- Author: Surendra K. Dara
- Author: Dave Peck, Manzanita Berry Farms
Botrytis cinerea infection appears as wilted flowers and a layer of spores on ripe fruit. Photo by Surendra Dara
Botrytis fruit rot or gray mold caused by Botrytis cinerea is an important disease of strawberry and other crops damaging flowers and fruits. Pathogen survives in the plant debris and soil and can be present in the plant tissues before flowers form. Infection is common on developing or ripe fruits as brown lesions. Lesions typically appear under the calyxes but can be seen on other areas of the fruit. As the disease progresses, a layer of gray spores forms on the infected surface. Severe infection in flowers results in the failure of fruit development. Cool and moist conditions favor botrytis fruit rot development. Sprinkler irrigation, rains, or certain agricultural practices can contribute to the dispersal of fungal spores.
Although removal of infected plant material and debris can reduce the source of inoculum in the field, regular fungicide applications are typically necessary for managing botrytis fruit rot. Since fruiting occurs continuously for several months and fungicides are regularly applied, botrytis resistance to fungicides is not uncommon. Applying fungicides only when necessary, avoiding continuous use of fungicides from the same mode of action group (check FRAC mode of action groups), exploring the potential of biological fungicides to reduce the risk of resistance development are some of the strategies for effective botrytis fruit rot management. In addition to several synthetic fungicides, several biological fungicides continue to be introduced into the market offering various options for the growers. Earlier field studies evaluated the potential of various biological fungicides and strategies for using them with synthetic fungicides against botrytis and other fruit rots in strawberry (Dara, 2019; Dara, 2020). This study was conducted to evaluate some new and soon to be released fungicides in fall-planted strawberry to support the growers, ag input industry, and to promote sustainable disease management through biological and synthetic pesticides.
Methodology
This study was conducted at the Manzanita Berry Farms, Santa Maria in strawberry variety 3024 planted in October, 2020. While Captan and Switch were used as synthetic standards, a variety of biological fungicides of microbial, botanical, and animal sources were included at various rates and different combinations and rotations. Products and active ingredients evaluated in this study included Captan Gold 4L (captan) from Adama, Switch 62.5 WG (cyprodinil 37.5% + fludioxinil 25%) from Syngenta, NSTKI-14 (potassium carbonate 58.04% + thyme oil 1.75%) from NovoSource, A22613 [A] (botanical extract) from Syngenta, Regalia (giant knotweed extract 5%) from Marrone Bio Innovations, EXP14 (protein 15-20%) from Biotalys, Gargoil (cinnamon oil 15% + garlic oil 20%) and Dart (caprylic acid 41.7% + capric acid 28.3%) from Westbridge, Howler (Pseudomonas chlororaphis strain AFS009), Theia (Bacillus subtilis strain AFS032321), and Esendo (P. chlororaphis strain AFS009 44.5% + azoxystrobin 5.75%) from AgBiome, ProBlad Verde (Banda de Lupinus albus doce – BLAD, a polypeptide from sweet lupine) from Sym-Agro with Kiplant VS-04 (chitosan 2.3%) or Nu-Film-P spreader/sticker, AS-EXP Thyme (thyme oil) from AgroSpheres, and AgriCell FunThyme (thyme oil) provided by AgroSpheres.
Table 1. List of treatments color coded according to the kind of fungicide (light blue=synthetic fungicide; dark blue=synthetic+biological fungicide active ingredient; peach=synthetic and biological fungicides alternated; green=biological fungicides)
Excluding the untreated control, rest of the 24 treatments can be divided into synthetic fungicides, a fungicide with synthetic + biological active ingredients (a formulation with two application rates), synthetic fungicides alternated with biological fungicides, and various kinds of biological fungicides (Table 1). Treatments were applied at a 7-10 day interval between 22 April and 17 May, 2021. Berries for pre-treatment disease evaluation were harvested on 19 April, 2021. Each treatment had a 5.67'X15' plot replicated four times in a randomized complete block design. Strawberries were harvested 3 days before the first treatment and 3-4 days after each treatment for disease evaluation. On each sampling date, marketable-quality berries were harvested from random plants within each plot during a 30-sec period and incubated in paper bags at outdoor temperatures under shade. Number of berries with botrytis infection were counted on 3 and 5 days after harvest (DAH) and percent infection was calculated. This is a different protocol than previous years' studies where disease rating was made on a 0 to 4 scale. Treatments were applied with a backpack sprayer equipped with Teejet Conejet TXVK-6 nozzle using 90 gpa spray volume at 45 PSI. Water was sprayed in the untreated control plots. Dyne-Amic surfactant at 0.125% was used for treatments that contained Howler, Theia, Esendo, AgriCell FunThyme, AS-EXP Thyme, and EXP 14. Research authorization was obtained for some products and crop destruction was implemented for products that did not have California registration.
Percent infection data were arcsine-transformed before subjecting to the analysis of variance using Statistix software. Significant means were separated using the least significant difference test.
Results
Pre-treatment infection was very low and occurred only in some treatments with no statistical difference (P > 0.05). Infection levels increased for the rest of the study period. There was no statistically significant difference (P > 0.05) among treatments for disease levels 3 or 5 days after the first spray application. Differences were significant (P = 0.0131) in disease 5 DAH after the second spray application where 13 treatments from all categories had significantly lower infection than the untreated control. After the third spray application, infection levels were significantly lower in eight treatments in 3 DAH observations (P = 0.0395) and 10 treatments in 5 DAH observations (P = 0.0005) compared to untreated control. There were no statistical differences (P > 0.05) among treatments for observations after fourth spray application or for the average of four applications. However, there were numerical differences where infection levels were lower in several treatments than the untreated control plots.
In general, the efficacy of both synthetic and biological fungicides varied throughout the study period among the treatments. When the average for post-treatment observations was considered, infection was numerically lower in all treatments regardless of the fungicide category. Multiple biological fungicide treatments either alone or in rotation with synthetic fungicides appeared to be as effective as synthetic fungicides.
Conclusions
Botanical and microbial fungicides can be effective against either for using alone or in rotation with synthetic fungicides for suppressing botrytis fruit rot in strawberry. Additional studies can help optimize the application rates and use strategies for those fungicides that were not as effective as others. Sanitation practices and use of synthetic and biological fungicides help manage botrytis fruit rot.
Acknowledgements: Thanks to AgBiome, AgroSpheres, Biotalys, NovaSource, Sym-Agro, Syngenta, and Westbridge for funding and Chris Martinez for his technical assistance.
References
Dara, S. K. 2019. Five shades of gray mold control in strawberry: evaluating chemical, organic oil, botanical, bacterial, and fungal active ingredients. UCANR eJournal of Entomology and Biologicals. https://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=30729
Dara, S. K. 2020. Evaluating biological fungicides against botrytis and other fruit rots in strawberry. UCANR eJournal of Entomology and Biologicals. https://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=43633
- Author: Surendra K. Dara
Botrytis fruit rot or gray mold, caused by Botrytis cinerea, is common fruit disease in California strawberries (Koike et al. 2018). Botrytis cinereahas a wide host range infecting several commercially important crops including blueberry (Saito et al. 2016), grapes (Saito et al., 2019), and tomato (Breeze, 2019). Fungal infection can cause flower or fruit rot. Fruit can be infected directly or through a latent infection in the flowers. Moist and cool conditions favor fungal infections and increased sugar content in the ripening fruit can also contribute to the disease development. Initial symptoms of infection appear as brown lesions and a thick mat of gray conidia is characteristic symptom in the later stages of infection. As chemical fungicides are primarily used for gray mold control, fungicide resistance is a common problem around the world (Panebianco et al., 2015; Liu et al., 2016; Stockwell et al., 2018; Weber and Hahn, 2019). In strawberry, cultural control options such as removing diseased plant material or using cultivars with traits that can reduce gray mold infections may not be practical when the disease is widespread in the field or cultivar choice is made based on other factors. Non-chemical control options are necessary to help reduce the risk of chemical fungicide resistance, prolong the life of available chemical fungicides, achieve desired disease control, and to maintain environmental health. Although there are several botanical and microbial fungicides available for gray mold control, limited information is available on their efficacy in California strawberries. A study was conducted in the spring of 2019 to evaluate the efficacy of several chemical, botanical, and microbial fungicides in certain combinations and rotations to help identify effective options for an integrated disease management strategy.
Methodology
Strawberry cultivar San Andreas was planted late November, 2018 and the study was conducted in April and May, 2019. Each treatment had a 20' long strawberry plot with two rows of plants replicated in a randomized complete block design. Plots were maintained without any fungicidal applications until the study was initiated. Table 1 contains the list of treatments, application rates and dates of application, and Table 2 contains the type of fungicide used and their mode of action. Beauveria bassiana and Metarhizium anisopliae s.l. are California isolates of entomopathogenic fungi, isolated from an insect and a soil sample, respectively. These fungi are pathogenic to a variety of arthropods and some strains are formulated as biopesticides for arthropod control. However, earlier studies in California demonstrated that these fungi are also known to antagonize plant pathogens such as Fusarium oxysporum f.sp. vasinfectum Race 4 (Dara et al., 2016) and Macrophomina phaseolina (Dara et al., 2018) and reduce the disease severity. To further evaluate their efficacy against B. cinerea, these two fungi were also included in this study alternating with two chemical fungicides.
Treatments were applied with a CO2-pressurized backpack sprayer using 66.5 gpa spray volume. Five days before the first spray application and 3 days after each application, all ripe fruit were harvested from each plot and incubated at the room temperature in vented plastic containers. The level of gray mold on fruit from each plot was rated using a 0 to 4 scale (where 0=no disease, 1=1-25% fruit with fungal infection, 2=26-50% infection, 3=51-75%, and 4=76-100%) 3 and 5 days after each harvest (DAH). Due to the rains, fruit could not be harvested after the 3rd spray application for disease rating, but was harvested and discarded after the rains to avoid cross infection for the following week's harvest. Data were analyzed using analysis of variance using Statistix software and significant means were separated using Least Significant Difference separation test.
Results
Gray mold occurred at low to moderate levels during the study period. Along with B. cinerea, there were a few instances of minor fungal infections from Rhizopus spp. (Rhizopus fruit rot) and Mucor spp. (Mucor fruit rot). Pre-treatment disease ratings were statistically not significant (P = 0.6197 and 0.5741) 3 and 5 DAH. While the chemical standard treatment with the rotation of Captan, Merivon, Switch, and Pristine (treatment 2) appeared to result in the lowest disease rating throughout the observation period, treatments 3 and 5 after the 1st spray application, treatments 5 and 11 along with 3, 4 and 6 after the 2nd spray application, and treatments 3 and 5 along with 11 after the 4th spray application also had similar disease control at 3 DAH. When disease at 5 DAH was compared, the lowest rating was seen in treatment 2 after the 1st and 2nd spray applications, and treatments 2, 3, and 11 after the 4th application. Several other treatments also provided statistically similar control during these days.
When the average disease rating for the three post-treatment observation events was considered, treatment 2, 3, 5, and 11 had the lowest disease at both 3 and 5 DAH. Treatments 4 and 12 at 3 DAH also had a statistically similar level of disease control to treatment 2.
In general, most of the treatments provided moderate to high control compared to the disease in untreated control when the post-treatment averages were considered. Only treatment 7 and 13 had lower control at 3 DAH.
Discussion
This study compared a variety of registered and developmental products along with two entomopathogenic fungi in managing B. cinerea. Considering the fungicide resistance problem in B. cinerea in multiple crops, having multiple non-chemical control options is very important to achieve desirable control with integrated disease management strategies. Since the active ingredients in the botanical and bacterial fungicides used in this study are not public, discuss will be limited on their modes of action and efficacy at this point. Similarly, the active ingredient of WXF-17001 is also not known, however, an earlier study by Calvo-Garrido et al. (2014) demonstrated that a fatty acid-based natural product reduced B. cinereaconidial germination by 54% and disease severity in grapes by 96% compared to untreated control. The product used by Calvo-Garrido et al. (2014) is thought to be fungistatic and reduce the postharvest respiratory activity and ethylene production in fruits.
While chemical fungicides have a specific mode of action, biological and other products act in multiple manners either directly antagonizing the plant pathogen or by triggering the plant defenses. For example, amending the potting medium with biochar resulted in induced systemic resistance in tomato and reduced B. cinerea severity by 50% (Mehari et al., 2015). Luna et al. (2016) also showed that application of β-aminobutyric acid and jasmonic acid promoted seed germination and long-term resistance to B. cinerea in tomato. Burkholderia phytofirmans, beneficial endophytic bacterium, offered protection against B. cinerea in grapes by mobilizing carbon resources (callose deposition), triggering plant immune system (hydrogen peroxide production and priming of defense genese), and through antifungal activity (Miotto-Vilanova et al. 2016). Similarly, entomopathogenic fungi such as B. bassiana are also known to induce systemic resistance against plant pathogens (Griffin et al. 2006). Compared to other options evaluated in the study, entomopathogenic fungi have an advantage of controlling both arthropod pests and diseases, while also having plant growth promoting effect (Dara et al. 2017).
Rotating fungicides with different mode of actions reduces the risk of resistance development and using some combinations will also maintain control efficacy. This study provided the efficacy of multiple control options and their combinations and rotations for B. cinerea. This is also the first study demonstrating the efficacy of entomopathogenic fungi against B. cinerea in strawberry.
Acknowledgements: Thanks to Sipcam Agro and Westbridge for funding the study, technical assistance of Hamza Khairi for data collection, and the field staff at the Shafter Research Station for the crop maintenance.
References
Breeze, E. 2019. 97 Shades of gray: genetic interactions of the gray mold, Botrytis cinerea, with wild and domesticated tomato. The Plant Cell 31: 280-281. https://doi.org/10.1105/tpc.19.00030
Calvo-Garrido, C., A.A.G. Elmer, F. J. Parry, I. Viñas, J. Usall, R. Torres, R.H. Agnew, and N. Teixidó. 2014. Mode of action of a fatty acid-based natural product to control Botrytis cinerea in grapes. J. Appl. Microbiol. 116: 967-979. https://doi.org/10.1111/jam.12430
Dara, S. K., S. S. Dara, S.S.R. Dara, and T. Anderson. 2016. First report of three entomopathogenic fungi offering protection against the plant pathogen, Fusarium oxysporum f.sp. vasinfectum. UC ANR eJournal of Entomology and Biologicals https://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=22199
Dara, S. K., S.S.R. Dara, and S. S. Dara. 2017. Impact of entomopathogenic fungi on the growth, development, and health of cabbage growing under water stress. Amer. J. Plant Sci. 8: 1224-1233. https://doi.org/10.4236/ajps.2017.86081
Dara, S.S.R., S. S. Dara, and S. K. Dara. 2018. Preliminary report on the potential of Beauveria bassiana and Metarhizium anisopliae s.l. in antagonizing the charcoal rot causing fungus Macrophomina phaseolina in strawberry. UC ANR eJournal of Entomology and Biologicals https://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=28274
Griffin, M. R., B. H. Ownley, W. E. Klingeman, and R. M. Pereira. 2006. Evidence of induced systemic resistance with Beauveria bassiana against Xanthomonas in cotton. Phytopathol. 96.
Koike, S. T., G. T. Browne, T. R. Gordon, and M. P. Bolda. 2018. UC IPM pest management guidelines: strawberry (diseases). UC ANR Publication 3468. https://www2.ipm.ucanr.edu/agriculture/strawberry/Botrytis-Fruit-Rot/
Liu, S., Z. Che, and G. Chen. 2016. Multiple-fungicide resistance to carbendazim, diethofencardb, procymidone, and pyrimethanil in field isolates of Botrytis cinerea from tomato in Henan Province, China. Crop Protection 84: 56-61.
Luna, E., E. Beardon, S. Ravnskov, J. Scholes, and J. Ton. 2016. Optimizing chemically induced resistance in tomato against Botrytis cinerea. Plant Dis. 100: 704-710. https://doi.org/10.1094/PDIS-03-15-0347-RE
Mehari, Z. H., Y. Elad, D. Rav-David, E. R. Graber, and Y. M. Harel. 2015. Induced systemic resistance in tomato (Solanum lycopersicum) against Botrytis cinerea by biochar amendment involves jasmonic acid signaling. Plant and Soil 395: 31-44.
Miotto-Vilanova, L., C. Jacquard, B. Courteaux, L. Wortham, J. Michel, C. Clément, E. A. Barka, and L. Sanchez. 2016. Burkholderia phytofirmans PsJN confers grapevine resistance against Botrytis cinerea via a direct antimicrobial effect combined with a better resource mobilization. Front. Plant Sci. 7: 1236. https://doi.org/10.3389/fpls.2016.01236
Panebianco, A., I. Castello, G. Cirvilleri, G. Perrone, F. Epifani, M. Ferrarra, G. Polizzi, D. R. Walters, and A. Vitale. 2015. Detection of Botrytis cinerea field isolates with multiple fungicide resistance from table grape in Sicily. Crop Protection 77: 65-73.
Saito, S., T. J. Michailides, and C. L. Xiao. 2016. Fungicide resistance profiling in Botrytis cinerea populations from blueberry in California and Washington and their impact on control of gray mold. Plant Dis. 100: 2087-2093. https://doi.org/10.1094/PDIS-02-16-0229-RE
Saito, S., T. J. Michailides, and C. L. Xiao. 2019. Fungicide-resistant phenotypes in Botrytis cinerea populations and their impact on control of gray mold on stored table grapes in California. European J. Plant Pathol. 154: 203-213.
Stockwell, V. O., B. T> Shaffer, L. A. Jones, and J. W. Pscheidt. 2018. Fungicide resistance profiles of Botrytis cinerea isolated from berry crops in Oregon. Abstract for International Congress of Plant Pathology: Plant Health in A Global Economy; 2018 July 29-Aug 3; Boston, MA.
Weber, R.W.S. and M. Hahn. 2019. Grey mould disease of strawberry in northern Germany: causal agents, fungicide resistance and management strategies. Appl. Microbiol. Biotechnol. 103: 1589-1597.
This article originally published in the E-Journal of Entomology and Biologicals.
- Author: Surendra K. Dara
Botrytis fruit rot or gray mold, caused by Botrytis cinerea, is common fruit disease in California strawberries (Koike et al. 2018). Botrytis cinerea has a wide host range infecting several commercially important crops including blueberry (Saito et al. 2016), grapes (Saito et al., 2019), and tomato (Breeze, 2019). Fungal infection can cause flower or fruit rot. Fruit can be infected directly or through a latent infection in the flowers. Moist and cool conditions favor fungal infections and increased sugar content in the ripening fruit can also contribute to the disease development. Initial symptoms of infection appear as brown lesions and a thick mat of gray conidia is characteristic symptom in the later stages of infection. As chemical fungicides are primarily used for gray mold control, fungicide resistance is a common problem around the world (Panebianco et al., 2015; Liu et al., 2016; Stockwell et al., 2018; Weber and Hahn, 2019). In strawberry, cultural control options such as removing diseased plant material or using cultivars with traits that can reduce gray mold infections may not be practical when the disease is widespread in the field or cultivar choice is made based on other factors. Non-chemical control options are necessary to help reduce the risk of chemical fungicide resistance, prolong the life of available chemical fungicides, achieve desired disease control, and to maintain environmental health. Although there are several botanical and microbial fungicides available for gray mold control, limited information is available on their efficacy in California strawberries. A study was conducted in the spring of 2019 to evaluate the efficacy of several chemical, botanical, and microbial fungicides in certain combinations and rotations to help identify effective options for an integrated disease management strategy.
Methodology
Strawberry cultivar San Andreas was planted late November, 2018 and the study was conducted in April and May, 2019. Each treatment had a 20' long strawberry plot with two rows of plants replicated in a randomized complete block design. Plots were maintained without any fungicidal applications until the study was initiated. Table 1 contains the list of treatments, application rates and dates of application, and Table 2 contains the type of fungicide used and their mode of action. Beauveria bassiana and Metarhizium anisopliae s.l. are California isolates of entomopathogenic fungi, isolated from an insect and a soil sample, respectively. These fungi are pathogenic to a variety of arthropods and some strains are formulated as biopesticides for arthropod control. However, earlier studies in California demonstrated that these fungi are also known to antagonize plant pathogens such as Fusarium oxysporum f.sp. vasinfectum Race 4 (Dara et al., 2016) and Macrophomina phaseolina (Dara et al., 2018) and reduce the disease severity. To further evaluate their efficacy against B. cinerea, these two fungi were also included in this study alternating with two chemical fungicides.
Treatments were applied with a CO2-pressurized backpack sprayer using 66.5 gpa spray volume. Five days before the first spray application and 3 days after each application, all ripe fruit were harvested from each plot and incubated at the room temperature in vented plastic containers. The level of gray mold on fruit from each plot was rated using a 0 to 4 scale (where 0=no disease, 1=1-25% fruit with fungal infection, 2=26-50% infection, 3=51-75%, and 4=76-100%) 3 and 5 days after each harvest (DAH). Due to the rains, fruit could not be harvested after the 3rd spray application for disease rating, but was harvested and discarded after the rains to avoid cross infection for the following week's harvest. Data were analyzed using analysis of variance using Statistix software and significant means were separated using Least Significant Difference separation test.
Results
Gray mold occurred at low to moderate levels during the study period. Along with B. cinerea, there were a few instances of minor fungal infections from Rhizopus spp. (Rhizopus fruit rot) and Mucor spp. (Mucor fruit rot). Pre-treatment disease ratings were statistically not significant (P = 0.6197 and 0.5741) 3 and 5 DAH. While the chemical standard treatment with the rotation of Captan, Merivon, Switch, and Pristine (treatment 2) appeared to result in the lowest disease rating throughout the observation period, treatments 3 and 5 after the 1st spray application, treatments 5 and 11 along with 3, 4 and 6 after the 2nd spray application, and treatments 3 and 5 along with 11 after the 4th spray application also had similar disease control at 3 DAH. When disease at 5 DAH was compared, the lowest rating was seen in treatment 2 after the 1st and 2nd spray applications, and treatments 2, 3, and 11 after the 4th application. Several other treatments also provided statistically similar control during these days.
When the average disease rating for the three post-treatment observation events was considered, treatment 2, 3, 5, and 11 had the lowest disease at both 3 and 5 DAH. Treatments 4 and 12 at 3 DAH also had a statistically similar level of disease control to treatment 2.
In general, most of the treatments provided moderate to high control compared to the disease in untreated control when the post-treatment averages were considered. Only treatment 7 and 13 had lower control at 3 DAH.
Discussion
This study compared a variety of registered and developmental products along with two entomopathogenic fungi in managing B. cinerea. Considering the fungicide resistance problem in B. cinerea in multiple crops, having multiple non-chemical control options is very important to achieve desirable control with integrated disease management strategies. Since the active ingredients in the botanical and bacterial fungicides used in this study are not public, discuss will be limited on their modes of action and efficacy at this point. Similarly, the active ingredient of WXF-17001 is also not known, however, an earlier study by Calvo-Garrido et al. (2014) demonstrated that a fatty acid-based natural product reduced B. cinerea conidial germination by 54% and disease severity in grapes by 96% compared to untreated control. The product used by Calvo-Garrido et al. (2014) is thought to be fungistatic and reduce the postharvest respiratory activity and ethylene production in fruits.
While chemical fungicides have a specific mode of action, biological and other products act in multiple manners either directly antagonizing the plant pathogen or by triggering the plant defenses. For example, amending the potting medium with biochar resulted in induced systemic resistance in tomato and reduced B. cinerea severity by 50% (Mehari et al., 2015). Luna et al. (2016) also showed that application of β-aminobutyric acid and jasmonic acid promoted seed germination and long-term resistance to B. cinerea in tomato. Burkholderia phytofirmans, beneficial endophytic bacterium, offered protection against B. cinerea in grapes by mobilizing carbon resources (callose deposition), triggering plant immune system (hydrogen peroxide production and priming of defense genese), and through antifungal activity (Miotto-Vilanova et al. 2016). Similarly, entomopathogenic fungi such as B. bassiana are also known to induce systemic resistance against plant pathogens (Griffin et al. 2006). Compared to other options evaluated in the study, entomopathogenic fungi have an advantage of controlling both arthropod pests and diseases, while also having plant growth promoting effect (Dara et al. 2017).
Rotating fungicides with different mode of actions reduces the risk of resistance development and using some combinations will also maintain control efficacy. This study provided the efficacy of multiple control options and their combinations and rotations for B. cinerea. This is also the first study demonstrating the efficacy of entomopathogenic fungi against B. cinerea in strawberry.
Acknowledgements: Thanks to Sipcam Agro and Westbridge for funding the study, technical assistance of Hamza Khairi for data collection, and the field staff at the Shafter Research Station for the crop maintenance.
References
Breeze, E. 2019. 97 Shades of gray: genetic interactions of the gray mold, Botrytis cinerea, with wild and domesticated tomato. The Plant Cell 31: 280-281. https://doi.org/10.1105/tpc.19.00030
Calvo-Garrido, C., A.A.G. Elmer, F. J. Parry, I. Viñas, J. Usall, R. Torres, R.H. Agnew, and N. Teixidó. 2014. Mode of action of a fatty acid-based natural product to control Botrytis cinerea in grapes. J. Appl. Microbiol. 116: 967-979. https://doi.org/10.1111/jam.12430
Dara, S. K., S. S. Dara, S.S.R. Dara, and T. Anderson. 2016. First report of three entomopathogenic fungi offering protection against the plant pathogen, Fusarium oxysporum f.sp. vasinfectum. UC ANR eJournal of Entomology and Biologicals https://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=22199
Dara, S. K., S.S.R. Dara, and S. S. Dara. 2017. Impact of entomopathogenic fungi on the growth, development, and health of cabbage growing under water stress. Amer. J. Plant Sci. 8: 1224-1233. https://doi.org/10.4236/ajps.2017.86081
Dara, S.S.R., S. S. Dara, and S. K. Dara. 2018. Preliminary report on the potential of Beauveria bassiana and Metarhizium anisopliae s.l. in antagonizing the charcoal rot causing fungus Macrophomina phaseolina in strawberry. UC ANR eJournal of Entomology and Biologicals https://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=28274
Griffin, M. R., B. H. Ownley, W. E. Klingeman, and R. M. Pereira. 2006. Evidence of induced systemic resistance with Beauveria bassiana against Xanthomonas in cotton. Phytopathol. 96.
Koike, S. T., G. T. Browne, T. R. Gordon, and M. P. Bolda. 2018. UC IPM pest management guidelines: strawberry (diseases). UC ANR Publication 3468. https://www2.ipm.ucanr.edu/agriculture/strawberry/Botrytis-Fruit-Rot/
Liu, S., Z. Che, and G. Chen. 2016. Multiple-fungicide resistance to carbendazim, diethofencardb, procymidone, and pyrimethanil in field isolates of Botrytis cinerea from tomato in Henan Province, China. Crop Protection 84: 56-61.
Luna, E., E. Beardon, S. Ravnskov, J. Scholes, and J. Ton. 2016. Optimizing chemically induced resistance in tomato against Botrytis cinerea. Plant Dis. 100: 704-710. https://doi.org/10.1094/PDIS-03-15-0347-RE
Mehari, Z. H., Y. Elad, D. Rav-David, E. R. Graber, and Y. M. Harel. 2015. Induced systemic resistance in tomato (Solanum lycopersicum) against Botrytis cinerea by biochar amendment involves jasmonic acid signaling. Plant and Soil 395: 31-44.
Miotto-Vilanova, L., C. Jacquard, B. Courteaux, L. Wortham, J. Michel, C. Clément, E. A. Barka, and L. Sanchez. 2016. Burkholderia phytofirmans PsJN confers grapevine resistance against Botrytis cinerea via a direct antimicrobial effect combined with a better resource mobilization. Front. Plant Sci. 7: 1236. https://doi.org/10.3389/fpls.2016.01236
Panebianco, A., I. Castello, G. Cirvilleri, G. Perrone, F. Epifani, M. Ferrarra, G. Polizzi, D. R. Walters, and A. Vitale. 2015. Detection of Botrytis cinerea field isolates with multiple fungicide resistance from table grape in Sicily. Crop Protection 77: 65-73.
Saito, S., T. J. Michailides, and C. L. Xiao. 2016. Fungicide resistance profiling in Botrytis cinerea populations from blueberry in California and Washington and their impact on control of gray mold. Plant Dis. 100: 2087-2093. https://doi.org/10.1094/PDIS-02-16-0229-RE
Saito, S., T. J. Michailides, and C. L. Xiao. 2019. Fungicide-resistant phenotypes in Botrytis cinerea populations and their impact on control of gray mold on stored table grapes in California. European J. Plant Pathol. 154: 203-213.
Stockwell, V. O., B. T> Shaffer, L. A. Jones, and J. W. Pscheidt. 2018. Fungicide resistance profiles of Botrytis cinerea isolated from berry crops in Oregon. Abstract for International Congress of Plant Pathology: Plant Health in A Global Economy; 2018 July 29-Aug 3; Boston, MA.
Weber, R.W.S. and M. Hahn. 2019. Grey mould disease of strawberry in northern Germany: causal agents, fungicide resistance and management strategies. Appl. Microbiol. Biotechnol. 103: 1589-1597.
- Author: Steven A. Tjosvold
Gray mold caused by the fungus Botrytis cinerea is one of the more destructive plant pathogens, and it attacks a wide variety of plants. It is a common springtime disease, favored by cool rainy periods and high humidity. Conditions just like we have seen in California recently. Under these conditions, the fungus may sporulate on infected tissues and produce masses of characteristic gray or brownish spores that become airborne and spread.
Spores must have moisture—from rainfall, morning dew, or irrigation-- to germinate and infect plant tissue. Flower petals and ripening fruits and vegetables are particularly susceptible to infection. Botrytis can directly attack the flowers of roses and many other cut flowers in the greenhouse, and it can even develop, although slowly, at refrigeration temperatures during shipment.
Young, weak, or dead leaves and stems may become infected. Even seeds and seedlings may be attacked and killed. It often limits the productive life of flowers, vegetables, and fruit at the end of their growing cycle in the fall.
Once healthy flower petals or dead, dying, and damaged stem and leaf tissues are colonized, this diseased tissue can be used as a launching pad for the fungus to develop into mature healthy tissue. For example, under conducive environmental conditions, a necrotic tuberous begonia flower can become colonized with Botrytis and drop onto a perfectly green and healthy mature leaf and begin a new infection that can colonize the leaf.
Another example is when Botrytis colonizes a broken or pruned stem, and then Botrytis develops into the attached mature stem, where it normally could not directly infect. In this example with poinsettia, a broken leaf left a stub of dying tissue that became infected, and this stub became the launching pad for the Botrytis to enter the main stem. This led to a serious stem canker and blight, and all plants infected this way needed to be rogued from the crop.
Another example is seen below where annual statice (Limonium sinuatum) was grown for cut flower production. The plants were densely grown in a greenhouse with chronic high humidity and poor air circulation. When flowers were cut, long stubs were left behind near the crown of the plant. The cut stubs became infected and then moved into the young petioles of nearby leaves.
Spores may readily develop in decaying vegetation and old flowers, so removing old flowers before they become infected and function as spore sources or launching pads for infection of nearby healthy tissue is important. Have good air circulation in greenhouses to reduce condensation and wetness. See https://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=28597
Botrytis can form black hardened resting structures called sclerotia in decaying plant matter, which allows for survival during adverse conditions; so remove and dispose fallen leaves and debris around plants. Prune out any dying tissue.
Avoid overhead watering; drip irrigation or hand watering is best to keep water off flowers and foliage. Irrigate early in the day so that the foliage can dry as rapidly as possible. Maximize the period between irrigations to further enhance drying of foliage and flowers. There are many fungicides that help protect against infection. They can be used during periods that are conducive to infection. Be careful to rotate fungicide classes because Botrytis cinerea is known for its ability to mutate to resistant strains.
- Author: Mark Bolda
- Author: Steven Koike
Summary: In 2014, the authors evaluated fungicide products against a slate of several registered fungicides and an untreated control. Fungicides were tested for efficacy against gray mold caused by Botrytis cinerea and powdery mildew caused by Podosphaera aphanis.
Introduction: The authors have been engaged in studying fruit and foliar pathogens in strawberry since 2007. While this group of pathogens includes anthracnose caused by species of Colletotrichum, leather rot caused by Phytophthora cactorum and angular leaf spot caused by Xanthomonas fragariae, the fungicide screening of 2014 concentrated on the two most common problems: gray mold caused by Botrytis cinerea, and powdery mildew caused by Podosphaera aphanis. Year after year these diseases are the most important foliar/fruit concerns for growers, and subsequently garner the most attention from fungicide distributors and manufacturers.
Materials and Methods:
Powdery Mildew: The trial consisted of treatments (Table 1) arranged in a randomized complete block design with each treatment replicated four times, on the Holly Ranch managed by Dole on the variety Monterey. Applications of all materials were made in the equivalent of 150 gallons per acre with a motorized backpack sprayer and hand held boom configured with ten 8001 flat fan nozzles operating at 120 psi, which is intended to closely mimic the conditions of commercial application. Applications of all materials were made two weeks apart: May 16, May 28, June 16, and June 24, 2014.
Powdery mildew evaluations were done on June 5, June 19 and July 7 and consisted of taking ten strawberry leaflets (per plot) of young to mid-age and assigning a percentage on a scale of 0-100% (in 10% increments) to the level of powdery mildew severity on the underside.
Table 1: 2014 Powdery Mildew Treatments
|
Test Material |
Rate/acre |
Thiram 24/7 |
2.6 qt |
|
Thiram 24/7 2.6 qt+ Procure 480 SC |
8 fl oz |
|
Thiram Granu-Flo |
4.4 lb |
|
Pyriofenone |
4 fl oz |
|
Pyriofenone |
5 fl oz |
|
Pyriofenone 4 fl oz + Quintec |
6 fl oz |
|
Quintec |
6 fl oz |
|
Rally |
5 oz |
|
Rally 5 oz w/ Quintec |
5 fl oz |
|
Merivon + Nufilm P |
8 fl oz + 0.01% v/v |
|
Merivon + Nufilm P |
10 fl oz + 0.01% v/v |
|
Pristine |
23 oz |
|
Torino 3.4 fl oz w/ Mettle |
5 fl oz |
|
Isofetamid |
17 fl oz |
|
Isofetamid + IB8111 |
10.3 fl oz + 5.57 fl oz |
|
Isofetamid + 18121 |
10.3 fl oz + 16.5 fl oz |
|
Isofetamid + IB18220 |
10.3 fl oz + 7.6 fl oz |
|
Untreated check |
- |
Results for 2014 Trial
Table 2: 2014 Powdery Mildew Evaluation- Percent Leaf Disease by Treatment
Character Rated |
% Infest |
% Infest |
% Infest |
||||
Rating Date |
Jun-5-2014 |
Jun-19-2014 |
Jul-7-2014 |
||||
Number of Decimals |
2 |
2 |
2 |
||||
Trt |
Treatment |
|
|
|
|
|
|
Name |
1 |
2 |
3 |
||||
1 |
Thiram 24/7 2.6 qt |
23.44 |
a |
17.25 |
bcd |
23.08 |
abc |
2 |
Thiram 24/7 2.6 qt+ Procure 480 SC 8 fl oz |
11.88 |
cde |
7.25 |
gh |
14.64 |
def |
3 |
Thiram Granu-Flo 4.4 lb |
16.25 |
bc |
18.00 |
bc |
26.35 |
a |
4 |
Pyriofenone 4 fl oz |
13.44 |
cde |
13.00 |
def |
15.85 |
cde |
5 |
Pyriofenone 5 fl oz |
13.13 |
cde |
8.25 |
fgh |
8.90 |
fgh |
6 |
Pyriofenone 4 fl oz + Quintec 6 fl oz |
15.31 |
bcd |
11.25 |
efg |
13.60 |
d-g |
7 |
Quintec 6 fl oz |
15.00 |
bcd |
15.50 |
b-e |
23.55 |
ab |
8 |
Rally 5 oz |
16.25 |
bc |
19.25 |
b |
29.40 |
a |
9 |
Rally 5 oz w/ Quintec 5 fl oz |
10.31 |
c-f |
14.00 |
cde |
17.26 |
bcd |
10 |
Merivon 8 fl oz + Nufilm P 0.01% |
6.88 |
ef |
4.25 |
h |
6.76 |
hi |
11 |
Merivon 10 fl oz + Nufilm P 0.01% |
3.75 |
f |
3.75 |
h |
3.49 |
i |
12 |
Pristine 23 oz |
21.25 |
ab |
13.00 |
def |
22.66 |
abc |
13 |
Torino 3.4 fl oz w/ Mettle 5 fl oz |
7.19 |
ef |
7.00 |
gh |
8.67 |
gh |
14 |
Isofetamid 17 fl oz |
11.88 |
cde |
8.75 |
gh |
11.47 |
d-h |
15 |
Isofetamid 10.3 fl oz + IB8111 5.57 fl oz |
10.63 |
cde |
11.75 |
efg |
15.71 |
cde |
16 |
Isofetamid 10.3 fl oz + 18121 16.5 fl oz |
11.94 |
cde |
4.75 |
h |
10.84 |
e-h |
17 |
Isofetamid 10.3 fl oz + IB18220 7.6 fl oz |
9.06 |
def |
7.25 |
gh |
10.98 |
d-h |
18 |
Untreated check |
20.94 |
ab |
24.75 |
a |
30.04 |
a |
LSD (P=0.05) |
6.768 |
4.920 |
0.838t |
||||
Standard Deviation |
4.786 |
3.479 |
0.593t |
||||
CV |
36.12 |
29.53 |
14.89 |
Means followed by same letter do not significantly differ (P=0.05, LSD)
Botrytis Gray Mold: The trial consisted of treatments (Table 3) arranged in a randomized complete block design with each treatment replicated four times, on the Holly Ranch managed by Dole on the variety Monterey. Applications of all materials were made in the equivalent of 150 gallons per acre with a motorized backpack sprayer and hand held boom configured with ten 8001 flat fan nozzles operating at 120 psi, which is intended to closely mimic the conditions of commercial application. Applications of all materials were made two weeks apart May 16, May 28, June 16, and June 24, 2014.
Evaluations for Botrytis infected fruit were made during the weekly fruit harvest by a professional crew of research plot harvesters beginning May 21 and continuing until July 16. Culls were sorted and examined for symptoms and signs of gray mold disease, and a percentage of gray mold infected fruit was calculated from the total fruit harvested from that plot. Data results (Table 4) is presented as a percentage of Botrytis infected fruit from the total amount harvested.
Table 3: Test materials for Botrytis study
|
Test Material |
Rate/acre |
Thiram 24/7 |
2.6 qt |
|
Thiram 24/7 2.6 qt+ Procure 480 SC |
8 fl oz |
|
Thiram Granu-Flo |
4.4 lb |
|
Merivon + Nufilm P |
8 fl oz + 0.01% v/v |
|
Merivon + Nufilm P |
10 fl oz + 0.01% v/v |
|
Pristine |
23 oz |
|
Isofetamid |
17 fl oz |
|
Isofetamid + IB8111 |
10.3 fl oz + 5.57 fl oz |
|
Isofetamid + 18121 |
10.3 fl oz + 16.5 fl oz |
|
Isofetamid + IB18220 |
10.3 fl oz + 7.6 fl oz |
|
Untreated check |
- |
Table 4: Results for 2014 trial
Character Rated |
% Bot |
% Bot |
% Bot |
%Bot |
%Bot |
||||||
Rating Date |
Jun-4-2014 |
Jun-11-2014 |
Jun-18-2014 |
Jun-25-2014 |
Jul-3-2014 |
||||||
Treatment Name |
3 |
4 |
5 |
6 |
7 |
||||||
1 |
Thiram 24/7 2.6 qt |
4.21 |
a |
1.68 |
a |
3.15 |
ab |
8.75 |
a |
18.01 |
a |
2 |
Thiram Granuflo 4.4 lbs |
7.22 |
a |
1.07 |
a |
1.95 |
abc |
15.17 |
a |
18.39 |
a |
3 |
Thiram 24/7 + Procure 480 SC |
9.27 |
a |
2.49 |
a |
1.64 |
abc |
14.36 |
a |
16.198 |
a |
4 |
Merivon @ 8 fl oz |
5.52 |
a |
1.49 |
a |
0.74 |
c |
15.56 |
a |
16.268 |
a |
5 |
Merivon @ 10 fl oz |
5.96 |
a |
1.25 |
a |
0.69 |
c |
15.73 |
a |
17.233 |
a |
6 |
Pristine @ 23 oz |
7.46 |
a |
1.44 |
a |
3.49 |
a |
12.32 |
a |
14.708 |
a |
7 |
Isofetamid @ 17 fl oz |
6.54 |
a |
1.07 |
a |
1.67 |
abc |
12.70 |
a |
17.975 |
a |
8 |
Isofetamid @ 10.3 fl oz + IB8111 @ 5.57 fl oz |
5.67 |
a |
1.58 |
a |
1.35 |
bc |
10.86 |
a |
20.643 |
a |
9 |
Isofetamid @ 10.3 fl oz + IB18121 @ 16.5 fl oz |
4.69 |
a |
2.11 |
a |
2.63 |
ab |
8.60 |
a |
12.815 |
a |
10 |
Isofetamid @ 10.3 fl oz + IB18220 7.6 fl oz |
5.59 |
a |
1.85 |
a |
1.87 |
abc |
9.22 |
a |
19.803 |
a |
11 |
UTC |
13.52 |
a |
1.68 |
a |
3.14 |
ab |
7.66 |
a |
14.720 |
a |
LSD P=0.05 |
0.344t |
0.276t |
0.265t |
0.282t |
8.9782 |
||||||
Standard Deviation |
0.238t |
0.191t |
0.183t |
0.196t |
6.2180 |
||||||
CV |
27.11t |
46.46t |
39.85t |
17.79t |
36.62 |
Means followed by same letter do not significantly differ (P=0.05, LSD)
Discussion of Results for 2014 Trial:
Powdery Mildew: Control of powdery mildew by both rates of Merivon and a rotation of Torino and Mettle was exceptional, with percentages of infection significantly lower than many treatments in each of the three evaluation dates.
Looking at the last rating date on July 7, neither formulation of Thiram controlled powdery mildew, but the inclusion of Procure together with Thiram 24/7 did result in disease percentages below the untreated control. Test compounds isofetamid and pyriofenone had lower percentages of mildew than the untreated control. Rally 40W did not have significantly lower percentages of mildew than the untreated control.
Botrytis: With the exception of the June 18 evaluation date, no significant differences were found between any of treatments. On June 18, both treatments of Merivon demonstrated lower levels of Botrytis infected fruit than the untreated control, Thiram 24/7, isofetamid @10.3 fl oz + IB8111 and Pristine.
Final Note: The use of fungicides, including unregistered materials, is the topic of this article. Before using any of these products, check with your local Agricultural Commissioner's Office and consult product labels for current status of product registration, restrictions, and use information.
Acknowledgments.
We thank Patty Ayala, Kat Kammeijer and Monise Sheehan for their assistance with this trial. We acknowledge the California Strawberry Commission and cooperating companies, in particular Dole, for supporting this work.