Relative Susceptibility of Selected Apple Cultivars to Powdery Mildew Caused by Podosphaera leucotricha

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1 2009 Plant Management Network. Accepted for publication 11 September Published 19 November Relative Susceptibility of Selected Apple Cultivars to Powdery Mildew Caused by Podosphaera leucotricha Alan R. Biggs, Kearneysville Tree Fruit Research and Education Center, West Virginia University, P.O. Box 609, Kearneysville, WV 25443; Keith S. Yoder, Department of Plant Pathology, Physiology, and Weed Science, Virginia Polytechnic Institute and State University Agricultural Research and Extension Center, 595 Laurel Grove Road, Winchester, VA 22602; and David A. Rosenberger, Hudson Valley Laboratory, Cornell University, P.O. Box 727, Highland, NY Corresponding author: Alan R. Biggs. Biggs, A. R., Yoder, K. S., and Rosenberger, D. A Relative susceptibility of selected apple cultivars to powdery mildew caused by Podosphaera leucotricha. Online. Plant Health Progress doi: /php rs. Abstract Apple powdery mildew thrives during dry spring and summer weather wherever apples are grown. The fungus perennates in buds, making it difficult to control and, although it can cause fruit russet, it primarily causes losses due to its chronic effect on tree vigor and yield. Data were collected over several years from 1995 (23 entries) and 1999 (22 entries) plantings of new apple cultivars and selections established at multiple locations as part of regional project NE-183. The cultivars Golden Delicious and McIntosh were the standards in both plantings. Incidence of powdery mildew on leaves and fruit was observed and data were analyzed to determine differences due to location and cultivar. One of the two planting group analyses indicated the significance of cultivar differences due to location. In general, the cultivars Ginger Gold, Suncrisp, GoldRush, Crimson Crisp, and Delblush, and the selection CQR10T17 were the most susceptible, whereas the cultivars Gala Supreme, Enterprise, Zestar, September Wonder, Hampshire, and the selections NY and NY exhibited the lowest incidences of mildew. Pinova was the most highly susceptible cultivar to mildew on fruit in Virginia, followed by Crimson Crisp and the selection NY Percent leaf area with mildew was related to incidence of mildew on leaves; however, fruit symptoms were not significantly related to disease incidence or severity on the foliage. Introduction Apple powdery mildew, caused by Podosphaera leucotricha, thrives during dry spring and summer weather wherever apples are grown (7). The fungus perennates in buds, making it difficult to control and, although it can cause fruit russet, it primarily causes losses due to its chronic effect on tree vigor and yield (19). Because of the chronic effects of the disease, increased control efforts under heavy inoculum conditions are required as part of the routine management program for highly susceptible cultivars. Cultivars that are moderately or highly susceptible to powdery mildew comprise more than 40% of the apple plantings in the Mid-Atlantic region and include Ginger Gold, Golden Delicious, Granny Smith, Idared, Jonagold, Jonathan, Paulared, Rome Beauty, Stayman Winesap, and Winesap. Losses can be severe in these cultivars, especially under periods of prolonged favorable weather conditions (19). Cultivars with resistance to mildew could result in increased profitability for producers from increased yields and decreased management costs. Several researchers have observed differences among apple cultivars to mildew, although there have been no new reports recently (1,12,13,21). In 1994, a regional project was initiated to examine the performance of new apple cultivars in replicated trials under a wide range of climatic and edaphic conditions. The project (NE-183), entitled "Multidisciplinary Evaluation of New

2 Apple Cultivars" (currently NECC-1009 "Multidisciplinary Evaluation of New Tree Fruit Cultivars"), began with 26 cooperators in 18 states and two Canadian provinces. A primary objective of project NE-183 was to evaluate horticultural qualities and pest and pathogen susceptibility of new apple cultivars, strains, and advanced selections with commercial potential and to determine the limitations and positive attributes of these cultivars (5,6,8). To date, researchers have documented the relative susceptibilities of the NE-183 apple cultivars to bitter rot (caused by Colletotrichum acutatum) (2), white rot (caused by Botryosphaeria dothidea) (3), and black rot (caused by Botryosphaeria obtusa) (4). Preliminary reports on relative susceptibility to apple scab (caused by Venturia inaequalis), powdery mildew (caused by Podosphaera leucotricha), and cedar apple rust (caused by Gymnosporangium juniperi-virginianae), have been published (9,11,14,20,21). This study reports the relative susceptibility of apple cultivars and selections to the powdery mildew pathogen. Images of symptoms of this disease are presented in Figs. 1 through 6. Fig. 1. Powdery mildew lesions on dormant apple shoots. Photo by A. B. Groves. Fig. 2. Rome apple tree with numerous shoots showing primary powdery mildew infections. Fig. 3. Closer view of an apple terminal shoot with primary powdery mildew infection. Fig. 4. Apple fruit bud with primary powdery mildew infection. Fig. 5. Abaxial surface of an apple leaf showing signs of secondary powdery mildew infection. Fig. 6. Apple fruit showing russetting caused by powdery mildew blossom infection.

3 Establishing and Maintaining Diverse Plantings of Apple Cultivars Data were collected from two cultivar groups established in 1995 and 1999, with 23 apple cultivars and selections (hereafter referred to only as cultivars) in the 1995 group and 22 apple cultivars in the 1999 group. Golden Delicious and McIntosh were the standards in both groups. Groups from which powdery mildew data were collected were located near Highland, NY (1995 and 1999), Winchester, VA (1995 and 1999), and Kearneysville, WV (1995) group. All 23 cultivars (Table 1) were propagated by Adams County Nursery, Aspers, PA, on M.9 NAKB 337 rootstock in Golden Delicious was included as a universal standard in all sites involved in the NE-183 project since it performs well across a wide variety of climates. In addition, Pioneer McIntosh served as an additional standard cultivar with known susceptibility to apple scab. Single tree plots were replicated five times in a randomized complete block design. Trees were planted in 1995 at an in-row spacing of 2 m with spacing between rows varying by location. Drive middles were planted with Kentucky-31 fescue (Festuca arundinacea), and a weed-free strip (1 m wide in 1995; 2 m wide in the remaining years) was maintained in the tree row with herbicides applied at recommended rates. Trees were headed at planting time and individually staked. Minimal pruning and training was done to allow assessment of natural tree structure, and to allow expression of natural flowering and fruit set tendencies. Trees were not allowed to crop the first 2 years and all flowers or young fruit were removed the first year by hand or by chemical means followed by hand thinning. Trees initially were allowed to set fruit in the second year. Fertilizer application, pest management, and orchard floor management were subsequently done according to recommended local standards and based on leaf analyses. Weather data were taken with different instrumentation at the different locations, and included daily maximum and minimum temperatures, wetting periods, and precipitation during the growing season. Trees were allowed to fruit in their third year, 1997, and in subsequent years. Insecticides were applied from 1996 through 2000, as were fixed copper and/or streptomycin to manage fire blight.

4 Table 1. Percent leaves with powdery mildew infection from 23 apple cultivars, from the 1995 group at three locations. Disease ratings by plot location Cultivar or selection x New York Virginia West Virginia Ginger Gold (most) 43.9 a y 51.9 a 6.0 b-e Suncrisp 22.5 c 36.4 b 5.3 b-f GoldRush z 29.9 b 28.1 cde 9.4 a Creston 19.4 cd 30.3 cd 7.5 abc Braeburn 17.2 de 30.3 cd 7.8 ab Shizuka 23.0 c 30.3 cd 4.0 d-h Pioneer Mac 15.1 def 33.0 bc 4.6 c-h Orin 17.1 de 29.3 cd 4.8 b-g Golden Delicious 15.7 def 30.7 cd 4.0 d-h Honeycrisp 14.4 ef 28.6 cd 4.2 d-h Cameo 14.6 ef 26.6 c-f 4.1 d-h Sunrise 13.0 e-h 17.2 hij 3.6 e-h Arlet 9.5 g-j 22.3 fgh 5.3 b-f Sansa 11.6 f-i 15.2 j 6.7 a-e Golden Supreme 13.8 efg 22.7 fgh 2.4 fgh Fortune 11.8 fgh 25.7 d-g 2.1 gh Yataka 3.3 l 18.6 hij 2.5 fgh Fuji Red Sport #2 5.4 jkl 19.2 hij 2.7 fgh Senshu 7.0 i-l 21.0 hij 1.8 gh Pristine z 8.2 h-k 16.0 ij 2.0 gh Enterprise z 5.3 jkl 13.6 jk 2.8 fgh NY z 5.8 jkl 8.3 k 2.4 fgh Gala Supreme (least) 3.0 l 8.8 k 1.6 h x The order of apple cultivars is from most susceptible to least susceptible, based on the mean ranks of % leaves infected across locations. y Means within columns represent observations from 1995 to 1998, inclusive, for New York, Virginia, and West Virginia. Different letters denote significant differences according to the Waller Duncan k-ratio t test (P = 0.05). z Indicates cultivars or selections with genetic resistance to the apple scab pathogen, Venturia inaequalis group. All 22 cultivars (Table 2) were budded in 1997 at Wafler Nursery in Walcott, NY, on M.9 NAKB 337 rootstock. Golden Delicious was included in the 1999 group as a standard for comparisons between planting dates. Rogers McIntosh was included in the 1999 group to serve as an additional standard cultivar with known susceptibility to apple scab. Subsequent orchard establishment, horticultural management, experimental design, and weather monitoring were as described above.

5 Table 2. Percent leaves, percent leaf area, and percent fruit injury following powdery mildew infection on 22 apple cultivars, from the 1999 group at two locations. Disease ratings by plot location Cultivar or selection w New York Virginia % leaves % leaves % leaf area % fruit CQR10T17x (most) 48.6 a y 31.4 ab 22.5 a 0.27 g Crimson Crisp (Co-op 39) x 46.4 a 30.4 ab 21.3 a 27.8 b Delblush 45.2 a NA NA NA Sundance (Co-op 29) x 33.6 bc 33.3 a 21.3 a 3.6 fg Cripps Pink NA z 27.2 bc 12.3 bc NA Golden Delicious 42.1 ab 22.2 c-f 5.2 efg 1.5 g Pinova 26.4 c-f 29.7 abc 11.7 bcd 39.9 a Chinook (BC 8S-27-51) 43.1 ab 20.2 fg 9.1 b-e 0.0 g NJ cd 21.5 d-g 7.6 c-g 13.0 de Runkel Hampshire 25.8 c-f 24.9 bcd 9.7 b-e 1.7 fg Rogers McIntosh 18.9 fg 30.6 ab 14.2 b 3.1 fg Scarlet O'Hara (Co-op 25) x 29.4 cde 19.5 g 6.3 d-g 21.7 bc NY x 19.1 fg 22.3 cde 7.3 d-g 17.6 cd BC 8S cde 18.3 g 5.7 efg 8.4 ef NJ fg 20.7 efg 4.8 efg 0.0 g Princess (CQR12T50) x 20.7 efg 18.7 g 3.6 fg 1.2 g Ambrosia 23.9 def 13.0 hi 3.2 fg 0.0 g NY x 22.7 d-g 13.1 hi 2.1 g 27.0 b NY x 17.8 fg 20.0 g 4.9 efg 0.98 g Hampshire 18.9 fg 17.6 gh 8.4 b-e NA Zestar! (MN 1824) 16.9 fg 12.1 i 3.4 fg 0.0 g September Wonder (least) 13.5 g 10.7 i 5.5 efg NA w The order of apple cultivars is from most susceptible to least susceptible, based on the mean ranks of % leaves infected across locations. x Indicates genotypes with genetic resistance to the apple scab pathogen, Venturia inaequalis. y Means within columns represent observations from 1999 to 2004, inclusive, from Virginia; and 2000 and 2004 from New York. Letters denote the differences among means according to the Waller Duncan k-ratio t test (P = 0.05). z NA = cultivar not available. Moderate to high pathogen inoculum levels were encouraged and minimal spray schedules were applied, based on local needs, to maintain tree growth and prevent severe defoliation. In the 1995 and 1999 groups in New York and in in the 1995 group in Virginia, a protectant fungicide (primarily captan 50W 1 lb per 100 gal dilute) was applied at a reduced rate three times in May or early June to suppress scab. No fungicide was applied in West Virginia, in in the 1995 group in Virginia or in the 1999 group in Virginia. Mildew inoculum was naturally abundant in New York and Virginia, but not in West Virginia.

6 Determining the Relative Susceptibility of Apple Cultivars to Powdery Mildew Cooperators followed established protocols for disease evaluation in mid to late summer after it appeared that terminal bud set was completed. Ratings in New York and West Virginia involved rating the eight youngest leaves on five to 10 terminal shoots after it appeared that terminal bud set was completed. Ratings in Virginia involved all leaves on five to ten terminal shoots. Evaluation dates for leaves usually were on or near June in West Virginia; 8 August to 4 October in Virginia; and 11 June to 3 July in New York. For fruit, a minimum of 5, and up to 25 fruit per cultivar were visually assessed at harvest for presence or absence of mildew-induced fruit russetting. At each location, evaluations were made to determine percentage of leaves with mildew symptoms, percentage of leaf area affected, and the percentage of fruit with symptoms. Data analysis. Although powdery mildew data were collected at all locations in all years, for the purposes of determining relative susceptibility, only data sets that showed 10% leaf infection incidence on at least one cultivar at that location were included in the analysis. For the 1995 group, those data sets included Virginia (1995, 1996, 1997, and 1998); West Virginia (1995, 1996, 1997, and 1998); and New York (1995, 1996, 1997, and 1998). For the 1999 group, those data sets included Virginia (1999 to 2004, inclusive); and New York (2000 and 2002). Each variable was analyzed in a mixed model analysis of variance (PROC MIXED, SAS Institute Inc., Cary, NC) in which sources of error were the fixed effects (cultivar and location) and random effects of replicate, year, interaction of replicate and year, and interaction of cultivar and year, where each of these was nested within location. The Waller Duncan k-ratio t- test method was used for determining the significance of differences among means. Results of Mildew Assessments In the 1995 group, across all cultivars and locations, mean disease incidence ranged from 1.6% for Gala Supreme in West Virginia to 51.9% for the cultivar Ginger Gold in Virginia (Table 1). For the standard, Golden Delicious, mean disease incidence ranged from 4.0% in West Virginia to 30.7% in Virginia. Incidence of powdery mildew on leaves varied significantly among cultivars (P = ), and locations (P = 0.05). The cultivar location interaction was significant (P = ). When data from West Virginia were excluded from the analysis, the location and cultivar location effects were not significant (P = 0.26 and P = 0.75, respectively). Ginger Gold was the most susceptible cultivar, followed by Suncrisp, GoldRush, Creston, and Braeburn. The cultivars Gala Supreme, NY , and Enterprise generally exhibited the lowest incidences of powdery mildew (Table 1). In the 1999 group, across all cultivars and locations, mean disease incidence ranged from 10.7% for the cultivar September Wonder in Virginia to 48.6% for CQR10T17 in New York (Table 2). For the standard, Golden Delicious, mean disease incidence ranged from 22.2% in Virginia to 42.1% in New York. Incidence of powdery mildew on leaves varied significantly among cultivars (P = ) and cultivar location (P = 0.037). The location main effect was not significant (P = 0.62). The greater susceptibility of Roger s McIntosh, Pinova, NY and NY in Virginia when compared to New York accounted for a large part of the cultivar x location interaction. The cultivars CQR10T17, Crimson Crisp, Delblush, and Sundance were the most susceptible. The cultivars Zestar!, NY , Hampshire, and September Wonder were the least susceptible to powdery mildew (Table 2). Leaf area affected with mildew in Virginia ranged from 2.1% for NY to 22.5% for CQR10T17 (Table 2). Differences among cultivars and selections were significant (P = 0.003). Percentage of fruit with powdery mildew russet symptoms in Virginia ranged from 0% for Cripps Pink, Chinook, NJ 109, Ambrosia, and Zestar! to 39.9% for the cultivar Pinova (Table 2). Percent leaf area affected by mildew was significantly and positively related to mildew incidence (R² = 0.53, P = ). Neither incidence nor leaf area affected were related to fruit symptoms (R² = , P = 0.76; and R² = , P = 0.26,

7 respectively); however, fruit russetting and their perceived causes may be affected and confounded by environmental factors and varietal differences in flower bud development. Recommendations There are few studies that demonstrate the relative susceptibility of apple cultivars and selections to powdery mildew. With the different locations that comprised this study, we were able to demonstrate significant genetic variability in apple to the same as well as different regional populations of P. leucotricha. Although the data were not strong, with only one of the two planting groups showing a significant location cultivar interaction, our results tend to support those of Urbanietz and Dunemann (15). These authors found, using a molecular characterization of P. leucotricha isolates in Europe, an overall low level of genetic variability accompanied by a high level of diversity in terms of virulence. Tests on detached leaves of a collection of 36 Malus genotypes showed differentiation of five isolates by their virulence patterns. The authors concluded that physiological races of P. leucotricha exist in Europe. Interestingly, reports of high phenotypic diversity among European isolates suggest that sexual reproduction may be involved in the disease cycle of the pathogen in Europe. This has not been reported for powdery mildew in North America (10). Although there was no relationship between relative susceptibility to P. leucotricha and the presence of genes for resistance to the apple scab pathogen, Venturia inaequalis, it is noteworthy that the scab-resistant cultivars Pristine, Enterprise, NY , and NY are among the most resistant to powdery mildew. The latter three are also among the most resistant to cedar apple rust based on previous results from these plantings (Biggs et al., unpublished data). This is an important attribute for early season disease management in areas where powdery mildew is a problem, and particularly so if one is attempting to grow fruit as certified organic where effective controls may require frequent applications of an organically-approved fungicide. By contrast, the scab-resistant cultivars Sundance, GoldRush, Scarlet O Hara, Princess, Crimson Crisp, and CQR10T17 are highly susceptible to powdery mildew and would require early season fungicide applications for mildew and rust management in high inoculum areas in spite of their resistance to scab. A special action threshold level at 20% leaf infection is used for mildew management in the Mid-Atlantic region. The threshold is based on yield effects in research plots in Virginia (16,17,18). Many of the cultivars tested in Virginia and New York regularly exceeded the action threshold and will likely require intensive disease management if they become widely planted. Acknowledgments We appreciate the technical support of Catherine Ahlers, Richard Christiana, A. E. Cochran II, Larry Crim, S. W. Kilmer, Frederick Meyer, W. S. Royston, Jr., Keri VanCamp, Isabelle Winfield, and Robert Young. We acknowledge the research support of the USDA-ARS Appalachian Fruit Research Station and the financial support of Virginia Agricultural Council, Virginia Apple Research Program, and USDA - CSREES via Hatch Act funding for Multi-State Research Project NE-183. Literature Cited 1. Aldwinckle, H. S Field susceptibility of 51 apple cultivars to apple scab and apple powdery mildew. Plant Dis. Rep. 58: Biggs, A. R., and Miller, S. S Relative susceptibility of selected apple cultivars to Colletotrichum acutatum. Plant Dis. 85: Biggs, A. R., and Miller, S. S Relative susceptibility of selected apple cultivars to Botryosphaeria dothidea. HortScience 38: Biggs, A. R., and Miller, S. S Relative susceptibility of selected apple cultivars to Botryosphaeria obtusa. HortScience 39:

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