Control of Phytophthora and Rhizoctonia Root Rot on Red Maple Using Fungicides and Biofungicides

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Madhav ParajuliDepartment of Agricultural and Environmental Sciences, College of Agriculture, Tennessee State University, Otis L. Floyd Nursery Research Center, 472 Cadillac Lane, McMinnville, TN 37110

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Fulya Baysal-GurelDepartment of Agricultural and Environmental Sciences, College of Agriculture, Tennessee State University, Otis L. Floyd Nursery Research Center, 472 Cadillac Lane, McMinnville, TN 37110

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Phytophthora nicotianae and Rhizoctonia solani are the well-described soilborne pathogens of concern causing Phytophthora and Rhizoctonia root rot, respectively, of red maple plants (Acer rubrum L.), resulting in substantial economic losses to nursery growers. The management of root and crown rot disease of red maple is a big challenge. The objective of this study was to test the efficacy of several fungicide and biofungicide products to control Phytophthora and Rhizoctonia root rot on red maple plants in greenhouse conditions. Treatments, including fungicides and biofungicides, and nontreated and inoculated and nontreated and noninoculated as controls were arranged in a completely randomized design with six replications. Red maples planted in number 1 nursery containers were artificially inoculated with P. nicotianae or R. solani. Plant height, plant width, total fresh weight, and root fresh weight were measured and roots were assessed for root rot disease severity based on a scale of 0% to 100% root damaged. The pathogen recovery percentage of plant roots was determined by culturing ten randomly selected root pieces (≈1 cm long) cut from the root tips on Phytophthora selective medium (PARPH-V8) or Rhizoctonia semi-selective medium. All tested fungicides and biofungicides reduced Phytophthora and Rhizoctonia root rot on red maple plants compared with the nontreated and inoculated control. Likewise, pathogen recovery was lower for fungicide-treated and biofungicide-treated plants. Fungicides, such as mefenoxam, oxathiapiprolin, pyraclostrobin plus boscalid, and pyraclostrobin provided the most effective control of Phytophthora root rot. Pyraclostrobin plus boscalid and pyraclostrobin followed by biofungicides Bacillus amyloliquefaciens strain F727 and Trichoderma harzianum Rifai strain T-22 plus T. virens strain G-41 were most effective for suppressing Rhizoctonia root rot. There were no differences in plant height, plant width, plant fresh weight, and root fresh weight among the treatments. These findings will help nursery producers make decisions while formulating soilborne disease management strategies for red maple production.

Abstract

Phytophthora nicotianae and Rhizoctonia solani are the well-described soilborne pathogens of concern causing Phytophthora and Rhizoctonia root rot, respectively, of red maple plants (Acer rubrum L.), resulting in substantial economic losses to nursery growers. The management of root and crown rot disease of red maple is a big challenge. The objective of this study was to test the efficacy of several fungicide and biofungicide products to control Phytophthora and Rhizoctonia root rot on red maple plants in greenhouse conditions. Treatments, including fungicides and biofungicides, and nontreated and inoculated and nontreated and noninoculated as controls were arranged in a completely randomized design with six replications. Red maples planted in number 1 nursery containers were artificially inoculated with P. nicotianae or R. solani. Plant height, plant width, total fresh weight, and root fresh weight were measured and roots were assessed for root rot disease severity based on a scale of 0% to 100% root damaged. The pathogen recovery percentage of plant roots was determined by culturing ten randomly selected root pieces (≈1 cm long) cut from the root tips on Phytophthora selective medium (PARPH-V8) or Rhizoctonia semi-selective medium. All tested fungicides and biofungicides reduced Phytophthora and Rhizoctonia root rot on red maple plants compared with the nontreated and inoculated control. Likewise, pathogen recovery was lower for fungicide-treated and biofungicide-treated plants. Fungicides, such as mefenoxam, oxathiapiprolin, pyraclostrobin plus boscalid, and pyraclostrobin provided the most effective control of Phytophthora root rot. Pyraclostrobin plus boscalid and pyraclostrobin followed by biofungicides Bacillus amyloliquefaciens strain F727 and Trichoderma harzianum Rifai strain T-22 plus T. virens strain G-41 were most effective for suppressing Rhizoctonia root rot. There were no differences in plant height, plant width, plant fresh weight, and root fresh weight among the treatments. These findings will help nursery producers make decisions while formulating soilborne disease management strategies for red maple production.

Red maple (Acer rubrum L.), which is native to the eastern United States, is a deciduous woody ornamental plant popularly known for its outstanding fall color. In the United States, red maple is an important component of the woody ornamental nursery industry, with a total annual sales value of $7.5 million (National Agricultural Statistics Service, 2020). Southeastern states are the major producers of red maple nursery plants. The suitable soil and climatic conditions result in this crop being among the dominating woody ornamentals grown in southeastern states (Barnard and Mitchell, 1993). Despite the high demand and increasing production for this crop, plant damage associated with root and crown rot, caused by soilborne pathogens, remains a serious problem that is often faced by nursery producers (Panth et al., 2020; Parajuli et al., 2022). Soilborne diseases ruin plant quality, making them unmarketable, and may cause complete loss. Several soilborne pathogens cause root and crown rot disease, but Phytophthora nicotianae Breda de Hann (oomycetes; also called “water molds”) and Rhizoctonia solani J. G. Kühn (fungal pathogen) are most commonly isolated from the infected roots of red maple plants grown in nursery and greenhouse settings.

Phytophthora nicotianae and R. solani are the most destructive and economically important soilborne pathogens of concern for red maple plants that result in substantial economic losses to nursery growers (Parajuli et al., 2022). The damaged root systems exhibit dark brown to black discoloration; furthermore, these pathogens may cause complete decay. In severe cases, there is a lag in root growth; damage progresses upward, extending to the crown. The foliage of the infected plants displays wilting, yellowing, browning, reduced plant growth, and dieback of branches, and may lead to whole plant death. Symptoms develop rapidly in the host plants when free water is present because moist conditions favor pathogen germination, growth, and root infection (Agrios, 1969; Erwin et al., 1983). These pathogens infect a wide range of annual as well as perennial crops worldwide, including woody ornamentals (Ajayi-Oyetunde and Bradley, 2018; Cline et al., 2008). Phytophthora nicotianae and R. solani can spread to new production facilities, mostly through the movement of infected planting materials, soil, and irrigation water (Bienapfl and Balci, 2014; Garbelotto et al., 2018; Parke and Grünwald, 2012). They survive in the soil or plant residues for an extended period of time by producing dormant structures such as sclerotia (R. solani) or oospores and chlamydospores (P. nicotianae); furthermore, they infect plant roots when the soil conditions, especially the temperature and moisture, become favorable (Agrios, 1969; Erwin and Ribeiro, 1996; Raaijmakers et al., 2009; van West et al., 2003). Therefore, soilborne disease management is challenging. Moreover, the heterogeneity in production systems and multiyear production cycles of woody ornamentals further complicate the control measures (Parke and Grünwald, 2012).

When those pathogens are introduced to the new production facilities, complete eradication is difficult or even impossible. The implementation of an integrated approach, including sanitation, cultural, biological, and chemical methods, or the use of resistant cultivars can provide successful control of soilborne diseases. Unfortunately, no root rot-resistant cultivars of red maple are available. As an important component of integrated management, it is necessary to find effective biological and chemical products. Recently, several fungicides have been developed by different manufacturing companies with a new mode of action because of environmental regulations. Different fungicide products available to use against soilborne pathogens are pyraclostrobin, azoxystrobin, oxathiapiprolin, and mefenoxam (Baibakova et al., 2019; Baysal-Gurel and Kabir, 2019; Neupane et al., 2021). Some of them specifically target oomycetes, whereas others are used against both fungi and oomycetes. In general, newly developed fungicides have a single-site mode of action and are considered relatively safe to plants and the environment compared with traditional multisite fungicides (McGrath, 2004; Yang et al., 2011; Baibakova et al., 2019). However, a serious problem with those fungicides is the development of pathogen resistance (Hwang and Benson, 2005). These products need to be tested thoroughly for their effectiveness against soilborne pathogens before making any recommendations to woody ornamental nursery producers. Moreover, growers and researchers are interested in integrating biocontrol agents (biofungicides) in their soilborne disease management strategies alone or in combination with fungicides (Gardener and Fravel, 2002). Trichoderma harzianum Rifai strain T-22, T. virens strain G-41, and Bacillus amyloliquefaciens strain F727 are the most explored biocontrol agents used against soilborne pathogens (Lecomte et al., 2016). Biocontrol agents are known to improve plant resistance to both biotic and abiotic stress factors including pathogens and to have fungicidal activities (Harman, 2006). Moreover, biocontrol agents induce suppression of soilborne pathogens through competition for space and resources. Nevertheless, these fungicides and biocontrol agents have not been explored widely for woody ornamental crops (Baysal-Gurel and Kabir, 2018; Brown et al., 2019). Therefore, growers are reluctant to use them until they are adequately tested. An evaluation of fungicides and biofungicides is necessary to find good candidates to effectively control P. nicotianae and R. solani on red maple plants. Based on these considerations, this study aimed to evaluate several fungicides and biofungicides to control Phytophthora root rot and Rhizoctonia root rot on red maple plants.

Materials and Methods

Inoculum preparation.

Isolate FBG201507 of P. nicotianae (GenBank accession MT579419) and isolate FBG201508 of R. solani (GenBank accession MT533254), both isolated from red maple, were obtained from the cultures maintained at the laboratory of Dr. Fulya Baysal-Gurel at Tennessee State University. The R. solani cultures were maintained on potato dextrose agar medium. To prepare P. nicotianae inoculum, 25 g of long grain rice and 20 mL of deionized water were measured in a 300-mL Pyrex bottle and autoclaved twice (each for 30 min). For the autoclaved rice, P. nicotianae isolates were mixed at the rate of six plugs (1.56 cm2)/bottle and allowed to colonize rice grains for 10 d. The bottle was lightly shaken every day until it was used. To prepare R. solani inoculums, 7-d-old to 10-d-old cultures of R. solani grown on potato dextrose agar medium were chopped and placed in a beaker with 1 L of sterile distilled water at a rate of 1 petri plate/L and then homogenized using a mixer (model number 59785R; Hamilton Beach, Glen Allen, VA) to prepare the slurry.

Experimental design.

The greenhouse experiments were performed at the Otis L. Floyd Nursery Research Center of Tennessee State University in McMinnville, TN. Eight-month-old bare-rooted seedlings of red maple (Acer rubrum L. ‘Brandywine’) plants were received from a private nursery (Belvidere, TN). They were prepared from the stem cuttings and raised in a nursery container using the soilless potting mixture. No fungicides or biofungicides were used when they were in the nursery. After we received bare-rooted seedlings of red maple, we planted them in number 1 nursery containers (16-cm diameter × 16-cm height; Hummert International, Earth City, MO) with Morton’s Nursery Mix (Morton’s Horticultural Products, McMinnville, TN) on 10 Feb. 2021. Red maple plants were watered for 3 min twice per day using an overhead automatic irrigation system and hand-watered when needed. Plants were fertilized on 7 Apr. 2021, with 18N–6P–8K Nutricode controlled-release granular fertilizer (Florikan E.S.A. LLC, Sarasota, FL) at a rate of 15 g/plant. Additionally, 7.5 g of Miracle-Gro Water Soluble All-Purpose Plant Food (Scott’s Miracle-Gro Products, Inc., Marysville, OH) was well-mixed in 1 L of water and applied to red maple plants on 5 Apr., 19 Apr., 3 May, and 17 May 2021.

Treatments were arranged in a completely randomized design with six replications, with each containing one containerized red maple plant. Experiments were performed separately for Phytophthora root rot (12 treatments × 6 replications = 72) and Rhizoctonia root rot (9 treatments × 6 replications = 54) under greenhouse conditions. We evaluated seven fungicides, two biofungicides, and one combination of fungicide and biofungicide against Phytophthora root rot (Table 1), and four fungicides (all with the exception of pyraclostrobin plus fluxapyroxad, oxathiapiprolin, and mefenoxam), two biofungicides, and one combination of fungicide and biofungicide against Rhizoctonia root rot (Table 1). The study was performed from 3 June to 15 Sept. 2021 (trial 1), and from 8 July to 20 Oct. 2021 (trial 2). Containerized red maple plants were artificially inoculated with P. nicotianae colonized on rice grains for 10 d. Four rice grains were buried 5 cm below the surface of the potting mix on four opposite sides of the red maple plant on 3 June 2021 (trial 1) and 8 July 2021 (trial 2). Plants in each container were drench-inoculated with R. solani slurry at the rate of 300 mL/plant on 3 June 2021 (trial 1) and 8 July 2021 (trial 2). Nontreated and noninoculated and nontreated and inoculated plants served as negative and positive controls, respectively. On 9 June 2021 (trial 1) and 14 July 2021 (trial 2), hydrogen peroxide plus peroxyacetic acid (0.2% volume/volume; BioSafe Systems, LLC, Hartford, CT) was drenched in the potting mix 24 h before transplanting in dedicated containers. On 10 June 2021 (trial 1) and 15 July 2021 (trial 2), Bacillus spp. plus Trichoderma harzianum (BioSafe Systems, LLC, Hartford, CT) at a rate of 0.5 g⋅L−1 was prepared, and dedicated rooted plants for this treatment were dipped into the mixed solution. On 1 July 2021 (trial 1) and 5 Aug. 2021 (trial 2), these plants received Bacillus spp. plus T. harzianum at 0.3 g⋅L−1 as a drench, and the application continued during 3-week interval. The rest of the fungicide and biofungicide treatments were applied at the rate of 300 mL/plant (the solution was prepared as presented in Table 1) as drench starting on 10 June 2021 and ending on 2 Sept. 2021 (trial 1) and starting on 15 July 2021 and ending on 7 Oct. 2021 (trial 2) following a particular application interval labeled by the manufacturer (Table 1). Average maximum greenhouse temperatures for June, July, Aug., Sept., and Oct. 2021 were 30.2, 29.8, 28.9, 28.6, and 27.3 °C; average minimum temperatures were 18.7, 20.4, 19.9, 15.1, and 16.2 °C, respectively. Average greenhouse relative humidity for June, July, Aug., Sept., and Oct. 2021 were 70.7%, 93.1%, 93%, 92.7%, and 70.5%, respectively.

Table 1.

Details of fungicides and biofungicides used for this study.

Table 1.

Recording plant growth and root rot disease.

We measured the plant height and width of red maple at the beginning of trials on 2 June 2021 (trial 1) and 7 July 2021 (Trial 2), and at the end of the trials on 14 Sept. 2021 (trial 1) and 19 Oct. 2021 (trial 2). Plant height was measured from the crown level to the shoot tip, and the plant width was the average of the widest part from leaf tip to leaf tip and the width perpendicular to the widest part. The increase in height or increase in width was calculated by subtracting the initial height/width from the final height/width. At the end of the trials, plants were taken out of the container, and nursery mix from the plant roots was removed. Plant roots were washed with running tap water. Plant fresh weight and root fresh weight were recorded for all plants on 14 Sept. 2021 (trial 1) and 20 Oct. 2021 (trial 2). Roots of all the tested plants were evaluated for disease severity and pathogen recovery. Phytophthora root rot or Rhizoctonia root rot disease severity was assessed visually based on a scale of 0% to 100% roots damaged. Similarly, the pathogen recovery percentage was determined by culturing ten randomly selected root samples (≈1 cm long) cut from the root tips of each plant on Phytophthora selective medium (PARPH-V8) (Ferguson and Jeffers, 1999) or Rhizoctonia semi-selective medium (Gutierrez et al., 2001). The number of root pieces showing P. nicotianae growth were counted after 4 to 5 d, and the number of root pieces showing R. solani growth were counted after 2 d.

Statistical analysis.

A one-way analysis of variance was performed to examine the treatment effects on plant height, plant width, total plant fresh weight, root fresh weight, disease severity, and pathogen recovery using the PROC GLM procedure in SAS software 9.4 (SAS Inc., Cary, NC). When the effects were significant, the post hoc Fisher’s least significant difference test was used for means comparisons (α = 0.05). The data met the assumption of normal distribution and homogeneity.

Results

Effectiveness of fungicides and biofungicides against Phytophthora root rot.

Fungicides and biofungicides had a significant effect on Phytophthora root rot disease severity (Fig. 1) and pathogen recovery (Fig. 2) on red maple plants grown under greenhouse conditions (P < 0.05). Phytophthora root rot disease severity was the highest for nontreated and inoculated control plants in both trials, with rates of 53.3% (trial 1) and 46.7% (trial 2) (Fig. 1). The nontreated and noninoculated control plants had the lowest root rot disease severity. All tested fungicides and biofungicides significantly reduced Phytophthora root rot disease severity compared with the nontreated and inoculated control plants in both trials, but the root rot severity was higher compared with that of the nontreated and noninoculated plants. Fungicides mefenoxam, oxathiapiprolin, pyraclostrobin plus boscalid, and pyraclostrobin demonstrated the most effective control of Phytophthora root rot disease, followed by pyraclostrobin plus fluxapyroxad. Fungicides copper octaonate and azoxystrobin plus benzovindiflupyr were comparatively less effective for controlling Phytophthora root rot. Likewise, plants treated with biofungicides Bacillus amyloliquefaciens strain F727, T. harzianum Rifai strain T-22 plus T. virens strain G-41, and the combination of fungicide and biofungicide comprising hydrogen peroxide plus peroxyacetic acid and Bacillus spp. plus T. harzianum provided partial control of Phytophthora root rot disease. Pathogen recovery in the roots of red maple plants had responses similar to those of root rot disease severity to fungicides and biofungicides (Fig. 2). Pathogen recovery in the roots of red maple plants was significantly lower for all the fungicide-treated and biofungicide-treated plants compared with the nontreated and inoculated plants, with rates of 50.0% (trial 1) and 65.0% (trial 2). There was no pathogen recovery in the nontreated and noninoculated plants. The least pathogen recovery in the roots was detected for mefenoxam, oxathiapiprolin, and pyraclostrobin plus boscalid. Plants treated with biofungicides had pathogen recovery rates higher than those of most effective fungicides. There were no differences in plant height and width increases, total fresh weight, and root fresh weight among the fungicide and biofungicide treatments (Table 2).

Fig. 1.
Fig. 1.

Means (±se) of Phytophthora root rot disease severity (%) of red maple plants treated with fungicides and biofungicides (trial 1 and trial 2) under greenhouse conditions. Values are the means per plant for six single-plant replicates. Different lowercase letters on the top of the bar denote significant difference at P ≤ 0.05. A one-way analysis of variance was used to evaluate treatment effects. When the effects were significant, Fisher’s least significant difference test was used for mean comparisons with α = 0.05. Disease severity of red maple was determined based on a scale of 0% to 100% roots damaged. Trichoderma harzianum plus T. virens, Bacillus amyloliquefaciens, and Bacillus spp. plus T. harzianum are biofungicides. The other treatments are fungicides. HA + PA = hydrogen peroxide plus peroxyacetic acid.

Citation: HortScience 57, 10; 10.21273/HORTSCI16673-22

Fig. 2.
Fig. 2.

Means (±se) of Phytophthora pathogen recovery (%) of red maple plants roots treated with fungicides and biofungicides (trial 1 and trial 2) under greenhouse conditions. Values are the means per plant for six single-plant replicates. Different lowercase letters on the top of the bar denote significant difference at P ≤ 0.05. A one-way analysis of variance was used to evaluate treatment effects. When the effects were significant, Fisher’s least significant difference test was used for mean comparisons with α = 0.05. The pathogen recovery percentage in plant roots was determined by culturing ten randomly selected root pieces (≈1 cm long) cut from the root tips on Phytophthora selective medium (PARPH-V8). Trichoderma harzianum plus T. virens, Bacillus amyloliquefaciens, and Bacillus spp. plus T. harzianum are biofungicides. The other treatments are fungicides. HA + PA = hydrogen peroxide plus peroxyacetic acid.

Citation: HortScience 57, 10; 10.21273/HORTSCI16673-22

Table 2.

Plant growth parameter (means ± se) of red maple plants treated with fungicides and biofungicides to control Phytophthora root rot caused by Phytophthora nicotianae (trial 1 and trial 2) under greenhouse conditions.

Table 2.

Effectiveness of fungicides and biofungicides against Rhizoctonia root rot.

Fungicides and biofungicides had a significant effect on Rhizoctonia root rot disease severity (Fig. 3) and pathogen recovery (Fig. 4) on red maple plants grown under greenhouse conditions (P < 0.05). All the fungicides and biofungicides reduced Rhizoctonia root rot disease severity compared with the nontreated and inoculated plants. The highest Rhizoctonia root rot disease severity was observed for the nontreated and inoculated plants, with rates of 51.7% (trial 1) and 41.7% (trial 2), and the lowest was observed for the nontreated and noninoculated plants. Pyraclostrobin plus boscalid and pyraclostrobin provided the best control of Rhizoctonia root rot disease, followed by biofungicides. Copper octaonate and azoxystrobin plus benzovindiflupyr were marginally effective for controlling root rot disease. The pathogen recovery rates were 51.7% (trial 1) and 66.7% (trial 2) for the nontreated and inoculated plants. The Rhizoctonia pathogen recovery was significantly suppressed by all tested fungicides and biofungicides during both trials compared with nontreated and inoculated plants. Nontreated and noninoculated plants exhibited no pathogen recovery. The lowest pathogen recovery was observed for the plants treated with pyraclostrobin plus boscalid and pyraclostrobin. There were no significant effects of fungicides and biofungicides on red maple plant height and width increases, total fresh weight, and root fresh weight during both trials (Table 3).

Fig. 3.
Fig. 3.

Means (±se) of Rhizoctonia root rot disease severity (%) of red maple plants treated with fungicides and biofungicides (trial 1 and trial 2) under greenhouse conditions. Values are the means per plant for six single-plant replicates. Different lowercase letters on the top of the bar denote significant difference at P ≤ 0.05. A one-way analysis of variance was used to evaluate treatment effects. When the effects were significant, Fisher’s least significant difference test was used for mean comparisons with α = 0.05. Disease severity of red maple was determined based on a scale of 0% to 100% roots damaged. Trichoderma harzianum plus T. virens, Bacillus amyloliquefaciens, and Bacillus spp. plus T. harzianum are biofungicides. The other treatments are fungicides. HA + PA = hydrogen peroxide plus peroxyacetic acid.

Citation: HortScience 57, 10; 10.21273/HORTSCI16673-22

Fig. 4.
Fig. 4.

Means (±se) of Rhizoctonia pathogen recovery (%) of red maple plant roots treated with fungicides and biofungicides (trial 1 and trial 2) under greenhouse conditions. Values are the means per plant for six single-plant replicates. Different lowercase letters on the top of the bar denote significant difference at P ≤ 0.05. A one-way analysis of variance was used to evaluate treatment effects. When the effects were significant, Fisher’s least significant difference test was used for mean comparisons with α = 0.05. Pathogen recovery percentages of plant roots were determined by culturing ten randomly selected root pieces (≈1 cm long) cut from the root tips on Rhizoctonia semi-selective medium. Trichoderma harzianum plus T. virens, Bacillus amyloliquefaciens, and Bacillus spp. plus T. harzianum are biofungicides. The other treatments are fungicides. HA + PA = hydrogen peroxide plus peroxyacetic acid.

Citation: HortScience 57, 10; 10.21273/HORTSCI16673-22

Table 3.

Plant growth parameters (means ± se) of red maple plants treated with fungicides and biofungicides to control Rhizoctonia root rot caused by Rhizoctonia solani (trial 1 and trial 2) under greenhouse conditions.

Table 3.

Discussion

To our knowledge, this is the first study to establish and compare the performance of several fungicides and biofungicides against Phytophthora root rot and Rhizoctonia root rot on red maple plants. All tested fungicides and biofungicides significantly reduced Phytophthora root rot and Rhizoctonia root rot compared with the nontreated and inoculated control during both trials. However, some of the fungicides and biofungicides were more effective than the others. Moreover, biofungicides were relatively less effective for suppressing root rot diseases compared with some of the fungicides that performed best. Nevertheless, biofungicides provided better control of root rot diseases when compared with other partially effective fungicides. There were no differences in plant growth among the treatments.

Biofungicides such as Bacillus spp. and Trichoderma spp. provided partial control of root rot disease on red maple. We assumed that they would provide successful suppression of root rot pathogens in the production facilities where pathogen pressure is low. During the current study, the pathogen pressure was medium to high. Biocontrol agents colonize root systems, thus preventing attacks from soilborne pathogens (Raaijmakers et al., 2009). Trichoderma spp. and Bacillus spp. suppress soilborne pathogens through competition for space and resources or through antibiotics and parasitism (Handelsman and Stabb, 1996). Because biocontrol agents improve host tolerance, their benefits may extend to control these pathogens. During recent years, there has been an increasing demand for the use of biocontrol agents to suppress soilborne diseases (Gardener and Fravel, 2002), partly because of the negative consequences of chemical fungicides. As such, growers and researchers have focused more effort on integrating biocontrol agents in soilborne disease management strategies alone or in combination with fungicides (Gardener and Fravel, 2002). Biocontrol agents can be effective tools if an integrated approach is followed by the growers. Another advantage of using biocontrol agents is that they offer broad-spectrum control of soilborne diseases.

Fungicides mefenoxam, oxathiapiprolin, pyraclostrobin plus boscalid, and pyraclostrobin demonstrated the most effective control of Phytophthora root rot disease. Likewise, pyraclostrobin plus boscalid and pyraclostrobin were highly effective for controlling Rhizoctonia root rot disease, followed by B. amyloliquefaciens strain F727 and T. harzianum Rifai strain T-22 plus T. virens strain G-41. Our findings are consistent with those of previous studies that used these products to control Phytophthora root rot caused by P. nicotianae on hydrangeas (Hydrangea spp.) (Baysal-Gurel and Kabir, 2019) and Rhizoctonia root rot caused by R. solani on viburnum (Viburnum odoratissimum) (Baysal-Gurel and Kabir, 2018). The mefenoxam and oxathiapiprolin are the most commonly explored fungicides for controlling oomycete plant pathogens. They reduce pathogen infection by reducing or completely stopping sporangia germination, zoospore formation/mobility, or mycelium growth (Cohen et al., 2018). The antifungal activity of mefenoxam is largely associated with its ability to inhibit the synthesis of ribosomal RNA, whereas oxathiapiprolin targets lipid homeostasis and transfer/storage (Fungicide Resistance Action Committee, 2021). Pyraclostrobin is used to control both fungal and oomycete pathogens. Pyraclostrobin inhibits mitochondrial respiration by targeting cytochrome-bc-1 complex (FRAC, 2021), resulting in reduced pathogenic activity, and it may lead to the death of pathogens (Kanungo and Joshi, 2014). Fungicides are also known to induce physiological changes in host plants, resulting in increased tolerance to biotic and abiotic stresses. During the current study, the efficacy of azoxystrobin plus benzovindiflupyr, both for targeting respiration of pathogens and controlling root rot disease, was comparatively lower than that of other fungicide products. Moreover, fungicide copper octaonate did not provide satisfactory control of root rot diseases. These products demand further exploration to determine their effectiveness against root rot diseases on red maple and other woody ornamental plants.

Although fungicides pyraclostrobin, pyraclostrobin plus boscalid, mefenoxam, and oxathiapiprolin are clearly effective products for controlling Phytophthora root rot based on these greenhouse trials, the major issue that might arise with these products is the development of pathogen resistance (Baysal-Gurel and Kabir, 2019; Hu and Li, 2014; Jeffers et al., 2004). Moreover, although pyraclostrobin and pyraclostrobin plus boscalid provided the most consistent control of Rhizoctonia root rot, using the same fungicide products repeatedly might lead to the development of pathogen resistance. The major reason for the development of pathogen resistance is the repeated use of fungicides from the same fungicide group or overdose applications of fungicides more often than recommended by the fungicide label. Therefore, these products need to be monitored for resistance management. For resistance management, as suggested by the Fungicide Resistant Action Committee (FRAC; https://www.frac.info/), growers can use the most effective fungicide candidates in rotation or in mixtures by strictly following the instructions provided with the products. They can also be integrated with biocontrol products used in the rotation plan for root rot disease management.

Phytotoxicity is another issue with the use of fungicide or biofungicide compounds (Baibakova et al., 2019). However, during our study, we did not observe any phytotoxicity of fungicides and biofungicides on red maple plants during these two trials. Moreover, plant growth parameters (height, width, total fresh weight, and root fresh weight) were monitored as critical plant health determinates. Although higher root rot disease severity is expected to cause reduced plant growth, such as plant height, plant width, total fresh weight, or root fresh weight, we did not observe such a correlation during our study, possibly because of shorter experimental durations (≈4 months). However, red maple plants remain for an extended period of time in growers’ nurseries and greenhouses, which may result in an inverse correlation between root rot disease and plant growth.

In conclusion, this experiment was designed to help nursery producers find effective fungicide and biofungicide candidates for the suppression of Phytophthora root rot and Rhizoctonia root rot. Fungicides mefenoxam, oxathiapiprolin, pyraclostrobin plus boscalid, and pyraclostrobin were most effective for controlling Phytophthora root rot, and pyraclostrobin plus boscalid and pyraclostrobin were proven to be the best for controlling Rhizoctonia root rot disease, followed by Bacillus amyloliquefaciens strain F727 and Trichoderma harzianum + T. virens, on red maple plants. It is recommended that growers should use those products in rotation or in mixtures to help increase the effectiveness of fungicides and biofungicides and reduce the likelihood of development of pathogen resistance. It is important to note that no single management technique can provide complete control of soilborne pathogens. Therefore, it is necessary to strictly follow the integrated approach involving sanitation, cultural, biological, and chemical methods.

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  • Barnard, E. & Mitchell, D.J. 1993 Phytophthora basal canker of red maple Fla. Department Agric. & Consumer Services, Division of Plant Industry. https://www.fdacs.gov/content/download/11368/file/pp361.pdf

    • Search Google Scholar
    • Export Citation
  • Baysal-Gurel, F. & Kabir, N. 2018 Comparative performance of fungicides and biocontrol products in suppression of Rhizoctonia root rot in viburnum J. Plant Pathol. Microbiol. 9 451 https://doi.org/10.4172/2157-7471.1000451

    • Search Google Scholar
    • Export Citation
  • Baysal-Gurel, F. & Kabir, N. 2019 Evaluation of fungicides and biocontrol products for the control of Phytophthora root rot of hydrangeas Arch. Phytopathol. Pflanzenschutz 52 481 496 https://doi.org/10.1080/03235408.2019.1648023

    • Search Google Scholar
    • Export Citation
  • Bienapfl, J. & Balci, Y. 2014 Movement of Phytophthora spp. in Maryland’s nursery trade Plant Dis. 98 134 144 https://doi.org/10.1094/PDIS-06-13-0662-RE

    • Search Google Scholar
    • Export Citation
  • Brown, M.S., Baysal-Gurel, F., Oliver, J.B. & Addesso, K.M. 2019 Evaluation of fungicides and biofungicide to control Phytophthora root rot (Phytophthora cinnamomi Rands) and ambrosia beetles (Coleoptera: Curculionidae: Scolytinae) on flowering dogwoods exposed to simulated flood events Crop Prot. 124 104834 https://doi.org/10.1016/j.cropro.2019.05.028

    • Search Google Scholar
    • Export Citation
  • Cline, E.T., Farr, D.F. & Rossman, A.Y. 2008 A synopsis of Phytophthora with accurate scientific names, host range, and geographic distribution Plant Health Prog. 9 32 https://doi.org/10.1094/PHP-2008-0318-01-RV

    • Search Google Scholar
    • Export Citation
  • Cohen, Y., Rubin, A.E. & Galperin, M. 2018 Oxathiapiprolin-based fungicides provide enhanced control of tomato late blight induced by mefenoxam-insensitive Phytophthora infestans PLoS One 13 e0204523 https://doi.org/10.1371/journal.pone.0204523

    • Search Google Scholar
    • Export Citation
  • Erwin, D.C., Bartinicki, S.C. & Tsao, P.H.T. 1983 Phytophtora. Its biology, taxonomy, ecology, and pathology Amer. Phytopathol. Soc.

  • Erwin, D.C. & Ribeiro, O.K. 1996 Phytophthora diseases worldwide Amer. Phytopathol. Soc. (APS Press)

  • Ferguson, A. & Jeffers, S. 1999 Detecting multiple species of Phytophthora in container mixes from ornamental crop nurseries Plant Dis. 83 1129 1136 https://doi.org/10.1094/PDIS.1999.83.12.1129

    • Search Google Scholar
    • Export Citation
  • Fungicide Resistance Action Committee 2021 FRAC code list 2020: Fungicides sorted by mode of action (including FRAC code numbering) 8 Dec. 2021. <https://www.frac.info/docs/default-source/publications/frac-code-list/frac-code-list-2021–final.pdf?sfvrsn=f7ec499a_2>

    • Search Google Scholar
    • Export Citation
  • Garbelotto, M., Frankel, S. & Scanu, B. 2018 Soil-and waterborne Phytophthora species linked to recent outbreaks in Northern California restoration sites Calif. Agr. 72 208 216 https://doi.org/10.3733/ca.2018a0033

    • Search Google Scholar
    • Export Citation
  • Gardener, B.B.M. & Fravel, D.R. 2002 Biological control of plant pathogens: Research, commercialization, and application in the USA Plant Health Prog. 3 17 https://doi.org/10.1094/PHP-2002-0510-01-RV

    • Search Google Scholar
    • Export Citation
  • Gutierrez, W., Shew, H. & Melton, T. 2001 A semi-selective medium to isolate Rhizoctonia solani from soil and tissue Plant Path. Ext. 1 2

  • Handelsman, J. & Stabb, E.V. 1996 Biocontrol of soilborne plant pathogens Plant Cell 8 1855 https://doi.org/10.1105%2Ftpc.8.10.1855

  • Harman, G.E. 2006 Overview of mechanisms and uses of Trichoderma spp Phytopathology 96 190 194 https://doi.org/10.1094/PHYTO-96-0190

  • Hu, J. & Li, Y. 2014 Inheritance of mefenoxam resistance in Phytophthora nicotianae populations from a plant nursery Eur. J. Plant Pathol. 139 545 555 https://doi.org/10.1007/s10658-014-0410-0

    • Search Google Scholar
    • Export Citation
  • Hwang, J. & Benson, D. 2005 Identification, mefenoxam sensitivity, and compatibility type of Phytophthora spp. attacking floriculture crops in North Carolina Plant Dis. 89 185 190 https://doi.org/10.1094/PD-89-0185

    • Search Google Scholar
    • Export Citation
  • Jeffers, S., Schnabel, G. & Smith, J. 2004 First report of resistance to mefenoxam in Phytophthora cactorum in the United States and elsewhere Plant Dis. 88 576 https://doi.org/10.1094/PDIS.2004.88.5.576A

    • Search Google Scholar
    • Export Citation
  • Kanungo, M. & Joshi, J. 2014 Impact of pyraclostrobin (F-500) on crop plants Plant Sci. Today 1 174 178 https://doi.org/10.14719/pst.2014.1.3.60

  • Lecomte, C., Alabouvette, C., Edel-Hermann, V., Robert, F. & Steinberg, C. 2016 Biological control of ornamental plant diseases caused by Fusarium oxysporum: A review Biol. Control 101 17 30 https://doi.org/10.1016/j.biocontrol.2016.06.004

    • Search Google Scholar
    • Export Citation
  • McGrath, M.T. 2004 What are fungicides The Plant Health instructor 10 109 115 https://doi.org/10.1094/PHI-I-2004-0825-01

  • National Agricultural Statistics Service (NASS) 2020 2019 census of horticultural specialties 2017 census of agriculture. 8 Dec. 2021. <https://www.nass.usda.gov/Publications/AgCensus/2017/Online_Resources/Census_of_Horticulture_Specialties/HORTIC.pdf>

    • Search Google Scholar
    • Export Citation
  • Neupane, K., Alexander, L. & Baysal-Gurel, F. 2021 Management of Phytophthora cinnamomi using fungicides and host plant defense inducers under drought conditions: A case-study of flowering dogwood Plant Dis. 106 475 485 https://doi.org/10.1094/PDIS-04-21-0789-RE

    • Search Google Scholar
    • Export Citation
  • Panth, M., Baysal-Gurel, F., Simmons, T., Addesso, K.M. & Witcher, A. 2020 Impact of winter cover crop usage in soilborne disease suppressiveness in woody ornamental production system Agron. 10 995 https://www.mdpi.com/2073-4395/10/7/995#

    • Search Google Scholar
    • Export Citation
  • Parajuli, M., Panth, M., Gonzalez, A., Addesso, K.M., Witcher, A., Simmons, T. & Baysal-Gurel, F. 2022 Cover crop usage for the sustainable management of soilborne diseases in woody ornamental nursery production system Can. J. Plant Pathol. 44 432 452 https://doi.org/10.1080/07060661.2021.2020336

    • Search Google Scholar
    • Export Citation
  • Parke, J.L. & Grünwald, N.J. 2012 A systems approach for management of pests and pathogens of nursery crops Plant Dis. 96 1236 1244 https://doi.org/10.1094/PDIS-11-11-0986-FE

    • Search Google Scholar
    • Export Citation
  • Raaijmakers, J.M., Paulitz, T.C., Steinberg, C., Alabouvette, C. & Moënne-Loccoz, Y. 2009 The rhizosphere: A playground and battlefield for soilborne pathogens and beneficial microorganisms Plant Soil 321 341 361 https://doi.org/10.1007/s11104-008-9568-6

    • Search Google Scholar
    • Export Citation
  • van West, P., Appiah, A.A. & Gow, N.A. 2003 Advances in research on oomycete root pathogens Physiol. Mol. Plant Pathol. 62 99 113 https://doi.org/10.1016/S0885-5765(03)00044-4

    • Search Google Scholar
    • Export Citation
  • Yang, C., Hamel, C., Vujanovic, V. & Gan, Y. 2011 Fungicide: Modes of action and possible impact on nontarget microorganisms Int. Sch. Res. Notices 2011 https://doi.org/10.5402/2011/130289

    • Search Google Scholar
    • Export Citation

Contributor Notes

This project was funded by the National Institute of Food and Agriculture (NIFA), United States Department of Agriculture (USDA) Evans-Allen grant under award numbers TENX-1926-CCOCP and TENX-S-1083. We thank Terri Simmons and Christina Jennings for their help with the experimental setup.

Mention of trade names of commercial products in the publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by Tennessee State University.

F.B.G. is the corresponding author: E-mail: fbaysalg@tnstate.edu.

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  • View in gallery
    Fig. 1.

    Means (±se) of Phytophthora root rot disease severity (%) of red maple plants treated with fungicides and biofungicides (trial 1 and trial 2) under greenhouse conditions. Values are the means per plant for six single-plant replicates. Different lowercase letters on the top of the bar denote significant difference at P ≤ 0.05. A one-way analysis of variance was used to evaluate treatment effects. When the effects were significant, Fisher’s least significant difference test was used for mean comparisons with α = 0.05. Disease severity of red maple was determined based on a scale of 0% to 100% roots damaged. Trichoderma harzianum plus T. virens, Bacillus amyloliquefaciens, and Bacillus spp. plus T. harzianum are biofungicides. The other treatments are fungicides. HA + PA = hydrogen peroxide plus peroxyacetic acid.

  • View in gallery
    Fig. 2.

    Means (±se) of Phytophthora pathogen recovery (%) of red maple plants roots treated with fungicides and biofungicides (trial 1 and trial 2) under greenhouse conditions. Values are the means per plant for six single-plant replicates. Different lowercase letters on the top of the bar denote significant difference at P ≤ 0.05. A one-way analysis of variance was used to evaluate treatment effects. When the effects were significant, Fisher’s least significant difference test was used for mean comparisons with α = 0.05. The pathogen recovery percentage in plant roots was determined by culturing ten randomly selected root pieces (≈1 cm long) cut from the root tips on Phytophthora selective medium (PARPH-V8). Trichoderma harzianum plus T. virens, Bacillus amyloliquefaciens, and Bacillus spp. plus T. harzianum are biofungicides. The other treatments are fungicides. HA + PA = hydrogen peroxide plus peroxyacetic acid.

  • View in gallery
    Fig. 3.

    Means (±se) of Rhizoctonia root rot disease severity (%) of red maple plants treated with fungicides and biofungicides (trial 1 and trial 2) under greenhouse conditions. Values are the means per plant for six single-plant replicates. Different lowercase letters on the top of the bar denote significant difference at P ≤ 0.05. A one-way analysis of variance was used to evaluate treatment effects. When the effects were significant, Fisher’s least significant difference test was used for mean comparisons with α = 0.05. Disease severity of red maple was determined based on a scale of 0% to 100% roots damaged. Trichoderma harzianum plus T. virens, Bacillus amyloliquefaciens, and Bacillus spp. plus T. harzianum are biofungicides. The other treatments are fungicides. HA + PA = hydrogen peroxide plus peroxyacetic acid.

  • View in gallery
    Fig. 4.

    Means (±se) of Rhizoctonia pathogen recovery (%) of red maple plant roots treated with fungicides and biofungicides (trial 1 and trial 2) under greenhouse conditions. Values are the means per plant for six single-plant replicates. Different lowercase letters on the top of the bar denote significant difference at P ≤ 0.05. A one-way analysis of variance was used to evaluate treatment effects. When the effects were significant, Fisher’s least significant difference test was used for mean comparisons with α = 0.05. Pathogen recovery percentages of plant roots were determined by culturing ten randomly selected root pieces (≈1 cm long) cut from the root tips on Rhizoctonia semi-selective medium. Trichoderma harzianum plus T. virens, Bacillus amyloliquefaciens, and Bacillus spp. plus T. harzianum are biofungicides. The other treatments are fungicides. HA + PA = hydrogen peroxide plus peroxyacetic acid.

  • Agrios, G.N. 1969 Plant pathology Plant Pathol. Acad. Press San Diego, California 390

  • Ajayi-Oyetunde, O.O. & Bradley, C.A. 2018 Rhizoctonia solani: Taxonomy, population biology and management of rhizoctonia seedling disease of soybean Plant Pathol. 67 3 17 https://doi.org/10.1111/ppa.12733

    • Search Google Scholar
    • Export Citation
  • Baibakova, E.V., Nefedjeva, E.E., Suska-Malawska, M., Wilk, M., Sevriukova, G.A. & Zheltobriukhov, V.F. 2019 Modern fungicides: Mechanisms of action, fungal resistance and phytotoxic effects Annu. Res. Rev. Biol. 32 1 16 https://doi.org/10.9734/arrb/2019/v32i330083

    • Search Google Scholar
    • Export Citation
  • Barnard, E. & Mitchell, D.J. 1993 Phytophthora basal canker of red maple Fla. Department Agric. & Consumer Services, Division of Plant Industry. https://www.fdacs.gov/content/download/11368/file/pp361.pdf

    • Search Google Scholar
    • Export Citation
  • Baysal-Gurel, F. & Kabir, N. 2018 Comparative performance of fungicides and biocontrol products in suppression of Rhizoctonia root rot in viburnum J. Plant Pathol. Microbiol. 9 451 https://doi.org/10.4172/2157-7471.1000451

    • Search Google Scholar
    • Export Citation
  • Baysal-Gurel, F. & Kabir, N. 2019 Evaluation of fungicides and biocontrol products for the control of Phytophthora root rot of hydrangeas Arch. Phytopathol. Pflanzenschutz 52 481 496 https://doi.org/10.1080/03235408.2019.1648023

    • Search Google Scholar
    • Export Citation
  • Bienapfl, J. & Balci, Y. 2014 Movement of Phytophthora spp. in Maryland’s nursery trade Plant Dis. 98 134 144 https://doi.org/10.1094/PDIS-06-13-0662-RE

    • Search Google Scholar
    • Export Citation
  • Brown, M.S., Baysal-Gurel, F., Oliver, J.B. & Addesso, K.M. 2019 Evaluation of fungicides and biofungicide to control Phytophthora root rot (Phytophthora cinnamomi Rands) and ambrosia beetles (Coleoptera: Curculionidae: Scolytinae) on flowering dogwoods exposed to simulated flood events Crop Prot. 124 104834 https://doi.org/10.1016/j.cropro.2019.05.028

    • Search Google Scholar
    • Export Citation
  • Cline, E.T., Farr, D.F. & Rossman, A.Y. 2008 A synopsis of Phytophthora with accurate scientific names, host range, and geographic distribution Plant Health Prog. 9 32 https://doi.org/10.1094/PHP-2008-0318-01-RV

    • Search Google Scholar
    • Export Citation
  • Cohen, Y., Rubin, A.E. & Galperin, M. 2018 Oxathiapiprolin-based fungicides provide enhanced control of tomato late blight induced by mefenoxam-insensitive Phytophthora infestans PLoS One 13 e0204523 https://doi.org/10.1371/journal.pone.0204523

    • Search Google Scholar
    • Export Citation
  • Erwin, D.C., Bartinicki, S.C. & Tsao, P.H.T. 1983 Phytophtora. Its biology, taxonomy, ecology, and pathology Amer. Phytopathol. Soc.

  • Erwin, D.C. & Ribeiro, O.K. 1996 Phytophthora diseases worldwide Amer. Phytopathol. Soc. (APS Press)

  • Ferguson, A. & Jeffers, S. 1999 Detecting multiple species of Phytophthora in container mixes from ornamental crop nurseries Plant Dis. 83 1129 1136 https://doi.org/10.1094/PDIS.1999.83.12.1129

    • Search Google Scholar
    • Export Citation
  • Fungicide Resistance Action Committee 2021 FRAC code list 2020: Fungicides sorted by mode of action (including FRAC code numbering) 8 Dec. 2021. <https://www.frac.info/docs/default-source/publications/frac-code-list/frac-code-list-2021–final.pdf?sfvrsn=f7ec499a_2>

    • Search Google Scholar
    • Export Citation
  • Garbelotto, M., Frankel, S. & Scanu, B. 2018 Soil-and waterborne Phytophthora species linked to recent outbreaks in Northern California restoration sites Calif. Agr. 72 208 216 https://doi.org/10.3733/ca.2018a0033

    • Search Google Scholar
    • Export Citation
  • Gardener, B.B.M. & Fravel, D.R. 2002 Biological control of plant pathogens: Research, commercialization, and application in the USA Plant Health Prog. 3 17 https://doi.org/10.1094/PHP-2002-0510-01-RV

    • Search Google Scholar
    • Export Citation
  • Gutierrez, W., Shew, H. & Melton, T. 2001 A semi-selective medium to isolate Rhizoctonia solani from soil and tissue Plant Path. Ext. 1 2

  • Handelsman, J. & Stabb, E.V. 1996 Biocontrol of soilborne plant pathogens Plant Cell 8 1855 https://doi.org/10.1105%2Ftpc.8.10.1855

  • Harman, G.E. 2006 Overview of mechanisms and uses of Trichoderma spp Phytopathology 96 190 194 https://doi.org/10.1094/PHYTO-96-0190

  • Hu, J. & Li, Y. 2014 Inheritance of mefenoxam resistance in Phytophthora nicotianae populations from a plant nursery Eur. J. Plant Pathol. 139 545 555 https://doi.org/10.1007/s10658-014-0410-0

    • Search Google Scholar
    • Export Citation
  • Hwang, J. & Benson, D. 2005 Identification, mefenoxam sensitivity, and compatibility type of Phytophthora spp. attacking floriculture crops in North Carolina Plant Dis. 89 185 190 https://doi.org/10.1094/PD-89-0185

    • Search Google Scholar
    • Export Citation
  • Jeffers, S., Schnabel, G. & Smith, J. 2004 First report of resistance to mefenoxam in Phytophthora cactorum in the United States and elsewhere Plant Dis. 88 576 https://doi.org/10.1094/PDIS.2004.88.5.576A

    • Search Google Scholar
    • Export Citation
  • Kanungo, M. & Joshi, J. 2014 Impact of pyraclostrobin (F-500) on crop plants Plant Sci. Today 1 174 178 https://doi.org/10.14719/pst.2014.1.3.60

  • Lecomte, C., Alabouvette, C., Edel-Hermann, V., Robert, F. & Steinberg, C. 2016 Biological control of ornamental plant diseases caused by Fusarium oxysporum: A review Biol. Control 101 17 30 https://doi.org/10.1016/j.biocontrol.2016.06.004

    • Search Google Scholar
    • Export Citation
  • McGrath, M.T. 2004 What are fungicides The Plant Health instructor 10 109 115 https://doi.org/10.1094/PHI-I-2004-0825-01

  • National Agricultural Statistics Service (NASS) 2020 2019 census of horticultural specialties 2017 census of agriculture. 8 Dec. 2021. <https://www.nass.usda.gov/Publications/AgCensus/2017/Online_Resources/Census_of_Horticulture_Specialties/HORTIC.pdf>

    • Search Google Scholar
    • Export Citation
  • Neupane, K., Alexander, L. & Baysal-Gurel, F. 2021 Management of Phytophthora cinnamomi using fungicides and host plant defense inducers under drought conditions: A case-study of flowering dogwood Plant Dis. 106 475 485 https://doi.org/10.1094/PDIS-04-21-0789-RE

    • Search Google Scholar
    • Export Citation
  • Panth, M., Baysal-Gurel, F., Simmons, T., Addesso, K.M. & Witcher, A. 2020 Impact of winter cover crop usage in soilborne disease suppressiveness in woody ornamental production system Agron. 10 995 https://www.mdpi.com/2073-4395/10/7/995#

    • Search Google Scholar
    • Export Citation
  • Parajuli, M., Panth, M., Gonzalez, A., Addesso, K.M., Witcher, A., Simmons, T. & Baysal-Gurel, F. 2022 Cover crop usage for the sustainable management of soilborne diseases in woody ornamental nursery production system Can. J. Plant Pathol. 44 432 452 https://doi.org/10.1080/07060661.2021.2020336

    • Search Google Scholar
    • Export Citation
  • Parke, J.L. & Grünwald, N.J. 2012 A systems approach for management of pests and pathogens of nursery crops Plant Dis. 96 1236 1244 https://doi.org/10.1094/PDIS-11-11-0986-FE

    • Search Google Scholar
    • Export Citation
  • Raaijmakers, J.M., Paulitz, T.C., Steinberg, C., Alabouvette, C. & Moënne-Loccoz, Y. 2009 The rhizosphere: A playground and battlefield for soilborne pathogens and beneficial microorganisms Plant Soil 321 341 361 https://doi.org/10.1007/s11104-008-9568-6

    • Search Google Scholar
    • Export Citation
  • van West, P., Appiah, A.A. & Gow, N.A. 2003 Advances in research on oomycete root pathogens Physiol. Mol. Plant Pathol. 62 99 113 https://doi.org/10.1016/S0885-5765(03)00044-4

    • Search Google Scholar
    • Export Citation
  • Yang, C., Hamel, C., Vujanovic, V. & Gan, Y. 2011 Fungicide: Modes of action and possible impact on nontarget microorganisms Int. Sch. Res. Notices 2011 https://doi.org/10.5402/2011/130289

    • Search Google Scholar
    • Export Citation
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