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Seasonal Dynamics of Resistance to QoI and DMI Fungicides in Podosphaera xanthii and Impact on Control of Cucurbit Powdery Mildew

Margaret T. McGrath
Department of Plant Pathology, Cornell University
Long Island Horticultural Research and Extension Center
3059 Sound Avenue, Riverhead, New York 11901-1098

ABSTRACT Resistance to QoI (strobilurin) fungicides in Podosphaera xanthii was first detected in the US in 2002. A seedling bioassay was used in 2003 to monitor QoI resistance in cucurbit fields at 10 commercial farms and 1 research facility in Suffolk Co., NY. Not all sites were included in each bioassay. Squash seedlings were dipped in solutions of QoI fungicide (50 mg/L trifloxystrobin formulated as Flint), DMI fungicide (20 mg/L myclobutanil; Nova), or both. About 12 hrs later they were put with nontreated seedlings in fields for up to 1 day, then kept in a greenhouse until severity was rated. On 27 Jul, when mildew was first seen in the area, QoI resistant strains were found in 1 of 5 commercial and research fields with early plantings of summer squash or pumpkin not QoI-treated. On 19-21 Aug, mildew severity in 4 commercial pumpkin fields where QoIs were used averaged 1% on upper leaf surfaces and 11% on lower surfaces. On 31 Aug, QoI resistance was common in these fields, 2 other pumpkin fields, and a winter squash experiment (61 to 100% frequency). Nova but no QoIs was used in 1 field. Moderate DMI insensitivity occurred in all fields (12 to 56%). Severity then exceeded 50% on most lower leaf surfaces. On 25 Sep, QoI resistance was detected in 3 commercial pumpkin fields where no QoIs or DMIs were used (2, 38, and 56%) and in fields where QoIs and/or DMIs were used (88 to 97%). In summary, QoI resistant strains were present at mildew onset, their frequency increased greatly during the season, efficacy was affected, and they occurred in crops not treated with QoIs.

INTRODUCTION Powdery mildew is the most common disease of cucurbit crops throughout the world and fungicides with systemic or translaminar activity play a critical role in managing this disease. These fungicides are better than contact fungicides for controlling powdery mildew because they are effective on the underside of leaves. Conditions are more favorable for disease development on the underside than on upper leaf surfaces (Figure 1).

Fungicide resistance is a major concern with cucurbit powdery mildew. Unfortunately, most systemic and translaminar fungicides are at risk for resistance development because they have a single-site mode of action. Three chemical classes of this type are registered for this disease in the US: benzimidazoles, quinone outside inhibitors (QoIs, a.k.a. strobilurins), and demethylation inhibitors (DMIs). The cucurbit powdery mildew fungus, Podosphaera xanthii, has demonstrated a high potential for developing resistance (McGrath 2001). Presence of resistant strains has been associated with control failure. In the US and in many other areas of the world, this pathogen has developed resistance to all three chemical classes. Most recently, resistance to QoI fungicides was detected in 2002 (McGrath and Shishkoff 2003). Cross resistance has been documented among QoI fungicides.

As long as QoI-resistant strains of P. xanthii are not common, QoI fungicides will continue to be important tools for managing both cucurbit powdery mildew and resistance to other groups of fungicides with high resistance risk. Resistance has already developed to the benzimidazoles and DMIs. Resistance to the benzimidazoles and the QoIs is qualitative. Thus isolates of the cucurbit powdery mildew fungus are typically either sensitive or highly resistant. Highly resistant strains cannot be effectively controlled with the fungicide. Benzimidazoles are rarely being used for cucurbit powdery mildew in the US due to resistance and to the introduction of more effective DMIs and QoIs.

Resistance to DMIs is quantitative. With this type of resistance, strains of the pathogen exhibit a range in sensitive to the effects of the fungicide. Strains with low sensitivity can often be controlled as well as fully sensitive strains wild-type by applying a DMI fungicide at high rate and/or short interval, or by selecting an inherently more active DMI fungicide. In the US, resistance to DMIs in the cucurbit powdery mildew pathogen is such that the first active ingredient registered, triadimefon, is no longer effective, while myclobutanil and triflumizole are still effective at high rates. DMIs should not be used exclusively when QoI fungicides are effective as this will put an undesirable amount of pressure on the powdery mildew pathogen population. Exclusive use of one mode of action will select for strains with a higher level of resistance.

If growers are to manage fungicides wisely, they need information from their area on the proportion of the pathogen population that is resistant before they make the first application. Because early spring-planted summer squash typically becomes infected with powdery mildew before main-season crops in the same area, the early crops can be used to determine the composition of the pathogen population for later planted pumpkin, gourd, winter squash and melon. If QoI-resistant strains are found to be uncommon in these early crops, then these fungicides will be recommended for use with other fungicides in a resistance management program.

The recommended weekly fungicide program for 2003 was a QoI fungicide plus a contact fungicide applied in alternation with a DMI fungicide plus a contact. The threshold level for starting applications was one infected leaf of 50 old leaves examined. The program has two strategies for managing resistance:

1. Alternation among systemic/translaminar fungicides in at least two chemical classes, and
2. Inclusion of contact multi-site mode of action fungicides.

MATERIALS AND METHODS An in-field seedling bioassay was used in 2003 to determine the fungicide sensitivity of the powdery mildew fungal pathogen population in cucurbit fields at 10 commercial farms and at the Cornell University Long Island Horticultural Research and Extension Center (LIHREC) in Suffolk County, NY. Suffolk is in the eastern portion of Long Island. Not all sites were included in each bioassay. Three early crops of zucchini and yellow summer squash that had not been sprayed with QoI or DMI fungicides were identified for the first bioassay. Two early plantings of pumpkin that had not been treated with fungicides were also selected for this bioassay because powdery mildew was observed in these plants in late July at the same time symptoms were first observed in the squash plants. The first bioassay was conducted at these five sites on 27 July (Table 1). Another bioassay was conducted on 31 Aug in six commercial pumpkin fields and a winter squash experiment at LIHREC after QoI and/or DMI fungicides were used in these fields (Table 2). Powdery mildew severity was assessed in some of these fields before the bioassay was conducted and again at the time of the bioassay. A third assay conducted on 25 Sep included pumpkin fields where no QoI or DMI fungicides were used (Table 2).

The seedling bioassay entailed placing fungicide-treated seedlings in a field of cucurbits with powdery mildew (Figure 2). Summer squash seedlings were grown in a growth chamber. Their growing point and unexpanded leaves were removed just before treatment. Seedlings varied in size from 1 to 9 true leaves. Treatments were no fungicide, QoI fungicide (50 mg/L trifloxystrobin formulated as Flint), DMI fungicide (20 mg/L myclobutanil; Nova), and a combination of the QoI and DMI fungicides. Seedlings were dipped in the fungicide solutions, then allowed to dry overnight before setting in a cucurbit crop in groups of four plants with the four treatments. There were 2 to 7 groups per field. After being in fields for 4 to 22 hours, seedlings were kept in a greenhouse until symptoms of powdery mildew were visible, which took at least one week. Then severity (percent tissue with symptoms) was visually estimated for each leaf on a 0 to 100% continuous scale. Frequency of resistant pathogen strains in a field was estimated by calculating the ratio of severity on fungicide-treated plants relative to non-treated plants for each group, then determining the field average.

The fungicide concentrations used were found to be good discriminating concentrations in previous studies (McGrath et, al, 1996, McGrath and Shishkoff 2003). Isolates able to tolerate 50 mg/L trifloxystrobin are considered to be resistant to QoI fungicides. These isolates were common in fungicide efficacy experiments where QoI fungicides were not as effective as in previous experiments at the same site. Isolates able to tolerate 20 mg/L myclobutanil are considered to be moderately insensitive to DMI fungicides because under field conditions these isolates have been associated with ineffective control with triadimefon and good control with myclobutanil applied at a high label rate.

Powdery mildew occurrence was monitored in 4 of the commercial pumpkin fields (sites 1, 2, 4, and 5). Severity was assessed on upper and lower leaf surfaces of 24 leaves in each field on 19-21 Aug and on 31 Aug.

RESULTS AND DISCUSSION QoI resistance was detected on 27 July in 1 of 5 fields with early plantings of summer squash and pumpkin (Table 1). A high proportion (61%) of the cucurbit powdery mildew fungus population in the field at site 4 was estimated to be resistant based on results from the seedling bioassay. No powdery mildew developed on QoI-treated seedlings placed in the other 4 fields. A low level of moderate DMI insensitivity was detected in all fields (Table 1). Thus QoI-resistant strains of Podosphaera xanthii and strains moderately insensitive to DMIs were present at a detectable level before these fungicides are known to have been applied in Suffolk County, NY, in 2003.

Powdery mildew was first observed on 29 July in the winter squash experiment at LIHREC and on 7-8 Aug in the 4 commercial pumpkin fields examined. Powdery mildew in these pumpkin fields became more severe on the lower surface of leaves than expected based on performance of QoIs in previous fungicide efficacy experiments (McGrath and Shishkoff 1999). Average severity on upper leaf surfaces on 19-21 Aug was 0.1%, 0%. 4%, and 0%, respectively, in the 4 pumpkin fields; whereas on lower leaf surfaces severity was 5%, 11%. 11%, and 18%. Good control on upper leaf surfaces indicates application timing was good. Contact fungicides (e.g. chlorothalonil, copper) only work where deposited, which is mostly the upper surface. Control on lower surfaces is provided by systemic/translaminar fungicides. Severity on 31 Aug exceeded 50% on most lower surfaces while there remained few symptoms on upper surfaces (0-5%). Several leaves died by 31 Aug, likely due to poor control of powdery mildew (Figure 3). In a fungicide efficacy experiment conducted on pumpkin at LIHREC in 2003, level of control on lower surfaces provided by programs with QoI and DMI fungicides was inferior to that provided by a new fungicide, Quintec (McGrath 2004).

QoI resistance was detected in all 7 fields where the second bioassay was conducted on 31 Aug, including one field where Nova was used but not QoIs (Tables 1 and 2, Figure 4). The proportion of the pathogen population estimated to be resistant was 61 - 100%. Moderate DMI insensitivity was detected in all fields as well (12 - 56%). Nontreated seedlings became severely infected, with some leaves completely white due to powdery mildew developing after infection, which revealed the large quantity of spores in the air.

A third bioassay was conducted on 25 Sep to determine if resistant strains were sufficiently widespread in Suffolk County to be present where no QoI or DMI fungicides were used. Two of these 3 fields were being organically managed (Table 2). QoI resistance was detected in these fields (2 - 56%) and also in the fields included in this bioassay where QoI and/or DMI fungicides had been used (88 - 97%) (Table 1).

Powdery mildew severity on seedlings treated with Nova generally was similar to severity on seedlings treated with both Nova and Flint for each field, which suggests that most isolates moderately insensitive to DMIs were also resistant to QoIs. Almost all individual isolates tested in 2002 using a laboratory assay were either sensitive to both chemical groups or insensitive to DMIs and also resistant to QoIs.

QoI resistant strains were present at the start of powdery mildew development in 2003 and their frequency increased greatly during the season, efficacy was affected, and they occurred in crops not treated with QoIs. Information from the first two fungicide sensitivity seedling bioassays, along with recommendations on how to modify fungicide programs, was provided to growers as soon as the results were known through newsletter articles. Where resistance had developed, growers were able to avoid unnecessary applications of an expensive fungicide during the second half of the epidemic when QoI resistant strains were sufficiently common that QoI fungicides were unlikely to have been effective.

REFERENCES

McGrath, M. T. 2001. Fungicide resistance in cucurbit powdery mildew: Experiences and challenges. Plant Disease 85(3):236-245.

McGrath, M.T., and Shishkoff, N. 1999. Evaluation of fungicide programs for managing powdery mildew of pumpkin, 1998. Fungicide and Nematicide Tests 54:230-231.

McGrath, M. T., and Shishkoff, N. 2001. Resistance to triadimefon and benomyl: dynamics and impact on control of cucurbit powdery mildew. Plant Disease 85(2):147-154.

McGrath, M. T. 2004. Evaluation of fungicide programs for managing powdery mildew of pumpkin, 2003. Fungicide and Nematicide Tests 59:V056.

McGrath, M. T., and Shishkoff, N. 2003. Resistance to strobilurin fungicides in Podosphaera xanthii associated with reduced control of cucurbit powdery mildew in research fields in the Eastern United States. Resistant Pest Management 12(2). (on line at http://whalonlab.msu.edu/rpmnews/vol.12_no.2/globe/rpm_g_mcgrath_shishkoff_2_.htm

McGrath, M. T, Staniszewska, H., Shishkoff, N., and Casella, G. 1996. Fungicide sensitivity of Sphaerotheca fuliginea populations in the United States. Plant Disease 80:697-703.

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