Adjusting Product Timing during the Powdery Mildew Critical Window to Improve Disease Management

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1 REPORT Adjusting Product Timing during the Powdery Mildew Critical Window to Improve Disease Management Michelle M. Moyer, 1 * Jensena M. Newhouse 2 and Gary G. Grove 3 Cite this article: Moyer MM, Newhouse JM, and Grove GG Adjusting product timing during the powdery mildew critical window to improve disease management. Catalyst 2: Associate Professor, Dept. of Horticulture; 2 Former research technician, Dept. of Horticulture; and 3 Professor, Dept. of Plant Pathology; Washington State University Irrigated Agriculture Research and Extension Center, N. Bunn Rd., Prosser, WA. *Corresponding author (michelle.moyer@wsu.edu) Acknowledgments: The authors would like to thank Mauricio Garcia, Brittany Komm, Katherine East, Steve Hoff, and Eric Gale for their technical assistance. This work was partially supported by the USDA National Institute of Food and Agriculture, Hatch Project #226789, and a grant from the Washington State Grape and Wine Research Program. Manuscript submitted Jan 2018; revised May 2018, accepted May 2018 Copyright 2018 by the American Society for Enology and Viticulture. All rights reserved. doi: /catalyst Summary Goals: This project was designed to answer questions about the timing of different cultural (leaf removal) and chemical (fungicide rotation) disease management practices and how they influence the overall efficacy of a powdery mildew management program. Key Findings: The timing of specific chemical modes of action plays an important role in the overall efficacy of powdery mildew fungicide programs. In this study, programs in which the evaluated products were applied once during the critical window performed as well as programs in which the same products were applied twice (during the critical window and at bunch closure). This finding indicates that disease control depends on application of sprays during the critical window rather than later in the season. As expected, leaf removal significantly improved spray coverage in the fruit zone; however, this improved coverage did not last the entire season. Canopy refill, which occurred as summer laterals developed, reduced fruit-zone coverage later in the season. Leaf removal also did not result in any positive additive effects on overall disease control. Impact and Significance: These findings can be used to aid growers in the selection and rotation of products used for powdery mildew management programs to maximize the efficacy of disease control and minimize the risk of fungicide resistance. While early fruit zone leaf removal did not improve overall disease control in this high-pressure scenario, leaf removal resulted in improved spray coverage, which may enhance disease control when low-volume spray applications or contact-active chemistries are emphasized in a commercial program. Key words: fungicide resistance, ontogenic resistance, spray programs Overview Management of grapevine powdery mildew was significantly affected by the discovery of ontogenic, or age-related, resistance. 1 This discovery demonstrated that grape berries were at their peak susceptibility to the grape powdery mildew pathogen during a limited window of development, from approximately prebloom to three to four weeks post-fruit set. This critical window concept for aligning spray programs with vine phenology has resulted in improved timing and reduced application of fungicides; in Washington alone, educational efforts focused on phenology-based mildew management have reduced the average number of annual sprays by one to two applications and have saved the industry ~$2,000,000 USD annually over the last five years. 2 However, even in climates normally classified as arid steppe, 3 there can be years where mildew management is challenging. Such years were experienced in 2010 and 2011, which were characterized by cooler and wetter than average conditions. 4 In those years, application of the standard six to eight page 7

2 8 Moyer et al. sprays per season 5 was insufficient for managing mildew in many commercial settings. However, some growers were still able to achieve control with three sprays. 6 In 2015 and 2016, conditions were hot, dry, and sunny, which is considered ideal for maximum mildew control, and some growers achieved acceptable control with only two sprays. 7 Why do some programs achieve equivalent mildew control using 25 to 50% of the industry standard number of sprays, regardless of product? There are clearly several factors that can influence disease control, not limited to proper sprayer calibration, ground speed at the time of application, and canopy management. However, one common factor for several of these low-frequency applicators was the choice of products used and the specifically-chosen timing of spray applications. The trial presented here aimed to answer and evaluate the question Is timing really everything?. We examined this question in the context of key grapevine phenological stages for mildew management, and different chemical modes of action that are commonly used in conventional vineyard production systems. The concept of timing was approached using fungicide rotation programs that focused on the application of one of three different fungicide modes of action at different time points between immediate prebloom and post-fruit set. Different fungicide modes of action are often described on their use labels as a specific FRAC (Fungicide Resistance Action Committee 8 ) group (multiple groups if the product is a premix of different fungicides). FRAC is an international group of industry specialists (private companies and university researchers) dedicated to determining how to prolong the effective use of fungicides and slow the development of resistance. Fungicides that have similar properties are grouped into the same FRAC category. The active ingredients chosen for this study were quinoxyfen (FRAC 13), cyflufenamid (FRAC U6), and metrafenone (FRAC U8), which were applied in a background spray program of myclobutanil (FRAC 3; Table 1). In Washington, grapegrowers rely heavily on FRAC 3 and strobilurin (FRAC 11); there is documented resistance to FRAC 11 9 fungicides and concerns that FRAC 3 fungicide resistance may be developing. Thus, Program b Table 1 Fungicide programs, product rotation, and application dates for 2013 and Application date Critical window for fruit infection a 21 May c (30-cm shoot) 4 June (Prebloom) 18 June (Full bloom) 2 July (Fruit set) 16 July 30 July (Bunch closure) Control Untreated Untreated Untreated Untreated Untreated Untreated Q1 Myclobutanil Quinoxyfen Myclobutanil Myclobutanil Myclobutanil Myclobutanil Q2 Myclobutanil Myclobutanil Quinoxyfen Myclobutanil Myclobutanil Quinoxyfen Q3 Myclobutanil Myclobutanil Myclobutanil Quinoxyfen Myclobutanil Myclobutanil Q4 Myclobutanil Myclobutanil Myclobutanil Myclobutanil Quinoxyfen Myclobutanil C2 Myclobutanil Myclobutanil Cyflufenamid Myclobutanil Myclobutanil Myclobutanil M2 Myclobutanil Myclobutanil Metrafenone Myclobutanil Myclobutanil Myclobutanil Program b 13 May c (30-cm shoot) 28 May (Prebloom) 2014 Application date Critical window for fruit infection a 10 June (Full bloom) 24 June (Fruit set) 8 July 22 July (Bunch closure) Control Untreated Untreated Untreated Untreated Untreated Untreated Q1 Myclobutanil Quinoxyfen Myclobutanil Myclobutanil Myclobutanil Myclobutanil Q2 Myclobutanil Myclobutanil Quinoxyfen Myclobutanil Myclobutanil Quinoxyfen Q3 Myclobutanil Myclobutanil Myclobutanil Quinoxyfen Myclobutanil Myclobutanil Q4 Myclobutanil Myclobutanil Myclobutanil Myclobutanil Quinoxyfen Myclobutanil C2 Myclobutanil Myclobutanil Cyflufenamid Myclobutanil Myclobutanil Cyflufenamid C3 Myclobutanil Myclobutanil Myclobutanil Cyflufenamid Myclobutanil Myclobutanil M2 Myclobutanil Myclobutanil Metrafenone Myclobutanil Myclobutanil Metrafenone M3 Myclobutanil Myclobutanil Myclobutanil Metrafenone Myclobutanil Myclobutanil a Defined from: Gadoury DM, Seem RC, Ficke A and Wilcox W Ontogenic resistance to powdery mildew in grape berries. Phytopathology 93: b These programs were designed for experimental evaluation. The authors do not recommend (nor is it recommended on product labels) repeated application of FRAC group 3 fungicides (demethylation inhibitors; DMI; e.g., myclobutanil) back-to-back in a fungicide program or more than two times in a single growing season. Improper application of these and other fungicides can result in fungicide resistance development. Always rotate products, or tank mix high-risk products with contact fungicides when appropriate and compatible. c Budbreak: 27 April 2013 and 17 April 2014.

3 Designing Fungicide Programs 9 while the use of these potentially compromised products can be a viable option within a spray program (provided they are tank mixed with another, noncompromised FRAC group), there is growing demand to understand how to achieve optimal performance of other FRACgroup products during the critical window for mildew management. Major Observations and Interpretations Disease ratings. In 2013, fungicide program 10 (Table 1) had a significant influence on disease outcomes (p < ; Figure 1A). All programs outperformed the untreated control. Program M2, which had a metrafenone application at full bloom, performed the best; Q1 (quinoxyfen at prebloom) and C2 (cyflufenamid at bloom) were intermediate to M2 and the remaining programs. Leaf removal did not have a statistically significant influence on cluster disease severity (p = 0.311). In 2013, disease was consistent throughout the vineyard block, likely because of consistent rainfall in late June that increased canopy growth (i.e., new tissue for disease infection) and humidity in and surrounding the canopy (Figure 2). Results were similar in 2014; fungicide program had a significant influence on disease outcomes (Figure 1B), and leaf removal nested within fungicide programs did not (p = 0.07). As in 2013, all programs outperformed the untreated control. The best performing program in 2014 was Q4, which consisted of a post-fruit-set application of quinoxyfen; Q4 performed significantly better than program C3, which involved application of cyflufenamid at fruit set. The remaining programs were intermediate in performance to Q4 and C3. Of interest is the comparison of the Q2 treatment to the other Q treatments. Program Q2 had both early (full bloom) and late-season (bunch closure) applications of quinoxyfen and was the only quinoxyfen program with this dual application. A typical assumption would be that the added end-of-program application would improve disease control, but in both 2013 and 2014, the performance of Q2 was not significantly different from that of the other, single-timed applications of quinoxyfen that occurred either just before or during the critical window Figure 1 Cluster disease severity as a result of different fungicide programs in: (A) 2013 and (B) In both years, the timing of leaf removal did not influence the overall severity of powdery mildew disease on clusters, but fungicide treatment did. Letters denote significance between transformed fungicide treatment means (Tukey s honest significant difference, α = 0.05). Fungicide programs are defined in Table 1. Figure 2 Daily maximum and minimum temperature and precipitation from 1 April to 30 Sept in 2013 (A) and 2014 (B). The 2013 growing season was marked by average temperatures and above-average precipitation in June, whereas 2014 was marked by above-average temperatures and below-average spring precipitation.

4 10 Moyer et al. for fruit infection. This highlights that the duration of ontogenic susceptibility could influence the perception of product performance: 1 fruit was already resistant at bunch closure, so additional application of fungicides at this stage to control cluster disease severity did not have any impact on season-long disease control. However, a field manager using a dual-application program might assume that a late application is needed to achieve that level of disease control, while the full-bloom application likely provided most of the control. We saw this repeated in 2014, when both the cyflufenamid and metrafenone had similar comparable treatments a program timing that had a dual application early (at full bloom) and late in the season (at bunch closure) (treatments C2 and M2), and then a single application at fruit set (C3, M3). In both cases, the dual applications were not significantly better than a single application (Figure 1). These findings reinforce the idea that management of grape powdery mildew on clusters should be emphasized earlier in the growing season, rather than later. To put disease management in a seasonal context, differences in vine development between the years should be considered. As noted in Table 1, 2014 was a much faster vine development year than All phenological stages started earlier in 2014 compared to In eastern Washington, earlier growing seasons are typically related to warmer winters. In most cases, when the region has warmer winters and earlier starts to the growing season, phenological stages can become protracted (extended) due to less-than-optimal winter chilling. As such, while a bloom spray is performed on a single date at a specified time (Table 1), the duration of bloom can be longer after a warmer winter, resulting in a longer period of cluster susceptibility to powdery mildew compared to conditions following a colder winter that would synchronize and retract (shorten) the duration of bloom. In rating the efficacy of a product or program for disease management, the consistency of typical disease outbreaks should be considered. While coverage was measured according to spray penetration, there is potential error in product delivery related to machine operation. While the sprayer used in this study was calibrated at the start of the season, calibration was not re-assessed throughout the year to ensure that nozzle wear or misalignment had not occurred. This could be a reason for the variation seen in cluster disease severity, as evenness of product delivery would ultimately influence the evenness of cluster disease severity. Spray coverage. In 2013, spray coverage was only evaluated on one day (Figure 3), whereas coverage was evaluated four times in 2014 to better assess the influence of leaf removal on spray penetration over time (Figure 3). In 2013, coverage was assessed on 2 July, which was 46 days after prebloom leaf removal, 25 days after the bloom leaf removal, and three days prior to postbloom leaf removal. As seen in Figure 3, spray coverage was increased even several weeks after leaf removal. In 2014, spray coverage was assessed 11 days after prebloom leaf removal (Figure 4A), three days after bloom leaf removal (Figure 4B), six days after postbloom leaf removal (Figure 4C), and on 31 July as a followup assessment near the end of the season (Figure 4D). As noted, when leaf removal had occurred, spray coverage was significantly improved; however, by the end of the season, the prebloom leaf removal treatment was no longer effective at improving spray coverage in the fruit zone because of canopy refill from lateral shoot development. Fruit quality assessments. In both years, the timing of leaf removal did not influence fruit quality (Brix, titratable acidity (TA), or juice ph), but fungicide program did (Table 2). However, there were few differences in final fruit quality between the untreated control and fungicide programs. In 2013, Program Q3, which had an application of quinoxyfen at fruit set, had the highest Brix and higher juice ph (in this case, higher ph was desirable due to overall low ph of the fruit). This program also performed well in 2014 and was not statistically different from the highest performing programs (based on juice Brix), which were Q2 (quinoxyfen at full bloom) and M2 (metrafenone at full bloom). Q2 and M2 performed equally well in 2013 as well. Past reports have also indicated that powdery mildew-diseased fruit can result in off-flavors in the final fermented product. 11 Off-flavors were not evaluated in this study; the lack of Figure 3 Influence of leaf removal on midseason spray coverage in the fruiting zone in Different letters indicate significance between treatments (Tukey s honest significant difference, α = 0.05). Bars indicate standard error.

5 Designing Fungicide Programs 11 Figure 4 Influence of leaf removal on early through midseason spray coverage in the fruiting zone in Asterisks indicate treatments in which leaves were removed prior to the spray date indicated. Different letters indicate significance between treatments (Tukey s honest significant difference, α = 0.05). Bars indicate standard error. disease control in some of the fungicide programs could lead to differences in wine quality, despite a lack of major differences in initial fruit quality. Broader Impact The understanding of grape powdery mildew management has progressed beyond knowledge of when and what to spray; we know the general efficacies of many standard products, and we know when key periods of infection and disease development are in vineyards. At the same time, growers juggle maximizing disease management programs with managing fungicide resistance development and labor availability. Our field trial explores how to optimize the efficiency of different chemical modes of action in a seasonal spray program while still incorporating cultural practices. The intention is to define management windows during which specific modes of action may have optimal performance, which could provide guidelines for planning fungicide rotations. Consistent with other studies that use ontogenic resistance as a basis for developing spray programs, 12 we saw that the best program performance was achieved when management was focused early Table 2 Fruit quality data for 2013 and For each year, different letters within a column indicate means separation (Tukey s honest significant difference, α = 0.05) Fungicide program Brix Titratable acidity (g/l) Control (ab) (cd) Q (ab) (d) Q (ab) (ab) Q (a) (a) Q (b) (ab) C (ab) (abc) M (ab) (bcd) 2014 Fungicide program Brix Titratable acidity (g/l) Control (ab) (a) 2.80 Q (ab) (ab) 2.78 Q (a) (ab) 2.80 Q (ab) (ab) 2.82 Q (ab) (b) 2.81 C (ab) (ab) 2.78 C (ab) (ab) 2.79 M (a) (ab) 2.78 M (b) (ab) 2.80 ph ph

6 12 Moyer et al. (fruit set and earlier) in the growing season, regardless of product mode of action. By improving the timing of specific chemical modes of action in a spray program and using different modes of action during the critical window for infection, disease can be effectively managed while being mindful of the risks of fungicide resistance development that can arise from repeated use of the same chemical mode of action. Of emphasis, however, is that while product selection and timing are key components to disease management, they are irrelevant if the product does not make it to the plant sprayer functionality, and matching of water carrier volume to canopy size are critical components of a management program. Given the high disease pressure 13 that occurred in this trial, leaf removal should not be considered as a standalone management option. In some cases, leaf removal may increase disease incidence on clusters by exposing them to high levels of powdery mildew inoculum when they are not protected by a fungicide. In other words, if cultural practices such as fruit zone removal are a part of a management program, their timing should be considered as part of the management regime. In the case of mildew management, leaf removal should not occur immediately after a fungicide spray, as this would remove product from the vineyard, nor should it take place substantially before a fungicide spray, as clusters would be left exposed to potential infection. Ideally, leaf removal should occur no more than two days before fungicide application. Experimental Design Vineyard description. Our experiments were conducted at the Roza Research Farm of Washington State University s Irrigated Agriculture Research and Extension Center (46 17 N; W) during the 2013 and 2014 growing seasons. The vineyard (~1 ha) contained a mixed planting of own-rooted Vitis vinifera Chardonnay and Riesling planted in 2001; only Riesling was used for the experiment to eliminate potential cultivar influence. Vines were planted with 1.8 m 2.7 m (6 ft vine 8 ft row) spacing, with north-south row orientation. Vines were spur-pruned and trained to a modified vertical shoot-positioned system with a single set of mobile catch wires above the cordon. Drip irrigation was used in the vineyard; a weed-free strip was chemically maintained directly under the vines, and natural vegetation was maintained between rows with periodic mowing. The vineyard block used in this study is reserved for pathology experiments, and as such, the eastern- and western-most rows have remained unsprayed since planting to provide a sufficient reservoir of Erysiphe necator inoculum. Weather data was collected from Washington State University s AgWeatherNet system. 14 The Roza weather station was used and is located within 4 m (13 ft) of the experimental vineyard. Daily maximum and minimum air temperatures and daily total precipitation for 2013 and 2014 are presented in Figure 2. Fungicide treatments. Specific fungicide treatments and application timing are listed in Table 1. This rotation was chosen to examine the effects of specific fungicide timing in a complete program rotation on final cluster disease severity. Fungicide treatment replicate plots consisted of six-vine panels; data was collected from the center four vines (Figure 5). Individual fungicide treatments were replicated four times. Treatments were applied using a modified Rears sprayer with a custom-built boom equipped with seven flat spray brass nozzles (TeeJet 8006; TeeJet Nozzles) at 100 psi (nozzle output at 1 gal/min). The sprayer consisted of two 95-L tanks and one 189-L tank. Tractor speed was 3.2 to 4.8 km/hr (2 to 3 mph). The total water volume applied changed as the canopy developed; the first spray was applied using three nozzles, resulting in L/ha (45 gal/acre). The second spray was applied using five nozzles, resulting in L/ha (75 gal/acre); the remaining sprays were applied using seven nozzles at L/ha (105 gal/acre). Regardless of total water volume applied, the product rate consisted of the following per-hectare equivalents: myclobutanil (Rally) at g (5 oz/acre); quinoxyfen (Quintec) at ml (4 fl. oz/acre); cyflufenamid (Torino) at ml (3.4 fl. oz/acre); and metrafenone (Vivando) at ml (15.4 fl. oz/acre). All treatments were applied with a surfactant (Break-Thru) at 62.5 ml/l (8 fl. oz/gal). The control treatment was unsprayed and used to develop a baseline idea of disease pressure in the block. When evaluating fungicide performance, untreated controls are recommended to help determine if disease control was a result of treatment or due to nonconducive environmental conditions or low inoculum levels. Leaf removal treatments. Fruit zone leaf removal consisted of removing leaves on a shoot from the base of the shoot up and adjacent to the secondary cluster. Leaves were removed on the east side of the canopy, per common practice in eastern Washington. The following timing of fruit zone leaf removal was evaluated: control (no leaf removal), prebloom (50% of clusters at rachis elongation), bloom (50% of clusters at 50% capfall), and 4 wks postbloom. In 2013, leaf removal treatments were implemented on 17 May (prebloom), 7 June (bloom), and

7 Designing Fungicide Programs 13 5 July (4 wks postbloom). In 2014, leaf removal treatments were implemented on 30 May (prebloom), 16 June (bloom) and 11 July (4 wks postbloom). Fruit zone leaf removal treatments were nested within each fungicide treatment. Of the four center data vines in each fungicide treatment replicate plot, one vine was dedicated to each leaf removal treatment. As with fungicide treatments, leaf removal within each fungicide treatment was replicated four times. Spray coverage. Spray coverage was evaluated in the leaf removal treatments using water-sensitive cards (Syngenta Crop Protection AG). Cards were affixed to the node between the basal and secondary clusters using a clothespin, with the water-sensitive side facing east. The cards were placed in the vineyard just prior to spraying and were removed promptly after they had dried in the field (~2 to 3 hrs). Four cards were placed in each leafremoval subplot for one fungicide treatment in 2013 and Coverage was visually estimated as percent area covered in three, 1-cm 2 areas per card. Spray coverage was assessed on 2 July 2013, and was expanded to 10 June, 19 June, 17 July, and 31 July Disease ratings. Powdery mildew ratings were collected by visually estimating the percent surface area of the cluster affected. Five clusters from each fungicide program and leaf removal treatment replicate (a total of 20 clusters per fungicide treatment replicate) were nondestructively assessed at the end of each growing season, on 18 Sept 2013 and 30 Sept Fruit quality assessments. To evaluate soluble solids (Brix), ph, and TA in the fruit, three whole clusters per fungicide + leaf removal treatment replicate were pressed in a 4-L plastic zip-top bag until all the berries were macerated. Juice from each bag was decanted into a dedicated 50-mL conical plastic centrifuge tube and used to determine soluble solids, ph, and TA. Juice soluble solids were measured using a digital refractometer (Quick-Brix 60, Mettler-Toledo). Juice ph was measured using a ph meter (InLab Versatile 413, Mettler-Toledo). The same juice was then used for TA measurements. 15 Statistical analyses. All statistical analyses were completed in JMP 9 (SAS Institute, Inc.) using the linear mixed model platform, with fungicide treatment as a fixed effect, leaf removal treatment nested within fungicide treatment, Figure 5 Field experimental design. Fungicide treatments were applied to a panel of six vines. To reduce potential carryover from adjacent treatments, data were only recorded from the center four vines. Stakes in the ground marked start and stop points for fungicide application to aid the sprayer operator. Fungicide treatments were replicated four times. Leaf removal treatments occurred on a single vine within the panel and were replicated four times.

8 14 Moyer et al. and replicate as a random factor. Means separation was done using Tukey s honest significant difference at α = References and Footnotes 1. Gadoury DM, Seem RC, Ficke A and Wilcox W Ontogenic resistance to powdery mildew in grape berries. Phytopathology 93: Hansen M. Research leads to better control for grape disease. 25 May Good Fruit Grower. Washington State Fruit Commission, Yakima, WA. Online: com/hansen-research-leads-to-better-control-for-grapedisease/. Accessed 7 June The area receives ~200 mm of annual precipitation, which predominately falls during the winter months. 4. Moyer MM and O Neal S Pest Management Strategic Plan for Washington State Wine Grape Production. Western Region IPM Center, USDA-NIFA. Online: ipmcenters.org/pmsp/pdf/wa_winegrape_pmsp_2014.pdf. 5. Moyer MM, Gadoury DM, Wilcox WF and Seem RC Weather during critical epidemiological periods and subsequent severity of powdery mildew on grape berries. Plant Dis 100: Grove G. Viticulturist (personal vineyard). Personal communication, Hoff R, Director of Viticulture, Mercer Canyons Inc. Personal communication, 2016; Schultz A, General Manager, Elephant Mountain Vineyards. Personal communication, Fungicide Resistance Action Committee: info/. Specific information on FRAC fungicide categories is updated annually and is found at: publications/downloads. 9. Prengaman K and Mullinax TJ. Resistance rising for powdery mildew. 26 Feb Good Fruit Grower. Washington State Fruit Commission, Yakima, WA. Online: goodfruit.com/resistance-rising-for-powdery-mildew/. Accessed 2 May Fungicide program (Table 1) name abbreviations are designed to reflect the active ingredient (Q = quinoxyfen; C = cyflufenamid; M = Metrafenone) and the timing of the application relative to the timing of the spray during the Critical Window. For example, Q2 indicates that quinoxyfen was applied in the second spray during the period, whereas M3 indicates that metrafenone was applied in the third spray. 11. Gadoury DM, Seem RC, Wilcox WF, Henick-Kling T, Conterno L, Day A and Ficke A Effects of diffuse colonization of grape berries by Uncinula necator on bunch rots, berry microflora, and juice and wine quality. Phytopathology 97: ; Ough CS and Berg HW Powdery mildew sensory effect on wine. Am J Enol Vitic 30:321; Stummer BE, Francis IL, Zanker T, Lattey KA and Scott ES Effects of powdery mildew on the sensory properties and composition of Chardonnay juice and wine when grape sugar ripeness is standardised. Aust J Grape Wine Res 11: Caffi T, Legler SE, Rossi V and Bugiani R Evaluation of a warning system for early-season control of grapevine powdery mildew. Plant Dis 96: ; Gadoury DM, Seem RC, Ficke A and Wilcox WF Ontogenic resistance to powdery mildew in grape berries. Phytopathology 93: ; Gadoury DM, Pearson RC, Seem RC and Park EW Integrating the control programs for fungal diseases of grapevine in the northeastern United States. Vitic Enol Sci 52: ; Moyer MM, Gadoury DM, Wilcox WF and Seem RC Release of Erysiphe necator ascospores and impact of early-season disease pressure on Vitis vinifera fruit infection. Am J Enol Vitic 65: ; Moyer MM, Gadoury DM, Wilcox WF and Seem RC Weather during critical epidemiological periods and subsequent severity of powdery mildew on grape berries. Plant Dis 100: Disease pressure is defined here as macro- and microclimate conditions that are conducive to rapid disease development when the pathogen and host plant are present. For grape powdery mildew, the primary drivers for rapid disease development are moderate temperatures (Delp CJ Effect of temperature and humidity on the grape powdery mildew fungus. Phytopathology 44: ; Moyer MM, Gadoury DM, Cadle-Davidson L, Dry IB, Magarey PA and Seem RC Effects of acute low temperature events on the development of Erysiphe necator and susceptibility of Vitis vinifera. Phytopathology 100: ; Choudhury RA, McRoberts N and Gubler WD Effects of punctuated heat stress on the grapevine powdery mildew pathogen, Erysiphe necator. Phytopathol Mediterr 53: ) and moderate to high relative humidity (Carroll JE and Wilcox WF Effects of humidity on the development of grapevine powdery mildew. Phytopathology 93: ). 14. AgWeatherNet can be accessed at: The samples were titrated to ph 8.20 using 0.1 M sodium hydroxide (NaOH).

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