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Revista mexicana de fitopatología

versión On-line ISSN 2007-8080versión impresa ISSN 0185-3309

Rev. mex. fitopatol vol.40 no.2 Texcoco may. 2022  Epub 03-Oct-2022

https://doi.org/10.18781/r.mex.fit.2202-4 

Phytopathological notes

Potassium silicate as a fungicide enhancer against Botrytis cinerea in blackberry

Daniel Nieto-Angel1 

José Terrones-Salgado2  * 

Santo Ángel Ortega-Acosta3 

Candelario Ortega-Acosta1 

Daniel Téliz-Ortiz1 

Francisco Javier Sánchez-Ruiz4 

Moisés Roberto Vallejo-Pérez5 

Francisco Palemón-Alberto3 

Luis Daniel Ortega-Martínez6 

1 Programa de Fitosanidad-Fitopatología, Colegio de Postgraduados, Campus Montecillo, Km 36.5 Carretera México-Texcoco, Montecillo, Texcoco, Estado de México, CP 56230, México;

2 Centro de Innovación Tecnológica en Agricultura Protegida, Decanato de Ciencias Biológicas, Facultad de Agronomía, Universidad Popular Autónoma del Estado de Puebla, 21 sur No. 1103, CP. 72410, Puebla, Puebla, México;

3 Departamento de Agronomía, Facultad de Ciencias Agropecuarias y Ambientales de la Universidad Autónoma de Guerrero, Iguala de la Independencia, C.P. 40020, Guerrero, México;

4 Facultad de Ingeniería Ambiental; Universidad Popular Autónoma del Estado de Puebla, 21 sur No. 1103, CP. 72410, Puebla, Puebla, México;

5 CONACyT-Universidad Autónoma de San Luis Potosí. Álvaro Obregón No. 64, Colonia Centro, San Luis Potosí, San Luis Potosí, CP 78000, México;

6 Facultad de Biotecnología, Universidad Popular Autónoma del Estado de Puebla, 21 sur No. 1103, CP. 72410, Puebla, Puebla, México


Abstract.

Blackberry gray mold, induced by Botrytis cinerea, is a fruit disease that causes important economic losses. The present study evaluated nine fungicides belonging to different chemical groups, alone and in combination with potassium silicate, using the dose recommended on the label for the control of B. cinerea in the field. The incidence and severity of the disease were evaluated, as well as the degrees Brix, silicon concentration, and yield. The experiment was carried out twice. Incidence and severity percentages were converted to area under the disease progress curve (AUDPC). Combined with potassium silicate, the fungicide azoxystrobin significantly reduced incidence and severity, showing the lowest percentages in the last evaluation of these variables. In the first repetition, the incidence and severity values ​​were 4% (AUDPC = 1320) and 0.1% (AUDPC = 298.5), respectively. In the second, 3% (AUDPC = 1099) and 0.1% (AUDPC = 214.5) respectively. The concentration of soluble solids and fruit yield increased (12.4 and 13.6 t ha-1 in the first and second repetition, respectively). The results indicate that potassium silicate enhances the effect of fungicides under field conditions and can thus be considered a management alternative against the gray mold disease in blackberries.

Key words: Silicon; AUDPC; incidence; severity; fungicides

Resumen.

El moho gris de la zarzamora causado por Botrytis cinerea, es una enfermedad que afecta los frutos y causa pérdidas económicas importantes. En la presente investigación se evaluaron nueve fungicidas pertenecientes a diferentes grupos químicos, solos y en combinación con silicato de potasio utilizando la dosis recomendada en la etiqueta para el control de B. cinerea en campo. Se evaluó la incidencia y severidad de la enfermedad, además de grados Brix, concentración de silicio y rendimiento, el experimento se realizó dos veces. Los porcentajes de incidencia y severidad se transformaron a área bajo la curva del progreso de la enfermedad (ABCPE). El fungicida azoxystrobin combinado con silicato de potasio redujo la incidencia y severidad significativamente, presentando los menores porcentajes en la última evaluación de dichas variables. En la primera repetición, los valores de incidencia y severidad fueron de 4% (ABCPE= 1320) y 0.1% (ABCPE= 298.5), respectivamente, y en la segunda 3% (ABCPE=1099) y 0.1% (ABCPE=214.5), respectivamente. Por lo tanto, aumentó la concentración de solidos solubles y rendimiento (12.4 y 13.6 t ha-1 en la primera y segunda repetición, respectivamente). Con base en los resultados obtenidos, se determinó que el silicato de potasio potencializa el efecto de los fungicidas bajo condiciones de campo, por lo tanto, puede ser una alternativa de manejo contra el moho gris en zarzamora.

Palabras clave: Silicio; ABCPE; incidencia; severidad; fungicidas

Blackberry (Rubus sp.) is a fruit crop grown in various regions throughout the world. However, blackberry production has suffered severe losses caused by diseases. Gray mold, caused by Botrytis cinerea, is considered the most important pre- and post-harvest disease (Li et al., 2012) of blackberries in Mexico and has been commonly reported in different blackberry producing regions (Terrones et al., 2019).

The initial symptoms caused by B. cinerea in blackberries are soft, light-brown areas. The infected tissue later dries and mummifies. Abundant conidiophores and conidia develop at this stage, producing the appearance of gray mold (Carisse et al., 2015). The fungus causes quiescent infections in which the disease manifests after harvest (Calvo-Garrido et al., 2014). Therefore, disease management actions must begin before harvest (Fillinger and Walker, 2016; Kim et al., 2016). Chemical control is the main control method against this disease. The use of fungicides against gray mold represents 8% of the global fungicide market (Fillinger and Walker, 2016). In Mexico, the products authorized for use in the control of blackberry gray mold, in compliance with US and European Union regulations, are fenhexamid, captan, pyrimethanil, fludioxonil, boscalid, azoxystrobin, and iprodione (ANEBERRIES, 2021). These fungicides, which are applied at intervals of 7-14 days, increase production costs and can exert selection pressure on resistant populations (Fernández-Ortuño, 2014).

The need to minimize the use of fungicides has led to the search for control alternatives, including Silicon (Si), which modifies plant cell wall properties (Iwasaki et al., 2002). When reinforced with Si, this mechanical defense significantly reduces the damage caused by insects and pathogens, mitigating the intensity of various diseases (Rodríguez et al., 2015). This method has reduced the incidence and severity of gray mold in cucumber (Cucumis sativus) and strawberry (Fragaria spp.) (Lopes et al., 2014). Furthermore, the foliar application of Si prevents the penetration of phytopathogenic fungi by activating the natural defenses of plants, mainly the expression of resistance genes (Fauteux et al., 2005).

Several studies have focused on the mitigation of plant diseases using Si. However, to date there no formal study has focused on the use of potassium silicate in blackberry plants to control gray mold. The present study aimed to evaluate the control of this disease in the field using nine fungicides from different chemical groups, alone and in combination with potassium silicate to potentiate their effect against B. cinerea.

Nine fungicides from different chemical groups were evaluated in an experimental plot with blackberry plants cv. Tupi in the physiological maturity stage: fluazinam (SHOGUN 500®, Syngenta) at a dose of 1 L ha-1; fenhexamid (ELEVAT®, UPL) at 1.5 kg ha-1; thiophanate-methyl (CERCOBIN M®, Basf) at 1 kg ha-1; captan (CAPTAN 50 WP®, Adama) at 2.5 kg ha-1; pyrimethanil (SCALA 400 SC®, Bayer CropScience) at 2 L ha-1; cyprodinil + fludioxonil (SWITCH® 62.5 WG, Syngenta) at 1 kg ha-1; boscalid (CANTUS®, Basf) at 1 kg ha-1; azoxystrobin (IMPALA® 25 SC, Adama) at 0.75 L ha-1; iprodione (ROVRAL® 50 PH, FMC) at 1 kg ha-1; control solution (sterile distilled water). These treatments were applied alone and in combination with potassium silicate (SUPA SILICA®, Agrisolver) at 0.5 L ha-1. The plot where the study was carried out had a history of presence of gray mold. An isolate of Botrytis cinerea (GenBank access number MG838557) had been previously collected and morphologically and molecularly characterized (Terrones et al., 2019). The fungicides, alone and in combination with potassium silicate, were applied at intervals of 15 days, starting in October 2019 and the second repetition was carried out in June 2020 until the end of the harvest in both cases. A total of six applications were made on each repetition using a motorized sprinkler (MS072H, Maruyama®) with a hollow cone nozzle previously calibrated to deliver a volume of 800 L ha-1.

An evaluation was carried out prior to the applications of the treatments, and six evaluations were carried out afterward, five days after each application. The fungicide applications were made directly in the field at the time of harvest when gray mold symptoms were found with different percentages of incidence and severity. The percentage of incidence was calculated by counting the number of fruits with symptoms of the disease and/or signs of the pathogen among 100 fruits chosen at random for each plant evaluated per experimental unit (treatment). The severity of the disease was determined in the same fruits (n=100) using a diagrammatic scale adjusted by Horsfall and Barratt and generated with 2LOG (Osada-Velázquez and Mora-Aguilera, 1997), with the following classes 0=0; 1= 0.1-3.2-7.8; 2= ​​7.9-25.4-48; 3= 48.1-63.62-83, 4= 83.1-94.58-100. This scale was used to determine the ranges and midpoint of disease severity (Tovar-Soto et al., 2002). The percentages of incidence and severity were converted to area under the disease progress curve values (AUCPE) with the SAS program version 9.3.

Six harvests were carried out (every 15 days, respecting the safety interval for fungicides). The fruits were weighed on an analytical balance (OHAUS®, USA). The total yield was calculated by adding all the harvested fruits from 14 plants in each repetition and extrapolating the yield per hectare later. Total soluble solids (degrees Brix) were determined at each harvest in randomly selected fruits using a digital palette refractometer PR-101α (ATAGO, Japan). Twenty measurements were made for each repetition, including asymptomatic and symptomatic fruits. The silicon content in the foliage was also evaluated at the end of the experiment by collecting 20 g of foliage from blackberry plants and subjecting the material to wet digestion with perchloric and nitric acid (Alcantar and Sandoval, 1999). The samples obtained from the digestion were analyzed using plasma induction atomic emission spectroscopy (ICP-VARIAN 725-ES).

The experiment was a 10×2 factorial design with 20 treatments, four replications and 80 experimental units, each one consisting of a plot 7 meters long and 2 m wide with 14 blackberry plants distributed along one row. Two repetitions of the experiment were carried out. The first from October to January (2019-2020) and the second one from June to September (2020). The data were subjected to analysis of normality and homogeneity of variances, data independence, analysis of variance and comparison of means (LSD, p ≤ 0.05). All analyses were carried out using the SAS program version 9.3.

In the evaluation of incidence, an interaction between the factors was identified (G.L.= 9, F= 238.09, p<0.0001) in the first repetition of the experiment. In addition, there were significant differences (F= 540.5, p<0.0001) in the AUCPE. The treatment based on azoxystrobin + potassium silicate was significantly different from the rest of the treatments, presenting the lowest AUCPE value (1320), as well as the lowest incidence percentages (Table 1). Interactions between the factors were also identified (G.L = 9, F= 289.04, p<0.0001) in the second repetition, as well as significant differences (F= 376.27, p<0.0001) in the AUCPE. The results showed again that the combination of azoxystrobin + potassium silicate was significantly different from the rest of the treatments, presenting the lowest AUCPE value (1099) and the lowest percentages of incidence of the disease (Table 1; Figure 1).

Table 1 Effect of potassium silicate on the control of blackberry gray mold disease caused by Botrytis cinerea under field conditions during two evaluation cycles. 

Tratamiento Primera repetición (octubre de 2019 a enero de 2020) Segunda repetición (mayo a agosto de 2020)
% Incidencia % severidad ° Brix Conc. Silicio Rendimientox % Incidencia % severidad ° Brix Conc. Silicio Rendimientox
E7z ABCPEy E7z ABCPEy Sanas Enfer. E7z ABCPEy E7z ABCPEy Sanas Enfer.
Fluazinam 39 5070bw 2.2 942.9b 8.99jz 6.51jkl 21.11kl 6.74l 38 4770bz 1.9 834.5b 9.01i 6.53ghi 20.59k 6.66m
Fenhexamid 33 3968cd 1.6 669.5e 9.14i 7.08c 20.49l 7.97k 29 3593c 1.3 594.7e 9.14h 7.06d 21.67k 8.12l
Tiofanato-metil 25 3188gh 1 636.5e 9.17hi 7.07cd 21.15kl 9.43fgh 23 2940fg 1 575.2e 9.16gh 7.05d 21.80k 9.35i
Captan 31 4110c 1.4 951.7b 9.21fg 6.49kl 21.86jk 8.01k 27 3585c 1.3 853.9b 9.21fg 6.46i 23.14ij 8.02l
Pyirimetanil 28 3739e 1.8 925.2bc 9.19gh 6.59hi 21.76jk 8.55ij 25 3345de 1.3 822.8bc 9.22fg 6.60g 22.78j 8.65k
Fludioxonil 25 3608e 1.4 798.8d 9.20fgh 6.59hi 21.79jk 8.76i 22 3169e 1 811.3bc 9.20fgh 6.62fg 23.10ij 8.80j
Boscalid 21 3034h 0.7 517.4g 9.24ef 7.00d 22.91i 9.61ef 20 2629h 0.6 455.6gh 9.29de 7.02d 23.75i 9.91g
Azoxistrobin 29 2029j 2.4 370.3hi 9.86b 7.45a 22.26ij 11.30c 28 1905k 2.4 329.9ij 9.99b 7.50a 23.59ij 11.42d
Iprodiona 10 1811k 0.3 355.8i 9.84b 7.34b 23.08i 11.54c 9 1631l 0.3 315.5j 10.01b 7.33b 24.01i 11.91c
Fluazinam + Si 30 3908d 1.2 772.9d 9.13i 6.70g 25.81gh 8.35j 22 3398d 0.9 688.4d 9.19fgh 6.70f 28.02g 8.66k
Fenhexamid + Si 23 3178gh 0.8 533.4fg 9.24ef 6.91e 26.32g 9.48efg 15 2779gh 0.6 488.1fg 9.31cd 6.97d 28.39fg 9.85g
Tiofanato-metil + Si 20 2771i 0.6 601.1ef 9.27de 6.77f 26.57fg 10.26d 17 2419i 0.6 537.6ef 9.35c 6.83e 28.97f 10.68f
Captan + Si 23 3030h 1.2 846.7cd 9.30cd 6.64gh 27.35f 9.67ef 18 2625h 1 743.2cd 9.33cd 6.63fg 29.22f 9.84g
Pyirimetanil + Si 23 3281fg 1.4 835.3cd 9.24ef 6.55ijk 28.70e 9.30gh 19 2846fg 1.3 723.6d 9.33cd 6.63fg 30.86e 9.55h
Fludioxonil + Si 24 3364f 1.2 650.2e 9.23efg 6.46l 29.62d 9.16h 19 2963f 1.1 596.9e 9.30cde 6.48hi 31.94d 9.60h
Boscalid + Si 22 2640i 0.7 461.6gh 9.29cd 6.57ij 37.84c 10.27d 16 2228j 0.5 402.9hi 9.35cd 6.58hg 39.96c 10.96e
Azoxistrobin + Si 4 1320m 0.1 298.5i 10.33a 7.09c 50.79a 12.44a 3 1099n 0.1 214.5k 10.47a 7.17c 53.75a 13.62a
Iprodiona + Si 10 1646l 0.3 338.2i 10.36a 7.49a 41.44b 11.98b 6 1286m 0.2 297.6j 10.43a 7.55ª 43.30b 12.80b
Silicato de potasio 25 3041h 1.1 657.1e 9.32c 5.21m 25.03h 9.72e 20 2606h 1 587.6e 9.24ef 5.31j 26.22h 9.83g
Testigo 79 7436a 41.7 3841.4a 8.75k 5.10n 19.76m 3.06m 69 6555a 31.2 2889.3a 8.78j 4.60k 20.27l 3.27n

w Mean values followed by the same letters within the same column are statistically equal (*= p≤0.05) according to the least significant difference (LSD) test.Yield in t ha-1.y Area Under the Disease Progress Curve calculated with the seven assessments over time.z Percentage of last evaluation performed.

Figure 1 Incidence of gray mold induced by B. cinerea in blackberry fruits sprayed with 20 different treatments in the field. Data from the last evaluation (seventh) of the second repetition of the experiment. 

The evaluation of disease severity showed an interaction between the factors (G.L = 9, F= 434.05, p<0.0001), as well as significant differences (F= 502.96, p<0.0001) in the AUCPE during the first repetition of the experiment. The treatments based on iprodione, iprodione + potassium silicate and azoxystrobin + potassium silicate were significantly different from the rest of the treatments, with AUCPE values ​​of 355.8, 338.2 and 298.5, respectively. These treatments also presented the lowest percentages of disease severity (Table 1). In the second repetition, there were interactions between the factors (G.L = 9, F= 317.02, p<0.0001) as well as significant differences (F= 373.06, p<0.0001) in the AUCPE. The treatment of azoxystrobin + potassium silicate showed significantly different results from the rest of the treatments, with the lowest AUCPE value (214.5) and the lowest percentage of the severity of the disease (Table 1; Figure 2).

With the addition of potassium silicate, all fungicides under study promoted a reduction in the incidence and severity of the disease induced by B. cinerea, compared to the application of the fungicides alone. This was reflected in the AUDPC. These results could be because Si modifies the properties of plant cell walls (Iwasaki et al., 2002) by forming a hard outer layer (Bélanger et al., 2003) that significantly reduces the penetration of phytopathogenic fungi (Rodrigues et al., 2015). It has been reported that the foliar application of Si activates the natural defenses of plants, mainly those associated with gene expression (Fauteux et al., 2005). According to the general concepts of Jennings (2007) on fungal nutrition and mycelial growth, when Si adheres to the cell wall, the enzymes released from the hyphae cannot act efficiently to break down cellulose to glucose, affecting the nutrition of the fungus and mitigating the disease caused by it (Datnoff et al., 2011).

Figure 2 Severity of gray mold disease induced by B. cinerea in blackberry fruits sprayed with 20 different treatments in the field. Data from the last evaluation (seventh) of the second repetition of the experiment. 

The application of azoxystrobin reduced the percentages of incidence and severity in the first three evaluations (three applications). However, the fourth evaluation showed poorer results in the control of the disease, which suggests that the pathogen possibly developed resistance since strobilurins, as mentioned above, have a high risk of inducing resistance (Villani and Cox, 2014). This was not observed when azoxystrobin was combined with potassium silicate, possibly due to the modifications in the cell walls induced by Si and its ability to activate the plant’s natural defenses (Bélanger et al., 2003; Rodriguez et al., 2015).

During the first repetition of the experiment, the total soluble solids variable showed interactions between factors in diseased (G.L = 9, F= 42.92, p<0.0001) and healthy (G.L = 9, F= 97.95, p<0.0001) fruits. In addition, significant differences were observed between diseased (F= 611.47, p<0.0001) and healthy fruits (F= 711.52, p<0.0001). The plants treated with azoxystrobin + potassium silicate and iprodione + potassium silicate showed significantly different results from the rest of the treatments, presenting the highest concentration of soluble solids in diseased and healthy fruits (Table 1). Similarly, in the second repetition of the experiment there was an interaction between factors in diseased (G.L = 9, F= 58.42, p<0.0001) and healthy fruits (G.L = 9, F = 104.52, p<0.0001). Significant differences were observed in diseased (F = 347.31, p<0.0001) and healthy fruits (F = 414.06, p<0.0001). The plants treated with azoxystrobin + potassium silicate and iprodione + potassium silicate showed significantly different results from the rest of the treatments with respect to the highest concentration of soluble solids in diseased and healthy fruits (Table 1).

In the present study, the concentration of soluble solids was higher in healthy fruits compared to diseased ones, but the plants treated with azoxystrobin + potassium silicate and iprodione + potassium silicate showed more degrees Brix. Marodin et al. (2014) found that the application of Si improved the physicochemical quality of tomato fruits (Solanum lycopersicum) by increasing the content of soluble solids. Similarly, Jarosz (2012) found a higher amount of soluble solids in cucumbers sprayed with Si. The response of plants to Silicon includes changes in the concentration of different elements, biomass production (including yield), photosynthetic rate, transpiration rate and production of enzymatic and non-enzymatic antioxidants, as well as changes in other components of agronomic or commercial interest such as the content of soluble solids (Guntzer et al., 2012; Haynes et al., 2013).

Regarding the concentration of Silicon, interactions between factors were identified (G.L = 9, F= 324.27, p<0.0001) in the first repetition of the experiment. Significant differences in the values of this variable were also observed (F= 661.90, p<0.0001). The combination of azoxystrobin + potassium silicate was significantly different from the rest of the treatments, presenting the highest concentration of Silicon (50.79 ppm) (Table 1). A similar result was observed in the second repetition, with interactions between factors (G.L = 9, F= 315.13, p<0.0001) and significant differences between treatments (F= 661.28, p<0.0001). The combination of azoxystrobin + potassium silicate was significantly different from the rest of the treatments, presenting the highest silicon concentration (53.75 ppm) (Table 1).

Regarding fruit yield, an interaction between the factors was identified (G.L = 9, F= 176.61, p<0.0001) during the first repetition, as well as significant differences between treatments (F= 429.24, p<0.0001). The plants treated with azoxystrobin + potassium silicate showed significantly different results from the rest of the treatments. This treatment was associated with the highest yield (12.4 t ha-1), followed by the treatments based on iprodione + potassium silicate and iprodione, with yields of 11.9 and 11.5 t ha-1, respectively (Table 1). In the second repetition there was also an interaction between factors (G.L = 9, F= 195.54, p<0.0001) as well as significant differences between treatments (F= 476.31.12, p<0.0001). The treatment of azoxystrobin + potassium silicate was significantly different from the rest of the treatments, presenting the highest yield (13.6 t ha-1), even higher than the result of the first repetition (Table 1).

The plants treated with azoxystrobin + potassium silicate presented the highest yield per hectare. This is pobably because Si alone, as a nutritive element, performs some metabolic and structural functions that have beneficial effects on the physiology of plants. Thus, the accumulation of Si results in an increase in productivity in different plant species. Marodine et al. (2014) evaluated the effect of three silicon sources on tomato yield and found that the yield increased as the dose of silicon increased. Lu et al. (2016) evaluated three different sources of Silicon on the agronomic variables of tomato and determined that the application of nanosilica was associated with increased height and dry and fresh weight of plant organs, and consequently with increased yield. Numerous studies suggest that Silicon increases the yield of crops such as strawberry (Ouellette et al., 2017), tomato (Lu et al., 2016; Marodin et al., 2014; Toresano et al., 2012), cucumber (Abd- Alkarim et al., 2017), courgette (Cucurbita pepo) (Savvas et al., 2009), potato (Solanum tuberosum) (Pilon et al., 2013), wheat (Triticum durum) (Hanafy et al., 2008), and other grasses (Ahmad et al., 2017).

One of the most notable effects of Silicon on plants is the reduction of the incidence and severity of diseases caused by pathogens, which is reflected in different agronomic characteristics, including yield. Silicon applications can work as well as fungicides to suppress plant diseases, which makes this element a valuable addition to an integrated disease management strategy (Fillinger et al., 2016).

In general, the data obtained in the present study showed that blackberry plants treated with a combination of different fungicides + potassium silicate, especially azoxystrobin, had a lower incidence and severity of gray mold disease. This was reflected in the component variables of yield. The conclusion is that potassium silicate enhances the effect of fungicides in field conditions and is a viable alternative for integrated management programs of blackberry gray mold caused by Botrytis cinerea.

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Received: February 21, 2022; Accepted: April 17, 2022

*Corresponding author: jose.terrones@upaep.mx.

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