High-efficiency control of gray mold by the novel SDHI fungicide

Article pubs.acs.org/JAFC

Cite This: J. Agric. Food Chem. 2018, 66, 6692−6698

High-Efficiency Control of Gray Mold by the Novel SDHI Fungicide Benzovindiflupyr Combined with a Reasonable Application Approach of Dipping Flower Leiming He,†,‡ Kaidi Cui,†,‡ Yufei Song,†,‡ Wei Mu,†,‡ and Feng Liu*,†,‡ †

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Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, 61 Daizong Street, Tai’an, Shandong 271018, People’s Republic of China ‡ College of Plant Protection, Shandong Agricultural University, Tai’an, Shandong 271018, People’s Republic of China S Supporting Information *

ABSTRACT: In this study, a novel succinate dehydrogenase inhibitor (SDHI) fungicide benzovindiflupyr was found to have strong inhibitory activity against gray mold caused by Botrytis cinerea. The sensitivity of B. cinerea to benzovindiflupyr was determined by testing 103 pathogen isolates with mean values of 2.15 ± 0.19 mg L−1 and 0.89 ± 0.14 mg L−1 for mycelial growth and spore germination inhibition, respectively. Furthermore, benzovindiflupyr had excellent long-lasting protective activity. Unfortunately, there were positive correlations between benzovindiflupyr and boscalid (r = 0.3, P = 0.04) and between benzovindiflupyr and isopyrazam (r = 0.31, P = 0.04). In the field, cucumber flowers are susceptible to infection by B. cinerea. Benzovindiflupyr applied at 20 mg L−1 by dipping flowers could successfully control cucumber gray mold, with the benzovindiflupyr dose of dipping flower application less than 1% of that of spraying application. Benzovindiflupyr combined with dipping flower application showed significant control of gray mold. KEYWORDS: benzovindiflupyr, gray mold, dipping flower, spraying, cucumber

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isolates.15 SDHIs with new chemical structures and high activity against phytopathogenic fungi have been developed.16−20 Benzovindiflupyr is one of the representatives, and it has been reported that benzovindiflupyr has strong activity against various diseases.21,22 However, no detailed information was reported on the activity of benzovindiflupyr on B. cinerea. Therefore, more valuable information needs to be provided to promote the registration of benzovindiflupyr as an effective control against gray mold. Briefly, the objectives of this study were to (i) measure the sensitivity of B. cinerea isolates to benzovindiflupyr in China, based on mycelial growth and spore germination inhibition assays; (ii) evaluate the correlation of B. cinerea sensitivity to benzovindiflupyr and other commonly used SDHIs for gray mold control; (iii) test the systemic translocation of benzovindiflupyr in cucumber seedlings for controlling cucumber gray mold; (iv) investigate the protective and curative activities of benzovindiflupyr for controlling B. cinerea on detached cucumber leaves; and (v) explore a reasonable approach for application of benzovindiflupyr against cucumber gray mold in the field.

INTRODUCTION Gray mold, caused by Botrytis cinerea Pers.:Fr. (teleomorph Botryotinia f uckeliania), is considered the second most common disease in the world, infecting more than 200 crop hosts such as cucumber, tomato, strawberry, pepper, and kidney bean.1,2 Flowers, leaves, and stems of these crops are susceptible to B. cinerea infection, while flowers are particularly prone to infection, providing an entrance for B. cinerea infection to expand to fruits.3,4 Furthermore, B. cinerea can cause significant economic losses during preharvest or postharvest transport to distant markets.5 Over the past several decades, due to a lack of appropriate cultivars, gray mold control has depended mostly on the application of many fungicide categories, including N-phenylcarbamate, benzimidazoles, anilinopyrimidines, dicarboximides, hydroxyanilides, and succinate dehydrogenase inhibitors (SDHIs).6,7 It is known that B. cinerea is considered to be a classical “high-risk” pathogen due to its short life cycle, prolific reproduction, and high genetic variability.8 The repeated use of fungicides against B. cinerea has led to serious resistance in China and worldwide,9−12 meaning the activities of the above fungicides no longer meet the need for control. Therefore, seeking alternative fungicides with higher activities will play a crucial role in resolution of the current serious resistance phenomenon and, subsequently, effective management of B. cinerea. SDHI fungicides inhibit the activities of complex II enzymes, resulting in cell energy cycle termination, thereby effectively controlling many phytopathogenic fungi.13,14 Recently, boscalid was introduced into the market to control B. cinerea, but its activity has begun to erode due to the emergence of resistant © 2018 American Chemical Society

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MATERIALS AND METHODS

Fungal Isolates and Fungicides. During 2017 and 2018, symptomatic fruits, leaves, and stems with characteristics of B. cinerea infection were collected from nine geographic districts in Shandong

Received: Revised: Accepted: Published: 6692

April 14, 2018 May 31, 2018 June 11, 2018 June 11, 2018 DOI: 10.1021/acs.jafc.8b01936 J. Agric. Food Chem. 2018, 66, 6692−6698

Article

Journal of Agricultural and Food Chemistry

Figure 1. Systemic translocation of benzovindiflupyr in cucumber seedlings. (a) Application diagram; (b) efficacy of benzovindiflupyr for acropetal and basipetal movements. Different letters indicate significant differences at the P < 0.05 level by Fisher’s least significant difference (LSD) test. CK, water control; B-200, benzovindiflupyr at 200 mg L−1. iprodione concentration was 500 mg L−1. The detailed procedures and disease efficacy can be found in the Supporting Information. Systemic Translocation of Benzovindiflupyr in Cucumber Seedlings. Systemic translocation of benzovindiflupyr was measured on cucumber seedlings at the five-leaf stage (Figure 1a), as described previously.25 The tested concentration of benzovindiflupyr was 200 mg L−1. The detailed procedures are included in the Supporting Information. Greenhouse Experiments. Greenhouse experiments were conducted on cucumber cultivar Xintai Mici in November 2017. The cucumber greenhouse was situated in the village of Simahe (36.21°N, 117.58°E), Laiwu City, Shandong Province, and B. cinerea infection was prevalent in this greenhouse. Before application of fungicides, this study investigated the incidence of B. cinerea in different organs of cucumber in 30 plots, with 10 plants randomly selected in each plot. The survey showed that the infection frequencies of B. cinerea in cucumber fruits, leaves, and stems were 61.0%, 26.33%, and 3.0%, respectively. In view of the above phenomenon, two application methods (i.e., spraying and dipping flower) were applied simultaneously in the same greenhouse to determine the efficacy of benzovindiflupyr against cucumber gray mold. The areas of these two application methods were separated by a thick plastic film, and the temperature and humidity of both environments were recorded every hour by a temperature and humidity recorder (Shanghai Fotel Precision Instrument Co., Ltd., China). Spray application treatments were as follows: (1−3) benzovindiflupyr at 100, 200, and 300 mg L−1, respectively; (4) control fungicide iprodione at 500 mg L−1; and (5) water control. Five treatment groups were arranged in a randomized complete block design with three replications, and the size of each plot was 15 m2 (5 m × 3 m) containing 60 plants. Spray treatments were applied twice at 7-day intervals. Before spray application, 40 bloom-period fruits without disease symptoms and 100 leaves with or without disease symptoms were randomly selected and marked with a red string in each plot. The disease index of marked leaves was recorded before fungicide application and 7 days after last application. The disease index and efficacy on leaves were calculated according to the description of Song et al.26 The disease index of each fruit was recorded using a 0 to 9 rating scale. The detailed grading method and the calculation of control efficacy on fruits are both included in the Supporting Information. Dipping flower application was performed according to a previously described method.26 Briefly, 40 bloom-period fruits without disease symptoms were selected and dipped in treatment solution for 3 s and the treated fruits were marked with a red string. Dipping flower treatments were as follows: (1−3) benzovindiflupyr at 20, 40, and 80 mg L−1, respectively; (4) control fungicide iprodione at

Province, China, including Tai’an (n = 15), Jinan (n = 8), Weifang (n = 12), Liaocheng (n = 13), Dezhou (n = 13), Laiwu (n = 12), Linyi (n = 12), Zaozhuang (n = 6), and Jining (n = 12). A total of 103 isolates from several species were obtained according to the methods of Fernández-Ortuño et al.,23 including samples from cucumber (n = 29), tomato (n = 27), strawberry (n = 21), pepper (n = 12), and kidney bean (n = 14). These strains were stored at 4 °C. Technical-grade benzovindiflupyr (97% a.i.; Syngenta (China) Investment Co., Ltd.), boscalid (96% a.i.; Shandong Weifang Runfeng Chemical Co., Ltd.), fluopyram (96% a.i.; Bayer Stock company), and isopyrazam (92% a.i.; Syngenta Switzerland Crop Protection Co., Ltd.) were dissolved in methanol to prepare stock solutions, which were then stored at 4 °C in the dark until sensitivity assays were completed in vitro. Formulated benzovindiflupyr (150 g L−1 EC; Syngenta (China) Investment Co., Ltd.) and iprodione (500 g L−1 SC; Jiangsu Hui Feng Agrochemical Co., Ltd.) were used in greenhouse experiments. Measurement of Sensitivities to Benzovindiflupyr. A total of 103 B. cinerea isolates were used to measure sensitivities to benzovindiflupyr based on measurements of mycelial growth and spore germination inhibition according to the methods of Song et al.1 The mycelial growth and spore germination inhibition assays were performed on potato dextrose agar (PDA; 200 g of potato, 20 g of dextrose, and 20 g of agar per liter of distilled water) and yeast peptone acetate medium (YBA; 10 g of yeast extract, 10 g of Bacto peptone, 20 g of sodium acetate, and 15 g of agar per liter of distilled water), respectively. The final concentrations of benzovindiflupyr were 0, 0.01, 0.05, 0.1, 0.5, 1, 5, 10, and 50 mg L−1 and 0, 0.01, 0.05, 0.1, 0.5, 1, 5, and 10 mg L−1 for the mycelial growth and spore germination inhibition assays, respectively. Furthermore, sporeinhibited morphology was observed by a digital microscope (VHX2000 series; Keyence (China) Co., Ltd.). Correlation of B. cinerea Sensitivities to Benzovindiflupyr and Three Other Widely Used SDHIs. Forty-three isolates of B. cinerea selected from the total of 103 isolates showed several levels of sensitivity to three SDHI fungicides (i.e., boscalid, fluopyram, and isopyrazam). The correlations of 43 B. cinerea isolate sensitivities to benzovindiflupyr and three SDHI fungicides were determined by measuring mycelial growth on PDA medium. The EC50 value (i.e., the fungicide concentration resulting in a 50% inhibition compared with that of the control) for each isolate was within the range of the concentrations of four fungicides in the sensitivity assays. Three replicates were used for each concentration and isolate. Protective and Curative Activities of Benzovindiflupyr. Protective and curative activities of benzovindiflupyr against B. cinerea were performed on true leaves of cucumbers based on a previously described method.24 The tested concentrations of benzovindiflupyr were 10, 50, 100, 150, and 200 mg L−1, and control fungicide 6693

DOI: 10.1021/acs.jafc.8b01936 J. Agric. Food Chem. 2018, 66, 6692−6698

Article


Figure 2. Frequency distributions of the EC50 values of 103 B. cinerea isolates to benzovindiflupyr for (a) mycelial growth inhibition and (b) spore germination. The EC50 values show fungicide concentrations resulting in 50% inhibition compared to that of the control.

Figure 3. Effect of benzovindiflupyr on the morphology of B. cinerea (a) colony and (b) spore. CK, control; B-0.1, -0.5, -1, -5, -10, and -50, benzovindiflupyr at 0.1, 0.5, 1, 5, 10, and 50 mg L−1, respectively. 200 mg L−1; and (5) water control. Five treatment groups were arranged in a randomized complete block design with three replications. The selected bloom-period fruits were dipped only once for each treatment. Fourteen days after treatments, the disease index and efficacy on fruits were calculated in the same way as that for the spray application treatments. Furthermore, the infection frequencies of B. cinerea in cucumber fruits, leaves, and stems in the areas of both application methods were recorded initially and 14 days after first application.

Data Analysis. The EC50 values were calculated by completing regressions of the percent relative growths against the log10 values of the fungicide concentrations. The sensitivity to benzovindiflupyr was plotted against the sensitivity to boscalid, fluopyram, and isopyrazam. The EC50 values were transformed to log10 values, and Pearson correlation coefficients (r) were carried out to evaluate the correlation of B. cinerea sensitivities to benzovindiflupyr and three other SDHIs. To determine whether there were statistically significant differences among treatments, variance analyses (ANOVA) were carried out 6694


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Figure 4. Pearson correlation coefficients of sensitivities of 43 B. cinerea isolates between benzovindiflupyr and (a) boscalid, (b) isopyrazam, or (c) fluopyram.

Figure 5. Protective (a) and curative (b) activities of benzovindiflupyr and iprodione against B. cinerea on detached cucumber leaves. Different letters indicate significant differences at the P < 0.05 level by Fisher’s LSD test. I-500, iprodione at 500 mg L−1; B-10, -50, -100, -150, and -200, benzovindiflupyr at 10, 50, 100, 150, and 200 mg L−1, respectively.

observed between benzovindiflupyr and fluopyram (r = 0.09, P = 0.57) (Figure 4). Protective and Curative Activities of Benzovindiflupyr. With concentration increase, the protective and curative activities of benzovindiflupyr against B. cinerea were significantly enhanced (Figure 5). However, compared with the curative activity, the protective activity of benzovindiflupyr was better at the same application time and dosage, with an efficacy of more than 80% at 24 h when used at concentrations of 100 to 200 mg L−1. Meanwhile, benzovindiflupyr at concentrations of 100 to 200 mg L−1 also provided satisfactory results, with efficacy ranging from 57.94 to 88.07% when inoculations were conducted at 48 and 96 h after application, respectively (Figure 5a). For curative efficacy, benzovindiflupyr at 200 mg L−1 provided good results, with efficacy ranging from 65.77% to 88.09% at all three preinoculation application times (24, 48, and 96 h) (Figure 5b). Furthermore, iprodione at 500 mg L−1 could also provide good efficacy, ranging from 52.27 to 81.51% and from 49.75 to 72.17% for the protective and curative activities, respectively, at all three application times. Interestingly, the protection and curative activities of benzovindiflupyr at 100 mg L−1 was comparable to that of iprodione at 500 mg L−1 at the same application time. Systemic Translocation of Benzovindiflupyr in Cucumber Seedlings. The efficacy of benzovindiflupyr at 200 mg L−1 was 44.24 and 36.77% for the acropetal and basipetal movements, respectively (Figure 1b). It seemed that benzovindiflupyr exhibited unsatisfactory systemic translocation. Greenhouse Experiments. After spraying application, the control efficacy of benzovindiflupyr at 100, 200, and 300 mg

using Fisher’s LSD test (SPSS v. 13.0 for Windows) (P < 0.05). The efficacy of fungicides on B. cinerea were arcsine-transformed prior to analysis.

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RESULTS Measurement of Sensitivity to Benzovindiflupyr. In total, 103 single-spored B. cinerea isolates were used to test the sensitivity to benzovindiflupyr. The EC50 values ranged from 0.01 to 9.49 mg L−1 with a mean value of 2.15 ± 0.19 mg L−1 for mycelial growth to 0.01 to 6.49 mg L−1 with a mean value of 0.89 ± 0.14 mg L−1 for inhibition of spore germination (Figure 2). The mean EC50 values of B. cinerea isolates obtained from Laiwu were the highest among the nine regions in the mycelial growth and spore germination inhibition assays (Table S1). Furthermore, among the five crops in both assays, the mean EC50 values for B. cinerea isolates obtained from cucumber were the highest (Table S2). Effect of Benzovindiflupyr on a B. cinerea Colony and Spores. Benzovindiflupyr had a strong inhibition on both mycelial growth and spore germination (Figure 3). It was clear that the concentrations tested could completely inhibit the activities of mycelia (50 mg L−1) and spores (10 mg L−1). Except for the inhibition of colony diameter, benzovindiflupyr weakened colony thickness (Figure 3a). In addition, benzovindiflupyr obviously inhibited the elongation and bifurcation of the germ tube (Figure 3b). Correlation of B. cinerea Sensitivities to Benzovindiflupyr and Three Other SDHIs. Positive correlations existed between benzovindiflupyr and both boscalid (r = 0.3, P = 0.04) and isopyrazam (r = 0.31, P = 0.04). No correlation was 6695


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Figure 6. Efficacy of benzovindiflupyr treatment by spraying application for cucumber gray mold. (a) Disease frequencies of B. cinerea infecting cucumber fruits, leaves, and stems before and after spraying application, (b) efficacy of spraying application on cucumber leaves, and (c) efficacy of spraying application on cucumber fruits. Different letters indicate significant differences at the P < 0.05 level by Fisher’s LSD test.

Figure 7. Efficacy of benzovindiflupyr treatment by dipping flower application for cucumber gray mold. (a) Frequencies of B. cinerea infecting cucumber fruits, leaves, and stems before and after dipping flower application, and (b) efficacy of dipping flower application on cucumber fruits. Different letters indicate significant differences at the P < 0.05 level by Fisher’s LSD test. ND = no disease.

L−1 on cucumber leaves was 73.51, 81.87, and 88.55%, respectively, which were significantly higher than that of iprodione at 500 mg L−1 (52.8%) (Figure 6b). However, the efficacy of benzovindiflupyr at 100, 200, and 300 mg L−1 on fruits were only 38.75, 64.54, and 76.19%, respectively, which were not significantly different from that of the value for the control fungicide iprodione at 500 mg L−1 (44.13%) (Figure 6c). In addition, the infection frequency of B. cinerea in cucumber fruits and leaves after spray application was reduced by 7.43 and 12.67%, respectively, but increased by 2.67% in stems (Figure 6a). An interesting result is that the lowest concentration of benzovindiflupyr (20 mg L−1) applied by dipping flower application achieved an efficacy of 93.7%, which was much higher than that of iprodione at 200 mg L−1 (59.8%) (Figure 7b). The infection frequency in cucumber fruits, leaves, and stems after dipping flower application was reduced by 43.33, 7.34, and 1.33%, respectively (Figure 7a). There was no significant difference in the temperature of the two application areas (Figure S1). However, 2 days after spray application, the ambient humidity in the spray treatment was significantly higher than that in the dipping treatment, but there was subsequently no difference in ambient humidity between the two application areas due to continuous ventilation of the greenhouse. Compared with the dipping flower application, ambient humidity of the sprayed area increased by 3.67% after two applications.

tion, and germ tube elongation of B. cinerea and had excellent long-lasting protective activity. However, this study also found some isolates with decreased sensitivity to benzovindiflupyr, which may be due to the positive correlations between benzovindiflupyr and boscalid or isopyrazam. The resistance risks of SDHI fungicides were assessed at moderate to high levels by the Fungicide Resistance Action Committee (FRAC) due to their single targets of action. Cases of resistance to boscalid and isopyrazam in B. cinerea that correlate with several mutations in the succinate dehydrogenase complex (complex II) have been reported around the world.28,29 It suggested that there is a real danger that resistance to benzovindiflupyr may be developed by strains of B. cinerea from several cultivars in China unless some control is exerted on the way benzovindiflupyr is used. In a variety of fruits and vegetables, including tomatoes, cucumbers, and strawberries, B. cinerea infection commonly begins on attached senescent flowers, and then lesions expand to fruits.30 In the field trial, this study found that the frequency of gray mold infecting cucumber fruits exceeded 60%, significantly higher than 26.33 and 3.0% for leaves and stems, respectively. Thus, the control of B. cinerea on flowers is very important. However, spray application against cucumber gray mold was obviously not a wise choice, given that the efficacy of benzovindiflupyr at 200 mg L−1 was 64.54% on fruits and 81.87% on leaves. The reason for poor efficacy in cucumber fruits may be that leaves block the application onto flowers that are small in size, resulting in only a fraction of the fungicide on the flowers. Meanwhile, poor translocation of benzovindiflupyr in cucumber and increased ambient humidity in the greenhouse after spray application may also be responsible for failure of disease control on the fruits. Control

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DISCUSSION Consistent with the reported characteristics of other SDHI fungicides,1,6,27 the new SDHI fungicide benzovindiflupyr had strong inhibitory activity on mycelial growth, spore germina6696



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failure will inevitably increase both dosage and number of fungicides applied, resulting in resistance development.31,32 The dipping flower application method adopted in this study gave a surprising result that benzovindiflupyr, at concentrations as low as 20 mg L−1, could successfully control B. cinerea on cucumber fruits, with efficacy of up to 90%. Moreover, the dipping flower application reduced the frequency of B. cinerea infections attacking leaves and stems. This phenomenon may be explained by the fact that the dipping flower application method could effectively control gray mold on fruits to decrease the pathogen population in the environment, thus reducing the chance of B. cinerea infection of leaves and stems. Furthermore, the dipping flower method is a targeted application practice. This study found that the dosage amount of benzovindiflupyr applied by the dipping flower application method was less than 1% than that of spray applications, thereby reducing a broad and potent selective force that stimulates resistance development in B. cinerea.33 Meanwhile, each cucumber bloom-period fruit was only dipped once, compared to two or three spray applications. Therefore, this study suggests that the dipping flower application method may be an effective way to solve the shortcomings of the spray application method and delay the development of resistance to benzovindiflupyr. In addition to the use in vegetable varieties, the dipping flower method is also very valuable to high added value cultivars, such as ornamental flowers. In conclusion, benzovindiflupyr had strong inhibitory activity against B. cinerea and can be registered in China to control gray mold. Considering that there is no correlation between benzovindiflupyr and fluopyram, it can be used alternatively or in combination with fluopyram to control gray mold but is not suitable for combining with boscalid or isopyrazam. Furthermore, benzovindiflupyr combined with the reasonable application approach of the dipping flower method can effectively exert its action and delay the development of resistance.

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REFERENCES

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.8b01936.

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Article

Pydiflumetofen sensitivities of Botrytis cinerea isolates collected from nine geographic districts; pydiflumetofen sensitivities of Botrytis cinerea isolates collected from five crops; environmental temperatures and humidities in plots treated by flower dip and spray methods; and materials and methods (PDF)

AUTHOR INFORMATION

Corresponding Author

*Phone/Fax: +86 0538 8242611. E-mail: fl[email protected]. ORCID

Wei Mu: 0000-0002-9836-478X Feng Liu: 0000-0002-7950-6172 Funding

This work was supported by grants from the Provincial Key Research and Development Program of Shandong Province (2017CXGC0207). Notes

The authors declare no competing financial interest. 6697


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High-efficiency control of gray mold by the novel SDHI fungicide

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