- Author: Surendra K. Dara
Several crown, fruit, and foliar diseases cause significant yield losses to strawberry. Gray mold or Botrytis fruit rot caused by Botrytis cinerea, mucor fruit rot by Mucor spp., and Rhizopus fruit rot by Rhizopus spp. are common fungal diseases in California. Botrytis cinerea is more prevalent and damaging fungus among these pathogens warranting regular fungicidal applications. Fungal spores survive in plant debris and soil and infection can occur before flower initiation. Both flowers and fruits are subjected to infection. Severely infected flowers fail to develop into fruits. Infection on developing or ripe fruit occurs as brown lesions, usually under calyxes. Infected areas rot and become dry and leathery under dry conditions or produce a thick, gray mat of spores under cool, moist conditions.
Mucor spp. invade the fruit through ruptured skin and cause leaky fruit rot. Under high humidity, profuse fungal growth of white, tough filaments with black spore-bearing structures is seen covering the fruit. In the case of Rhizopus fruit rot, discolored, water-soaked spots develop on fruit eventually leading to wilting. Similar to the Mucor fruit rot, Rhizopus rot also leads to leaky fruits and development of black spore-bearing structures on white mycelia under high humidity. Both pathogens survive in dead and decaying plant material and can persist in the field.
In a fall-planted conventional strawberry, growers usually make 12 or more fungicidal applications during a four-month period to control Botrytis and other fruit rots. Although fungicides with different modes of action are present and growers try to rotate them, fungicide resistance in B. cinerea is common and effective integrated disease strategies are necessary. Using biostimulants that might improve plant's ability to withstand diseases and alternating chemicals with biological fungicides could be some options to mitigate chemical fungicide resistance. Previous studies looked at the response of fruit diseases to various treatments that received biological soil amendments (Dara, 2020a), soil fungicides (Dara, 2020b), or chemical and biological fungicides (Dara, 2019). This study was conducted to evaluate the efficacy of some biological fungicides along with a chemical fungicide primarily against Botrytis fruit rot.
This study was conducted at a research strawberry field at the Shafter Research Station. Strawberry cultivar San Andreas was planted on 31 October 2019. Other than regular irrigation and fertigation, plants in this study were not treated with any agricultural inputs for agronomic or pest management purposes. Treatments included i) untreated control, ii) Elevate 50 WDG (fenhexamid) at 8 oz/ac, iii) Serifel (Bacillus amyloliquefaciens) at 8 oz/ac, iv) ProBlad Verde (Banda de Lupinus albus doce – BLAD, a polypeptide from sweet lupine) at 36 fl oz with Cinnerate (cinnamon oil) at 0.25% followed by ProBlad Verde at 36, 43, and 43 fl oz/ac on subsequent applications, and v) ProBlad Verde at 36 fl oz with Cinnerate at 0.25% followed by three subsequent applications of ProBlad Verde at 32 fl oz/ac. Each treatment had a 3.2' wide and 14' long plot with two rows of plants and replicated four times in a randomized complete block design. Treatments were applied using a CO2-pressurized backpack sprayer using a 45 gpa spray volume on 26 March, 2, 10, and 20 April 2020. Flowers and fruits were removed from all the plants before the first application. Fruit was harvested on 14 and 27 April and 2 and 10 May and stored in vented plastic containers for postharvest quality assessment. The severity of Botrytis and other fruit rots was recorded 3 and 5 days after harvest on a scale of 0 to 4 where 0=no disease, 1=1-25% fruit with fungal infection, 2=26-50% infection, 3=51-75%, and 4=76-100%. Compared to Botrytis fruit rot, other rots occurred as mixed infections at different times and it was not possible to accurately measure them separately. Data presented in this study primarily represent Botrytis fruit rot with other fruit rots included on some data sets. Data were subjected to analysis of variance using Statistix software to compare disease severity for individual harvest dates and their average.
Fruit rots occurred from low to moderate levels during the observation period. Disease severity followed the usual trend with higher levels 5 days after harvest compared to 3 days after harvest. Compared to untreated control, disease severity was numerically lower in some treatments especially 3 days after harvest, but differences were not statistically significant (P > 0.05) when individual harvest dates or their average were considered. The average disease severity from four harvests was 0.25 in Elevate and Serifel, 0.50 in ProBlad Verde low rate with Cinnerate, and 0.81 in ProBlad Verde high rate with Cinnerate treatment and untreated control 3 days after harvest. The average disease severity was 1.13 for Serifel, 1.19 for Elevate and the low rate of ProBlad Verde with Cinnerate, 1.81 for the high rate of ProBlad Verde with Cinnerate, and 2.0 for untreated control 5 days after harvest. Although statistically significant differences could not be found among treatments, this study indicates the potential of non-chemical alternatives and warrants additional studies for further investigation.
Acknowledgements: Thanks to BASF and Sym-Agro for funding this study and Marjan Heidarian Dehkordi and Zach Woolpert for the technical assistance.
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. 2020a. Improving strawberry yields with biostimulants and nutrient supplements: a 2019-2020 study. UCANR eJournal of Entomology and Biologicals. https://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=43631
Dara, S. K. 2020b. Impact of drip application of fungicides on strawberry health and yields. UCANR eJournal of Entomology and Biologicals. https://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=43632
- 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.
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.
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.
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.
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