Relative Susceptibility of Selected Apple Cultivars to Sooty Blotch and Flyspeck

2010 Plant Management Network. Accepted for publication 13 May 2010. Published. Relative Susceptibility of Selected Apple Cultivars to Sooty Blotch and Flyspeck Alan R. Biggs, Kearneysville Tree Fruit Research and Education Center, West Virginia University, P.O. Box 609, Kearneysville, WV 25443; Daniel R. Cooley, Department Plant, Soil, and Insect Science, University of Massachusetts, Amherst, MA 01003; David A. Rosenberger, Hudson Valley Laboratory, Cornell University, Highland, NY 12528; and Keith S. Yoder, Department of Plant Pathology, Physiology, and Weed Science, Virginia Polytechnic Institute and State University Agricultural Research and Extension Center, Winchester, VA 22602 Corresponding author: Daniel R. Cooley. dcooley@microbiol.umass.edu Biggs, A. R., Cooley, D. R., Rosenberger, D. A., and Yoder, K. S. 2010. Relative susceptibility of selected apple cultivars to sooty blotch and flyspeck. Online. Plant Health Progress doi:10.1094/php-2010-0726-01-rs. Abstract Incidence data for sooty blotch and flyspeck (SBFS), apple diseases caused by a complex of fungi that includes Schizothyrium pomi, Peltaster fructicola, Leptodontidium elatius, and Geastrumia polystigmatis, were collected over several years from planting groups of new apple cultivars and selections planted at multiple locations in either 1995 (23 entries) or 1999 (22 entries) as part of the NE-183 Multistate Project. SBFS incidence on fruit was analyzed, and data from sites in Massachusetts, New York, and Virginia were compared to determine if there were differences among cultivars. Incidence of SBFS varied among cultivars in both the 1995 and 1999 plantings, and among locations in the 1999 plantings. These differences were primarily the result of harvest date, with cultivars that were harvested latest having the highest disease incidences. Lower SBFS incidence on the earlier maturing cultivars apparently resulted from disease avoidance, as these apples were exposed to fewer hours of wetting and high relative humidity, environmental factors favorable for growth of SBFS fungi. Management tactics targeting SBFS are especially critical for cultivars that mature late in the season. Introduction Fig. 1. Sooty blotch and flyspeck on the apple cultivar Cameo before harvest. Sooty blotch and flyspeck (SBFS) are diseases caused by a complex of different species of fungi that colonize the cuticles of apple and pear fruit, resulting in cosmetic damage that significantly decreases crop value (Fig. 1). In the northeastern United States, three to five fungicide applications in the latter half of the production season are made primarily to control SBFS, and these applications may represent as much as 40% of the total fungicides applied to the crop each year (15). Initially, sooty blotch and flyspeck were considered two diseases that commonly occurred together on the surface of apple fruit, the result of two different fungi, one producing diffuse, dark areas (sooty blotch, Fig. 2) and one producing clusters of shiny, black, round to ovoid specks (flyspeck, Fig. 3) (1,3,14). More recent genetic and morphological studies have identified over 60 species of fungi in the complex (4,5,19,25). These fungi are widely distributed across the eastern half of the United

States, with many occurring across the whole region, while others are limited to parts of it (19). However, the major species of SBFS fungi in the study areas described herein are generally similar (18,19), and included Schizothyrium pomi (flyspeck phenotype), Peltaster fructicola, Geastrumia polystigmatis, and Pseudocercosporella sp. (RH1 and RH3) (the latter three are all sooty blotch phenotypes) (19). Fig. 2. Sooty blotch and flyspeck on the apple cultivar Cameo. Fig. 3. Flyspeck and sooty blotch on apple cultivar Golden Delicious. Differences in SBFS incidence among apple cultivars are largely related to harvest date and fruit color (2,14). Generally, the longer fruit remain on trees without fungicide protection, the more likely it is that SBFS fungi can develop and produce signs (28). These signs are more visible on yellow and other lightcolored fruit than on dark-colored fruit. Belding et al. (6) examined sooty blotch incidence on several apple cultivars and selections harvested on the same date to determine whether epicuticular waxes influence SBFS incidence. They found that the sooty blotch severity varied significantly between cultivars and suggested that this was the result of differences in fungal nutrients that leach from fruit. However, to our knowledge no other studies have been done to identify relative susceptibility of apple cultivars to colonization by the SBFS complex. 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 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 (21,22,24). To date, researchers have documented the relative susceptibilities of the NE-183 apple cultivars to apple scab (12), powdery mildew (caused by Podosphaera leucotricha) (11), rust diseases (10), bitter rot (caused by Colletotrichum acutatum) (7), white rot (caused by Botryosphaeria dothidea) (8), and black rot (caused by Botryosphaeria obtusa) (9). Preliminary reports on relative susceptibility to apple scab, powdery mildew, and cedar apple rust (caused by Gymnosporangium juniperi-virginianae), also have been published (26,27,29,33). The objective of this study was to evaluate, at several field locations, the relative susceptibility of new apple cultivars and selections to sooty blotch and flyspeck infestations. Establishing and Maintaining Diverse Plantings of Apple Cultivars Data were collected from two groups of apple cultivars and selections (hereafter referred to as cultivars) established in 1995 (23 entries) and 1999 (22 entries). Planting groups from which data were collected were located near

Winchester, VA (1995 and 1999); Kearneysville, WV (1995); Belchertown, MA (1999); and Highland, NY (1995 and 1999). 1995 group. All trees of the 23 apple cultivars were propagated by Adams County Nursery, Aspers, PA, on M.9 NAKB 337 rootstock in 1993. Golden Delicious was included as a universal standard in all sites involved in project NE-183 since it performs well across a wide variety of climates. In addition, the Pioneer strain of McIntosh was included to serve as an additional standard cultivar with known susceptibility to apple scab. All locations had five replications of all 23 cultivars. The NE-183 Horticulture Subcommittee made cultural and management decisions the first two years (1995 and 1996) that were applied over all plantings. 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, but the persisting fruit were counted and then all fruit was removed by hand to assure good return bloom for the third 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. The experimental planting design was a randomized complete block design with five single-tree replicates. 1999 group. All trees of the 22 apple cultivars were budded in 1997 at Wafler Nursery in Walcott, NY, on M.9 NAKB 337 rootstock. Golden Delicious and Rogers McIntosh were included in the 1999 group as standards for comparisons among plantings. Subsequent orchard establishment, horticultural management, experimental design, and weather monitoring were as described above. Moderate to high pathogen inoculum levels were encouraged in the dedicated disease plantings and a minimal spray schedule was applied to maintain tree growth and prevent severe defoliation. In Massachusetts, New York, and Virginia, a protectant fungicide (primarily captan 50W at 1 lb per 100 gal dilute) was applied at a reduced rate one to three times in May or early June to suppress, but not eliminate, scab. Sooty blotch and flyspeck inoculum was naturally abundant at all locations. Determining the Relative Susceptibility of Apple Cultivars to Sooty Blotch and Flyspeck Cooperators followed established protocols for disease evaluation, which involved rating 10 to 50 fruit per replicate, depending on availability. Evaluation dates usually were on or near the respective harvests of the cultivars. The dependent variables were the percentage of fruit with sooty blotch and flyspeck signs. Maturity dates for cultivars are based on published observations (16,17). Although incidence data were collected at all locations in all years, only data sets that showed a minimum of 10% flyspeck incidence on the cultivar Golden Delicious were included in the final analyses. For the 1995 planting, those data sets included Virginia (1997 to 2001, inclusive) and New York (1997, 1998, 1999, 2003, and 2004). Data from West Virginia were excluded. For the 1999 planting, those data sets included Massachusetts (2001, 2003, and 2004), New York (2001, 2003, and 2004), and Virginia (2001-2004). 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. The relationship between maturity date and disease incidence and between sooty blotch incidence and flyspeck incidence was determined with the Spearman s rank correlation test (PROC CORR SPEARMAN, SAS, and Spearman s rho, JMP 8, SAS Institute Inc., Cary, NC). The relationship between fruit color and disease incidence was determined similarly, with color data and disease incidence from cultivars grown in Virginia and rated visually at harvest in 2001 as percent red overcolor or on a scale of 0 to 5 for yellow cultivars. Results from the 1995 Group Flyspeck incidence varied significantly by cultivar (P < 0.0001), but not by location (P = 0.92), and the interaction of location and cultivar was not significant (P = 0.16). Sooty blotch incidence varied among cultivars (P < 0.0001), but not locations (P = 0.74), and the cultivar x location interaction was not significant (P = 0.24). Across all cultivars and locations, mean disease incidence for flyspeck ranged from 0.5% incidence for Sansa to 62% for GoldRush (Table 1). In addition to Sansa, cultivars with the lowest flyspeck incidence included Sunrise and Pristine, all of which were among the earliest maturing cultivars. In addition to GoldRush, cultivars with the highest flyspeck incidence included Fuji and Braeburn, which were all in the latest maturing group (Table 1). Midseason cultivars had flyspeck incidence ranging from 17 to 46% on Arlet and Senshu, respectively. Mean disease incidence for sooty blotch ranged from about 13% for Sansa and Pristine in the early season group to 77% for Braeburn in the late season group. GoldRush and Shizuka, also late season cultivars, had mean sooty blotch incidences approaching 70% (Table 1). Mid-season sooty blotch incidence ranged from 27 to 61% on Arlet and Gala Supreme, respectively. Cultivars were ranked in a similar order in terms of flyspeck and sooty blotch incidence, as indicated by the high Spearman rank correlation coefficient (r s = 0.93, P < 0.0001). For the cultivar Golden Delicious, sooty blotch and flyspeck incidence showed large differences among years and between New York and Virginia. In New York, flyspeck incidence ranged between 12.8% and 100% in the four years reported from 1997 to 2004. Over the same period in Virginia, flyspeck incidence ranged from 7.7% to 77.6%. Similarly, sooty blotch incidence ranged from 17.3% to 100% in New York and from 8.5% to 100% in Virginia.

Table 1. Percent fruit with signs of flyspeck and sooty blotch infestation for 23 apple cultivars in the 1995 NE-183 group. Maturing Cultivar or selection x Flyspeck Sooty blotch Early season Sansa 0.5 l z 13.1 n Pristine y 3.6 kl 13.5 n Sunrise 5.1 k 15.9 n Ginger Gold 20.6 ij 35.0 l Mid-season Arlet 16.7 j 27.2 m Honeycrisp 24.4 hi 37.2 l NY 75414-1 y 26.7 h 45.2 jk Golden Supreme 33.4 g 41.9 k Pioneer Mac 34.5 g 52.4 i Creston 34.5 g 56.9 h Gala Supreme 40.4 f 61.3 ef Yataka 42.0 ef 56.1 hi Senshu 46.4 cd 57.2 gh Late season Cameo 43.2 def 57.9 fgh Suncrisp 43.6 def 62.9 de Orin 43.8 def 61.0 efg Enterprise y 44.8 cdef 63.8 cde Fortune 45.9 cde 52.6 i Golden Delicious 48.2 c 62.2 de Shizuka 48.6 c 67.7 bc Braeburn 53.6 b 76.7 a Fuji Red Sport #2 56.8 b 65.4 bcd GoldRush y 61.8 a 69.3 b x The order of apple cultivars is from least susceptible to most susceptible to flyspeck within each maturity group, based on the mean ranks across all locations. Data are from New York (from 1997, 1998, 1999, 2003, and 2004) and Virginia (1997-2001, inclusive). y Indicates cultivars with genetic resistance to the apple scab pathogen, Venturia inaequalis. z Letters denote the differences among means according to the Waller Duncan k- ratio t test (P = 0.05). Results for the 1999 Group Flyspeck incidence varied significantly by location (P = 0.05) and cultivar (P < 0.0001), and the interaction of location and cultivar was not significant (P = 0.27). Sooty blotch incidence also varied among cultivars (P < 0.0001) and locations (P = 0.04) with no significant cultivar location interaction (P = 0.07). Means from the individual locations are presented because of the significant location main effect. Flyspeck and sooty blotch incidences were significantly higher in New York than in Virginia, and they were higher in Virginia than in Massachusetts. Mean incidences for flyspeck were 92, 49, and 38% for New York, Virginia, and Massachusetts, respectively. Mean incidences for sooty blotch were 79, 54, and 18% for New York, Virginia, and Massachusetts, respectively. Within each location, cultivars were ranked in

similar orders in terms of flyspeck and sooty blotch incidence, with highly significant (P < 0.0001 in all cases) rank correlation coefficients of 0.80 in Massachusetts, 0.81 in New York, and 0.86 in Virginia. The variation by location allowed us to more effectively determine differences among cultivars. While in New York more than half of the cultivars tested showed flyspeck incidences greater than 90% [only one cultivar (Zestar!) had < 60% incidence in New York], in Virginia and Massachusetts differences in flyspeck incidence between cultivars were more readily apparent (Table 2). The rank correlations for flyspeck means between Massachusetts and Virginia (r s = 0.79, P < 0.0001) and between New York and Virginia (r s = 0.65, P = 0.002) were both highly significant, though the rank correlation for flyspeck between New York and Massachusetts (r s = 0.36, P = 0.12) was not. Similarly, sooty blotch incidence in New York was relatively higher, with only two cultivars showing < 30% sooty blotch incidence and two-thirds of the cultivars exhibiting more than 80% (Table 3). The rank correlations between Massachusetts and Virginia (r s = 0.69, P = 0.001), New York and Virginia (r s = 0.77, P < 0.0001), and New York and Massachusetts (r s = 0.73, P = 0.0002) were all highly significant. Incidence of flyspeck ranged from about 4% for Zestar! in Virginia to 100% for Chinook, Sundance, Golden Delicious, and Ambrosia in New York (Table 2). The latter four cultivars generally had the highest flyspeck incidence at the other locations, as well. In New York and Virginia, Zestar! had significantly less flyspeck incidence than any other cultivar. Other cultivars with lower incidences of flyspeck included only NY 79507-72. Incidence of sooty blotch ranged from about 3% for Zestar! in Massachusetts to near 100% for several cultivars in New York, including Delblush, Chinook, and Golden Delicious (Table 3). Other highly susceptible cultivars included Ambrosia and Hampshire. Other less susceptible cultivars included only NY 79507-72 (Table 3). In the two years where Massachusetts, New York, and Virginia each had data, 2001 and 2003, Golden Delicious had flyspeck and sooty blotch incidence levels above 84% in all locations in 2003, and above 84% in New York and Virginia in 2001. In 2001, sooty blotch and flyspeck incidence was 23.5% and 30.6%, respectively, in Massachusetts.

Table 2. Percent fruit with signs of flyspeck infestation from 23 apple cultivars, from the 1999 NE-183 group. Cultivar x MA NY VA Early season Zestar! 19.7 i z 58.3 h 4.3 k Silken 27.2 ghi NJ109 27.5 ghi 94.0 abcd 30.4 ij Early midseason NY 79507-72 y 17.6 i 88.5 defg 19.5 j Crimson Crisp (Co-op 39) y 22.9 hi 90.8 cdef 29.9 ij NY 79507-49 y 29.4 ghi 90.8 cdef 47.1 gh September Wonder Fuji 34.4 fgh 88.6 defg 50.0 fgh Rogers McIntosh 37.3 efg 85.9 efg 60.8 def CQR10T17 y 47.7 cde 97.2 ab 48.6 gh Late midseason NJ90 25.4 ghi 91.4 bcde 39.3 hi BC 8S-26-50 49.7 abcd 83.3 g 33.1 i NY 65707-19 y 54.8 abcd 88.2 defg 45.6 gh Princess (CQR12T50) y 57.8 abc 85.0 fg 61.9 de Runkel 48.3 bcde 97.2 ab 55.2 efg Scarlet O Hara (Co-op 25) y 36.9 efg 95.4 abc 70.4 cd Hampshire 59.8 ab 96.3 abc 82.0 ab Late season Pinova 34.6 fgh 88.6 defg 31.4 i Delblush 42.9 def 99.8 a Ambrosia 55.0 abc 100.0 a 70.6 cd Sundance (Co-op 29) y 48.6 abcde 100.0 a 77.5 abc Cripps Pink (Pink Lady) 77.3 abc Golden Delicious 60.3 a 100.0 a 75.0 bc Chinook 100.0 a 86.3 a x The order of apple cultivars from least susceptible to most susceptible to flyspeck within each maturity group, based on the mean ranks across all locations. Data are from Massachusetts (2001, 2003, and 2004), New York (2001, 2003, and 2004), and Virginia (2001-2004, inclusive). y Indicates cultivars with genetic resistance to the apple scab pathogen, Venturia inaequalis. z Letters denote the differences among means according to the Waller Duncan k- ratio t test (P = 0.05).

Table 3. Percent fruit with signs of sooty blotch infestation from 23 apple cultivars, from the 1999 NE-183 group. Cultivar x MA NY VA Early season Silken 4.3 fg z Zestar! 3.1 g 26.8 h 7.2 j NJ109 7.1 fg 86.3 de 33.5 hi Early midseason NY 79507-72 y 4.5 fg 29.0 h 24.4 i Crimson Crisp (Co-op 39) y 4.7 fg 32.3 h 36.8 gh Rogers McIntosh 2.4 g 59.7 g 50.8 def September Wonder Fuji 6.7 fg 74.8 f 44.0 fg NY 79507-49 y 1.6 g 69.3 f 50.9 def CQR10T17 y 22.8 e 82.8 e 48.5 ef Late midseason NJ90 3.3 g 82.9 e 33.8 hi BC 8S-26-50 41.3 bc 71.3 f 55.9 cde NY 65707-19 y 30.6 de 85.1 de 56.0 cde Princess (CQR12T50) y 24.9 e 85.2 de 62.2 c Runkel 23.6 e 92.4 bcd 58.7 cd Scarlet O Hara (Co-op 25) y 12.4 f 90.5 cd 80.5 b Hampshire 41.2 bc 91.4 cd 92.0 a Late season Pinova 31.7 de 88.6 de 51.6 def Ambrosia 48.9 ab 97.7 abc 55.5 cde Sundance (Co-op 29) y 23.0 e 96.4 abc 86.5 ab Delblush 37.5 cd 99.8 ab Golden Delicious 53.7 a 99.5 ab 87.2 ab Cripps Pink (Pink Lady) 80.9 b Chinook 99.9 a 83.2 ab x The order of apple cultivars from least susceptible to most susceptible to flyspeck within each maturity group, based on the mean ranks across all locations. Data are from Massachusetts (2001, 2003, and 2004), New York (2001, 2003, and 2004), and Virginia (2001-2004, inclusive). y Indicates cultivars with genetic resistance to the apple scab pathogen, Venturia inaequalis. z Letters denote the differences among means according to the Waller Duncan k- ratio t test (P = 0.05). Relationship Between Harvest Date and Fruit Color with Sooty Blotch and Flyspeck Incidence Cultivar rank for incidence of both fungal complexes was significantly correlated with harvest date. The correlation analysis showed that cultivars that matured later had more sooty blotch (r s = 0.86, P < 0.0001) and more flyspeck (r s = 0.82, P < 0.0001) than those that matured earlier. This is likely because these fungal infestations develop signs slowly over periods of several days or weeks in the field, and fruit that is on trees longer have a greater chance of developing visible SBFS signs. Several researchers have shown that accumulated wetting hours (13,23,28,30) or accumulated hours of relative humidity 97% (20) can accurately predict the first appearance of SBFS signs,

and it is likely these environmental factors drive fungal development, thereby favoring higher disease incidence on later maturing cultivars that can accumulate more hours of favorable conditions prior to harvest. Disease incidence for either disease was not associated with fruit color (r s = 0.11, P < 0.60 and r = 0.13, P < 0.61 for sooty blotch and flyspeck, respectively). s Discussion and Recommendations Though most of the variability in SBFS incidence between cultivars could be explained by harvest period, there were a few exceptions. In the 1995 group, Ginger Gold had significantly more flyspeck and sooty blotch than other early season cultivars that were harvested a week or more later, and it had more sooty blotch than the lowest levels observed in the mid-season cultivars. In the 1999 group, Pinova generally had less flyspeck and sooty blotch than other cultivars in the late season group. These examples offer some support for the conclusions of Belding et al. (6) that anatomical or physiological factors in fruit may impact susceptibility to SBFS infestation, though in this study the length of time a fruit was in the field had the greatest impact on cultivar differences. The results also suggest that factors affecting sooty blotch incidence have similar effects on flyspeck incidence, as the order of the cultivar ratings for each disease were much the same in both years and within each location. Location had a significant impact on ratings in the 1999 test, but not in 1995. Location would be expected to affect SBFS development, as environmental factors, particularly the length of wetting periods and the number of hours of very high relative humidity, vary across broad geographic regions. Generally it is felt that SBFS disease pressure is highest in the southeastern United States and decreases in northern latitudes, largely the result of increasingly humid climate in the southeast (32), although this assumption was not validated in the present study, given the high disease levels observed in New York. Factors related to block location, including the distance to a wooded border, the number of wooded borders, and slope in the block, also impact SBFS incidence, as they would be expected to affect the abundance of inoculum and humidity (31). These factors may be at least partially responsible for the higher disease incidence that was recorded for the 1999 New York planting compared to the 1995 New York planting and the Virginia plantings. The 1995 New York planting was located on the crest of a hill and was surrounded by other orchards, whereas the 1999 planting had less air drainage and was bounded by woodlots on three sides. In addition to the factors already cited, the fungal species responsible for SBFS may also vary from region to region, but the major species of SBFS fungi in Massachusetts, New York, and Virginia are generally similar (18,19). While location had a significant effect on SBFS incidence when all cultivars were compared in the 1999 planting, a comparison of SBFS incidence for the late-season cultivar Golden Delicious in years for which each location had data showed levels at or approaching 100% in most cases. This indicates that for late season cultivars, location is less important than the harvest date. The fact that maturation date and location had the greatest impacts on SBFS incidence suggests that cultivar resistance is unlikely to contribute very much to integrated management approaches for SBFS. Other considerations determining cultivar selection, particularly market factors, will have much more impact on the environmental and economic sustainability of commercial apple orchards. However, this study emphasizes that SBFS management cannot end in late summer, but must be continued throughout the harvest season, with particular attention paid to late season cultivars. Acknowledgments We appreciate the technical support of Catherine Ahlers, Richard Christiana, A. E. Cochran II, S. W. Kilmer, Frederick Meyer, W. S. Royston, Jr., Arthur Tuttle, 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

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