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A 33-Year Evaluation of Resistance and Pathogenicity in the Apple

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A 33-Year Evaluation of Resistance and Pathogenicity in the Apple 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.
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