© 2011 Plant Management Network.
Efficacy of Fungicides and Biopesticides for Management of Phytophthora Crown and Root Rot of Gerber Daisy
D. M. Benson and K. C. Parker, Department of Plant Pathology, North Carolina State University, Raleigh, NC 27695
Benson, D. M., and Parker, K. C. 2011. Efficacy of fungicides and biopesticides for management of Phytophthora crown and root rot of Gerber daisy. Online. Plant Health Progress doi:10.1094/PHP-2011-0512-01-RS.
Several fungicides and biopesticides were evaluated for control of Phytophthora crown and root rot of Gerber daisy caused by P. cryptogea, a frequently encountered pathogen in greenhouse production. In greenhouse trials, biopesticides were applied 3 to 5 days before inoculation with P. cryptogea, while fungicides were applied at the time of inoculation. Efficacy of the treatments was assessed according to fresh plant top weights and root rot ratings at the end of experiments. Phosphite salt fungicides such as AgriFos, Aliette, Alude, Magellan and Vital sprayed to run off prior to inoculation were ineffective. Similarly, the strobulurins (Disarm, Heritage, and Insignia) as a drench and the biopesticides (Muscodor albus, Remedier, and Taegro) incorporated or as a drench failed to prevent root and crown rot and collapse of plants. Adorn as a drench at 2 fl oz/100 gal prevented Phytophthora crown and root rot in two of three trial years. Fenstop as a drench at 14 fl oz/100 gal or Orvego as a drench at rates of 22.5 to 34 fl oz/100 gal consistently controlled disease in three years of trials. Segway as a drench at 6 fl oz/100 gal varied in efficacy but in all trials, disease development was less than the non-treated, inoculated control. Because the effective fungicides are in different Fungicide Resistance Action Committee codes, growers have valuable rotation options for managing crown and root rot caused by P. cryptogea on Gerber daisy and avoiding pathogen resistance in the Phytophthora populations.
Gerbera jamesonii Bolus ex Hook., known by the common names Gerber daisy, Transvaal daisy, and Barberton daisy, is a popular floral crop grown both as a potted plant and for cut flower production. Gerber daisy, also sold as a perennial, is hardy in USDA Zones 9 to 11, and some cultivars will re-grow each year from the roots in colder zones. In greenhouse production, P. cryptogea, P. drechsleri, P. nicotianae and P. palmivora have been associated with root and crown rot of Gerber daisy (3,4,11). The first report of the disease in the United States was from California in the mid-1930s and implicated P. cryptogea (12). More recently, P. cryptogea was recovered from Gerber daisy at two greenhouse locations in North Carolina (11). Phytophthora cryptogea also has been isolated from Gerber daisy in Australia, Bulgaria, China, France, Germany, Greece, Korea, New Zealand, and Poland (4).
One of the plant pathology priorities in the national IR4 Ornamental Horticulture Program is new fungicide chemistries for Phytophthora management. Since P. cryptogea is such a devastating pathogen on Gerber daisy and is prevalent in North Carolina, we investigated the efficacy of new and standard fungicides and biopesticides to prevent infection of plants growing in artificially-infested potting mix in IR4 trials over a 3-year period.
Pathogen, Plant Culture, and Products Tested
Pathogen cultured on rice grains. Isolate 1804 of P. cryptogea, originally isolated from Gerber daisy growing in a North Carolina commercial greenhouse in 1993 (Plant Disease and Insect Clinic, North Carolina State University), was used in all three trials. Inoculum was prepared by culturing the isolate on sterilized rice grains for 9 to 14 days depending on the trial (10). The fungus was cultured from 100% of the rice grains sampled after the colonization period prior to inoculation.
Gerber daisy transplanted and grown in the greenhouse. Each year small, well-rooted plants (plugs) of G. jamesonii Yellow Revolution were obtained from a commercial greenhouse and transplanted into 4-inch plastic pots containing Fafard 4P soilless mix (peat moss, processed pine bark, perlite, vermiculture, starter nutrients, wetting agent and lime; Conrad Fafard Inc., Agawam, MA). Plugs were transplanted 19 March 2007, 8 May 2008, and 26 May 2009 and were then allowed to establish on the greenhouse bench for 31 days (2007 experiment), 22 days (2008 experiment), or 5 days (2009 experiment), respectively, before applying test treatments described below. In 2007 and 2008 extra pots of mix without plants were set up for Muscador albus treatments as described below. After transplanting, for the remainder of the experiments, plants received 9.6 fl oz drip irrigation per pot per day and were fertilized weekly with Peters soluble 20-10-20 at 200 ppm-N (The Scotts Company, Marysville, OH).
Fungicides and biopesticides tested. Phosphite salt fungicides (Agri-Fos 46%L, 64 fl oz/100 gal; Aliette 80WP, 80 oz/100 gal; Alude 46%L, 12.7 fl oz/100 gal; Biophos 43%L, 64 fl oz/100 gal; Magellan 53.7%L 12 or 64 fl oz/100 gal; and Vital 55%L, 64 fl oz/100 gal) were applied as foliar sprays to run-off with a hand-pressurized sprayer 5 days (2007, 2008) or 3 days (2009) before inoculation. The biopesticides, Remedier (Trichoderma harzianum and T. viride) and Taegro (Bacillus subtilis var. amyloliquefaciens), were drenched at 7.5 oz and 3.5 oz per 100 gal, respectively (3.4 fl oz per pot) 5 days or 3 days before inoculation. At inoculation, a single rice grain that had been colonized for 12 days (2007), 14 days (2008), or 9 days (2009) by isolate 1804 of P. cryptogea was placed in the root zone of each plant. The other fungicide treatments included: Adorn 4L (fluopicolide) at 1, 2, or 4 fl oz/100 gal; Disarm 480SC (fluoxastrobin) at 3, 4, or 8 fl oz/100 gal; Fenstop 500SC (fenamidone) at 7 or 14 fl oz/100 gal; Heritage 50 WP (azoxystrobin) at 0.9 or 1.8 oz/100 gal; Insignia 20WP (pyraclostrobin) at 8 oz/100 gal; NOA446510 250SC (mandipropamid) at 4 or 8 fl oz/100 gal; Orvego 525SC (ametoctradin + dimethomorph, BAS651) at 22.5 or 34 fl oz/100 gal; Segway 400SC (cyazofamid) at 3 or 6 fl oz/100 gal; Stature 500SC (dimethomorph) at 6.12 fl oz/100 gal; Subdue MAXX 21.3%EC (mefenoxam) at 1 fl oz/100 gal; and Tanos 50WDG (famoxadone + cymoxanil) at 12 oz/100 gal) were applied as drenches at 3.4 fl oz per pot within a 4-hour period after inoculation. Fungicides were re-applied once (2007, 2008) or twice (2009) at 14-day intervals. Additional applications were not made since untreated, inoculated plants wilted within 7 to 10 days of inoculation and were dead within 21 days in most trials.
In two trials (2007 and 2008), the biopesticide Muscador albus QST20799 was tested. The formulation was incorporated at a rate of 1.2 oz/dry gal of moist Fafard 4P mix in the pots that had not yet received the Gerber daisy transplants. The soil in each of these pots was infested with a single rice grain colonized by P. cryptogea immediately after the Muscador treatment, which coincided with the time of plant inoculation in the other treatments. After a 5-day incubation period under drip irrigation on the greenhouse bench, a Gerber daisy transplant was up rooted from the media in the original transplant pot and re-potted in the Muscador treated mix.
In all of the IR4 experiments, treatments included a non-treated, inoculated control and a non- treated, non-inoculated control. In the 2007 and 2008 experiments, there were four replications per treatment with two pots per replication. In the 2009 experiment there were eight replications per treatment, with two pots per replication. All experiments had a randomized complete block design on a greenhouse bench. Greenhouse air temperature averaged 81, 83, and 85°F for the 2007, 2008, and 2009 experiments, respectively. No supplemental lighting was provided.
In addition to the IR4 trials described above, three supplementary trials were conducted, two in 2009 (one transplanted 5 February and inoculated and drenched on 6 March, and the second transplanted 26 May, inoculated and drenched 5 June) and one in 2010 (transplanted 6 May and inoculated and drenched 18 May). The supplementary trials evaluated efficacy of Orvego rates from 11 to 67.3 fl oz/100 gal applied as a drench and used the methods and conditions described for the IR4 trials above. For each trial there were four replications of each treatment and two pots per replication arranged in a randomized complete block design on the greenhouse bench with drip irrigation. The same cultivar of G. jamesonii Yellow Revolution and the same isolate of P. cryptogea were used.
Disease assessment and statistical analysis. At harvest on 21 May 2007 (day 27 after inoculation), 1 July 2008 (day 27 after inoculation) or 9 July 2009 (day 34 after inoculation), the top fresh weight was measured and the severity of root rot was scored for all plants (Fig. 1). Data for fresh top weight were expressed as percent of the non-treated, non-inoculated control to facilitate comparisons across trials because mean plant weight in the non-treated, non-inoculated control varied by trial. Plants with a healthy, light-brown root system and root ball that filled the pot volume were rated 1, root systems with up to 25% of the roots necrotic were rated 2, root systems with 26 to 50% of the roots necrotic were rated 3, root systems with 51 to 75% were rated 4, and plants that died with all roots necrotic were rated 5. All data were analyzed by analysis of variance with PROC GLM (SAS Institute Inc., Cary, NC). In experiments that had significant treatment effects, means were separated by a Waller-Duncan K-ratio t-test (P = 0.05).
Phytophthora Crown and Root Rot Development
In our experiments with Gerber daisy Yellow Revolution, Phytophthora crown and root rot caused by P. cryptogea was a fast-developing disease; wilted plants were observed within 7 to 10 days of inoculation if the plants were left untreated. Initial symptoms of Phytophthora crown and root rot in Gerber daisy included slightly chlorotic leaves with darkened mid-rib and veins followed within a few days by flaccid, dried-out leaves. In the non-treated, inoculated control the mean root rot rating was 5.0 in 2007 and 2008 and 4.8 in 2009; mean top weights of the non-treated, inoculated control were 5 to 18% of the non-treated, non-inoculated control. Over the three IR4 trials, root rot rating and top weight as a percent of the non-treated, non-inoculated control over all treatments were highly correlated (r = -0.98).
Responses to phosphite fungicides. The phosphite generating fungicides, which were sprayed to run-off 3 to 5 days prior to inoculation because they may induce a host resistance response in combination with direct toxicity towards the pathogen, were ineffective (Fig. 2). None of the tested materials protected Gerber daisy from infection by P. cryptogea as root rot ratings were above 4 in all cases except Vital (3.6) in the 2008 trial (Fig. 2A), and top weights were generally only 5 to 30% of the non-treated, non-inoculated control (Fig. 2B).
Previously, another pathogen of Gerber daisy, P. drechsleri, which is closely related to P. cryptogea (13), was partially controlled with a 3-day post-inoculation drench application of Alude at 12.85 fl oz/100 gal (9). In another pathosystem with Phytophthora root rot of azalea caused by P. cinnamomi, phosphite fungicides were quite effective in prevention of disease (1). The difference in activity may be due to slower disease development over weeks in the latter pathosystem compared to rapid disease development over days in the Gerber daisy, P. cryptogea pathosystem.
Responses to strobulurin fungicides. As a class, the strobulurin fungicides did not demonstrate adequate disease control for P. cryptogea on Gerber daisy (Fig. 3). The mean root rot ratings for Disarm at 8 fl oz/100 gal were less (P ≤ 0.05) than that for the non-treated, inoculated controls in both the 2008 and 2009 trials, but this treatment was of little value because plants with ratings > 3 would be unsaleable (Fig. 3A). The top weights of Gerber daisy treated with Disarm were only 7 to 53% of those for plants in the non-treated, non-inoculated control, regardless of the rate applied (Fig. 3B). Gerber daisy plants treated with drenches of Heritage at 0.9 and 1.8 oz/100 gal were not protected from crown and root rot in either of two trials (Fig. 3A), and top weights of Heritage-treated plants were less than 40% of plants in the non-treated, non-inoculated control (Fig. 3B). Insignia at 8 oz/100 gal was ineffective in prevention of crown and root rot over all three trials (Fig 3A), and top weights of treated plants were 30% or less of plants in the non-treated, non-inoculated control (Fig. 3B). The standard fungicide, Subdue MAXX at 1 fl oz/100 gal did not protect Gerber daisy from crown and root rot caused by P. cryptogea in the 2007 trial, but it did so in the 2008 and 2009 trials as root rot ratings were not different (P ≤ 0.05) from those of the non-treated, non-inoculated control (Fig. 3A), and top weights of plants in 2008 and 2009 trials were comparable to the non-treated, non-inoculated control (Fig 3B).
In previous trials involving P. drechsleri on Gerber daisy and poinsettia, results generally were similar to those described above for P. cryptogea on Gerber daisy. For example, Disarm was ineffective at 4 or 8 fl oz/100 gal for P. drechsleri on Gerber daisy (2). Similarly, Heritage at the same rates as used above for P. cryptogea was ineffective for control of P. drechsleri on poinsettia (8). However, Heritage at 0.9 or 1.8 oz/100 gal was highly effective in control of P. drechsleri on Gerber daisy (9). On Gerber daisy and poinsettia, Insignia at 8 oz/100 gal was ineffective in control of P. drechsleri (2,8).
Responses to biopesticides. The biopesticides provided little or no control of disease (Fig. 4). Remedier at 2 or 7.5 oz/100 gal and Taegro at 3.5 oz/100 gal applied as drenches 3 to 5 days prior to inoculation and then at 14-day intervals did not prevent development of Phytophthora crown and root rot in Gerber daisy (Fig. 4A). Top weights of plants treated with Remedier and Taegro were less than 20% of the weight of plants in the non-treated, non-inoculated control (Fig. 4B). In general, biopesticides have been most effective in pathosystems where disease pressure is moderate to low (personal observations). In the aggressive P. cryptogea-Gerber daisy pathosystem, it is possible that the host is overwhelmed before the biocontrol agents can be effective. Muscodor albus was incorporated only once as a pre-plant treatment with infested potting mix 5 days prior to transplanting Gerber daisy. In both the 2007 and 2008 trials, pre-plant treatment with M. albus failed to eradicate the inoculum as subsequent development of crown and root rot in Gerber daisy was severe (Fig. 4A).
Responses to new fungicide chemistries. For some of the new fungicide chemistries, control of Phytophthora crown and root rot of Gerber daisy caused by P. cryptogea was rate dependent (Fig. 5). Adorn provided promising but variable results. Root rot ratings for Gerber daisy treated with Adorn (fluopicolide) at 2 fl oz/100 gal in two of three trials were less (P ≤ 0.05) than the rating for plants in the non-treated, inoculated control and not different than (P ≤ 0.05) the rating for plants in the non-treated, non-inoculated control (Fig. 5A). Adorn at 1 fl oz/100 gal also was inconsistent between trials for prevention of Phytophthora crown and root rot. At 4 fl oz/100 gal root rot ratings for plants treated with Adorn were less (P ≤ 0.05) than the non-treated, inoculated control but greater than (P ≤ 0.05) ratings for plants in the non-treated, non-inoculated control (Fig. 5A). No phytotoxicity symptoms were observed at any rate of Adorn tested. In other trials, Adorn at 1 or 2 fl oz/100 gal protected Gerber daisy and poinsettia from P. drechsleri (8,9).
Fenstop reduced severity of disease in all trials (Fig. 5). Gerber daisy treated with 14 fl oz of Fenstop (fenamidone) per 100 gal had root rot ratings that ranged from 1.0 to 1.3 in each of the three trials, which did not differ significantly (P ≤ 0.05) from the ratings for plants in the non-treated, non-inoculated control (Fig. 5A). Top weights of Gerber daisy treated with 14 fl oz/100 gal of Fenstop were equivalent to top weights of plants in the non-treated, non-inoculated control in two trials and were 27% greater (P ≤ 0.05) than the non-treated, non-inoculated control plants in the 2008 trial (Fig. 5B). At 7 fl oz/100 gal, the Fenstop root rot rating for treated plants was 1.5 and top weight was 102% of the non-treated, non-inoculated control (Fig. 5). No phytotoxicity was observed on Gerber daisy treated with Fenstop at 14 fl oz/100 gal in any trial conducted. In previous reports, Fenstop at 14 fl oz/100 gal controlled Phytophthora root rot in Gerber daisy and poinsettia caused by P. drechsleri; however, at the 7 fl oz rate Gerber daisy was protected while plant mortality was 33% in poinsettia (8,9).
Segway reduced severity of disease caused by P. cryptogea on Gerber daisy in some trials, and the high rate tested was more effective than the low rate. At 3 fl oz/100 gal of Segway, the root rot rating for treated plants was 4.3 in the 2007 trial and 1.0 in the 2008 trial with top weight of treated plants 22 and 118%, respectively, of the non-treated, non-inoculated control (Fig. 5). Segway at 6 fl oz/100 gal was more consistent in preventing root rot with ratings of 2.5 (2007 trial), 1.0 (2008 trial), and 2.5 (2009) all of which were less than (P ≤ 0.05) the non-treated, inoculated control (Fig. 5A). Top weight of plants treated at 6 fl oz/100 gal of Segway were less than (P ≤ 0.05) the mean weight for plants in the non-treated, inoculated control in the 2007 and 2009 trial but greater than (P ≤ 0.05) the non-treated, non-inoculated control in the 2008 trial (Fig. 5B). No phytotoxicity was observed on plants treated with Segway at 6 fl oz/100 gal in any trial conducted. In other trials, Segway known by the trade name Ranman on agronomic crops, was variable in control of P. drechsleri depending on rate (2,5,6,7,8). At 0.75 or 1 fl oz/100 gal Ranman did not control P. drechsleri on poinsettia (5), but at 3 or 6 fl oz/100 gal Segway was very effective in control P. drechsleri on calibrachoa (6) on poinsettia (7,8) and on Gerber daisy (2).
In two trials, mandipropamid at 8 fl oz/100 gal was inconsistent in preventing crown and root rot with ratings of 1.4 in the 2007 trial and 4.9 in the 2008 trial (Fig. 5A). Corresponding top weights at the 8 fl oz/100 gal rate of mandipropamid were 101% of the mean weight of plants in the non-treated, non-inoculated control for the 2007 trial but only 27% of the top weight of the non-treated, non-inoculated control plants in the 2008 trial (Fig. 5B). Plants treated with mandipropamid at 4 fl oz/100 gal had a mean root rot rating of 4.6 a value that was not different than (P ≤ 0.05) the non-treated, inoculated control (Fig. 5A).
Responses to combination products. The two combination fungicides tested, Tanos and Orvego, gave mixed results. Tanos (famoxadone + cymoxanil) at 12 oz/100 gal resulted in plants with root rot ratings of 4.9 and 3.7 in the 2008 and 2009 trials, respectively (data not shown). Corresponding top weights for Tanos-treated plants were 34 and 36% of the mean weight of plants in the non-treated, non-inoculated control (data not shown).
The efficacy of several different rates of Orvego (ametoctradin + dimethomorph, BAS651) was investigated in the 2009 IR4 trial and in three separate but independent trials all under similar greenhouse conditions as described above. At the low rate range of 11 to 14 fl oz Orvego /100 gal, root rot ratings were inconsistent, ranging from 1.0 to 3.0 and top weight of treated plants ranged from 66 to 113% of the mean top weight of plants in the non-treated, non-inoculated control (Table 1). At intermediate rates of Orvego from 22.5 to 34 fl oz/100 gal, root rot ratings ranged from 1.0 to 1.5, values that were not different than (P ≤ 0.05) than those for plants in the non-treated, non-inoculated control. Top weights of plants treated at intermediate rates of Orevgo were not different than (P ≤ 0.05) (range 94 to 115%) weights for plants in the non-treated, non-inoculated control, with the exception of plants treated at 34 fl oz/100 gal in the 2009 trial 2 that were only 78% of the non-treated, non-inoculated control (Table 1). Plants treated at high rates of Orvego (54.8 and 67.3 fl oz/100 gal) had root rot ratings of 1.1 and 1.0 and top weights that were 94 and 96% of the weight of plants in the non-treated, non-inoculated control. In some trials, a marginal chlorosis appeared on leaves after the second application of Orvego. The chlorosis developed on the outer leaf tip as the new growth emerged from the crown of the plant. Chlorosis was most severe at the highest rates of Orvego. Since the chlorosis was not observed in every trial, clonal differences in the cultivar Yellow Revolution received for each trial or different greenhouse temperature ranges from trial to trial may account for the presence or absence of phytotoxicity.
Table 1. Efficacy of Orvego (ametoctradin + dimethomorph, BAS651) for prevention of Phytophthora crown and root rot of Gerbera daisy caused by P. cryptogea.
x Fresh top weight is percent of the non-treated, non-inoculated control for a given trial.
y Root rot rating: 1 = healthy; 2 = 25% or less roots necrotic; 3 = 26 to 50% roots necrotic; 4 = more than 50% necrotic; and 5 = crown rot, plant dead.
z Means within a column and trial followed by the same letter are not different according to the Waller-Duncan k ratio, t-test, k = 100, P = 0.05.
In addition to control of P. cryptogea on Gerber daisy, Orvego has shown promise for control of P. dreschleri, P. cinnamomi, P. tropicalis, and P. nicotianae on rhododendron, English ivy, and pansy (14). Stature (dimethomorph) was used a standard in the Orvego trials since it contains one of the active ingredients in Orvego. At rates of 6.12 or 12.25 fl oz/100 gal plants treated with Stature had root rot ratings that ranged from 1.1 to 3.0 depending on trial and top weights that were 50 to 95% of the weight of plants in the non-treated, non-inoculated control of the corresponding trial (Table 1).
Conclusion and Management Implications
Control of Phytophthora crown and root rot of Gerber daisy caused by P. cryptogea, a highly aggressive pathogen in this pathosystem, requires effective fungicides that protect plant root systems before infection occurs. In the case of the biopesticides, phosphite salt fungicides and strobulurin fungicides tested in this study, none of these products were effective in preventing disease development. Fenstop at 14 fl oz/100 gal was the most consistent fungicide tested across trials for prevention of Phytophthora crown and root rot of Gerber daisy. Adorn at 1 or 2 fl oz/100 gal, and Segway at 3 or 6 fl oz/100 gal were inconsistent in one trial but highly effective in two of three trials. Orvego at intermediate rates of 22.5 to 34 fl oz/100 gal consistently prevented Phytophthora crown and root rot of Gerber daisy and phytotoxicity on cultivar Yellow Revolution was minimal in this rate range. Since many of the new fungicides effective against Phytophthora crown and root rot of Gerber daisy caused by P. cryptogea are in different Fungicide Resistance Action Committee (FRAC) codes, growers have new options for rotation schemes to avoid developing fungicide resistance in the Phytophthora population. For example, Adorn (FRAC 43), Fenstop (FRAC 11), Orvego (FRAC 40 and 45), and Segway (FRAC 21) could all be used in a rotation for multiple Gerber daisy crops. In the first crop cycle two of the four products could be alternated, followed by the other two products in a subsequent crop to avoid over using any one product in the same greenhouse range during a production year. Of course, other low risk fungicides effective against Phytophthora pathogens such as etridiazole and propamocarb could be added to the rotation scheme to reduce the resistance risk even further.
The authors gratefully acknowledge the support of the IR4 Ornamental Horticulture Program, Rutgers, NJ, and that of the North Carolina Agricultural Research Service, North Carolina State University, Raleigh. We would like to thank each of the agricultural chemical companies which provided products for evaluation and Van Wingerden International, Mills River, NC, for supplying the Gerber daisy plugs.
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