to be sustained across multiple generations in vitro and in plant hosts (Zhao et al., 2010). Therefore, the PP fungicide fludioxonil is a potential candidate for developing resistance against other classes of fungicides. From 2010 to 2020, the EC₅₀ values remained in the same range or were slightly reduced against the QoI and SDHI fungicides. QoI inhibitor fungicides were introduced relatively recently (in 1996) and have been reported to be effective, especially against oomycete pathogens (Morton and Staub, 2008; Oliver, 2024). Fusarium, however, belongs to Ascomycota, and although we found no significant changes in EC₅₀ values against QoI and SDHI fungicides, prior reports indicate that FHB fungi develop resistance against these fungicides, even upon short-term exposure (Andrade et al., 2022; Chen et al., 2012; de Chaves et al., 2022; Feksa et al., 2019; Paul et al., 2018).

In this study, F. asiaticum was the predominant FHB pathogen, representing more than 90% of the isolates in both the time periods. F. graminearum was present in low numbers, and its resistance patterns partially overlapped with those of the fungicide treatments. The two species were consistently resistant to DMI fungicide combinations (DMI + DMI, DMI + MBC, and QoI + DMI) and phthalimide (captan) (discontinuous upward arrows in Fig. 2). Furthermore, F. graminearum isolates showed higher EC₅₀ values than F. asiaticum for DMI, MBC, and phthalimide fungicides (‘less than’ sign between species in the charts in Fig. 2). Previous research indicates contradictory results when comparing fungicide sensitivity between these two species. In an earlier study, the average EC₅₀ of F. graminearum isolates against DMI fungicides tebuconazole and prochloraz were actually lower, but not statistically significant as compared to that of F. asiaticum isolates (Yin et al., 2009). Responses to the MBC fungicide carbendazim also indicate that F. graminearum isolates had lower baseline EC50 values (0.08–0.98 μg/mL) compared to F. asiaticum isolates (0.47–0.77 μg/mL) (Chen et al., 2019; Liu et al., 2019). Resistance to fungicides in F. asiaticum and F. graminearum may arise from genetic mutations and gene expression regulation mechanisms, which are dependent on ecological factors (Jayawardana and Fernando, 2024; Jie et al., 2025; Zheng et al., 2014; Zhou et al., 2023). Therefore, geographical and environmental factors can have a major impact as compared to genealogy on the development of fungicide resistance among the species.

Although fungicides can effectively control FHB fungi, their effect on mycotoxin production has been mixed (Barro et al., 2023; D’Angelo et al., 2014; Magan et al., 2002; Paul et al., 2008, 2018; Yoshida et al., 2012). Field experimental data indicate that while fungicides can control FHB disease incidence, they do not always reduce the mycotoxin content in grains (Caldwell et al., 2017; Magan et al., 2002). Here, we observed that the DMI fungicides difenoconazole, hexaconazole, metconazole, and tebuconazole, and the PP fungicide fludioxonil had a sustained ability to control FHB across a 10-year period. Mycotoxin production profiles indicated that DMI and PP fungicides at high doses could also control mycotoxin (NIV and 4-ANIV) concentrations in F. asiaticum and F. graminearum (DON and 15-ADON). Previous reports have also indicated that DMI fungicides successfully control FHB and associated mycotoxins (Paul et al., 2008, 2018; Wegulo et al., 2015). Although the PP fungicide fludioxonil has been widely used in China to control FHB in wheat, its effect on mycotoxin production has not been reported (Qiu et al., 2018; Wen et al., 2022; Zhang et al., 2023a; Zhou et al., 2020). We also identified an MBC fungicide and used it in combination with DMI to control mycotoxin production in F. asiaticum (NIV and 4-ANIV) and F. graminearum (DON and 15-ADON). However, in the past, MBC fungicides have been reported to have low efficacy, widespread resistance, and increased mycotoxin levels in grains when pathogens develop resistance to MBC (de Chaves et al., 2022; González-Domínguez et al., 2021; Zhang et al., 2009). Our results also indicated that compared to the DMI and PP fungicides, the ability to control growth and mycotoxin production was less efficient with the MBC fungicide and its combination, but could still be used at high doses. None of the other fungicide treatments in the current study resulted in significant control of mycotoxin production. The QoI fungicide azoxystrobin increased 4-ANIV levels at incremental doses in F. asiaticum. Previously, strobilurin-based QoI fungicides were associated with high DON levels in wheat and barley (de Chaves et al., 2022; Drakopoulos et al., 2021; Ellner, 2005). The phthalimide captan is generally not considered as a primary fungicide for the control of FHB fungi and has been found to be ineffective in controlling the growth of F. graminearum (Broders et al., 2007). Our results indicate that although captan could reduce the growth of FHB fungi at high doses (≥50 μg/mL), it could not reduce mycotoxin production. Among the mycotoxins, ZEA is commonly produced by both species, and only fluxapyroxad (SDHI) could control its levels. Previous research on fluxapyroxad has only reported its ability to control DON; however, its effect on ZEA has not been widely reported (Barro et al., 2023; Xu et al., 2019). We also observed that among the F. asiaticum isolates, DMI fungicides, PP, MBC, and combination treatments initially increased NIV and 4-ANIV at lower doses despite reduced growth, but inhibited both growth and mycotoxins at higher concentrations. In the past, low non-lethal doses of the DMI fungicide metconazole were reported to initially increase DON and 15-ADON levels before controlling them at higher concentrations, both in vitro and in fields (Liu et al., 2023; Magan et al., 2002; Ramirez et al., 2004).

Among the two species, the predominance of F. asiaticum (92.6%) in FHB-infected wheat and barley in Korea exposes it as the target species to be controlled by fungicides. Earlier reports of FHB-causing Fusarium in Korea and China have reported the prevalence of these two species as the only causative pathogens of the disease (Jeon et al., 2024, 2025; Xu et al., 2021). Moreover, F. asiaticum has often been reported to be the most abundant FHB pathogen infecting cereal crops, including wheat, barley, oats, rice, and even weeds across Japan, Korea, and southeastern China (Ahn et al., 2022; Choi et al., 2019; Jeon et al., 2024, 2025; Karugia et al., 2009; Xu et al., 2021; Zhang et al., 2007). It has been hypothesized that warmer climatic conditions encourage the growth of F. asiaticum, whereas other FHB fungi, such as F. culmorum and F. poae, cause disease under cooler climatic conditions (Jeon et al., 2025; Zhang et al., 2023b). In China, wheat and barley grown in rotation with rice have been reported to be favored by F. asiaticum (Zhang et al., 2023b). The fields sampled in this study followed a rotation system for cultivating wheat, barley, and rice during alternate seasons. In addition to the above factors, F. asiaticum has been reported to rapidly and efficiently adapt to environmental changes and infect plant hosts (Choi et al., 2023; Jang et al., 2019). Therefore, in Asia, F. asiaticum has developed into a major FHB pathogen owing to agricultural practices, genetic plasticity, and changing climatic conditions.

Over the past decade, the FHB pathogens have developed resistance to DMI, propiconazole, and fungicide combinations that include propiconazole, probably because of prolonged exposure to the fungicide. As DMI, PP, and MBC fungicides at higher doses could still control FHB disease and mycotoxin production compared to the phthalimide, SDHI, and QoI classes of fungicides, we recommend their use under closely monitored conditions. Development of strategies to reduce and/or improve fungicide efficiency is becoming increasingly important for sustainable agriculture. This includes appropriate timing of fungicide application, complementing fungicides with living microbes or other organic/inorganic supplements (Pazdiora et al., 2023), and searching for novel fungicides, such as benziothiazolinone (1,2-benzisothiazol-3-one), which can control FHB and mycotoxin levels in wheat (Chen et al., 2025). Given the potential threat of the development of resistance, it is essential to develop sustainable strategies that effectively manage both the incidence of FHB and mycotoxin contamination.

Notes

Conflicts of Interest

No potential conflict of interest relevant to this article was reported.

Acknowledgments

This study was supported by “Research Program for Agricultural Science & Technology Development (Project No. PJ017227)”, National Institute of Agricultural Sciences, Rural Development Administration, Republic of Korea.

References

Ahn S., Kim M., Lim J. Y., Choi G. J., Seo J.-A.. 2022;Characterization of Fusarium asiaticum and F. graminearum isolates from gramineous weeds in the proximity of rice fields in Korea. Plant Pathol. 71:1164–1173.

Andrade S. M. P., Augusti G. R., Paiva G. F., Feksa H. R., Tessmann D. J., Machado F. J., Mizubuti E. S. G., Del Ponte E. M.. 2022;Phenotypic and molecular characterization of the resistance to azoxystrobin and pyraclostrobin in Fusarium graminearum populations from Brazil. Plant Pathol. 71:1152–1163.

Baek J., Nah J.-Y., Lee M.-J., Lim S.-B., Choi J.-H., Jang J. Y., Lee T., Choi H.-W., Kim J.. 2022;Change in the sensitivity to propiconazole of Fusarium graminearum species complex causing head blight of barley and wheat in Jeolla Province. Korean J. Mycol. 50:281–289. (in Korean).

Barro J. P., Santana F. M., Tibola C. S., Machado F. J., Schipanski C. A., Chagas D. F., Guterres C. W., Casarotto G., Capitanio C. G., Dallagnol L. J., Kuhnem P., Feksa H. R., Venancio W. S., Del Ponte E. M.. 2023;Comparison of single- or multi-active ingredient fungicides for controlling Fusarium head blight and deoxynivalenol in Brazilian wheat. Crop Prot. 174:106402.

Becher R., Hettwer U., Karlovsky P., Deising H. B., Wirsel S. G. R.. 2010;Adaptation of Fusarium graminearum to tebuconazole yielded descendants diverging for levels of fitness, fungicide resistance, virulence, and mycotoxin production. Phytopathology 100:444–453.

Broders K. D., Lipps P. E., Paul P. A., Dorrance A. E.. 2007;Evaluation of Fusarium graminearum associated with corn and soybean seed and seedling disease in Ohio. Plant Dis. 91:1155–1160.

Caldwell C. D., MacDonald D., Jiang Y., Cheema M. A., Li J.. 2017;Effect of fungicide combinations for Fusarium head blight control on disease incidence, grain yield, and quality of winter wheat, spring wheat, and barley. Can. J. Plant Sci. 97:1036–1045.

Cervini C., Naz N., Verheecke-Vaessen C., Medina A.. 2024;Impact of predicted climate change environmental conditions on the growth of Fusarium asiaticum strains and mycotoxins production on a wheat-based matrix. Int. J. Food Microbiol. 416:110658.

Chen H., Wu Q., Zhang G., Wu J., Zhu F., Yang H., Zhuang Y.. 2019;Carbendazim-resistance of Gibberella zeae associated with Fusarium head blight and its management in Jiangsu province, China. Crop Prot. 124:104866.

Chen J., Wei J., Fu L., Wang S., Liu J., Guo Q., Jiang J., Tian Y., Che Z., Chen G., Liu S.. 2021;Tebuconazole resistance of Fusarium graminearum field populations from wheat in Henan Province. J. Phytopathol. 169:525–532.

Chen X., Liu C., Liu W., Yang J., Gu C., Sun Y., Cao H., Chen Y.. 2025;Study on the mechanism of benziothiazolinone and its synergistic effect with tebuconazole in inhibiting Fusarium asiaticum and DON production. J. Agric. Food Chem. 73:4947–4957.

Chen Y., Zhang A.-F., Gao T.-C., Zhang Y., Wang W.-X., Ding K.-J., Chen L., Sun Z., Fang X.-Z., Zhou M.-G.. 2012;Integrated use of pyraclostrobin and epoxiconazole for the control of Fusarium head blight of wheat in Anhui Province of China. Plant Dis. 96:1495–1500.

Choi J.-H., Nah J.-Y., Jin H.-S., Lim S.-B., Paek J.-S., Lee M.-J., Jang J.-Y., Lee T., Hong S. K., Kim J.. 2019;Identification and chemotype profiling of Fusarium species in Korean oat. Res. Plant Dis. 25:157–163. (in Korean).

Choi S., Yang J. W., Kim J.-E., Jeon H., Shin S., Wui D., Kim L. S., Kim B. J., Son H., Min K.. 2023;Infectivity and stress tolerance traits affect community assembly of plant pathogenic fungi. Front. Microbiol. 14:1234724.

D’Angelo D. L., Bradley C. A., Ames K. A., Willyerd K. T., Madden L. V., Paul P. A.. 2014;Efficacy of fungicide applications during and after anthesis against Fusarium head blight and deoxynivalenol in soft red winter wheat. Plant Dis. 98:1387–1397.

de Chaves M. A., Reginatto P., da Costa B. S., de Paschoal R. I., Teixeira M. L., Fuentefria A. M.. 2022;Fungicide resistance in Fusarium graminearum species complex. Curr. Microbiol. 79:62.

Drakopoulos D., Sulyok M., Jenny E., Kägi A., Bänziger I., Logrieco A. F., Krska R., Vogelgsang S.. 2021;Fusarium head blight and associated mycotoxins in grains and straw of barley: influence of agricultural practices. Agronomy 11:801.

Dubos T., Pasquali M., Pogoda F., Hoffmann L., Beyer M.. 2011;Evidence for natural resistance towards trifloxystrobin in Fusarium graminearum. Eur. J. Plant Pathol. 130:239–248.

Ellner F. M.. 2005;Results of long-term field studies into the effect of strobilurin containing fungicides on the production of mycotoxins in several winter wheat varieties. Mycotoxin Res. 21:112–115.

Feksa H. R., Do Couto H. T. Z., Garozi R., De Almeida J. L., Gardiano C. G., Tessmann D. J.. 2019;Pre- and postinfection application of strobilurin-triazole premixes and single fungicides for control of Fusarium head blight and deoxynivalenol mycotoxin in wheat. Crop Prot. 117:128–134.

Food and Agriculture Organization of the United Nations. 2021. Climate change fans spread of pests and threatens plants and crops, new FAO study URL https://www.fao.org/newsroom/detail/Climate-change-fans-spread-of-pests-and-threatens-plants-and-crops-new-FAO-study/en [31 January 2025].

Food and Agriculture Organization of the United Nations. 2024. FAOSTAT database URL https://www.fao.org/faostat/en/#home [31 January 2025].

Ganesan A. R., Mohan K., Karthick Rajan D., Pillay A. A., Palanisami T., Sathishkumar P., Conterno L.. 2022;Distribution, toxicity, interactive effects, and detection of ochratoxin and deoxynivalenol in food: a review. Food Chem. 378:131978.

Gaurilčikienė I., Mankevičienė A., Supronienė S.. 2011;The effect of fungicides on rye and triticale grain contamination with Fusarium fungi and mycotoxins. Žemdirbystė 98:19–26.

González-Domínguez E., Meriggi P., Ruggeri M., Rossi V.. 2021;Efficacy of fungicides against Fusarium head blight depends on the timing relative to infection rather than on wheat growth stage. Agronomy 11:1549.

Goswami R. S., Kistler H. C.. 2004;Heading for disaster: Fusarium graminearum on cereal crops. Mol. Plant Pathol. 5:515–525.

Hellin P., Scauflaire J., Van Hese V., Munaut F., Legrève A.. 2017;Sensitivity of Fusarium culmorum to triazoles: impact of trichothecene chemotypes, oxidative stress response and genetic diversity. Pest. Manag. Sci. 73:1244–1252.

Jang J. Y., Baek S. G., Choi J.-H., Kim S., Kim J., Kim D.-W., Yun S.-H., Lee T.. 2019;Characterization of nivalenol-producing Fusarium asiaticum that causes cereal head blight in Korea. Plant Pathol. J. 35:543–552.

Jayawardana M. A., Fernando W. G. D.. 2024;The mechanisms of developing fungicide resistance in Fusarium graminearum causing Fusarium head blight and fungicide resistance management. Pathogens 13:1012.

Jeon H., Yang J.-W., Lee N.-H., Shin D., Min D., Lee N., Baek S. G., Nah J.-Y., Kim B., Lee M.-J., Kang I.-J., Kim Y.-H., Kim K.-H., Son H., Lee T.. 2025. Systematic surveillance of Fusarium head blight in the southern region of the Republic of Korea. Plant Dis. Online publication. https://doi.org/10.1094/PDIS-02-25-0282-SR.

Jeon H., Yang J. W., Shin D., Min D., Kim B. J., Min K., Son H.. 2024;Development of a selective medium for surveillance of Fusarium head blight disease. Plant Pathol. J. 40:106–114.

Jiang J., Hu B., Gao X., Cui Y., Qian L., Xu J., Liu S.. 2025;In vitro determination of the sensitivity of Fusarium graminearum to fungicide fluopyram and investigation of the resistance mechanism. J. Agric. Food Chem. 73:4001–4011.

Jie Z., SiYu S., Yu G., Fuhao R., Guilin S., Huan W., Baoquan Z., Yiqiang C., Chunyan G., Yabing D.. 2025;Risk assessment and resistant mechanism of Fusarium graminearum to fluopyram. Pestic. Biochem. Phys. 212:106449.

Johns L. E., Bebber D. P., Gurr S. J., Brown N. A.. 2022;Emerging health threat and cost of Fusarium mycotoxins in European wheat. Nat. Food 3:1014–1019.

Karugia G., Suga H., Gale L., Nakajima T., Tomimura K., Hyakumachi M.. 2009;Population structure of the Fusarium graminearum species complex from a single Japanese wheat field sampled in two consecutive years. Plant Dis. 93:170–174.

Lee J., Kim H., Jeon J.-J., Kim H.-S., Zeller K. A., Carter L. L. A., Leslie J. F., Lee Y.-W.. 2012;Population structure of and mycotoxin production by Fusarium graminearum from maize in South Korea. Appl. Environ. Microbiol. 78:2161–2167.

Lee T., Paek J.-S., Lee K. A., Lee S., Choi J.-H., Ham H., Hong S. K., Ryu J.-G.. 2016;Occurrence of toxigenic Fusarium vorosii among small grain cereals in Korea. Plant Pathol. J. 32:407–413.

Limay-Rios V., Schaafsma A. W.. 2018;Effect of prothioconazole application timing on Fusarium mycotoxin content in maize grain. J. Agric. Food Chem. 66:4809–4819.

Liu S., Fu L., Wang S., Chen J., Jiang J., Che Z., Tian Y., Chen G.. 2019;Carbendazim resistance of Fusarium graminearum from Henan wheat. Plant Dis. 103:2536–2540.

Liu X., Wang S., Fan Z., Wu J., Wang L., He D., Mohamed S. R., Dawood D. H., Shi J., Gao T., Xu J.. 2023;Antifungal activities of metconazole against the emerging wheat pathogen Fusarium pseudograminearum. Pestic. Biochem. Phys. 190:105298.

Lux L., Halvorson J., Hansen B., Meyer S., Carruth D., Fitterer S., Friskop A.. 2023;Effects of metconazole + prothioconazole, pydiflumetofen + propiconazole, and variety resistance on Fusarium head blight and yield in hard red spring wheat. Plant Health Prog. 24:155–161.

Magan N., Hope R., Colleate A., Baxter E. S.. 2002;Relationship between growth and mycotoxin production by Fusarium species, biocides and environment. Eur. J. Plant Pathol. 108:685–690.

McMullen M., Bergstrom G., De Wolf E., Dill-Macky R., Hershman D., Shaner G., Van Sanford D.. 2012;A unified effort to fight an enemy of wheat and barley: Fusarium head blight. Plant Dis. 96:1712–1728.

Mengesha G. G., Abebe S. M., Lera Z. T., Shertore M. M., Fedilu K. B., Tadesse Y. B., Mekonnen A. A., Esho A. G. M., Cheleko D. C., Silassie A. B. W.. 2021;Integration of host resistance, fungicides, and spray frequencies for managing Fusarium head blight of bread wheat under field conditions in southern Ethiopia. Heliyon 7:e07938.

Miedaner T., Juroszek P.. 2021;Climate change will influence disease resistance breeding in wheat in northwestern Europe. Theor. Appl. Genet. 134:1771–1785.

Morton V., Staub T.. 2008;A short history of fungicides. APSnet Features 308:1–12.

Munkvold G. P., O’Mara J. K.. 2002;Laboratory and growth chamber evaluation of fungicidal seed treatments for maize seedling blight caused by Fusarium species. Plant Dis. 86:143–150.

Oliver R. P.. 2024. Chapter 10 - Control of plant diseases. Agrios’ plant pathology sixth editionth ed. In : Oliver R. P., ed. p. 279–316. Academic Press. Cambridge, MA, USA:

Pasquali M., Pallez-Barthel M., Beyer M.. 2020;Searching molecular determinants of sensitivity differences towards four demethylase inhibitors in Fusarium graminearum field strains. Pestic. Biochem. Phys. 164:209–220.

Paul P. A., Bradley C. A., Madden L. V., Lana F. D., Bergstrom G. C., Dill-Macky R., Esker P. D., Wise K. A., McMullen M., Grybauskas A., Kirk W. W., Milus E., Ruden K.. 2018;Meta-analysis of the effects of QoI and DMI fungicide combinations on Fusarium head blight and deoxynivalenol in wheat. Plant Dis. 102:2602–2615.

Paul P. A., Lipps P. E., Hershman D. E., McMullen M. P., Draper M. A., Madden L. V.. 2008;Efficacy of triazole-based fungicides for Fusarium head blight and deoxynivalenol control in wheat: a multivariate meta-analysis. Phytopathology 98:999–1011.

Pazdiora P. C., Crizel R. L., da Rosa Dorneles K., da Silva S. M., Morello T. N., Chaves F. C., Dallagnol L. J.. 2023;Silicon amendment improves wheat defence against Fusarium graminearum and complements the control by fungicide of Fusarium head blight. Plant Pathol. 72:53–66.

Qiu J. B., Yu M. Z., Yin Q., Xu J. H., Shi J. R.. 2018;Molecular characterization, fitness, and mycotoxin production of Fusarium asiaticum strains resistant to fludioxonil. Plant Dis. 102:1759–1765.

Rai A., Das M., Tripathi A.. 2020;Occurrence and toxicity of a Fusarium mycotoxin, zearalenone. Crit. Rev. Food Sci. Nutr. 60:2710–2729.

Ramirez M. L., Chulze S., Magan N.. 2004;Impact of environmental factors and fungicides on growth and deoxinivalenol production by Fusarium graminearum isolates from Argentinian wheat. Crop Prot. 23:117–125.

Rekanović E., Mihajlović M., Potočnik I.. 2010;In vitro sensitivity of Fusarium graminearum (Schwabe) to difenoconazole, prothioconazole and thiophanate-methyl. Pestic. Phytomed. 25:325–333.

Savary S., Willocquet L., Pethybridge S. J., Esker P., McRoberts N., Nelson A.. 2019;The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 3:430–439.

Tini F., Beccari G., Onofri A., Ciavatta E., Gardiner D. M., Covarelli L.. 2020;Fungicides may have differential efficacies towards the main causal agents of Fusarium head blight of wheat. Pest Manag. Sci. 76:3738–3748.

Wegulo S. N., Baenziger P. S., Hernandez Nopsa J., Bockus W. W., Hallen-Adams H.. 2015;Management of Fusarium head blight of wheat and barley. Crop Prot. 73:100–107.

Wen Z., Wang J., Jiao C., Shao W., Ma Z.. 2022;Biological and molecular characterizations of field fludioxonil-resistant isolates of Fusarium graminearum. Pestic. Biochem. Physiol. 184:105101.

Xu C., Li M., Zhou Z., Li J., Chen D., Duan Y., Zhou M.. 2019;Impact of five succinate dehydrogenase inhibitors on DON biosynthesis of Fusarium asiaticum, causing Fusarium head blight in wheat. Toxins 11:272.

Xu F., Liu W., Song Y., Zhou Y., Xu X., Yang G., Wang J., Zhang J., Liu L.. 2021;The distribution of Fusarium graminearum and Fusarium asiaticum causing Fusarium head blight of wheat in relation to climate and cropping system. Plant Dis. 105:2830–2835.

Yin Y., Liu X., Li B., Ma Z.. 2009;Characterization of sterol demethylation inhibitor-resistant isolates of Fusarium asiaticum and F. graminearum collected from wheat in China. Phytopathology 99:487–497.

Yoshida M., Nakajima T., Tomimura K., Suzuki F., Arai M., Miyasaka A.. 2012;Effect of the timing of fungicide application on Fusarium head blight and mycotoxin contamination in wheat. Plant Dis. 96:845–851.

Zhang J.-B., Li H.-P., Dang F.-J., Qu B., Xu Y.-B., Zhao C.-S., Liao Y.-C.. 2007;Determination of the trichothecene mycotoxin chemotypes and associated geographical distribution and phylogenetic species of the Fusarium graminearum clade from China. Mycol. Res. 111:967–975.

Zhang N., Xu Y., Zhang Q., Zhao L., Zhu Y., Wu Y., Li Z., Yang W.. 2023a;Detection of fungicide resistance to fludioxonil and tebuconazole in Fusarium pseudograminearum, the causal agent of Fusarium crown rot in wheat. PeerJ. 11:e14705.

Zhang Y.-J., Yu J.-J., Zhang Y.-N., Zhang X., Cheng C.-J., Wang J.-X., Hollomon D. W., Fan P.-S., Zhou M.-G.. 2009;Effect of carbendazim resistance on trichothecene production and aggressiveness of Fusarium graminearum. Mol. Plant Microbe Interact. 22:1143–1150.

Zhang Y.-Z., Li Z., Man J., Xu D., Wen L., Yang C., Xu Q., Jiang Q.-T., Chen G.-Y., Deng M., Peng Y.-L., Zhong K., Qi P.-F., Wei Y.-M.. 2023b;Genetic diversity of field Fusarium asiaticum and Fusarium graminearum isolates increases the risk of fungicide resistance. Phytopathol. Res. 5:51.

Zhao H., Kim Y. K., Huang L., Xiao C. L.. 2010;Resistance to thiabendazole and baseline sensitivity to fludioxonil and pyrimethanil in Botrytis cinerea populations from apple and pear in Washington State. Postharvest Biol. Technol. 56:12–18.

Zheng Z., Gao T., Zhang Y., Hou Y., Wang J., Zhou M.. 2014;FgFim, a key protein regulating resistance to the fungicide JS399-19, asexual and sexual development, stress responses and virulence in Fusarium graminearum. Mol. Plant Pathol. 15:488–499.

Zhou F., Li D. X., Hu H. Y., Song Y. L., Fan Y. C., Guan Y. Y., Song P. W., Wei Q. C., Yan H. F., Li C. W.. 2020;Biological characteristics and molecular mechanisms of fludioxonil resistance in Fusarium graminearum in China. Plant Dis. 104:2426–2433.

Zhou F., Zhou H.-H., Han A.-H., Guo K.-Y., Liu T.-C., Wu Y.-B., Hu H.-Y., Li C.-W.. 2023;Mechanism of pydiflumetofen resistance in Fusarium graminearum in China. J. Fungi 9:62.

Zhou F., Zhou X., Jiao Y., Han A., Su H., Wang L., Zhou H., Li W., Liu R.. 2024;Potential mechanisms of hexaconazole resistance in Fusarium graminearum. Plant Dis. 108:3133–3145.

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