Sensitivity of Cercospora spp. to SDHI, QoI, DMI and SBI fungicides and resistance to QoI fungicides in Brazil

doi:10.21203/rs.3.rs-4533152/v1

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Sensitivity of Cercospora spp. to SDHI, QoI, DMI and SBI fungicides and resistance to QoI fungicides in Brazil

https://doi.org/10.21203/rs.3.rs-4533152/v1

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The most widely used control strategy for PSS (Purple Seed Stain) and CLB (Cercospora Leaf Blight), caused by the fungus Cercospora, is fungicides, which are essential for managing these diseases. However, cases of reduced sensitivity of these fungi to fungicides have been reported, as well as an increase in mutations for different chemical groups. Therefore, it is crucial to monitor the sensitivity of fungal species to the main fungicides used in soybean crops and identify the presence of mutations. This study aimed to evaluate the sensitivity alteration of Cercospora spp. species in response to different fungicides, as well as to identify the G143A mutation in the cytb gene, related to resistance to the QoI chemical group. Isolates of Cercospora spp. were collected from different soybean-producing regions in Brazil. To determine the sensitivity of the isolates, the effective concentration (EC₅₀) was determined in vitro using fungicides from different chemical groups, including SDHI, QoI, DMI, and SBI. The fungicide concentrations added to the PDA culture medium were: 1 mg.L^-1, 10 mg.L^-1, 50 mg.L^-1, and 100 mg.L^-1, with a control treatment of 0 mg.L^-1. For the identification of the G143A mutation in the cytb gene, genetic sequencing was performed on 29 isolates. The SDHI fungicides showed EC₅₀ values ranging from 53.91 to 100 mg.L^-1 for Cercospora spp., indicating reduced sensitivity. The AZB fungicide (QoI) presented an EC₅₀ value of 100 mg.L^-1 for the tested species, which were insensitive. The DMI fungicides showed variations in EC₅₀ values (0.12 to 100 mg.L^-1), with species exhibiting variable sensitivity. The FPM fungicide (SBI) showed the lowest EC₅₀ values <1 mg.L^-1, with species being extremely sensitive. Resistance mutations in the G143A gene were detected in 86% of the isolates. Therefore, the results show that Cercospora species exhibited variations in sensitivity to fungicides, with DFZ, MFTZ, and FPM fungicides being the most fungitoxic and BFZ, BIX, FXD, PFF, and AZB being the least fungitoxic. The identification of the G143A mutation in the isolates underscores the importance of continuous monitoring and the use of practices that contribute to resistance management.

Cercospora cf. flagellaris

Glycine max

EC50

chemical control

Cercospora leaf blith

purple seed stain

strobilurins.

Brazil stands out as one of the largest producers and exporters of soybean (Glycine max (L.) Merr.), one of the world's major commodities. However, the expansion of the cultivation area, combined with the no-till farming system and soybean monoculture, has the potential to limit the crop's productive potential during the growth phase. This limitation stems from its dependence on biotic and abiotic factors, associated with climatic factors that favor the development of diseases caused by fungi such as Cercospora spp. (Hartman et al. 2011). Among the predominant species associated with diseases in soybean cultivation areas are C. kikuchii, responsible for causing purple seed stain and Cercospora leaf blight (Hartman et al. 2015).

Purple seed stain (PSS) and Cercospora leaf blight (CLB) are widespread in soybean-producing regions of Brazil, with PSS predominantly found in seed lots. The causal agent of these diseases, historically considered singular, is the fungus Cercospora kikuchii (Matsu & Tomoyasu) Gardner. However, recent research validates the presence of other species associated with PSS and CLB, such as C. cf. sigesbeckiae, C. cf. nicotianae, and C. cf. flagellaris, with the latter being more frequent in Brazilian soybean-producing regions (Albu et al. 2016; Sautua et al. 2019; 2020; Silva 2022; Soares et al. 2015).

Management strategies for PSS and CLB can encompass genetic, cultural, and chemical approaches, with the latter proving to be more effective. The fungicides used for the control of CLB generally belong to chemical groups such as triazoles (demethylation inhibitors, DMI), strobilurins (Quinone outside inhibitors, QoI), benzimidazoles (Methyl-benzimidazole-carbamate, MBC), and multi-site dithiocarbamates (mancozeb, M3) and isophthalonitriles (chlorothalonil, M4) (AGROFIT 2024; FRAC 2024a).

Initially recommended for the control of powdery mildew (Erysiphe diffusa) following an epidemic in 1996/97, fungicides in soybean cultivation areas were subsequently used against late-season diseases (LSDs) Septoria glycines and Cercospora kikuchii, attributed to soybean monoculture and the absence of crop rotation. The emergence of Asian soybean rust (Phakopsora pachyrhizi) in 2001, coupled with the lack of resistant soybean varieties, led to an increase in the registration of new products and the intensified use of fungicides (GODOY 2015; GODOY et al. 2007).

Despite the efficacy of disease control through fungicides, fungal resistance to these products can result in control failures. Recent studies document the reduced sensitivity of Cercospora spp. isolates to fungicides from the MBC and QoI chemical groups in several countries, including the United States (Price et al. 2015), Argentina (Sautua et al. 2020), and more recently, Brazil (Mello et al. 2021). The QoI chemical group, when used alone, shows low control efficiency for the PSS and CLB complex in soybeans (GODOY 2017).

However, information on the efficacy of fungicides with different mechanisms of action for Cercospora spp. species causing PSS and CLB in soybeans is still limited. In this context, it becomes essential to identify the species present in cultivation areas and monitor the sensitivity alteration of these species to the main chemical groups of fungicides used in soybean cultivation. Thus, the objectives of this study were to evaluate the sensitivity alteration of Cercospora spp. species in response to different fungicides and to identify the G143A mutation in the cytb gene related to resistance to the QoI chemical group.

Collection of Cercospora spp. Isolates

Cercospora spp. isolates were obtained from soybean seeds showing symptoms of purple seed stain (PSS) and Cercospora leaf blight (CLB) from various Brazilian states. Fragments of leaves and seeds were isolated and transferred to Petri dishes containing V8 agar culture medium (20 g.L^− 1 agar, 1 g.L^− 1 sucrose, 0.60 g.L^− 1 calcium carbonate, 0.2 g.L^− 1 yeast extract, and 40 ml.L^− 1 V8 vegetable juice "Campbell's") (Alfenas et al. 2016). The pure colonies cultivated on Petri dishes were incubated in a growth chamber at 25 ± 2°C under a 12-hour photoperiod for 20 days. In total, twenty-nine isolates were obtained (Table 1).

Initially, the identification of the fungal genus was based on the morphological characteristics of the fungal structures (Barnett and Hunter 1972) and pathogenicity tests on soybean plants. Subsequently, the isolates were identified by molecular analysis, using two regions: ITS (Internal Transcribed Spacer) and DNA (White et al. 1990).

In Vitro Determination of the Effective Concentration ( _EC50 ) of Fungicides by Mycelial Growth Inhibition Method and Identification of QoI Resistance

To determine the EC₅₀, the mycelial growth inhibition method was used, performed on Petri dishes with fungicides added to the culture medium. Six Cercospora spp. isolates, from different species, were selected for the study. These isolates were cultured in V8 agar medium at 25 ± 2°C under a 12-hour photoperiod for a period of 20 days. Petri dishes with a 9 cm diameter were used as experimental units, with five replicates for each isolate. Mycelial discs with an 8 mm diameter were taken from each isolate and transferred to Petri dishes containing PDA (potato dextrose agar) culture medium (4 g.L^− 1 potato infusion, 20 g.L^− 1 dextrose, 15 g.L^− 1 agar, pH 5.6 ± 0.2) with the respective concentrations of fungicides, while the control did not receive any fungicide addition.

The fungicides from the following chemical groups were used: SDHI (benzovindiflupyr, bixafen, fluxapyroxad, and pydiflumetofen), QoI (azoxystrobin), DMI (difenoconazole, mefentrifluconazole, propiconazole, prothioconazole, tebuconazole, and tetraconazole), and SBI (fenpropidin and fenpropimorph).

The methodology for determining the EC₅₀ followed the guidelines established by Price et al. (2015) and Sautua et al. (2020). The fungicide concentrations added to the culture medium were: 1 mg.L^− 1, 10 mg.L^− 1, 50 mg.L^− 1, and 100 mg.L^− 1, with the control treatment without fungicide addition (0 mg.L^− 1). The fungicides were diluted in sterilized distilled water and added to the PDA culture medium at the respective concentrations. In the case of QoI fungicides, the salicylhydroxamic acid (SHAM) inhibitor of the alternative respiration pathway (AOX) was not used, as it proved toxic to C. kikuchii isolates in vitro and had no significant effect on mycelial growth for C. kikuchii and other Cercospora spp. species (Mello et al. 2021; Price et al. 2015; Sautua et al. 2020).

After 24 hours, an 8 mm diameter mycelial disc from each isolate was transferred to each Petri dish with the respective fungicide concentrations. The plates were incubated at 25°C ± 2°C under a 12-hour photoperiod for 20 days. The mycelial growth of each isolate was measured with a digital caliper. Due to the scarce sporulation of the fungus in culture medium, the germinated spores assay was not performed.

Data were subjected to regression analysis using RStudio version 1.2.5033 software, with the "drc" package (R CORE TEAM 2020). To determine the sensitivity of the isolates to fungicides, the methodology proposed by Edgington and Klew (1971) was used, where fungi are sensitive to fungicides when the EC₅₀ is less than 1 mg.L^− 1, moderately sensitive to fungicides when the EC₅₀ is between 1 and 50 mg.L^− 1, and fungi are insensitive to fungicides when the EC₅₀ value is greater than 50 mg.L^− 1. To verify the resistance of Cercospora spp. isolates, sequencing of the cytb region was performed to check for the G143A mutation (Sautua et al. 2020), as this region is associated with loss of sensitivity to fungicides of the strobilurin group (QoI).

The fungicides from the SDHI chemical group presented EC₅₀ values ranging from 48.88 to 100 mg.L^-1. For the fungicide BZF (Table 2), the EC₅₀ values for Cercospora species were between 53.91 and 100 mg.L^-1, with no inhibition of mycelial growth for C. cf. flagellaris (UPFCe02), C. helianthicola (UPFCe06), and C. canescens (UPFCe18), which were considered insensitive to the fungicide. For the fungicide BIX, an EC₅₀ of 100 mg.L^-1 was observed for C. cf. flagellaris, 89.10 mg.L^-1 for C. helianthicola, 61.94 mg.L^-1 for C. lagenariae strain, 74.03 mg.L^-1 for C. beticola, and 66.05 mg.L^-1 for C. canescens, all classified as insensitive. For the species C. dichondrae, the EC₅₀ value of the BIX fungicide was 48.88 mg.L^-1, classified as moderately sensitive. The FXD and PFF fungicides were the least fungitoxic for Cercospora spp., with an EC₅₀ of 100 mg.L^-1 for all species, being considered insensitive.

The fungicide azoxystrobin from the QoI chemical group showed EC₅₀ values of 100 mg.L^-1 for all evaluated species, indicating that these species are insensitive to this fungicide.

The DMI fungicides showed EC₅₀ variations from 0.12 to 100 mg.L^-1. The DFZ fungicide showed values lower than 1 mg.L^-1 for C. cf. flagellaris (0.90 mg.L^-1), C. dichondrae (0.50 mg.L^-1), C. helianthicola (1.88 mg.L^-1), C. beticola (0.50 mg.L^-1), and C. canescens (0.88 mg.L^-1), all classified as sensitive. The highest EC⁵⁰ value for DFZ was 28.66 mg.L^-1 for C. lagenariae strain, classified as moderately sensitive. The MFTZ fungicide had EC₅₀ values ranging from 0.12 to 1.74 mg.L^-1, with 0.49 mg.L^-1 for C. cf. flagellaris, 0.52 mg.L^-1 for C. helianthicola, 0.12 mg.L^-1for C. lagenariae strain, 0.20 mg.L^-1 for C. beticola, and 0.80 mg.L^-1 for C. canescens, all classified as sensitive. The highest value was observed for C. dichondrae (1.74 mg.L^-1), classified as moderately sensitive. The PPZ fungicide had EC₅₀ values between 0.53 and 100 mg.L^-1, with C. cf. flagellaris (0.81 mg.L^-1) and C. beticola (0.53 mg.L^-1) classified as sensitive, while C. dichondrae (3.31 mg.L^-1), C. helianthicola (19.23 mg.L^-1), and C. canescens (4.15 mg.L^-1) were classified as moderately sensitive, and C. lagenariae strain (100 mg.L^-1) as insensitive. The PTZ fungicide showed EC₅₀ values between 0.30 to 9.60 mg.L^-1, with C. dichondrae (1.64 mg.L^-1), C. helianthicola (6.36 mg.L^-1), and C. lagenariae strain (9.60 mg.L^-1) classified as moderately sensitive, and C. cf. flagellaris (0.33 mg.L^-1), C. beticola (0.30 mg.L^-1), and C. canescens (0.80 mg.L^-1) classified as sensitive. For the TBZ fungicide, all species were classified as moderately sensitive, with the highest EC₅₀ value for C. lagenariae strain (92.10 mg.L^-1) and the lowest for C. beticola (6.85 mg.L^-1). The same behavior was observed for the TTZ fungicide, with the highest EC₅₀ value for C. lagenariae strain (100 mg.L^-1) and the lowest for C. beticola (4.70 mg.L^-1).

The SBI fungicides showed EC₅₀ values ranging from 0.04 to 16.43 mg.L^-1. For the FPD fungicide, C. cf. flagellaris (0.96 mg.L^-1) was classified as sensitive, while all other species were moderately sensitive: C. dichondrae (6.80 mg.L^-1), C. helianthicola (7.40 mg.L^-1), C. lagenariae strain (16.43 mg.L^-1), C. beticola (8.43 mg.L^-1), and C. canescens (4.50 mg.L^-1). The FPM fungicide presented the lowest EC₅₀ values for all studied species: 0.04 mg.L^-1 for C. cf. flagellaris, 0.09 mg.L^-1 for C. dichondrae, 0.64 mg.L^-1 for C. helianthicola, 0.20 mg.L^-1 for C. lagenariae strain, 0.96 mg.L^-1 for C. beticola, and 0.18 mg.L^-1 for C. canescens, all classified as sensitive.

Regarding the sensitivity of Cercospora spp. species, following the classification by Edgington and Klew (1971), C. cf. flagellaris was sensitive to DFZ, MFTZ, PPZ, and PTZ (DMI), moderately sensitive to TBZ and TTZ (DMI), and insensitive to BZF, BIX, FXD, and PFF (SDHI) and AZB (QoI). C. dichondrae was highly sensitive to DFZ and FPM, moderately sensitive to BIX (SDHI), MFTZ, PPZ, PTZ, TTZ (DMI), and FPD (SBI), and insensitive to BZF, FXD, and PFF (SDHI), as well as AZB (QoI) and TBZ (DMI). C. helianthicola was highly sensitive to MFTZ (DMI) and FPM (SBI), moderately sensitive to DFZ, PPZ, PTZ, and FPD (DMI), and insensitive to BFZ, BIX, FXD, and PFF (SDHI), as well as AZB (QoI), TBZ, and TTZ (DMI). C. lagenariae strain was highly sensitive to MFTZ (DMI) and FPM (SBI), moderately sensitive to DFZ, PTZ (DMI), and FPD (SBI), and insensitive to BZF, BIX, FXD, PFF (SDHI), AZB (QoI), PPZ, TBZ, and TTZ (DMI). C. beticola was highly sensitive to DFZ, MFTZ, PPZ, PTZ (DMI), and FPM (SBI), moderately sensitive to TBZ, TTZ (DMI), and FPD (SBI), and insensitive to SDHI and QoI fungicides. C. canescens was highly sensitive to DFZ, MFTZ, PTZ (DMI), and FPM (SBI), moderately sensitive to PPZ, TBZ, TTZ (DMI), and FPD (SBI), and insensitive to SDHI and QoI fungicides.

The sequencing results of the cytb gene region for twenty-nine Cercospora spp. isolates (Table 1) indicated the presence of the G143A mutation in twenty-five tested isolates, that is, 86% of Cercospora spp. isolates presented the mutation in the gene, characterized by the substitution of the nucleotide sequence GGT by GCT in the fungal cytb gene. The resistance of fungi to QoI fungicides is linked to the G143A mutation, and the identification of this mutation in the tested isolates confirms the occurrence of resistance in these Cercospora populations. Analyzing the EC₅₀ results for the QoI fungicide azoxystrobin (AZB), which presented a value of 100 mg.L^-1, indicating that isolates of C. cf. flagellaris (UPFCe02), C. dichondrae (UPFCe05), C. helianthicola (UPFCe06), C. lagenariae strain (UPFCe07), C. beticola (UPFCe09), and C. canescens (UPFCe18) are insensitive, corroborates the detection of the G143A mutation. This mutation was found in isolates from different states, indicating potential dissemination of resistance to soybean-producing areas. Additionally, the presence of the mutation in different Cercospora species suggests a widespread occurrence of pathogen resistance within this genus.

The EC₅₀ varied among the chemical groups of fungicides evaluated in this study for Cercospora species. This variation is related to the pathogen's adaptability to fungicides, as well as the diversity within populations regarding their aggressiveness (genetic and physiological), resulting in decreased fungicide performance and the selection of resistant organisms. Additionally, the intensive and repetitive use of fungicides with the same mechanisms of action may lead to reduced fungal sensitivity to fungicides and consequently, failure in disease control in the field. In this study, only C. dichondrae species showed moderate sensitivity to the fungicide BIX (SDHI), while the other evaluated species were insensitive. Fungicides from this chemical group are widely used to control Asian rust (Phakopsora pachyrhizi), anthracnose (Colletotrichum truncatum), and target spot (Corynespora cassicola) in soybeans. However, recurrent applications of SDHI group fungicides have intensified the selection of these less sensitive fungi to molecules (Godoy 2019; Mello 2019; Mello et al. 2021). For Cercospora spp., there is limited information on the use of SDHI in controlling PSS and CLB in vitro (EC₅₀). In a study conducted by Silva (2022), isolates of C. cf. flagellaris showed EC₅₀ values ranging from 43.12 to 100 mg.L^− 1, classified as moderately sensitive/insensitive, indicating low sensitivity to SDHI fungicides (unpublished data). This suggests the need for more research on the efficiency of this chemical group for Cercospora spp.

The QoI fungicide AZB demonstrated that all evaluated Cercospora species had EC₅₀ values greater than 100 mg.L^− 1. Mello et al. (2021) reported that applications of this fungicide in Brazil are usually more focused on controlling soybean Asian rust (Phakopsora phachyrhizi), and a reduction in sensitivity of populations of this pathogen has been observed. However, selection pressure affects all fungi affecting soybean cultivation, even those causing minimal damage (Mello et al. 2021), or occurring to a lesser extent in the field, such as PSS and CBL. To understand the complexity of reduced sensitivity of fungi to fungicides, as reported by Mello et al. (2021), they used fungicides from the QoI chemical groups (azoxystrobin, picoxystrobin, and pyraclostrobin) and reported changes in sensitivity and resistance to Cercospora spp. isolates involving the G143A mutation in Brazil during the 2015/2016 season.

The IDM and SBI group fungicides used in this study showed greater fungitoxicity and higher sensitivity of Cercospora species, although there is still limited information on DMI and SBI for Cercospora spp. This highlights the need to monitor fungal populations. Price (2013) observed changes in the sensitivity of C. kikuchii to DMI, identifying lower sensitivity to the fungicides flutriafol and propiconazole, but did not report mutational resistance of the tested isolates. Mello et al. (2021) suggest that changes in sensitivity of Cercospora spp. and loss of fungicide efficiency have been occurring since the 2008 season in Brazil. This is concerning, as studies confirm the possibility of cross-resistance, where fungi resistant to a particular fungicide are also resistant to others with the same mechanism of action. Regarding the resistance mechanism of Cercospora species to QoI fungicides, this study highlights insensitivity of these fungi, and the presence of the G143A mutation identified in 86% of isolates. As pointed out by FRAC (2024b), there are three point mutations, namely amino acid substitutions, identified in the cytb gene associated with QoI resistance in phytopathogenic fungi: G143A, F129L, and G137R. These mutations differ, with F129L and G137R mutations showing partial resistance to QoIs, while the G143A mutation exhibits complete resistance. These fungicides interfere with the fungal mitochondrial respiration process, affecting spore germination, and are classified as highly susceptible to resistance development (FRAC 2024b). Mello et al. (2020) identified the G143A mutation in 97% of Cercospora spp. isolates, resistant to at least two QoI fungicides. In the United States, Price et al. (2015) reported a prevalence of resistance of 89% among C. kikuchii isolates to QoI fungicides. In Argentina, Sautua et al. 2020 also reported that 82% of Cercospora isolates were resistant to QoIs, exposed to more than one fungicide from the same chemical group. This study highlights the need to adopt a comprehensive strategy for controlling PSS and CLB in soybeans. This involves identifying Cercospora species, monitoring fungicide efficiency to identify variability in populations, and anticipate possible changes in fungicide sensitivity, as well as implementing appropriate strategies to mitigate the impact on managing these diseases. Additionally, this study provides relevant information on the variable susceptibility of C. cf. flagellaris, C. dicondrae, C. helianthicola, C. lagenariae strain, C. beticola, and C. canescens species to SDHI, QoI, DMI, and SBI fungicides, emphasizing the importance of a well-informed and cautious approach to fungicide use to control PSS and CLB, diseases that are becoming more prevalent in soybean cultivation areas in Brazil.

Compliance with ethical standards

The authors declare that this manuscript has not been published elsewhere. All authors read and approved the final version of this manuscript. The authors declare that the present work was developed without any potential conflict of interest, with no human or animal participants.

Conflict of interest

The authors declare that they have no conflict of interest.

Data availability

The authors declare that the data supporting this study are available in the article, and if any raw data files are needed in other formats, they will be available upon reasonable request to the corresponding author.

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Sensitivity of Cercospora spp. to SDHI, QoI, DMI and SBI fungicides and resistance to QoI fungicides in Brazil

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