Improving Orchard Productivity Using Novel Disease Management Practices for Control of Apple Powdery Mildew in the Northeast USA

Final report for GNE20-240

Project Type: Graduate Student
Funds awarded in 2020: $14,434.00
Projected End Date: 03/31/2023
Grant Recipient: Cornell University
Region: Northeast
State: New York
Graduate Student:
Faculty Advisor:
Kerik Cox
Cornell University
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Project Information

Summary:

Apple powdery mildew (caused by the fungus Podosphaera leucotricha) is endemic in production regions statewide. Left unmanaged, the disease renders fruit unmarketable due either to flower bud malformation or fruit russet damage and negatively impacts tree vigor by colonization of the host trees’ foliar tissues. Currently, the disease is not of extreme concern in New York compared to the rapidity with which other diseases – namely apple scab and fire blight – may devastate an orchard. However, long-term observations of the northeast’s shifting climate indicates that the environment of the state’s production regions will likely become more conducive to survival, development, and spread of P. leucotricha in coming decades. In the absence of durable host resistance, commercial producers rely on fungicide programs to manage apple powdery mildew. Misuse of single-site fungicides with specific modes of action, however, may lead to resistance selection in populations of P. leucotricha and render these limited tools ineffective. The scope of this work was to investigate improved management options for apple powdery mildew and disseminate this information to the larger apple producer community in the Northeast USA via extension articles, on-farm consultations, and presentations at regional meetings. The first goal of this research was to evaluate a the current suite of biological products commercially available in New York State to determine their suitability for apple powdery mildew management, and find ways to integrate them with existing single-site fungicide management programs. The work contained herein did show - in multiple field trial years - that biologicals could suitably replace single-site fungicide inputs whilst still maintaining disease control. The second goal of this research evaluated a series of fungicide programs timing applications to weather thresholds conducive to development of P. leucotricha. This work demonstrated that said programs managed apple powdery mildew just as well as a standard “calendar-interval” program while using significantly fewer fungicide inputs. The third goal was to conduct a thorough survey of commercial orchards statewide and assess collected samples for mutations in genes (CYP51, cytb, and sdhB) known to confer fungicide resistance in P. leucotricha. We found no evidence of such mutations nor observed control failures in orchards, indicating that these single-site chemistries should remain useful for future growing seasons with proper rotation. The work detailed here contributes to the continued management of apple powdery mildew in the Northeast USA, and better prepares us for the uncertain effects of global climate change.

Project Objectives:

The goal of this multi-year project was to leverage novel technologies and ideas to better manage the disease apple powdery mildew in the northeast USA, and proactively develop methods to assess resistance to highly effective single-site fungicides so that these tools are not lost in later years. Specific objectives include:

(1) Evaluation of fungicide management programs that integrate commercially available biopesticide and reduced-risk single-site fungicide products for effective management of apple powdery mildew.

(2) Innovate on timing of management practices using weather metrics as a form of disease forecasting to improve control and reduce fungicide inputs.

(3) Screen orchard populations of P. leucotricha via a robust PCR assay to identify mutations in target genes involved in single-site fungicide resistance in Podosphaera leucotricha, so that the longevity of current commercial products is supported.

Introduction:

The purpose of this project was to leverage contemporary disease management technologies and novel research for improved control of apple powdery mildew in the northeast United States. Powdery mildew may be of mounting importance in northeastern commercial apple production due to climate change’s influence on precipitation patterns causing unexpected periods of dry weather during susceptible developmental stages, which increases disease risk. Climate assessments report that since the 1990s the northeastern United States has experienced more pronounced year-to-year precipitation variability (more in the winter, less in the summer) and an average temperature increase region wide (Hayhoe et al., 2008). These trends are predicted to continue and raise concern that apple powdery mildew may become a greater threat as the region’s general climate becomes more conducive for the disease in the next decade. Increasingly earlier springs may also favor early bud break in apples (Wolfe et al., 2005), providing the pathogen additional time for mildew epidemics to develop and spread. Concern also exists that the geographical distribution of both the host and pathogen will also be shifted further due to fluctuating environmental shifts at the continental scale (Coakley et al., 1999), placing production regions in the northeast into warmer climates favoring pathogen development.

Research

Materials and methods:

Objective 1: Evaluate fungicide management programs that integrate commercially available biopesticide and reduced-risk single-site fungicide products for effective management of apple powdery mildew.

Field studies were conducted at Cornell AgriTech in a research orchard to evaluate fungicide management programs integrating commercially available biopesticide and reduced-risk single-site fungicide products for effective management of apple powdery mildew. The orchard was planted to semi-dwarfing 22-year-old ‘Jonagold’ trees on M.111 rootstocks in a randomized block design with four replications. The block had history of severe powdery mildew epidemics and the cultivar ‘Jonagold’ is highly susceptible to powdery mildew. Fungicide programs evaluated are listed in Table 1, and all applications were made in 7-to-10 day intervals from tight cluster to second cover. Biopesticide products were chosen based on promising efficacy shown in preliminary trials, and single site fungicide products were chosen based on their low-risk for resistance development. Powdery mildew disease incidence was assessed in late summer, defined as the percentage of leaves with sporulating lesions for eight fully expanded leaves from the terminal end of ten shoots. The incidence of apple scab was similarly assessed to determine the impacts of these programs on a disease that co-occurs with powdery mildew. Disease incidence data was subjected to analysis of variance (ANOVA) for a randomized block design using accepted statistical procedures and software (i.e. Generalized Linear Mixed Models (GLIMMIX)) procedure of SAS (version 9.4; SAS Institute Inc., Cary, NC). All percentage data was subjected to arcsine square root transformation prior to analysis.

Table 1: Proposed Management Programs using Biopesticides integrated with Conventional Single-Site Fungicides

Treatment Number

Disease Management Program

Timing

1

Untreated Control (no fungicides)

-

2

2.4 qt Manzate Max (mancozeb) + 2.5lbs Captan 80 Alternated with Microthiol Disperss 15 lbs/A

TC – 2nd Cover

3

Rampart (phosphorous acid) 48 fl.oz/A alternated with Cevya (mefentrifluconazole) 5.0 fl.oz/A

TC – 2nd Cover

4

Rampart (phosphorous acid) 48 fl.oz/A alternated with Flint Extra (trifloxystronbin) 5.0 fl.oz/A

TC – 2nd Cover

5

Double Nickel LC 1qt/A alternated with Cevya (mefentrifluconazole) 5.0 fl.oz/A

TC – 2nd Cover

6

Double Nickel LC 1qt/A alternated with Flint Extra (trifloxystronbin) 5.0 fl.oz/A

TC – 2nd Cover

 

Objective 2: Innovative timing of management practices using weather metrics as a form of disease forecasting to improve control and reduce fungicide inputs.

A trial to evaluate weather-based protocols for timing fungicide applications for apple powdery mildew was conducted at Cornell AgriTech. The trial was conducted in three research orchards with four apple cultivars of differing susceptibility to powdery mildew. Orchard 1 had cultivars ‘GingerGold’ and ‘Cortland’, which were planted in 2008 on B.9 rootstocks. Orchard 2 had cultivar ‘Jonagold’ planted in 1998 on M.111. Orchard 2 had a breeding selection, ‘HH1501’ (progeny of a ‘Golden Delicious’ cross) planted in 2016 on G.935 rootstocks. Weather-based application protocols (treatments) were arranged in a randomized complete block design with four single-tree replications with buffer trees present. Three weather-based protocols for timing fungicide applications were evaluated (detailed below): the standard calendar-based application schedule (positive control), applications based on a forecasting model developed to manage barley powdery mildew, and applications based on the apple powdery mildew conidia release model. An untreated (negative) control was included to assess effectiveness of the protocols. Irrespective of protocol, a standard fungicide management program was applied to protect trees from apple scab, which included fungicides that have not impact on powdery mildew. The program will occurred from tight cluster until terminal bud set. Each application protocol implemented a standard program for powdery mildew consisting of single-site fungicides (DMIs and QoIs) and sulfur, in rotation as necessary to adhere to label requirements. The application protocols began at tight cluster and ended by 2nd cover. Fungicides found to be successful against apple powdery mildew in prior research trials in Geneva included: sulfur (Microthiol Disperss, FRAC Code M02, UPI), Rhyme (flutriafol, DMI FRAC code 3, FMC Agricultural Solutions), Flint Extra (trifloxystrobin, QoI, FRAC Code: 11, Bayer CropScience), and Sercadis (fluxapyroxad, FRAC Code: 7. BASF). Whenever 7-10 days passed, but weather conditions do not dictate a protocol-based application, Captan (Captec 4L Drexel), which has no effect on powdery mildew, was used to suppress the competitive influence of apple scab.

 

  1. Calendar-based Management Program

Fungicides applications will be made every 7-10 days until terminal bud set (typically late July, early August in Geneva).

 

  1. Barley Powdery Mildew Forecasting Model (Polley and King 1973) [Program A]

Applications of fungicides were made whenever a “high risk period” is forecast until terminal bud set. High risk weather was defined at point which three of the four following weather conditions listed below were met:

            Daily maximum temperature > 60.08°F (15.6°C)

            Dew point deficit temperature > 41°F (5°C)

            Daily rainfall < 0.0393 in (1 mm)

            Day run of wind > 153 mi (246 km)

 

  1. Apple Powdery Mildew Conidia Release Forecasting Model (Sutton and Jones 1979) [Program B]

Applications of fungicides were made whenever a “high risk period” is forecast until terminal bud set. High risk weather was defined at point which three of the four following weather conditions listed below were met:

            Daily maximum temperature > 68°F (14.4°C)

            Average wind speed > 5 mph (8.04 kmph)

            Average relative humidity > 60%

            Average solar radiation > 224.7 Lang/hr

 

To determine the impact of each management program on disease development, disease severity was assessed for each of the programs every two weeks until terminal bud set in August. Powdery mildew severity was defined as the percentage of leaf surface area covered with sporulating lesions for eight fully expanded leaves from the terminal end of ten shoots per replicate plot. Disease progress curves based on severity was then used to calculate Area Under the Disease Progress Curves (AUPDC) to assess the effectiveness of each forecasting system in a quantitative manner. Mean AUDPC values for each replicated plot was subject to ANOVA for a randomized block design using the (GLIMMIX) procedure of SAS (version 9.4; SAS Institute Inc., Cary, NC.).

 

Objective 3: Continued support for development of a robust PCR assay to identify mutations in target genes involved in single-site fungicide resistance in Podosphaera leucotricha.

While no reports exist of resistance to single-site fungicides in populations of P. leucotricha in the United States, historical efforts to screen for resistance in P. leucotricha have been hindered previously by the lack of reliable in vivo experimentation due to the pathogen’s obligate nature. Recently, the baseline sensitivity of P. leucotricha for several classes of single-site fungicides has been established by Gañán-Betancur et al. 2021. The authors reported baseline sensitivity to active ingredients belonging to the DMI, SDHI, and QoI fungicide classes by use of a detached leaf assay for isolates collected mainly from the state of Washington, as well as from limited orchards in New York and Virginia. Among the assessed P. leucotricha isolates collected, the authors found no amino acid substitutions in the CYP51, sdhB, and cytb genes historically known to confer fungicide resistance in other fungal pathogens. Their work establishes a molecular toolset with which to rapidly conduct an extensive monitoring effort of fungicide resistance in populations of P. leucotricha in New York orchards. Given the predominant use of single-site fungicides for fungal disease management programs in New York, we conducted an exploratory multi-year survey of commercial orchards in the state’s primary production regions to assess the statewide prevalence of apple powdery mildew, and whether mutations in fungicide target genes (potentially conferring resistance) were present in orchard populations of P. leucotricha. Using these previously published primer sequences to target the P. leucotricha CYP51, cytb, and SdhB genes. Gene sequences were amplified and submitted to the Cornell BRC for Sanger sequencing, then analyzed and annotated in CLC Main Workbench (v.8.1.2, Qiagen, Redwood City) to confirm the PCR assay successfully and reliably amplifies the regions of interest in fungicide resistance development. Powdery mildew isolates were collected from research and commercial orchards from around the northeast US region, then genomic DNA was extracted as described previously.

Research results and discussion:

Objective 1: Evaluate fungicide management programs that integrate commercially available biopesticide and reduced-risk single-site fungicide products for effective management of apple powdery mildew.

In both years (2021-2022) of the trial, a moderate level powdery mildew disease pressure was observed in the orchard due to humid, warm weather conditions throughout each growing season. In 2021, mean incidence of powdery mildew symptoms on terminal leaves ranged from 6.3-46.6%. Every fungicide program sufficiently reduced powdery mildew disease incidence to or below the recommended 20% disease incidence level suggested as an action threshold. Of the managed treatments, the incidence of powdery mildew was highest for the Double Nickel / Cevya (20.3%) and Microthiol Disperss (16.3%) programs. By comparison, the Double Nickel / Flint Extra (6.3%) program had the lowest mean incidence of powdery mildew (Table 1). In 2022, mean incidence of powdery mildew symptoms on terminal leaves among treatments ranged from 2.8 - 33.7%. Every fungicide program sufficiently reduced powdery mildew disease incidence to or below the recommended 20% disease incidence level suggested as an action threshold. Of the managed treatments, the incidence of powdery mildew was highest for the Double Nickel / Flint Extra (4.06%) and Microthiol Disperss (5.63%) programs. By comparison, the Rampart / Flint Extra (2.81%) program had the lowest mean incidence of powdery mildew (Table 2). 

 

Overall, we found that programs utilizing either biopesticide product, Rampart or Double Nickel, in conjunction with either single-site conventional fungicide, Flint Extra or Cevya, maintained disease incidence well below the recommended 20% incidence threshold even in a growing season with moderate disease pressure. Hence, these biopesticide products may be suitable in rotation with single-site fungicides for effective management of apple powdery mildew and could be introduced to current management plans as a replacement for sulfur.

 

Table 1. Integrated biopesticide/single-site fungicide programs used in trial on ‘Jonagold’, including products, application rate, application timing, and powdery mildew disease incidence.

 

Treatment (amt./A)

Timing*

Incidence of powdery mildew on terminal leaves (%)**

1.

Untreated

n/a

46.6 ± 4.9 a

2.

Captec 2 qts. + Manzate Max 2.4 qts.

Microthiol Disperss 10lbs. + Manzate Max 2.4 qts.

1-3, 5, 7

 

4, 6

 

16.3 ± 1.4 b

3.

Captec 2 qts. + Manzate Max 2.4 qts.

Rampart 64 fl. oz.

Cevya 5 fl. oz.

1-3

4, 6

5, 7

 

14.7 ± 3.8 bc

4.

Captec 2 qts. + Manzate Max 2.4 qts.

Rampart 64 fl. oz.

Flint Extra 3 oz.

1-3

4, 6

5, 7

 

11.3 ± 1.8 bc

5.

Captec 2 qts. + Manzate Max 2.4 qts.

Double Nickel 32 fl. oz.

Cevya 5 fl. oz.

1-3

4, 6

5, 7

 

20.3 ± 2.6 b

6.

Captec 2 qts. + Manzate Max 2.4 qts.

Double Nickel 32 fl. oz.

Flint Extra 3 oz.

1-3

4, 6

5, 7

 

6.3 ± 1.4 c

 *Application timings: 19 Apr – green tip (application 1); 27 Apr – tight cluster (application 2); 4 May – pink (application 3); 11 May – bloom (application 4); 18 May – petal fall (application 5); 27 May – 1st cover (application 6); 7 Jun – 2nd cover (application 7).

**All values are disease incidence and the means and standard errors of 10 terminal shoots from each of four replicate trees. Values within columns followed by the same letter are not significantly different (P < 0.05) according to the LSMEANS procedure in SAS 9.4 with an adjustment for Tukey’s HSD to control for family-wise error.

 

Table 2. Integrated biopesticide/single-site fungicide programs used in trial on ‘Jonagold’, including products, application rate, application timing, and powdery mildew disease incidence.

 

Treatment (amt./A)

Timing*

Incidence of powdery mildew on terminal leaves (%)**

1.

Untreated

n/a

33.75 ± 3.4 a

2.

Captec 2 qts. + Manzate Max 2.4 qts.

Microthiol Disperss 10lbs. + Manzate Max 2.4 qts.

1-3, 5, 7

 

4, 6

 

5.63 ± 3.3 b

3.

Captec 2 qts. + Manzate Max 2.4 qts.

Rampart 64 fl. oz.

Cevya 5 fl. oz.

1-3

4, 6

5, 7

 

3.13 ± 0.8 b

4.

Captec 2 qts. + Manzate Max 2.4 qts.

Rampart 64 fl. oz.

Flint Extra 3 oz.

1-3

4, 6

5, 7

 

2.81 ± 0.93 b

5.

Captec 2 qts. + Manzate Max 2.4 qts.

Double Nickel 32 fl. oz.

Cevya 5 fl. oz.

1-3

4, 6

5, 7

 

3.44 ± 1.4 b

6.

Captec 2 qts. + Manzate Max 2.4 qts.

Double Nickel 32 fl. oz.

Flint Extra 3 oz.

1-3

4, 6

5, 7

 

4.06 ± 0.6 b

 *Application timings: 19 Apr – green tip (application 1); 28 Apr – tight cluster (application 2); 5 May – pink (application 3); 13 May – bloom (application 4); 23 May – petal fall (application 5); 2 Jun – 1st cover (application 6); 10 Jun – 2nd cover (application 7).

**All values are disease incidence and the means and standard errors of 10 terminal shoots from each of four replicate trees. Values within columns followed by the same letter are not significantly different (P < 0.05) according to the LSMEANS procedure in SAS 9.4 with an adjustment for Tukey’s HSD to control for family-wise error.

 

Objective 2: Innovative timing of management practices using weather metrics as a form of disease forecasting to improve control and reduce fungicide inputs.

In 2021, fungicide management programs implemented based on environmental thresholds conducive to powdery mildew growth and spread successfully reduced disease incidence below the 20% threshold commonly used as a target for effective management (Table 1). These programs performed equally as well as a calendar-based application schedule but used considerably fewer mildew-specific fungicide applications (75-83.3%), as shown in Table 2. These findings provide a proof-of-concept work that weather-based management programs could be implemented into a regional decision support system (DSS) - as exists for other apple diseases fire blight and apple scab in NEWA - to improve sustainable apple production regionwide.

Table 1. Mean apple powdery mildew disease incidence observed on each cultivar at the end of the growing season 2021.

 

Program

End-of-Season Apple Powdery Mildew Mean Disease Incidence (%)*

Jonagold

GingerGold

Cortland

Cordera

2021

 

 

 

 

 

 

Untreated

55.00 ± 8.22 a

32.19 ± 7.31 a

13.13 ± 4.69 a

4.84 ± 2.57 a

 

Calendar

0.625 ± 0.625 b

1.88 ± 1.51 b

0.16 ± 0.16 b

0.78 ± 0.50 b

 

Program A

1.56 ± 1.35 b

6.61 ± 3.16 b

1.09 ± 0.82 b

0.63 ± 0.63 b

 

Program B

2.19 ± 1.77 b

2.34 ± 1.52 b

0.94 ± 0.83 b

0.62 ± 0.49 b

* Values within columns followed by a different letter are significantly different (P < 0.05) according to the LSMEANS procedure in SAS 9.4 with an adjustment for Tukey’s HSD to control for family-wise error.

 

Table 2. Cumulative number of applications at end-of-season for mildewcidal fungicides within each treatment in replicated trials evaluating the utility of environmental factor-based programs compared with a calendar program on apple powdery mildew, 2021.

 

Treatment

Microthiol Disperss + Manzate Max*

Merivon / Rhyme*

Captan + Manzate Max

Total Mildewcide Applications by Treatment / Total

2021

 

 

 

 

 

 

Untreated

-

-

-

-

 

Calendar

7

5

0

12 / 12 (100%)

 

Program A

1

2

9

3 / 12 (25.0%)

 

Program B

0

2

10

2 / 12 (16.7%)

*The tank mix of Microthiol Disperss + Manzate Max and the Merivon / Rhyme applications were made specifically to manage apple powdery mildew symptoms, and contribute to the mildewcide count in the final column. The percentage refers to the amount of mildew-specific fungicides required that season to manage disease symptoms, with the remaining applications being protectant against apple scab.

 

In 2022, management programs based on environmental thresholds conducive to powdery mildew growth and spread successfully reduced disease incidence below the 20% threshold used as a target for effective management (Table 3). These programs performed equally as well as a calendar-based application schedule but used considerably fewer mildew-specific fungicide applications (60% fewer applications needed), as shown in Table 4.

This work has been published in the peer-reviewed journal Plant Disease, entitled "Refining management of apple powdery mildew in New York State with weather-based fungicide application timing programs", and is currently available as a First Look manuscript (without the finalized proofreading and formatting of a scientific journal) with the DOI #: https://doi.org/10.1094/PDIS-08-22-1825-RE.

 

Table 3. Mean apple powdery mildew disease incidence observed on each cultivar at the end of the growing season 2022.

 

Program

End-of-Season Apple Powdery Mildew Mean Disease Incidence (%)*

Jonagold

2022

 

 

 

Untreated

71.56 ± 8.58 a

 

Calendar

3.75 ± 3.06 b

 

Program A

4.37 ± 2.79 b

 

Program B

3.13 ± 2.08 b

* Values within columns for a given year followed by a different letter are significantly different (P < 0.05) according to the LSMEANS procedure in SAS 9.4 with an adjustment for Tukey’s HSD to control for family-wise error.

 

Table 4. Cumulative number of applications at end-of-season for mildewcidal fungicides for each program in replicated trials evaluating the utility of weather-based programs compared with a calendar program for apple powdery mildew management, 2022.

 

Treatment

Captan + Manzate Max

Microthiol Disperss + Manzate Max*

Merivon / Rhyme*

Total Mildewcide Applications by Treatment / Total**

2022

 

 

 

 

 

 

Untreated

-

-

-

-

 

Calendar Program

0

6

4

10 / 10 (100%)

 

‘Barley’ Program

6

1

3

4 / 10 (40%)

 

‘Apple’ Program

6

1

3

4 / 10 (40%)

*The tank mix of Microthiol Disperss + Manzate Max and the Merivon / Rhyme applications were mildewcides made specifically to manage apple powdery mildew symptoms. Note, these applications contribute to the mildewcide count in the final rightmost column.

**The percentage refers to the mildew-specific fungicides required to manage disease out of the total application number, with the remaining Captan + Manzate Max tank mix applications being applied as protectants against apple scab, which is endemic in New York orchards.

 

Objective 3: Continued support for development of a robust PCR assay to identify mutations in target genes involved in single-site fungicide resistance in Podosphaera leucotricha.

In this two-year survey (2021-2022), we collected 160 samples of P. leucotricha from 43 orchards, representing conventional, organic, low-input, and unmanaged orchards from New York’s primary production regions. Samples were screened for mutations in the target genes (CYP51, cytb, and sdhB) historically known to confer fungicide resistance in other fungal pathogens to the DMI, QoI, and SDHI fungicide classes, respectively. Across all samples, no nucleotide sequence mutations that translated into problematic amino acid substitutions were found in the target genes, suggesting that New York populations of P. leucotricha remain sensitive to the DMI, QoI, and SDHI fungicide classes, provided no other fungicide resistance mechanism is at play in the population. This work has been published in the peer-reviewed journal Plant Disease, entitled "Assessment of fungicide resistance via molecular assay in populations of Podosphaera leucotricha, causal agent of apple powdery mildew, in New York", and is currently available as a First Look manuscript (without the finalized proofreading and formatting of a scientific journal), with the DOI #: https://doi.org/10.1094/PDIS-12-22-2820-SR.

In addition, a grower-focused version of Objective 3's results was written as an extension article for publication in New York Fruit Quarterly. Entitled "No evidence of fungicide resistance in populations of Podosphaera leucotricha (apple powdery mildew) from commercial orchards in New York.", the article has been accepted by the NYFQ staff and is expected to be published in either the Summer or Fall 2023 edition of this publication, depending on their internal publication process. The funding from this grant is noted in the Acknowledgements section of this manuscript.

Research conclusions:

Objective 1: Evaluate fungicide management programs that integrate commercially available biopesticide and reduced-risk single-site fungicide products for effective management of apple powdery mildew.

Based on the two years of trials in our research orchard at Cornell AgriTech, we are confident that biopesticides can be used in conjunction with a single-site fungicide management program to (1) manage apple powdery mildew successfully, and (2) reduce single-site fungicide inputs. Our experimental programs used 50% fewer single-site fungicide applications and replaced them with biopesticide chemistries, and maintained tree health as well as currently recommended programs. In addition, in comparison with a broad spectrum sulfur program, our biopesticide/single-site program was equally effective.

In short, biopesticides may have great potential replacing some single-site and/or broad spectrum fungicide inputs. Reduction of single-site fungicide inputs will reduce the selective pressure put on populations of P. leucotricha in orchards, delaying the onset of fungicide resistance and extending the lifetime of what limited single-site chemistries are commercially available. Reduction of broad spectrum fungicide inputs, such as sulfur in these trials, has sustainability benefits. Broad spectrum fungicides are nonspecific in which organisms they impact, and have off-target effects in both the orchard, groundwater, and humans, so the replacing them with products with reduced concerns is ultimately beneficial.

From this trial, our recommendations to growers are that some single-site and/or broad spectrum chemistries may be replaced with biopesticides effective against apple powdery mildew. There are still efficacy concerns for many biopesticide chemistries, and they may require more frequent applications to handle orchards experiencing severe disease pressure, but these trials have suitably shown they have a place in modern disease management programs for apple.

 

Objective 2: Innovative timing of management practices using weather metrics as a form of disease forecasting to improve control and reduce fungicide inputs.

The results of Objective 2 provides the proof-of-concept for replacing standard calendar-based fungicide programs for apple powdery mildew management and instead offers application timing based on environmental factors that favors powdery mildew disease development and spread. Our weather-based fungicide application timing programs sufficiently controlled apple powdery mildew symptoms as well as a calendar-based program yet required substantially fewer mildew-specific applications to do so (50-83% fewer mildew-specific inputs). The weather factors considered here could be implemented in a future DSS as elements of a disease forecast model to assist grower decision making in the northeast United States

Several reasons may sway apple growers to implement a management paradigm like those described in Objective 2 instead of using a standard calendar program. Primarily, an economic incentive may convince growers of the programs’ utility should the reduction of fungicide applications (and associated labor costs) substantially improve financial returns. Indeed, New York apple growers currently use disease forecasting (NEWA) to better time pesticide applications for fire blight and apple scab to their economic benefit, so its use for apple powdery mildew should not require much re-training. In the future, instead of speculating at high-risk mildew infection periods and swapping in an expensive single-site fungicide into their calendar program, growers experiencing considerable powdery mildew inoculum in their orchard(s) could use the information from the present study to identify periods of weather conditions ideal for timings to make mildew-specific applications. Additionally, a grower intrinsically motivated to produce apples more sustainably may favor this disease management paradigm in combination with biopesticide us.

 

Objective 3: Continued support for development of a robust PCR assay to identify mutations in target genes involved in single-site fungicide resistance in Podosphaera leucotricha.

Our findings suggest that the existing suite of commonly used single-site fungicides remain effective options for apple powdery mildew management in New York. DMIs, SDHIs, and QoIs should continue to prove useful for the foreseeable future, provided they are used within the framework of an integrated pest management program. These findings are consistent with similar surveys reported out of Canada and Washington state (Grigg-McGuffin et al. 2013; Gañán-Betancur et al. 2021). To date, no population of P. leucotricha in North America has been found to have resistance to DMIs, QoIs, or SDHIs. The present lack of fungicide resistance in scouted orchards does not mean that resistance couldn’t develop in the future, or that a commercial orchard bearing a resistant population was overlooked during the survey. It is still important to rotate fungicides of different chemical classes so that the selection pressure put on populations of P. leucotricha does not shift towards resistance to a particular mode of action. Use of broad spectrum fungicides such as sulfur or a number of commercially available biopesticides (such as Double Nickel or Serenade Opti; Objective 1) can also suitably manage apple powdery mildew to the point of prolonging the utility of single-site fungicides, particularly in years when the season is not conducive to mildew development (e.g. cool, wet) or in orchards experiencing low disease pressure.

Participation Summary
43 Farmers participating in research

Education & Outreach Activities and Participation Summary

43 Consultations
2 Journal articles
2 Published press articles, newsletters
1 Tours
7 Webinars / talks / presentations
1 Other educational activities: Podcast episode on 'Orchard Outlook': E10S2 Ghosts and Skeletons of Powdery Mildew

Participation Summary:

183 Farmers participated
5 Number of agricultural educator or service providers reached through education and outreach activities
Education/outreach description:

Results were communicated via well-established channels relied upon by apple growers statewide for orchard recommendations.  On-farm consultations while collecting mildew samples with farmers whose orchards are screened for fungicide-resistant populations of apple powdery mildew also led to productive discussions. A detailed list of conducted outreach follows for 2021-2022 in chronological order:

1. Bishop Kearney High School virtual lesson: On 1/7/21, I virtually met with the agriculture class as Bishop Kearny HS in Monroe County, NY with a handful of other Cornell AgriTech graduate students. We discussed our research (mine, this powdery mildew management investigation) and answered questions about careers in agriculture. 10 junior/senior high school students were in attendance.

2. Fruit Notes newsletter: In early 2021, I wrote a newsletter announcement for the coming growing season discussing apple powdery mildew biology and management, as well as some aspects of the research being conducted at Cornell AgriTech. This newsletter was delivered to growers via Cornell Cooperative Extension. It was also published on our research lab's website here (scroll to the bottom of the page): https://blogs.cornell.edu/coxlab/category/newsletters/

3. APS Potomac/Northeastern Division Joint Meeting: On 3/10/21 - 3/12/21 I attended the annual APS division meeting for my region, held virtually this year due to the pandemic. I presented my research to date on Objective 2 of this investigation (see attached PDF of the poster) during the graduate research poster session on 3/12.

4. Bishop Kearney High School virtual lesson: On 5/10/21, I virtually met with another agriculture class as Bishop Kearny HS in Monroe County, NY with a handful of other Cornell AgriTech graduate students. We discussed our research (mine, this powdery mildew management investigation) and answered questions about careers in agriculture. 15 junior/senior high school students were in attendance.

5. Perennia 'Orchard Outlook' Podcast Episode: On 7/23/21, Dr. Kerik Cox (my PI) and I were interviewed for Perennia's 'Orchard Outlook' podcast, discussing powdery mildew biology and management. I discussed the research being conducted in this investigation at length. The podcast episode was released on 8/11/21 to the general public and is available at the following link: https://anchor.fm/orchard-outlook/episodes/E10-S2--Ghosts-and-Skeletons-of-Powdery-Mildew-e15p4ib

6. Lake Champlain Summer Tour presentation: On 8/19/21, I traveled to the Lake Champlain growing region to give a talk on powdery mildew management to local apple growers, and to answer their disease management questions. 32 growers were in attendance.

7. Western NY / Northeast NY Scouting Trips: During the growing season, I scouted >45 locations around two major apple production regions in NYS for apple powdery mildew samples (Objective 3). During this time I met with growers and answered general management questions about apple production.

8. On 1/26/2022, I gave a grower talk at the virtual Nova Scotia Fruit Grower's Association annual meeting. I discussed general apple powdery mildew management, and the new research being conducted as part of this grant's efforts. 171 viewers were in attendance.

9. On 2/22/2022, I gave a presentation to the University of Wisconsin-Madison department of Plant Pathology as part of a graduate student seminar exchange series. I discussed my research on apple powdery mildew management. 21 people were in attendance.

10. On 2/24/2022, I gave a virtual talk at the OFVC 2022 annual convention held in Ontario, Canada. I discussed general apple powdery mildew management as well as the new research being conducted as part of this grant's efforts. Unfortunately, I do not know how many people were in attendance.

11. Hudson Valley Scouting Trips: During the growing season, I scouted locations around the Hudson Valley for apple powdery mildew samples (Objective 3). During this time I met with growers and answered general management questions about apple production.

Project Outcomes

60 Farmers reporting change in knowledge, attitudes, skills and/or awareness
Project outcomes:

With respect to sustainability, I feel the results of Objective 2 best showcase the success of this work. My multiyear trials showed a ~50-80% reduction in mildew specific fungicide inputs (namely, single-site and multi-site inputs) for the treatments whose applications were based on weather conditions conducive to mildew development, yet had equivalent disease control to a calendar program that used 10-12 mildew-specific applications in a year. I feel this work contributes to future sustainability efforts in the northeast USA, as apple powdery mildew is not of highest management concern (compared to apple scab and fire blight). Management programs that reduce fungicide inputs >50% have significant economic and environmental potential considering the reduction of chemicals and labor used for apple production in those scenarios. The work of Objective 2 lays the groundwork so that, as the northeast USA's climate continues to warm and have more erratic precipitation due to climate change, if mildew becomes more prevalent and problematic, we will have ready answers to target this disease.

In that same vein, the NYS survey for fungicide resistance in populations of P. leucotricha will also pay dividends both now and in the future. We know from Objective 3's results that the existing suite of fungicides adequately control the disease, and for the first time have a baseline understanding of the state's populations going forward should fungicide resistance arise.

Lastly, the biopesticide evaluations of Objective 1 have immediate benefit for growers in this upcoming growing season and beyond. Here we report successful integration of biorational products with the existing single-site chemistries for apple powdery mildew management. Growers can be confident that these biorational products will serve them well, whilst reaping the improved environmental and social benefits of use of these products.

Knowledge Gained:

During the course of this project, I performed various field trials that successfully managed apple powdery mildew in a more sustainable manner (e.g. fewer fungicide inputs, and/or integration of biorational products instead of multi-site and single-site fungicide products). The knowledge gained from this work can be implemented in the apple production guidelines of institutions in the northeast USA (such as at Cornell) to refine chemical recommendations for apple powdery mildew management. Indeed, of the numerous extension presentations I gave on these topics in the northeast USA, mid-Atlantic, and northeast Canada (Ontario, Nova Scotia), I received feedback from growers (~60) indicating their enhanced awareness of mildew and its successful management using this type of technology.

Through this work, I have a greater appreciation for the quality and efficacy of the biorational products on the commercial market today, and am confident in recommending them to apple growers in order to manage plant diseases of concern. In fact, as I near graduation, I am searching for an industry role in the crop protection section with an emphasis on biorational product development so that I may continue to contribute to the the successful implementation of this type of technology.

Assessment of Project Approach and Areas of Further Study:

With respect to Objective 3, the fungicide resistance survey, vigilance is needed going forward. Just because fungicide resistance was not observed in the populations of P. leucotricha we sampled, it does not mean that we did not miss a resistant sample, or that resistance won't appear later. Growers must continue to rotate different fungicide modes of action to help delay the onset of this issue. Vigilance is needed from researchers and extension agents to watch for the rise of fungicide resistance in populations of the causal agent, so that rapid efforts can be made to address the problem as it develops. Expanded use of biorational products, such as those evaluated in Objective 1, have the benefit of limiting needed single-site fungicide inputs, reducing the possibility for fungicide resistance development. Expanded efficacy trials for these products, and improved educational initiatives to advocate for them to growers will promote better adoption of this technology, ultimately improving our efforts for sustainable apple production.

Information Products

Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture or SARE.