HORTSCIENCE 44(3):599–608. 2009. tification of scab-resistant cultivars is impor- tant for both commercial producers and retailers of crabapples (Romer et al., 2003) A 33-year Evaluation of Resistance and for commercial apple breeding programs that seek to develop scab-resistant apples and Pathogenicity in the Apple (Janick, 2002; Shay et al., 1962). Host plant resistance is considered one of Scab–crabapples Pathosystem the most efficient and effective methods to control plant diseases with much of the Janna Beckerman1 breeding effort within the genus Malus Department of Botany and Plant Pathology, Purdue University, 915 directed to evaluate resistance to apple scab. West State Street, West Lafayette, IN 47907 The V. inaequalis–Malus interaction is one of the earliest examples demonstrating gene- James Chatfield for-gene interactions (Boone, 1971; Hough, Department of Horticulture and Crop Science, The Ohio Agricultural 1944; Williams and Shay, 1957). The gene- for-gene theory states that for every major Research and Development Center, Wooster, OH 44691-4096 gene conferring resistance (R) in the host, Erik Draper there exists a corresponding avirulence (AVR) gene in the pathogen (Flor, 1956; Hammond- The Ohio State University Extension Service, Geauga County, OH Kosack and Jones, 1997). Disease resistance 44021-9521 results only when the corresponding product Additional index words. Malus, Venturia inaequalis, avirulence, durable resistance of a dominant resistance gene (R) recognizes a dominant Avr gene product from the path- Abstract. Crabapples (Malus spp.) are popular ornamental trees in the commercial and ogen. Disease results when the loss or alter- residential landscape. Over a 33-year period at the Secrest Arboretum, Wooster, OH, 287 ation of the pathogen avirulence gene (now accessions of ornamental crabapple were evaluated for their resistance to apple scab denoted as avr) fails to trigger recognition by caused by the fungus Venturia inaequalis. Of these 287 accessions, 31 had no symptoms of the corresponding product of the host resis- scab for longer than a 10-year period and were identified as resistant to the disease. Of tance (R) gene (Hammond-Kosack and these 31 resistant accessions, 14 eventually displayed symptoms, presumably as a result of Jones, 1997). This model suggests a strong infection by one or more newly present races of the pathogen in the trial plot. Notable selection pressure exists against avirulence resistance breakdowns in accessions previously classified as resistant include the (AVR) within a pathogen population with any development of scab on M. · ‘Prairifire’, M. · ‘Bob White’, M. · ‘Red Jewel’, and M. loss of avirulence (avr) resulting in new floribunda. Corresponding to these changes of resistance is the putative development of virulent races that are identified only when new V. inaequalis races in North America: Race 5, possessing virulence to the Vm gene in cultivars previously scored as resistant suc- ‘Prairifire’; Race 3 that infects M. · ‘Geneva’ but not M. baccata ‘Dolgo’; and the first cumb to disease (MacHardy, 1996). This identification and report of scab on a M. floribunda population that was reported as phenomenon is referred to as ‘‘resistance resistant even before the first 25 years of the evaluation. The detection of scab on this breakdown’’ (McDonald and Linde, 2002). species suggests the presence of Race 7 in North America for the first time. Five named However, it is better understood and more accessions remained free from scab for the entire 33-year trial: M. sargentii ‘Sargent’, M. correctly stated as ‘‘avirulence breakdown,’’ baccata ‘Jackii’, M. · ‘Beverly’, M. · ‘Silver Moon’, and M. · ‘White Angel’ and may as the pathogen population has shifted, serve as sources of durable resistance in crabapple and commercial apple breeding in the whereas the host genotype remains fixed Midwest. (McDonald and Linde, 2002). In both agricultural and horticultural crops, fungal pathogens are under consider- The genus Malus includes both commercial States and in southern Canada. Crabapple able selection pressure to infect resistant host apple and crabapple with the primary differ- trees vary in size and shape and can provide cultivars. In a mixed population of crabapple, ence between them being fruit size; crabapple four seasons of interest: spectacular displays differences in pathogenicity and virulence fruit is less than 2 inches in diameter, whereas of single, double, and semi-double flowers in would be expected to develop over time, commercial apples have fruit greater than 2 shades of pure white to clear red in the spring; and these differences would manifest as loss inches. Although apple (Malus ·domesticus) foliage that exists in a variety of shapes and of resistance within the population of crabap- arose primarily from M. sieversii,manycom- colors for the summer and fall; fall fruit of ple. On resistance ‘‘breakdown,’’ the success- monly used crabapple species such as M. varying size and color and persistence; and ful infection by one ascospore creates a prunifolia (Willd) Borkh., M. baccata (L.) strong architectural forms in the winter. This founder effect for that successful individual Borkh., M. mandshurica (Maxim) Kom., and variation in size, tree structure, bloom, and pathogen; in V. inaequalis, this successful M. sieboldii (Regel) Rehder may have hybrid- fruit is a testimony not only to the popularity infection quickly amplifies itself through ized with M. sieversii (Luby, 2003). Many of of crabapples, but also to the diversity of asexual reproduction resulting in thousands these potential progenitors to the commercial genetic backgrounds that has been selected of conidia reinfecting the once-resistant host apple are used in the breeding of both crabap- and bred to create superior selections of plant (Guerin and Le Cam, 2004). Over time, ple and commercial apple and serve as a source crabapples. Proof of this popularity is readily these differences in the ability to infect one of durable resistance to scab and other major observable; over 700 varieties of crabapple cultivar but not another are identified as diseases of Malus (Fiala, 1994; Shay et al., have been named within the nursery industry physiological races (Bagga and Boone, 1962). (Dirr, 1990; Fiala, 1994). Many of these 1968a; MacHardy, 1996). The term ‘‘physio- Crabapples are among the most widely selections and much of the breeding effort logical race’’ is used to describe a subpopula- cultivated ornamental trees in the northeast- have been directed to evaluate resistance to tion of a pathogen possessing a specific pattern ern and midwestern regions of the United apple scab caused by the fungal pathogen of virulence and avirulence on specific culti- Venturia inaequalis (Cke). In scab-susceptible vars of apple (Malus ·domestica), termed crabapples, symptoms of infection include differentials (MacHardy, 1996). Received for publication 9 Dec. 2008. Accepted for defoliation by early summer coupled with In crabapple, classical major genes con- publication 5 Feb. 2009. loss of winter hardiness and even death result- ferring resistance to scab have been identified 1To whom reprint requests should be addressed; ing from repeated defoliation and attack by and include Vf (from Malus floribunda 821), e-mail [email protected]. opportunistic insects or pathogens. The iden- Vm (from M. micromalus 245-38 and M.
HORTSCIENCE VOL. 44(3) JUNE 2009 599 ·atrosanguinea 804), Vb (from M. baccata Cultural care. The crabapple research Sandskar and Liljeroth, 2005; Shay and ‘Hansen’s baccata #2’), Vbj from M. baccata plot is located at Secrest Arboretum on the Hough, 1952). With different scales used by ‘Jackii’, Vr from M. pumila R12740-7A, and OARDC campus. Early ratings (before 1983) at least 11 people during the 33 years of Va from Antonovka PI172623 (or ‘‘true’’ Va involved between two and five replicates per evaluations, we began by converting the resistance as per Dayton and Williams, 1968; accession. In 1983, the National Crabapple observations to a basic scale that recognized Hough et al., 1970; Lespinasse, 1989; as Evaluation Project (NCEP) plot (Crablandia I) only four classes of infection (Table 1). This explained by Gessler et al., 2006). Resistance used three replicates per accession in a resulted in greater consistency of scab resis- breakdown resulted in the identification of completely randomized design. The second tance scores in cultivars evaluated over the races of scab capable of infecting different NCEP trial in 2001 (Crablandia II) uses five span of many years (data not shown). Despite cultivars and species of apple (Table 1) replicates of each accession in a completely the broader categories in scoring resistance, (Dayton and Williams, 1968; Schmidt, randomized design. The soil type is silt loam. qualitative assessments remained intact; trees 1938). Historically, Race 1 is described as a Data collection. Apple scab is an endemic described as highly resistant to immune to well-sporulating isolate on popular domestic problem in the Midwest, and no additional scab retained a score of zero and trees that apple cultivars (M. ‘Gala’, M. ‘Fuji’, and M. inoculations were required to drive the dis- could be infected received scores of 1, 2, or 3 ‘Red Delicious’) but elicits a hypersensitive ease. Many trees included in the trial after depending on scab severity. response without sporulation on M. baccata 1982 were part of the NCEP. From 1972 to Accessions with changes in resistance ‘Dolgo’, R12740-7A, and M. · ‘Geneva’ 2005, 287 crabapple species, hybrids, and status. Over the 33-year period of evaluation, (Shay and Williams, 1956). Race 2 can spor- cultivars were evaluated at different times numerous cultivars exhibited increased sus- ulate on M. baccata ‘Dolgo’, M. · ‘Geneva’, between June and August. Apple scab sus- ceptibility, including M. · ‘Adams’, M. · and certain offspring of M. ‘R12740-7A’. Race ceptibility ratings and observations were ‘Bob White’, M. · ‘Coralburst’, M. · ‘Liset’, 3 is characterized as being able to only conducted in 1972, 1978, 1982 to 1991, and M. ‘Mary Potter’, M. · ‘Molten Lava’, a sporulate on common commercial apple culti- 1993 to 2005 during the months of June selection of M. sieboldii, M. · ‘Ormiston vars and M. · ‘Geneva’, but not M. baccata through August by the following individuals: Roy’, M. · ‘Purple Prince’, M. · ‘Selkirk’, M. · ‘Dolgo’, and Race 4 differs from Race 1 by P.C. Kozel, Thomas Dugan, Elton Smith, ‘Sentinel’, M. · ‘Sugar Tyme’, M. sieboldii sporulating on some (but not all) progeny of Sharon Treaster, James Chatfield, Erik (formerly designated as M. zumi)‘Calocarpa’, M.‘R12740-7A’. Race 5 has the ability to Draper, Kenneth Cochran, Peter Bristol, M. · ‘Red Jewel’, M. halliana ‘Parkmanii’ sporulate on carriers of the Vm resistance gene, Charles Tubesing, and David Allen. Their and M. floribunda. Most other named selec- whereas Race 6 can infect some (but not all) findings over this 33-year period were com- tions either were initially identified as scab- progeny of M. floribunda 821. Race 7 is piled for this report. These observers pro- susceptible or were deaccessioned as a result capable of infecting M. floribunda 821, the vided descriptive climate information for of fire blight, animal damage, or other major source of Vf resistance that has been intro- each period evaluated. Additional data to disease problems (Table 2). gressed into scab-resistant commercial apples confirm observers’ assessments of the con- Periods conducive to scab outbreaks coincided worldwide. Additional races have been ditions at the Wooster Experiment Station with putative changes in the scab population described as well (Bus et al., 2005). Many of were obtained from the National Climatic corresponding with a loss of avirulence/ these genes are also present in commercial Data Center at http://www7.ncdc.noaa.gov/ resistance. Susceptibility of previously resistant apples, and their use is of increasing impor- CDO/normalsproduct for years 1972 to 2001. accessions occurred in the high rainfall years of tance as growers adopt organic approaches to Data from 2001 to 2005 were obtained by the 1989 (M. · ‘Adams’), 1990 (M. · ‘Molten disease control (Crosby et al., 1992; Janick, OARDC and are available online at http:// Lava’), 1993 (M. · ‘Liset’, M. · ‘Professor 2002). However, a greater genetic diversity www.oardc.ohio-state.edu/newweather/. Sprenger’, M. · ‘Selkirk’, M. · ‘Sugar Tyme’, exists within the crabapple population, Data analysis and standardization. To M. halliana ‘Parkmanii’), 2000 (M. · ‘Prairi- because tree appearance drives selection rather standardize 33 years of data collecting with fire’), and 2003 (M. · ‘Lancelot’, M. · ‘Purple than fruit size and flavor. different scales used by different observers, Prince’, M. · ‘Sentinel’). Breakdown of other To develop long-term, durable disease noted observations were defined with the cultivars in 1994 (M. · ‘Mary Potter’) and 1996 management (McDonald and Linde, 2002), following numerical values to the described (M. floribunda) occurred during average to low plant breeding must be integrated with plant symptoms: 0 = highly resistant to immune, no rainfall years. These data are highlighted in bold pathology to understand the evolution of path- scab; 1 = resistant but with a trace of scab; 2 = in Table 1. ogen populations and resistance breakdown. susceptible to minor scab infection but with- Species, hybrids, and cultivars with The purpose of this study is to use over 30 years out defoliation; and 3 = highly susceptible to durable resistance. Crabapple trees defined of scab evaluation data from 287 accessions of scab and extensive defoliation. Scores were here as having durable resistance possessed crabapple planted at the Secrest Arboretum at averaged among at least three trees per season, resistance at the end of the study or for the Ohio Agricultural Research and Develop- and scab assessments were performed between greater than 10 years. Throughout the entire ment Center in Wooster, OH, for the purpose of one and five times per season. study, M. baccata ‘Jackii’ [resistance gene identifying durable scab resistance and to Vbj (Gygax et al., 2004)], possessed durable examine the evolution of races of V. inaequalis Results resistance, although occasional trace infec- concomitant with the loss of avirulence/devel- tions were reported in 1986 and 1987 (Table opment of resistance breakdown. This report A low incidence of tree loss occurred as a 2). M. · ‘Silver Moon’ exhibited no scab for examines and documents the breakdown of result of trunk cankers and fire blight. Some the entire 33 years. M. baccata ‘Dolgo’ scab resistance in popular crabapple cultivars cultivars were deaccessioned resulting from possessed very stable resistance, although in one location in North America resulting lack of ornamental interest, only to be ‘‘reac- infection was noted in 2003; M. sargentii from the development of new races within the cessioned’’ on recognition of superior scab ‘Sargent’ possessed solid resistance/immunity scab population over time. resistance. Data collected from all 287 acces- for the entire trial, and named M. sargentii sions with respect to scab are presented in cultivars like M. · ‘Firebird’, M. · ‘Rose Materials and Methods Table 1. Year-to-year variation in scab sever- Low’, and M. · ‘Tina’ possessed resistance ity occurred regularly with more severe scab for the entire time they were evaluated. M. Accessions. The crabapple evaluation was outbreaks reported in 1983, 1984, 1989, ·robusta and M. ·robusta ‘Percifolia’, the initiated in 1959 by L.C. Chadwick at the 1990, 1991, 1993, 2000, and 2003. peachleaf crabapple, showed no incidence of Secrest Arboretum at the Ohio Agricultural Scab evaluation. Apple scab is difficult to scab for almost 20 years of the trial until Research and Development Center (OARDC) assess in the field (Croxall et al., 1952). As a deaccessioned as a result of fire blight. M. · in Wooster, OH. Confirmation of tree identity result, there are several different published ‘Rosseau’ showed no incidence of scab for 20 is solely based on taxonomic and cultivar scales to evaluate scab susceptibility (Croxall years before being deaccessioned as a result release descriptions. et al., 1952; den Boer and Green, 1995; of fire blight. M. · ‘Strawberry Parfait’
600 HORTSCIENCE VOL. 44(3) JUNE 2009 Table 1. Relative resistancez of crabapple cultivars to scab at Secrest Arboretum 1972 to 2005. Year Cultivar 1972 1978 1982 1984 1985 1986 1987 1988 1989 1990 1991 1993 1994 1995 1997 1999 2000 2002 2003 2005 M. · Adams 00010001.5 2.5 1.5 1 2 3 2 2 3 3 3 M. · Adirondack 000000 M. ·adstringens 323323333 M. · Almey 3323222.53333 M. · Amberina 2.5 2232 M. · American Beauty 22312 3 23 M. · American 33 3 Masterpiece M. · American Salute 23 3 M. · American Spirit 33 3 M. · American Triumph 33 3 M. · Amisk 2.5 333332333 M. · Amur 003023 M. · Ann E 0 0.5 0 1 0 M. · Arrow 2.5 13333332.53 M. · Arnold Arboretum 1.5 03320 M. · Arnold 3 2.5 3 3 2.5 333333 M. ·atrosanguinea 11313 3 M. ·atrosanguinea 0 Carmine M. · Autumn Glory 0 M. baccata 2000202010 M. baccata Ceratocarpa 3 2 3 M. baccata Columnaris 2111.50.50.50.50110 M. baccata Jackii 000000.50.50000000 000000 M. baccata Mandshurica 0 1 1.5 1.5 1 1 3 1.5 0.5 0 M. baccata var. Midwest 000000010 M. baccata var Serbian 3 0 M. · Barbara Ann 03233333 M. · Beverly 0000000000000 0000 M. · Blanche Ames 0 0 0 M. · Bob White 00000000000000 0000 1 M. · Brandywine 0.5 1.5 0 0.5 0001.50 021 M. brevipes 33323333 M. · Burgundy 21010321 M. · Calloway 0 1 0 0 0.5 0.5 M. · Camelot 0 1 0 1 1 0.5 1 M. · Canary 1212222 M. · Candied Apple 1.5 2110.5222003 32 M. · Candy Mint 001112 M. · Canterbury 0 0 0.5 M. · Cardinal 00 M. · Cashmere 0.5 1.5 22200 M. · Centennial 0000000000 M. · Centurion 0 2.5 1 2 1.5 0.5 1.5 3 3 2 2.5 2 2 1.5 3 M. · Cheals Crimson 2.5 2332.531323 M. · Chestnut 101000011.50 M. · Chilko 1.5 02000.51000 M. · Christmas Cheer 0 0 M. · Christmas Holly 0000000 M. · Cinderella 1.5 1 2 2 M. · Coralburst 1 0.5 0.5 0 1 1 0.5 0.5 0 0.5 0 22 1 M. coronaria 2 1.5 M. coronaria Charlotte 322221.52.5331.5 M. coronaria Dasycalyx 2132.5 M. coronaria Nieuwlandiana 1.5 03222.522.522 M. · Cowichan 203332.52.5332 M. · Crimson Brilliant 33332.533333 M. · Dainty 1022230.5331.5 M. · Dauphin 3 M. · Dawsonianan 000001.5 M. · David 01000000.50.50.5112 10.50122 M. baccata Dolgo 10000000000000 00000.50 M. · Donald Wyman 000000.5011.51112 222232 M. · Dorthea 1.5 22202.52.53333 M. · Dorothy Rowe 000000 3 M. · Doubloons 23 M. · Ellen Gerhart 0 1 1.5 2.5 3 3 3 1.5 3 3 2.5 M. · Evelyn 1 1.5 3323 333 M. · Excaliber 01 0 M. · Exzellenz Theil 3 3 1.5 3333 M. · Firebird 00 0 M. · Flame 2232.5031.5333
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HORTSCIENCE VOL. 44(3) JUNE 2009 601 Table 1. (Continued) Relative resistancez of crabapple cultivars to scab at Secrest Arboretum 1972 to 2005. Year Cultivar 1972 1978 1982 1984 1985 1986 1987 1988 1989 1990 1991 1993 1994 1995 1997 1999 2000 2002 2003 2005 M. · Flexilius 00002.50000 M. florentine 000 0 M. floribunda 0000000 00000 111133 M. · Foxfire 00 0 M. · Fusca 2 1 0.5 0 0 0 0 0 M. · Geneva 2 0 1.5 0 1 1 1.5 1 0 M. glauscecens 02111 031 M. · Glen Mills 21 3 3 M. gloriosa 12112.532.53 M. · Goldfinch 3 3 3 3 0 M. · Gorgeous 1 0 3 0 0 2 0 M. · Girards Dwarf 000110 Weeping M. · Girards Pendula 0 Nana M. · Golden Hornet 0000000 000 M. · Golden Gem 00000 000 M. · Golden Raindrops 000000 M. · Guinevere 1 0.5 M. · Gwendolyn 000001 000 0 M. halliana 000000 000 M. halliana Keller 0 M. halliana Parkmanii 000000 0000.5 0 1 1 2 M. · Hamlet 0 0 1 0 M. · hartwigii 0000 0 M. · Harvest Gold 01113 2.5233323333 M. · Henrietta Crosby 3 2.5 3 3 2 3 3 M. · Henningi 0 1 1 2 2.5 2.5 1 3 3 3 2 3 M. · Henry Dupont 1.5 13111.52.523 M. · Henry Kohankie 0 3 M. · Holiday Gold 00 0 M. · Hopa 3 3 2.5 2.5 3 2 3 3 2 2.3 3 3 3 3 3 M. · Hopa Rosea 333222 332 M. · Hopa Austrian 2 2 3 2 3 1.5 M. · Hopa Dwarf 0 0 2 2 2 M. hupehensis 0000200 000.5 M. hupehensis Rosea 0 M. · Indian Magic 0 0.5 0.5 1.5 0.5 1.5 0 3 3 3333 333333 M. · Indian Summer 0001.51.5231233 32.5333 M. ioensis 1.5 1.5 0 0 1.5 M. ioensis Plena Bechtel 2 2 1 M. ioensis Palmeri 0 0 M. ioensis Prairie Rose 1 0 0 M. · Jay Darling 3 2.5 3333 333 M. · Joan 0000 000 M. · Jewelberry 0 0 0 0.5 2 2233 333 M. · Katherine 2 1.5 3 1.5 1.5 2 2.5 2 M. · Klehms 1 1.5 0 2 1 0 1.5 M. · Klehms Improved 2 0 1.5 0 0 0.5 0 1.5 0 M. · Irene 333333 333 M. · Dwarf Kaido 3 1 M. · Dwarf Katherine 1.5 3 2 M. · Kibele 0 1 0 3 3 0 M. · Khirgisorum 0 0 1 0 0 0.5 M. · King Arthur 0 0 0 0 M. · Kingsmere 2 3 0 3 M. · Kola 2.5 0 0 M. · Lancelot 0 1 0 0 0 2 2 M. lancifolia 213203 2.530.5 M. lancifolia Allegheny 1 0 1.5 M. · Leslie 3 0 1.5 0 3 1 3 1.5 0 M. · Liset 0000000 0000.5111111 M. · Lollipop 00 0 M. · Louisa 000000 M. · Madonna 1001 21113 3 M. madgeburgensis 0.5 0 2 1 1.5 1.5 1 0.5 0 M. · Makamik 000000 000 M. · Manbeck Weeper 23 2 M. · Marshall Oyama 0.5 02001 0.500 M. · Mary Potter 0000000 000011 111122 M. · Masek 1 2 2.5 0 3 2.5 3 0 3 M. · Mays Delight 0 M. ·micromalus Midget 0000000 000
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602 HORTSCIENCE VOL. 44(3) JUNE 2009 Table 1. (Continued) Relative resistancez of crabapple cultivars to scab at Secrest Arboretum 1972 to 2005. Year Cultivar 1972 1978 1982 1984 1985 1986 1987 1988 1989 1990 1991 1993 1994 1995 1997 1999 2000 2002 2003 2005 M. · Milton Barron 3 2 0 M. · Mollie Ann 0 M. · Molten Lava 0 0 0.5 0 0.5 1.5 0 1 1 3 2 1 2 2 3 2 M. · Naragansett 31 3 3 M. · Nevile Copman 33233 31.50 M. · Oakes 2.5 23032 32.53 M. · Oekonomicrat 2.533333 333 Echternmeyer M. · Ohio 2 M. · Oporto 2 3 2 3 M. · Orange Crush 0 M. · Ormiston Roy 000000 0001011011 M. · Patricia 222001.5303 M. · Pink Beauty 2 0 2 0.5 0 1.5 1 2.5 1 0 M. · Pink Cascade 2 0.5 1.5 1.5 1 1 0 1.5 3 2.5 M. · Pink Dawn 0.5 1.5 2 1.5 0 M. · Pink Flame 22331.533330 M. · Pink Perfection 333333 33 M. · Pink Princess 1 1 0.2 M. · Pink Satin 1.5 2 1.3 3 3 1 3 M. · Pink Spires 1.5 0.5 3 3 1.5 3233 M. · Pink Weeper 233323332.52 M. · Prairie Maid 000000 M. · Prairie Rose 0010000000 0 M. · Prairiefire 0000000000 00 1111 M. · Pretty Margorie 22100010 M. · Prince Georges 0220.500113 M. · Profusion 0 0 1 1.5 1.5 1 2.5 2.5 1.5 2 3 3 3 3 M. · Professor Sprenger 00000000.513 101232 M. prunifolia 2.53323 M. prunifolia Fastigiata 0 0 1.5 0033 M. prunifolia Pendula 03332.50000 M. prunifolia Rinkii 32000 M. pumila Elise Rathke 2 2 2.5 3 0 2.5 1.5 3 2.5 1 M. pumila Niedzwetzkyana 2.5 223332333 M. pumila Paradise 1 000330 Foleus Aureus M. · Pumpkin Pie 0 M. · Purple Prince 00 0 1 2 0.5 M. · Purple Wave 2.5 332333303 M. purpurea 2.532.5333333 M. purpurea 2232.52.522332 Aldenhamemsis M. purpurea Eleyi 33333233333 M. purpurea Lemoine 0 2 2.5 33322.5332.5 M. · Pygmy 1 2320321 M. · Radiant 1332.532.513333 3 33 3 M. · Ralph Shay 0.5 1.5 1.5 1 1 0.5 1.5 2.5 1 2 2 3 3 2 3 M. · Rawhide 00 0 M. · Red Baron 0.5 2 1 2 1.5 1.5 2 2.5 1.5 1 1.3 3 3 2 3 M. · RedBud 0.5030223 M. · Red Edinburgh 1323333 M. · Redfield 2.5 0 M. · Red Flesh 1103322 M. · Red Jade 1 0.5 0 1.5 0 0 0.5 0 1 0.5 0.5 1 2 2 2 1.5 2 2 3 3 M. · Red Jewel 0000000000.50000 00 1110.5 M. Red Silver 2 1.5 0.5 2 2.5 022333 M. Red Splendor 1 0.5 2 1.5 2 1.5 1 2 1.5 0 1 2 2 3 1 3 3 3 3 M. Red Swan 00100 1 M. Ringo 1 3222321 M. Robinson 0 0 0.5 2 1.5 1.5 1 3 3 1.5 2 3 3 3 2.5 3 M. ·robusta 0000000000 M. ·robusta Erecta 3 0.5 0.5 1 1.5 0 0 3 0.5 1 M. ·robusta Leucocarpa 0 0 1 0 3 3 M. ·robusta Percifolia 0 0 0000000 M. · Rose Tea 0 0001 M. · Rosy Bloom 0200 M. · Rosseau 0000000000 M. · Royal Fountain 2 3 2.5 M. · Royal Raindrop 01 M. · Royal Ruby 2 1.5 3 2 1.5 21232 M. · Royal Scepter 33 3 M. · Royalty 2 0.5 2 1.5 3 2 1 2.5 2 2.5 1 2 3 3 2 3
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HORTSCIENCE VOL. 44(3) JUNE 2009 603 Table 1. (Continued) Relative resistancez of crabapple cultivars to scab at Secrest Arboretum 1972 to 2005. Year Cultivar 1972 1978 1982 1984 1985 1986 1987 1988 1989 1990 1991 1993 1994 1995 1997 1999 2000 2002 2003 2005 M. · Ruby Luster 321323115 3 M. · Rudolf 1.5 0232.53 2 M. sargentii Candy Mint 1.5 1 1.5 M. sargentii Rosea 0.5 1.5 0 0 0.5 1.5 0 0 1.5 0 M. sargentii Sargent 00000000000000 000000 M. sargentii Rose Low 000000 M. sargentii Tina 00 0 M. · Satin Cloud 0 0 M ·scheideckeri 2 1.5 1.5 3 0 1.5 2 3 2.5 3 3 3 1 M ·scheideckeri Hillieri 1.5 2 1.5 0 3 2.5 2.5 2 1.5 2.5 M ·scheideckeri 1 Dwarf Hillieri M. sieboldia f. Zumi 10 0 Calocarpa M. · Scugog 1.5 03001.51.51.50 M. · Selkirk 1 0.5 0210000.500122 21.5 3 M. · Sentinel 00000.500.50000.51212233 M. · Shakespeare 2333333 M. sieboldi 0 M. sieboldi Arborescens 0 M. sieboldi Fuji 0 M. sikkimensis 00 00 M. · Silver Drift 101232 M. · Silver Moon 00000000000000 000000 M. · Simcoe 1.5 0.5 00112012 M. · Sinai Fire 0 0 0 0 0.2 0 M. · Sissipuk 0001.500000 M. · Snowbank 0 M. · Snowcap 0.5 020010 M. · Snowcloud 1 1.5 0.5 3 1.5 1.5 3 1.5 1.5 M. · Snowdrift 00011.51.51.51.52.532.5233333233 M. · Snowmagic 30232231.5 M. soulardia 213131101.50.5 M. · Sparkler 0 2 0.5 3 1.5 3 2.5 3 3 3 1.5 M. spectabilis 1 13230032.51.5 M. spectablilis 1.531.52.5031331 Albi-Plena M. spectablilis Riversi 1001 0.50 M. spectablilis 1 0.5 1.5 1 2 2.5 0 3 1.5 0.5 Van Elseltinei M. · Spring Song 0 2 0 0 M. · Spring Snow 1.5 0211.51.50331 333 M. · Strathmore 2 3 2.5 33333333 M. · Strawberry Parfait 000000000 101100 M. ·sublobata 1.502.5211120.50 M. · SugarTyme 1000000.50011 10.51232 M. · Sundog 1000000200 M. sylvestris Plena 02000.5100.50 M. · Tanner 1.5 033333333 M. · ThunderChild 32 3 M. torigoides 232230321.5 M. torigoides Macrocarpa 2323 0323 M. · Trail 0300 0000 M. transitoria 00 M. tschonoskii 0000000000000 0 M. · Turesei 2033233333 M. · Valley City 2.5 322323232 M. · Van Eseltine 1.5 2 3 1 M. · Vanguard 2 2.5 2 2.5 1333033 M. · Wabiskaw 2.5 2 3 2 3 2.5 3 3 3 M. · Weeping 10 2 333 Candied Apple M. · White Angel 0000000000000 0000 M. · White Candle 1.5 0 2.5 1 2.5 3 2.5 3 3 2 M. · White cascade 11031.52.5123323333 M. · Wickson 000100 M. · Wilson 2.5 232231 30 M. · Winters Gem 0 M. · Winters Gold 1 1.5 3 2 2 1.5 1.5 3 3 2.5 1 3 3 3 2.5 3 M. · Wooster No. 1 000110000 M. yannanensis Veitchi 0000100000 M. yannanensis 0200000.50 Veitchs Scarlet
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604 HORTSCIENCE VOL. 44(3) JUNE 2009 Table 1. (Continued) Relative resistancez of crabapple cultivars to scab at Secrest Arboretum 1972 to 2005. Year Cultivar 1972 1978 1982 1984 1985 1986 1987 1988 1989 1990 1991 1993 1994 1995 1997 1999 2000 2002 2003 2005 M. zumi 1.5 1.5 1 0.5 0 0.5 2 0 3 1.5 M. zumi Calocarpa 00000 0 10111.51111 3 M. zumi Rang 0 M. zumi Wooster 0.5 M. zumi Zumarang 0 zResistance was evaluated as: 0 = highly resistant to immune, no scab; 1 = resistant, but with a trace of scab; 2 = susceptible to minor scab infection but without defoliation; 3 = highly susceptible to scab and extensive defoliation. Numbers in bold highlight changes in the status of scab resistance.
Table 2. A summary of cultivars identified in this study with 10+ years resistance to scab. Races of scab present based on susceptible Cultivar 10+ years resistance Eventual scab development cultivars. In evaluating Table 1, it must be M. Adams X Y noted that the inclusion of the universal M. baccata Jackii X N susceptible cultivar M. · ‘Royal Gala’ or M. M. · Bob White X Y · ‘Red Delicious’ for identification of Race 1 M. · Centennial X Nz (Bus, 2006) from commercial apples did not M. · David X Y occur. However, M. · ‘Hopa’, a universally M. baccata Dolgo X N known scab-susceptible cultivar wherever M. · Beverly X N crabapples are grown in North America, M. floribunda XY M. · Golden Hornet X Nz serves as an adequate substitute that demon- M. halliana XNz strates reliable susceptibility throughout the M. halliana Parkman X Y entire 33-year study. M. · Liset X Y Race 2, capable of infecting M. baccata M. · Makamik X Nz ‘Dolgo’ and M. · ‘Geneva’ (Shay and Williams, M. · Mary Potter X Y 1956), was not observed over the course of M. · micromalus Midget X Nz this study. The existence of stable resistance M. · Ormiston Roy X Y z in M. baccata ‘Dolgo’ suggests the absence M. · Prairie Rose X N of Race 2 at Secrest Arboretum. However, M. · Red Jewel X Y M. ·robusta Percifolia X Y the presence of Race 3 is suggested by the M. · Rosseau X Nz susceptibility of M. · ‘Geneva’ that devel- M. sargentii Sargent X N oped in 1986, whereas M. baccata ‘Dolgo’ M. · Silver Moon X N essentially remained uninfected. Race 4, M. · Strawberry Parfait X Y capable of infecting some progeny of M. M. tschonoskii XNz ‘12740-7A’, cannot be considered in this M. · White Angel X N study as a result of an absence of differentials M. · Wooster No. 1 X Nz z for this race. M. yunnanensis Veitchi X N Unlike Europe, where Races 5, 6, and 7 M. zumi Calocarpa X Y z were found, only Races 1 through 4 have Deaccesssion as a result of other reasons (e.g., fire blight susceptibility, juniper rust susceptibility, and so on). been reported in North America (Dayton and Williams, 1968). The recurring presence of Table 3. Pathogenicity of different Venturia inaequalis races on the set of differential host cultivars, scab on M. · ‘Prairifire’ suggests the devel- associated R-gene, or identified pathogenicity factor (P-factorz).y opment of Race 5 in North America. M. · Venturia inaequalis races ‘Prairifire’, a Vm-resistant crabapple (Mattison Differential cultivar R-Gene/p-genez 12345678and Nybom, 2005; S. Korban, personal com- M. Galax/M. · Hopax None/p-14, p-15 SSSSSSSSmunication), first developed scab in 2000. M. baccata Dolgo, h2 Unnamed/p-8 R S RRRRRRThere are no differentials present at the M. · Geneva, h3 Unnamed/p-10, p-11 R S S RRRRRSecrest Arboretum to identify the presence Russian R-12740-7A Vr1, Vr2, Vx RRRSRRRRof Race 6. Race 6 is not able to infect the M. M. floribunda h6 Vf RRRRRRSR M. baccata (h2 and h3?) Vb R floribunda 821. M. baccata Jackii Vbj R The presence of scab on a M. floribunda M. ·micromalus, h5 and Vm RRRRSRRRselection that was reliably scab-resistant for M. atrosanguinea 804 at least 40 years suggests, but does not (Prairifire) conclusively demonstrate, the development M. sargentii Unnamed of Race 7 in North America. An overview of M. sikkimensis Unnamed/p-12, p-13 Venturia race breakdown and susceptible zPathogenicity gene (P-gene) designation developed from Williams and Shay (1957) and MacHardy hosts at Secrest can be seen in Table 3. (1996). yUpdated from MacHardy (1996) and Gessler et al. (2006). Cultivars in bold were found to be infected with scab. Discussion xGala is considered a universal susceptible control but was not included in this trial. ‘Hopa’ is serving as the universal susceptible control, despite identification of some minor resistance genes indicated by p-14 and The Malus species, hybrids, and named p15 (Bagga and Boone, 1968a); similar minor gene resistances have been noted in ‘Royal Gala’ (Bus, cultivars in this study represent a tremendous 2006; Parisi et al., 2004). diversity of genetic background, aesthetic characteristics, and scab resistance and included Malus species from Asia (M. floribunda, M. possessed solid resistance for almost 25 years removal. M. yunnanensis ‘Veitchii’, an halliana, M. spectabilis, M. toringoides, M. before scab infection. M. tschonoskii, a rare unusual crabapple with excellent scab resis- transitoria, M. tschonoskii, M. yunnanensis), crabapple grown mostly in arboreta, was tance, but very susceptible to fire blight, was North America (M. coronaria, M. ioensis), and scab-resistant for over 20 years until other removed in 1992. See Table 2 for a list of Europe (M. florentine, M. pumila). It is impor- foliar diseases and fire blight necessitated its durable, scab-resistant accessions. tant to note that the delineation of species
HORTSCIENCE VOL. 44(3) JUNE 2009 605 within the genus Malus has been problematic included in Table 3 for the sake of comple- atic species of crabapples (Williams and (Luby, 2003; Robinson et al., 2001). Acces- tion. Based on the increased understanding of Brown, 1968). A tightly linked DNA marker sions were reported as recorded with additional the V. inaequalis–Malus gene-for-gene inter- for Vm, SCAR B12, was previously used to notes provided by the authors if changes of actions, it is apparent that a new system of identify Vm in M. · ‘Prairifire’ (Mattison and taxonomy have occurred as is the case for designating the nomenclature of these inter- Nybom, 2005; S. Korban, personal commu- M.sieboldii/M. zumi varieties (Fiala, 1994; actions is needed because the current one is nication). Cheng et al. (1998) and Patocchi Luby, 2003). Unfortunately, as noted, ‘‘scores both confusing and inadequate (Bus, 2006). et al. (2005) have identified markers tightly were averaged between at least three trees per In evaluating the composition of scab linked to Vm resistance in M. · hartwigii, M. season’’; no effort was made on the part of any races at the arboretum, M. · ‘Hopa’ serves halliana, M. hupehensis, M. fusca, and in of the observers to note the novel occurrence of as our universally susceptible cultivar and M. · ‘Prairifire’ (S. Korban, personal com- scab on any previously ‘‘resistant varieties’’ demonstrated reliable susceptibility through- munication). However, not every accession until 2005 (Chatfield et al., 2005). out the entire 33-year study. This cultivar is a of these species was found to possess the The results from this study indicate that Race 1 indicator despite previously being markers for Vm (Cheng et al., 1998; Patocchi various levels of both qualitative (major) and identified as possessing p-14 and p-15 avir- et al., 2005). M. ·atrosanguinea developed quantitative (minor) resistance to V. inaequa- ulence factors (Bagga and Boone, 1968a). It scab as early as 1978, and M. ·micromalus lis exist within the genus Malus. Aderhold should be stressed that even the Race 1 ‘Midget’ was deaccessioned in 1993. The (1899) previously observed that V. inaequalis differential used in apple breeding, M. ‘Royal breakdown in resistance in M. · ‘Prairifire’ could be divided into distinct physiological Gala’ possesses some resistance factors (Parisi was first reported in 1997 (P. Pecknold, races distinguishable by their different ability et al., 2004). In reality, Race 1 exists as a personal communication) in Indiana but to induce sporulating lesions or only flecks on highly complex, structured population with was not detected at the Secrest Arboretum various cultivars. These differences of V. an undetermined number and frequency of until 2000. Unfortunately, other carriers of inaequalis pathogenicity patterns were iden- avirulence alleles that prevent this race from the Vm gene, M. ·hartwigii, M. halliana, M. tified as regional in nature as early as 1938 infecting previously identified differentials hupehensis, and M. fusca were deaccessioned (Schmidt, 1938). This regionality of races (Bus et al., 2005; Gessler et al., 2006). as a result of fire blight in the early 1990s. M. was again observed with M. sieversii seed Race 2, capable of infecting M. baccata · ‘Mary Potter’, a hybrid of M. sargentii collected in Central Asia and grown and ‘Dolgo’, M. · ‘TSR34T132’, and M. · ‘Rosea’ · M. ·atrosanguinea, developed screened in the United States. When M. ‘Geneva’ (Gessler et al., 2006), was not scab in 1994. Work is currently underway sieversii seed (collected in Central Asia) observed over the course of this study. This to examine these cultivars for the existence of were raised in the United States, these seed- race has been reported in Sweden on some the linked Vm marker and to look at M. · lings had high levels of apple scab resistance segregants of the Russian cultivar R12740- ‘Liset’, a multibred with M. ·atrosanguinea that varied with the geographic region where 7A (Sandskar and Liljeroth, 2005), but no in the background, to determine if Vm exists the seedlings were screened; from 27% of the work has been performed to confirm that M. in this cultivar as well (Patocchi et al., 2005) population exhibiting resistance in New York baccata ‘Dolgo’ and these accessions carry and if the breakdown of resistance was to 65% of the population screened in Minne- the same resistance gene. Race 2 was reported attributable solely to the development of sota. The parents of these seedlings (wild previously in South Dakota (Shay and Wil- Race 5 at Secrest. Curiously, Race 5 has only apples from Central Asia, specifically those liams, 1956) and has also been observed in been reported in Europe (Dayton and Wil- from the Karatau mountains) were without Minnesota (J. Beckerman, personal observa- liams, 1968); the development of scab on M. scab; the Zailisky site was 35% scab free, and tion). The existence of stable resistance in M. · ‘Prairifire’ suggests a race with virulence the Tarbagatai site did not have observable baccata ‘Dolgo’ suggests the absence of similar to Race 5 has developed North Amer- scab (Forsline et al., 2003). These sites are Race 2 at Secrest Arboretum. However, the ica. A cultivar recorded as M. ·atrosanguinea considered xeric, and the absence of free presence of Race 3 is suggested by the was evaluated as scab-susceptible for the water for germination would reduce the susceptibility of M. · ‘Geneva’ that devel- entire 10 years it was included in the trial; it incidence of scab. This suggests the differ- oped in 1986, whereas M. baccata ‘Dolgo’ is unknown if this selection possesses the Vm ences in scab evaluations in the United States essentially remained uninfected. gene or if it is M. ·atrosanguinea 804. M. [e.g., Jacobs and Spravka (1996) compared There is no evidence that Race 4, capable atrosanguinea 804 was included in the with the data here] may be the result of: 1) of infecting some progeny of M. ‘12740-7A’, release of cultivars by The Arnold Arboretum changes in environment between arid Central is present in the arboretum as a result of an in the early 1900s (Crandall, 1926). Asia and the wet and humid eastern half of absence of differentials for this race. Tre- Race 6 isolates, capable of infecting some the United States; and 2) regional differences mendous confusion exists in the literature Vf scab-resistant commercial apples, includ- in races of scab present at those locales. regarding Race 4 (Bus, 2006). This confusion ing M. · ‘Prima’, M. ‘Judeline’, and M. · The study of V. inaequalis–Malus genet- arises from Shay et al. (1962) who stated that ‘Florina (querina)’ (Parisi and Lespinasse, ics began before scab resistance breeding the original Russian apple accession contains 1996; Parisi et al., 1993), could not be scored programs (Keitt and Langford, 1941; Keitt ‘‘at least 3 gene pairs, only one of which is as a result of the absence of these cultivars in and Palmiter, 1938) or even an understanding resistant to all known races’’ without refer- the trial. Other M. floribunda selections or of gene-for-gene systems (Flor, 1956). Boone encing any specific races of V. inaequalis. hybrids include M. · ‘Exzellenz Theil’, an M. and Keitt (1957) identified seven R–Avr However, it is safe to assume that Races 1 floribunda · M. prunifolia ‘Pendula’ hybrid interactions involving moderately resistant through 3, the only ones identified to that (Fiala, 1994) that was very susceptible to cultivars and identified several multigenic point, are understood as ‘‘all known races.’’ scab when evaluated, M. ·arnoldiana, and M. gene-for-gene relationships. In these studies Based on this report (Shay et al., 1962), none ·Scheideckeri. There is no evidence to sug- on V. inaequalis, the avirulence-resistant of the accessions in this study could know- gest that any of these cultivars possesses Vf gene interaction was designated ‘‘p-x,’’ with ingly serve as reported differentials for Race resistance. p describing the pathogenicity gene and x 4, although other susceptible selections of M. M. floribunda, the Japanese flowering indicating the allele number. In keeping with pumila were included in this location (e.g., crabapple, is considered one of the finest previous literature describing avirulence M. pumila ‘Niedzwetzkyana’, M. pumila crabapples in cultivation and was introduced (Boone and Keitt, 1957; Williams and Shay, ‘Elise Rathke’, and M. pumila ‘Paradise into Europe by von Siebold in 1853 from 1957), only the p-8 avirulence locus is pre- Foley’) and were susceptible to scab through- Nagasaki, Japan. The place where this tree sent in the population at Wooster, OH (Table out most of the evaluation. grows wild still remains unknown (Fiala, 3). The loss of avirulence genes in this The Vm resistance gene, derived from either 1994). The selections at Secrest match the population includes p-10 through p-19 M. micromalus 245-38 or M. ·atrosanguinea taxonomic description of Crandall (1926). (Bagga and Boone, 1968a, 1968b; Williams 804 (Hough, 1944), is one of several resis- Selection M. floribunda 821 was identified and Shay, 1957). This information is tance genes found in the small-fruited, Asi- as resistant in 1943 by Hough (1944) and
606 HORTSCIENCE VOL. 44(3) JUNE 2009 Hough et al. (1953) and has been used Nursery managers also report the durable Literature Cited extensively as a source of resistance in resistance of M. baccata ‘Jackii’, an obser- commercial cultivars (Crosby et al., 1992; vation confirmed in this study. However, scab Aderhold, R. 1899. Auf welche Weise konnen wir dem immer weiteren Umsichgreifen des Fusi- Janick, 2002). Concomitantly, many of these has been reported on M. baccata ‘Jackii’ in cladiums in unseren Apfelkulturen begegnen selections were regularly distributed to arbo- Sweden (Sandskar and Liljeroth, 2005), so und welche Sorten haben sich bisher dem Pilz reta throughout the United States in the 1940s resistance breakdown of this selection is gegenu¨ber am widerstandsfa¨higsten gezeigt. to 1960s for crabapple evaluations (Fiala, possible in North America in the future. Pomol. Monatsh. XLV:266–272. 1994); unfortunately, many were misidenti- The breakdown of scab resistance in sev- Bagga, H.S. and D.M. Boone. 1968a. Genes in fied or misnamed (Jefferson, 1970). Records eral hybrid Malus taxa is interesting. M. · Venturia inaequalis controlling pathogenicity and morphology indicate that this tree is, in ‘Bob White’, introduced in 1876 (Jefferson, to crabapples. Phytopathology 58:1176–1182. fact, M. floribunda, although whether it is a 1970), is a suspected M. sieboldii var. zumi Bagga, H.S. and D.M. Boone. 1968b. Inheritance scion of M. floribunda 821, the parent tree hybrid and would therefore be expected to of resistance to Venturia inaequalis in crabap- ples. Phytopathology 58:1183–1187. that provided both the Vf and Vfh resistance possess comparable polygenic resistance Belfanti, E., E. Silfverberg-Dilworth, S. Tartarini, genes that were introgressed into most scab- of other M. sieboldii var. zumi selections A. Patocchi, M. Barbieri, J. Zhu, B. Vinatzer, L. resistant commercial apples (Janick, 2002), (e.g., M. var. zumi ‘Wooster’ and var. zumi Gianfranceschi, C. Gessler, and S. Sansavini. remains undetermined. The identification of ‘Calocarpa’). M. · ‘Strawberry Parfait’, a 2004. The HcrVf2 gene from a wild apple Race 7 in the United Kingdom parallels its cross between M. hupehensis and M. confers scab resistance to a transgenic cultivated potential discovery here; a backyard crabapple ·atrosanguinea, also was resistant in 1994, variety. Proc. Natl. Acad. Sci. USA 101:886– was identified as a M. floribunda with scab. developing scab the same time as M. · ‘Mary 890. Inoculation of M. floribunda 821 with scab Potter’, the offspring of a M. ·atrosanguinea Boone, D.M. 1971. Genetics of Venturia inaequa- from the backyard crabapple demonstrated · M. sargentii ‘Rosea’ cross (Fiala, 1994), lis. Annu. Rev. Phytopathol. 9:297–318. Boone, D.M. and G.W. Keitt. 1957. Venturia susceptibility and confirmed the development strongly suggesting the development of a new inaequalis (Cke.) Wint. XII. Genes controlling of Race 7 (Roberts and Crute, 1994). The work race of scab concomitant with Vm resistance pathogenicity of wild-type lines. Phytopathol- to conclusively establish the host range and breakdown. The long-term scab resistance and ogy 47:403–409. specificity of this M. floribunda-infecting iso- subsequent development of scab on this selec- Bus, V.G.M. 2006. Differential host–pathogen late is currently underway. tion suggests a minimal oligogenic resistance interactions of Venturia inaequalis and Malus. Until recently (Parisi et al., 1993), Vf was or that re-evaluation is warranted of the dogma Thesis, Doctor of Philosophy in Biological considered to be the most durable source of that polygenic resistance is more durable than Sciences. University of Auckland. resistance with Vf-derived cultivars resistant monogenic resistance. Other crabapples with Bus,V.G.M.,F.N.D.Laurens,W.E.VandeWeg, to scab for over 50 years. Not all selections of durable, and probably multigenic, resistance R.L.Rusholme,E.H.A.Rikkerink,S.E.Gardiner, H.C.M. Bassett, and K.M. Plummer. 2005. The M. floribunda possess this allele and that include: M. · ‘Beverly’, a large, upright Vh8 locus of a new gene-for-gene interaction selfed M. floribunda 821 had a segregation crabapple with pink flower buds, fragrant, between Venturia inaequalis and the wild apple of resistance that indicates that Vf is a domi- white, five-petaled flowers, bright green Malus sieversii is closely linked to the Vh2 locus nant resistance gene (Hough et al., 1953). leaves and small, red, persistent, glossy fruits in Malus pumila R12740-7A. New Phytol. However, the fact that resistance in this isolate strongly suggestive of M. baccata parentage; 166:1035–1049. was effective for at least 40 years at Secrest M. · ‘Silver Moon’, another probable M. Buttner, R., M. Geibel, and C. Fischer. 2000. The (Chadwick, 1965; this publication) under baccata hybrid with white flower buds that genetic potential of scab and mildew resis- intense selection pressure supports the con- was described as scab-susceptible by Nichols tance in Malus wild species. Acta Hort. tention that it is a selection of M. floribunda but did not develop scab at Falconskeape 538:67–70. Chadwick, L.C. 1965. Ornamental crabapples. with the Vf gene, if not in fact the original M. (Fiala, 1994), or throughout our study or in Lawn and ornamentals research. Ohio Agricul- floribunda 821 (J. Janick, personal communi- the study by Jacobs and Spravka (1996); and tural Research and Development Center, Woos- cation). The resistance observed at Secrest M. · ‘White Angel’, a chance seedling of ter, OH. before 1997 was complete immunity (Score putative M. sieboldii parentage (Fiala, 1994), Chatfield, J.A., E.A. Draper, D.A. Herms, and K.A. 0), not the light infection (Score 1) described also reported by Jacobs and Spravka (1996) Cochran. 2005. Apple scab on crabapple at by Parisi et al. (1993) with respect to the as resistant. Secrest Arboretum: 2005. The Ohio Agricultural identification of Race 6 on commercial apples In conclusion, data presented in this arti- Research and Development Center. p. 117–121. with Vf resistance. This is consistent with the cle demonstrate the durability of resistance of 11 Mar. 2009.
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