A 33-year Evaluation of Resistance and Pathogenicity in the Apple Scab–crabapples Pathosystem

in HortScience

Crabapples (Malus spp.) are popular ornamental trees in the commercial and residential landscape. Over a 33-year period at the Secrest Arboretum, Wooster, OH, 287 accessions of ornamental crabapple were evaluated for their resistance to apple scab caused by the fungus Venturia inaequalis. Of these 287 accessions, 31 had no symptoms of scab for longer than a 10-year period and were identified as resistant to the disease. Of these 31 resistant accessions, 14 eventually displayed symptoms, presumably as a result of infection by one or more newly present races of the pathogen in the trial plot. Notable resistance breakdowns in accessions previously classified as resistant include the development of scab on M. × ‘Prairifire’, M. × ‘Bob White’, M. × ‘Red Jewel’, and M. floribunda. Corresponding to these changes of resistance is the putative development of new V. inaequalis races in North America: Race 5, possessing virulence to the Vm gene in ‘Prairifire’; Race 3 that infects M. × ‘Geneva’ but not M. baccata ‘Dolgo’; and the first identification and report of scab on a M. floribunda population that was reported as resistant even before the first 25 years of the evaluation. The detection of scab on this species suggests the presence of Race 7 in North America for the first time. Five named accessions remained free from scab for the entire 33-year trial: M. sargentii ‘Sargent’, M. baccata ‘Jackii’, M. × ‘Beverly’, M. × ‘Silver Moon’, and M. × ‘White Angel’ and may serve as sources of durable resistance in crabapple and commercial apple breeding in the Midwest.

Abstract

Crabapples (Malus spp.) are popular ornamental trees in the commercial and residential landscape. Over a 33-year period at the Secrest Arboretum, Wooster, OH, 287 accessions of ornamental crabapple were evaluated for their resistance to apple scab caused by the fungus Venturia inaequalis. Of these 287 accessions, 31 had no symptoms of scab for longer than a 10-year period and were identified as resistant to the disease. Of these 31 resistant accessions, 14 eventually displayed symptoms, presumably as a result of infection by one or more newly present races of the pathogen in the trial plot. Notable resistance breakdowns in accessions previously classified as resistant include the development of scab on M. × ‘Prairifire’, M. × ‘Bob White’, M. × ‘Red Jewel’, and M. floribunda. Corresponding to these changes of resistance is the putative development of new V. inaequalis races in North America: Race 5, possessing virulence to the Vm gene in ‘Prairifire’; Race 3 that infects M. × ‘Geneva’ but not M. baccata ‘Dolgo’; and the first identification and report of scab on a M. floribunda population that was reported as resistant even before the first 25 years of the evaluation. The detection of scab on this species suggests the presence of Race 7 in North America for the first time. Five named accessions remained free from scab for the entire 33-year trial: M. sargentii ‘Sargent’, M. baccata ‘Jackii’, M. × ‘Beverly’, M. × ‘Silver Moon’, and M. × ‘White Angel’ and may serve as sources of durable resistance in crabapple and commercial apple breeding in the Midwest.

The genus Malus includes both commercial apple and crabapple with the primary difference between them being fruit size; crabapple fruit is less than 2 inches in diameter, whereas commercial apples have fruit greater than 2 inches. Although apple (Malus ×domesticus) arose primarily from M. sieversii, many commonly used crabapple species such as M. prunifolia (Willd) Borkh., M. baccata (L.) Borkh., M. mandshurica (Maxim) Kom., and M. sieboldii (Regel) Rehder may have hybridized with M. sieversii (Luby, 2003). Many of these potential progenitors to the commercial apple are used in the breeding of both crabapple and commercial apple and serve as a source of durable resistance to scab and other major diseases of Malus (Fiala, 1994; Shay et al., 1962).

Crabapples are among the most widely cultivated ornamental trees in the northeastern and midwestern regions of the United States and in southern Canada. Crabapple trees vary in size and shape and can provide four seasons of interest: spectacular displays of single, double, and semi-double flowers in shades of pure white to clear red in the spring; foliage that exists in a variety of shapes and colors for the summer and fall; fall fruit of varying size and color and persistence; and strong architectural forms in the winter. This variation in size, tree structure, bloom, and fruit is a testimony not only to the popularity of crabapples, but also to the diversity of genetic backgrounds that has been selected and bred to create superior selections of crabapples. Proof of this popularity is readily observable; over 700 varieties of crabapple have been named within the nursery industry (Dirr, 1990; Fiala, 1994). Many of these selections and much of the breeding effort have been directed to evaluate resistance to apple scab caused by the fungal pathogen Venturia inaequalis (Cke). In scab-susceptible crabapples, symptoms of infection include defoliation by early summer coupled with loss of winter hardiness and even death resulting from repeated defoliation and attack by opportunistic insects or pathogens. The identification of scab-resistant cultivars is important for both commercial producers and retailers of crabapples (Romer et al., 2003) and for commercial apple breeding programs that seek to develop scab-resistant apples (Janick, 2002; Shay et al., 1962).

Host plant resistance is considered one of the most efficient and effective methods to control plant diseases with much of the breeding effort within the genus Malus directed to evaluate resistance to apple scab. The V. inaequalis–Malus interaction is one of the earliest examples demonstrating gene-for-gene interactions (Boone, 1971; Hough, 1944; Williams and Shay, 1957). The gene-for-gene theory states that for every major gene conferring resistance (R) in the host, there exists a corresponding avirulence (AVR) gene in the pathogen (Flor, 1956; Hammond-Kosack and Jones, 1997). Disease resistance results only when the corresponding product of a dominant resistance gene (R) recognizes a dominant Avr gene product from the pathogen. Disease results when the loss or alteration of the pathogen avirulence gene (now denoted as avr) fails to trigger recognition by the corresponding product of the host resistance (R) gene (Hammond-Kosack and Jones, 1997). This model suggests a strong selection pressure exists against avirulence (AVR) within a pathogen population with any loss of avirulence (avr) resulting in new virulent races that are identified only when cultivars previously scored as resistant succumb to disease (MacHardy, 1996). This phenomenon is referred to as “resistance breakdown” (McDonald and Linde, 2002). However, it is better understood and more correctly stated as “avirulence breakdown,” as the pathogen population has shifted, whereas the host genotype remains fixed (McDonald and Linde, 2002).

In both agricultural and horticultural crops, fungal pathogens are under considerable selection pressure to infect resistant host cultivars. In a mixed population of crabapple, differences in pathogenicity and virulence would be expected to develop over time, and these differences would manifest as loss of resistance within the population of crabapple. On resistance “breakdown,” the successful infection by one ascospore creates a founder effect for that successful individual pathogen; in V. inaequalis, this successful infection quickly amplifies itself through asexual reproduction resulting in thousands of conidia reinfecting the once-resistant host plant (Guerin and Le Cam, 2004). Over time, these differences in the ability to infect one cultivar but not another are identified as physiological races (Bagga and Boone, 1968a; MacHardy, 1996). The term “physiological race” is used to describe a subpopulation of a pathogen possessing a specific pattern of virulence and avirulence on specific cultivars of apple (Malus ×domestica), termed differentials (MacHardy, 1996).

In crabapple, classical major genes conferring resistance to scab have been identified and include Vf (from Malus floribunda 821), Vm (from M. micromalus 245-38 and M. ×atrosanguinea 804), Vb (from M. baccata ‘Hansen's baccata #2’), Vbj from M. baccata ‘Jackii’, Vr from M. pumila R12740-7A, and Va from Antonovka PI172623 (or “true” Va resistance as per Dayton and Williams, 1968; Hough et al., 1970; Lespinasse, 1989; as explained by Gessler et al., 2006). Resistance breakdown resulted in the identification of races of scab capable of infecting different cultivars and species of apple (Table 1) (Dayton and Williams, 1968; Schmidt, 1938). Historically, Race 1 is described as a well-sporulating isolate on popular domestic apple cultivars (M. ‘Gala’, M. ‘Fuji’, and M. ‘Red Delicious’) but elicits a hypersensitive response without sporulation on M. baccata ‘Dolgo’, R12740-7A, and M. × ‘Geneva’ (Shay and Williams, 1956). Race 2 can sporulate on M. baccata ‘Dolgo’, M. × ‘Geneva’, and certain offspring of M. ‘R12740-7A’. Race 3 is characterized as being able to only sporulate on common commercial apple cultivars and M. × ‘Geneva’, but not M. baccata ‘Dolgo’, and Race 4 differs from Race 1 by sporulating on some (but not all) progeny of M.‘R12740-7A’. Race 5 has the ability to sporulate on carriers of the Vm resistance gene, whereas Race 6 can infect some (but not all) progeny of M. floribunda 821. Race 7 is capable of infecting M. floribunda 821, the source of Vf resistance that has been introgressed into scab-resistant commercial apples worldwide. Additional races have been described as well (Bus et al., 2005). Many of these genes are also present in commercial apples, and their use is of increasing importance as growers adopt organic approaches to disease control (Crosby et al., 1992; Janick, 2002). However, a greater genetic diversity exists within the crabapple population, because tree appearance drives selection rather than fruit size and flavor.

Table 1.

Relative resistancez of crabapple cultivars to scab at Secrest Arboretum 1972 to 2005

Table 1.

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To develop long-term, durable disease management (McDonald and Linde, 2002), plant breeding must be integrated with plant pathology to understand the evolution of pathogen populations and resistance breakdown. The purpose of this study is to use over 30 years of scab evaluation data from 287 accessions of crabapple planted at the Secrest Arboretum at the Ohio Agricultural Research and Development Center in Wooster, OH, for the purpose of identifying durable scab resistance and to examine the evolution of races of V. inaequalis concomitant with the loss of avirulence/development of resistance breakdown. This report examines and documents the breakdown of scab resistance in popular crabapple cultivars in one location in North America resulting from the development of new races within the scab population over time.

Materials and Methods

Accessions.

The crabapple evaluation was initiated in 1959 by L.C. Chadwick at the Secrest Arboretum at the Ohio Agricultural Research and Development Center (OARDC) in Wooster, OH. Confirmation of tree identity is solely based on taxonomic and cultivar release descriptions.

Cultural care.

The crabapple research plot is located at Secrest Arboretum on the OARDC campus. Early ratings (before 1983) involved between two and five replicates per accession. In 1983, the National Crabapple Evaluation Project (NCEP) plot (Crablandia I) used three replicates per accession in a completely randomized design. The second NCEP trial in 2001 (Crablandia II) uses five replicates of each accession in a completely randomized design. The soil type is silt loam.

Data collection.

Apple scab is an endemic problem in the Midwest, and no additional inoculations were required to drive the disease. Many trees included in the trial after 1982 were part of the NCEP. From 1972 to 2005, 287 crabapple species, hybrids, and cultivars were evaluated at different times between June and August. Apple scab susceptibility ratings and observations were conducted in 1972, 1978, 1982 to 1991, and 1993 to 2005 during the months of June through August by the following individuals: P.C. Kozel, Thomas Dugan, Elton Smith, Sharon Treaster, James Chatfield, Erik Draper, Kenneth Cochran, Peter Bristol, Charles Tubesing, and David Allen. Their findings over this 33-year period were compiled for this report. These observers provided descriptive climate information for each period evaluated. Additional data to confirm observers’ assessments of the conditions at the Wooster Experiment Station were obtained from the National Climatic Data Center at http://www7.ncdc.noaa.gov/CDO/normalsproduct for years 1972 to 2001. Data from 2001 to 2005 were obtained by the OARDC and are available online at http://www.oardc.ohio-state.edu/newweather/.

Data analysis and standardization.

To standardize 33 years of data collecting with different scales used by different observers, noted observations were defined with the following numerical values to the described symptoms: 0 = highly resistant to immune, no scab; 1 = resistant but with a trace of scab; 2 = susceptible to minor scab infection but without defoliation; and 3 = highly susceptible to scab and extensive defoliation. Scores were averaged among at least three trees per season, and scab assessments were performed between one and five times per season.

Results

A low incidence of tree loss occurred as a result of trunk cankers and fire blight. Some cultivars were deaccessioned resulting from lack of ornamental interest, only to be “reaccessioned” on recognition of superior scab resistance. Data collected from all 287 accessions with respect to scab are presented in Table 1. Year-to-year variation in scab severity occurred regularly with more severe scab outbreaks reported in 1983, 1984, 1989, 1990, 1991, 1993, 2000, and 2003.

Scab evaluation.

Apple scab is difficult to assess in the field (Croxall et al., 1952). As a result, there are several different published scales to evaluate scab susceptibility (Croxall et al., 1952; den Boer and Green, 1995; Sandskar and Liljeroth, 2005; Shay and Hough, 1952). With different scales used by at least 11 people during the 33 years of evaluations, we began by converting the observations to a basic scale that recognized only four classes of infection (Table 1). This resulted in greater consistency of scab resistance scores in cultivars evaluated over the span of many years (data not shown). Despite the broader categories in scoring resistance, qualitative assessments remained intact; trees described as highly resistant to immune to scab retained a score of zero and trees that could be infected received scores of 1, 2, or 3 depending on scab severity.

Accessions with changes in resistance status.

Over the 33-year period of evaluation, numerous cultivars exhibited increased susceptibility, including M. × ‘Adams’, M. × ‘Bob White’, M. × ‘Coralburst’, M. × ‘Liset’, M. ‘Mary Potter’, M. × ‘Molten Lava’, a selection of M. sieboldii, M. × ‘Ormiston Roy’, M. × ‘Purple Prince’, M. × ‘Selkirk’, M. × ‘Sentinel’, M. × ‘Sugar Tyme’, M. sieboldii (formerly designated as M. zumi) ‘Calocarpa’, M. × ‘Red Jewel’, M. halliana ‘Parkmanii’ and M. floribunda. Most other named selections either were initially identified as scab-susceptible or were deaccessioned as a result of fire blight, animal damage, or other major disease problems (Table 2).

Table 2.

A summary of cultivars identified in this study with 10+ years resistance to scab.

Table 2.

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Periods conducive to scab outbreaks coincided with putative changes in the scab population corresponding with a loss of avirulence/resistance.

Susceptibility of previously resistant accessions occurred in the high rainfall years of 1989 (M. × ‘Adams’), 1990 (M. × ‘Molten Lava’), 1993 (M. × ‘Liset’, M. × ‘Professor Sprenger’, M. × ‘Selkirk’, M. × ‘Sugar Tyme’, M. halliana ‘Parkmanii’), 2000 (M. × ‘Prairifire’), and 2003 (M. × ‘Lancelot’, M. × ‘Purple Prince’, M. × ‘Sentinel’). Breakdown of other cultivars in 1994 (M. × ‘Mary Potter’) and 1996 (M. floribunda) occurred during average to low rainfall years. These data are highlighted in bold in Table 1.

Species, hybrids, and cultivars with durable resistance.

Crabapple trees defined here as having durable resistance possessed resistance at the end of the study or for greater than 10 years. Throughout the entire study, M. baccata ‘Jackii’ [resistance gene Vbj (Gygax et al., 2004)], possessed durable resistance, although occasional trace infections were reported in 1986 and 1987 (Table 2). M. × ‘Silver Moon’ exhibited no scab for the entire 33 years. M. baccata ‘Dolgo’ possessed very stable resistance, although infection was noted in 2003; M. sargentii ‘Sargent’ possessed solid resistance/immunity for the entire trial, and named M. sargentii cultivars like M. × ‘Firebird’, M. × ‘Rose Low’, and M. × ‘Tina’ possessed resistance for the entire time they were evaluated. M. ×robusta and M. ×robusta ‘Percifolia’, the peachleaf crabapple, showed no incidence of scab for almost 20 years of the trial until deaccessioned as a result of fire blight. M. × ‘Rosseau’ showed no incidence of scab for 20 years before being deaccessioned as a result of fire blight. M. × ‘Strawberry Parfait’ possessed solid resistance for almost 25 years before scab infection. M. tschonoskii, a rare crabapple grown mostly in arboreta, was scab-resistant for over 20 years until other foliar diseases and fire blight necessitated its removal. M. yunnanensis ‘Veitchii’, an unusual crabapple with excellent scab resistance, but very susceptible to fire blight, was removed in 1992. See Table 2 for a list of durable, scab-resistant accessions.

Races of scab present based on susceptible cultivars.

In evaluating Table 1, it must be noted that the inclusion of the universal susceptible cultivar M. × ‘Royal Gala’ or M. × ‘Red Delicious’ for identification of Race 1 (Bus, 2006) from commercial apples did not occur. However, M. × ‘Hopa’, a universally known scab-susceptible cultivar wherever crabapples are grown in North America, serves as an adequate substitute that demonstrates reliable susceptibility throughout the entire 33-year study.

Race 2, capable of infecting M. baccata ‘Dolgo’ and M. × ‘Geneva’ (Shay and Williams, 1956), was not observed over the course of this study. The existence of stable resistance in M. baccata ‘Dolgo’ suggests the absence of Race 2 at Secrest Arboretum. However, the presence of Race 3 is suggested by the susceptibility of M. × ‘Geneva’ that developed in 1986, whereas M. baccata ‘Dolgo’ essentially remained uninfected. Race 4, capable of infecting some progeny of M. ‘12740-7A’, cannot be considered in this study as a result of an absence of differentials for this race.

Unlike Europe, where Races 5, 6, and 7 were found, only Races 1 through 4 have been reported in North America (Dayton and Williams, 1968). The recurring presence of scab on M. × ‘Prairifire’ suggests the development of Race 5 in North America. M. × ‘Prairifire’, a Vm-resistant crabapple (Mattison and Nybom, 2005; S. Korban, personal communication), first developed scab in 2000. There are no differentials present at the Secrest Arboretum to identify the presence of Race 6. Race 6 is not able to infect the M. floribunda 821.

The presence of scab on a M. floribunda selection that was reliably scab-resistant for at least 40 years suggests, but does not conclusively demonstrate, the development of Race 7 in North America. An overview of Venturia race breakdown and susceptible hosts at Secrest can be seen in Table 3.

Table 3.

Pathogenicity of different Venturia inaequalis races on the set of differential host cultivars, associated R-gene, or identified pathogenicity factor (P-factorz).y

Table 3.

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Discussion

The Malus species, hybrids, and named cultivars in this study represent a tremendous diversity of genetic background, aesthetic characteristics, and scab resistance and included Malus species from Asia (M. floribunda, M. halliana, M. spectabilis, M. toringoides, M. transitoria, M. tschonoskii, M. yunnanensis), North America (M. coronaria, M. ioensis), and Europe (M. florentine, M. pumila). It is important to note that the delineation of species within the genus Malus has been problematic (Luby, 2003; Robinson et al., 2001). Accessions were reported as recorded with additional notes provided by the authors if changes of taxonomy have occurred as is the case for M.sieboldii/M. zumi varieties (Fiala, 1994; Luby, 2003). Unfortunately, as noted, “scores were averaged between at least three trees per season”; no effort was made on the part of any of the observers to note the novel occurrence of scab on any previously “resistant varieties” until 2005 (Chatfield et al., 2005).

The results from this study indicate that various levels of both qualitative (major) and quantitative (minor) resistance to V. inaequalis exist within the genus Malus. Aderhold (1899) previously observed that V. inaequalis could be divided into distinct physiological races distinguishable by their different ability to induce sporulating lesions or only flecks on various cultivars. These differences of V. inaequalis pathogenicity patterns were identified as regional in nature as early as 1938 (Schmidt, 1938). This regionality of races was again observed with M. sieversii seed collected in Central Asia and grown and screened in the United States. When M. sieversii seed (collected in Central Asia) were raised in the United States, these seedlings had high levels of apple scab resistance that varied with the geographic region where the seedlings were screened; from 27% of the population exhibiting resistance in New York to 65% of the population screened in Minnesota. The parents of these seedlings (wild apples from Central Asia, specifically those from the Karatau mountains) were without scab; the Zailisky site was 35% scab free, and the Tarbagatai site did not have observable scab (Forsline et al., 2003). These sites are considered xeric, and the absence of free water for germination would reduce the incidence of scab. This suggests the differences in scab evaluations in the United States [e.g., Jacobs and Spravka (1996) compared with the data here] may be the result of: 1) changes in environment between arid Central Asia and the wet and humid eastern half of the United States; and 2) regional differences in races of scab present at those locales.

The study of V. inaequalis–Malus genetics began before scab resistance breeding programs (Keitt and Langford, 1941; Keitt and Palmiter, 1938) or even an understanding of gene-for-gene systems (Flor, 1956). Boone and Keitt (1957) identified seven R–Avr interactions involving moderately resistant cultivars and identified several multigenic gene-for-gene relationships. In these studies on V. inaequalis, the avirulence-resistant gene interaction was designated “p-x,” with p describing the pathogenicity gene and x indicating the allele number. In keeping with previous literature describing avirulence (Boone and Keitt, 1957; Williams and Shay, 1957), only the p-8 avirulence locus is present in the population at Wooster, OH (Table 3). The loss of avirulence genes in this population includes p-10 through p-19 (Bagga and Boone, 1968a, 1968b; Williams and Shay, 1957). This information is included in Table 3 for the sake of completion. Based on the increased understanding of the V. inaequalis–Malus gene-for-gene interactions, it is apparent that a new system of designating the nomenclature of these interactions is needed because the current one is both confusing and inadequate (Bus, 2006).

In evaluating the composition of scab races at the arboretum, M. × ‘Hopa’ serves as our universally susceptible cultivar and demonstrated reliable susceptibility throughout the entire 33-year study. This cultivar is a Race 1 indicator despite previously being identified as possessing p-14 and p-15 avirulence factors (Bagga and Boone, 1968a). It should be stressed that even the Race 1 differential used in apple breeding, M. ‘Royal Gala’ possesses some resistance factors (Parisi et al., 2004). In reality, Race 1 exists as a highly complex, structured population with an undetermined number and frequency of avirulence alleles that prevent this race from infecting previously identified differentials (Bus et al., 2005; Gessler et al., 2006).

Race 2, capable of infecting M. baccata ‘Dolgo’, M. × ‘TSR34T132’, and M. × ‘Geneva’ (Gessler et al., 2006), was not observed over the course of this study. This race has been reported in Sweden on some segregants of the Russian cultivar R12740-7A (Sandskar and Liljeroth, 2005), but no work has been performed to confirm that M. baccata ‘Dolgo’ and these accessions carry the same resistance gene. Race 2 was reported previously in South Dakota (Shay and Williams, 1956) and has also been observed in Minnesota (J. Beckerman, personal observation). The existence of stable resistance in M. baccata ‘Dolgo’ suggests the absence of Race 2 at Secrest Arboretum. However, the presence of Race 3 is suggested by the susceptibility of M. × ‘Geneva’ that developed in 1986, whereas M. baccata ‘Dolgo’ essentially remained uninfected.

There is no evidence that Race 4, capable of infecting some progeny of M. ‘12740-7A’, is present in the arboretum as a result of an absence of differentials for this race. Tremendous confusion exists in the literature regarding Race 4 (Bus, 2006). This confusion arises from Shay et al. (1962) who stated that the original Russian apple accession contains “at least 3 gene pairs, only one of which is resistant to all known races” without referencing any specific races of V. inaequalis. However, it is safe to assume that Races 1 through 3, the only ones identified to that point, are understood as “all known races.” Based on this report (Shay et al., 1962), none of the accessions in this study could knowingly serve as reported differentials for Race 4, although other susceptible selections of M. pumila were included in this location (e.g., M. pumila ‘Niedzwetzkyana’, M. pumila ‘Elise Rathke’, and M. pumila ‘Paradise Foley’) and were susceptible to scab throughout most of the evaluation.

The Vm resistance gene, derived from either M. micromalus 245-38 or M. ×atrosanguinea 804 (Hough, 1944), is one of several resistance genes found in the small-fruited, Asiatic species of crabapples (Williams and Brown, 1968). A tightly linked DNA marker for Vm, SCAR B12, was previously used to identify Vm in M. × ‘Prairifire’ (Mattison and Nybom, 2005; S. Korban, personal communication). Cheng et al. (1998) and Patocchi et al. (2005) have identified markers tightly linked to Vm resistance in M. × hartwigii, M. halliana, M. hupehensis, M. fusca, and in M. × ‘Prairifire’ (S. Korban, personal communication). However, not every accession of these species was found to possess the markers for Vm (Cheng et al., 1998; Patocchi et al., 2005). M. ×atrosanguinea developed scab as early as 1978, and M. ×micromalus ‘Midget’ was deaccessioned in 1993. The breakdown in resistance in M. × ‘Prairifire’ was first reported in 1997 (P. Pecknold, personal communication) in Indiana but was not detected at the Secrest Arboretum until 2000. Unfortunately, other carriers of the Vm gene, M. ×hartwigii, M. halliana, M. hupehensis, and M. fusca were deaccessioned as a result of fire blight in the early 1990s. M. × ‘Mary Potter’, a hybrid of M. sargentii ‘Rosea’ × M. ×atrosanguinea, developed scab in 1994. Work is currently underway to examine these cultivars for the existence of the linked Vm marker and to look at M. × ‘Liset’, a multibred with M. ×atrosanguinea in the background, to determine if Vm exists in this cultivar as well (Patocchi et al., 2005) and if the breakdown of resistance was attributable solely to the development of Race 5 at Secrest. Curiously, Race 5 has only been reported in Europe (Dayton and Williams, 1968); the development of scab on M. × ‘Prairifire’ suggests a race with virulence similar to Race 5 has developed North America. A cultivar recorded as M. ×atrosanguinea was evaluated as scab-susceptible for the entire 10 years it was included in the trial; it is unknown if this selection possesses the Vm gene or if it is M. ×atrosanguinea 804. M. atrosanguinea 804 was included in the release of cultivars by The Arnold Arboretum in the early 1900s (Crandall, 1926).

Race 6 isolates, capable of infecting some Vf scab-resistant commercial apples, including M. × ‘Prima’, M. ‘Judeline’, and M. × ‘Florina (querina)’ (Parisi and Lespinasse, 1996; Parisi et al., 1993), could not be scored as a result of the absence of these cultivars in the trial. Other M. floribunda selections or hybrids include M. × ‘Exzellenz Theil’, an M. floribunda × M. prunifolia ‘Pendula’ hybrid (Fiala, 1994) that was very susceptible to scab when evaluated, M. ×arnoldiana, and M. ×Scheideckeri. There is no evidence to suggest that any of these cultivars possesses Vf resistance.

M. floribunda, the Japanese flowering crabapple, is considered one of the finest crabapples in cultivation and was introduced into Europe by von Siebold in 1853 from Nagasaki, Japan. The place where this tree grows wild still remains unknown (Fiala, 1994). The selections at Secrest match the taxonomic description of Crandall (1926). Selection M. floribunda 821 was identified as resistant in 1943 by Hough (1944) and Hough et al. (1953) and has been used extensively as a source of resistance in commercial cultivars (Crosby et al., 1992; Janick, 2002). Concomitantly, many of these selections were regularly distributed to arboreta throughout the United States in the 1940s to 1960s for crabapple evaluations (Fiala, 1994); unfortunately, many were misidentified or misnamed (Jefferson, 1970). Records and morphology indicate that this tree is, in fact, M. floribunda, although whether it is a scion of M. floribunda 821, the parent tree that provided both the Vf and Vfh resistance genes that were introgressed into most scab-resistant commercial apples (Janick, 2002), remains undetermined. The identification of Race 7 in the United Kingdom parallels its potential discovery here; a backyard crabapple was identified as a M. floribunda with scab. Inoculation of M. floribunda 821 with scab from the backyard crabapple demonstrated susceptibility and confirmed the development of Race 7 (Roberts and Crute, 1994). The work to conclusively establish the host range and specificity of this M. floribunda-infecting isolate is currently underway.

Until recently (Parisi et al., 1993), Vf was considered to be the most durable source of resistance with Vf-derived cultivars resistant to scab for over 50 years. Not all selections of M. floribunda possess this allele and that selfed M. floribunda 821 had a segregation of resistance that indicates that Vf is a dominant resistance gene (Hough et al., 1953). However, the fact that resistance in this isolate was effective for at least 40 years at Secrest (Chadwick, 1965; this publication) under intense selection pressure supports the contention that it is a selection of M. floribunda with the Vf gene, if not in fact the original M. floribunda 821 (J. Janick, personal communication). The resistance observed at Secrest before 1997 was complete immunity (Score 0), not the light infection (Score 1) described by Parisi et al. (1993) with respect to the identification of Race 6 on commercial apples with Vf resistance. This is consistent with the descriptions by Hough et al. (1953) and Janick (2002). Furthermore, the breakdown of this resistance was absolute with defoliating scab occurring by 2003 and continuing in subsequent years. Current work is underway to confirm the presence of the Vf resistance gene, HcrVf2, in this isolate, the resistance gene that was identified as sufficient to confer scab resistance in M. ‘Gala’, a universally susceptible cultivar for Race 1 differentiation (Belfanti et al., 2004).

Despite the apparent breakdown in Vm and Vf resistance, this study confirms anecdotal reports from nursery managers and landscapers regarding the resistance of M. sargentii selections (‘Sargent’; ‘Firebird’®, = ‘Select A’ PP 12,621, and ‘Tina’), all of which demonstrate considerable resistance to scab. Buttner et al. (2000) identified M. sargentii as a potential source of scab resistance for commercial apple in Europe, although it should be noted that, in addition to small fruit, it is fairly susceptible to fire blight (Richter et al., 2005; Shay et al., 1962). Nursery managers also report the durable resistance of M. baccata ‘Jackii’, an observation confirmed in this study. However, scab has been reported on M. baccata ‘Jackii’ in Sweden (Sandskar and Liljeroth, 2005), so resistance breakdown of this selection is possible in North America in the future.

The breakdown of scab resistance in several hybrid Malus taxa is interesting. M. × ‘Bob White’, introduced in 1876 (Jefferson, 1970), is a suspected M. sieboldii var. zumi hybrid and would therefore be expected to possess comparable polygenic resistance of other M. sieboldii var. zumi selections (e.g., M. var. zumi ‘Wooster’ and var. zumi ‘Calocarpa’). M. × ‘Strawberry Parfait’, a cross between M. hupehensis and M. ×atrosanguinea, also was resistant in 1994, developing scab the same time as M. × ‘Mary Potter’, the offspring of a M. ×atrosanguinea × M. sargentii ‘Rosea’ cross (Fiala, 1994), strongly suggesting the development of a new race of scab concomitant with Vm resistance breakdown. The long-term scab resistance and subsequent development of scab on this selection suggests a minimal oligogenic resistance or that re-evaluation is warranted of the dogma that polygenic resistance is more durable than monogenic resistance. Other crabapples with durable, and probably multigenic, resistance include: M. × ‘Beverly’, a large, upright crabapple with pink flower buds, fragrant, white, five-petaled flowers, bright green leaves and small, red, persistent, glossy fruits strongly suggestive of M. baccata parentage; M. × ‘Silver Moon’, another probable M. baccata hybrid with white flower buds that was described as scab-susceptible by Nichols but did not develop scab at Falconskeape (Fiala, 1994), or throughout our study or in the study by Jacobs and Spravka (1996); and M. × ‘White Angel’, a chance seedling of putative M. sieboldii parentage (Fiala, 1994), also reported by Jacobs and Spravka (1996) as resistant.

In conclusion, data presented in this article demonstrate the durability of resistance of M. baccata ‘Jackkii’, M. sargentii selections, including ‘Sargent’, which was introduced to The Arnold Arboretum in 1892 from Japan, M. × ‘Beverly’, M. × ‘Silver Moon’, and M. × ‘White Angel, and the identification of other potentially stable resistance genes in plants with susceptibility to fire blight or other diseases (Table 2). Over a 33-year period, the evolution of races of V. inaequalis can be observed and the corresponding breakdown of resistance of at least one and possibly two major genes, Vm and Vf/Vfh. The absence of Races 2 and 4 within this population is noteworthy. Work is underway to confirm the presence of HcrVf2 in the susceptible M. floribunda trees at Secrest and conclusively demonstrate the existence of Race 7 and the breakdown of Vf/Vfh resistance in North America. With further integration of the plant pathology and plant breeding efforts, ultimately, the durability of host resistance may be predicted by careful evaluation of pathogen population structure and can result in more effective and durable disease control.

Literature Cited

  • AderholdR.1899Auf welche Weise konnen wir dem immer weiteren Umsichgreifen des Fusicladiums in unseren Apfelkulturen begegnen und welche Sorten haben sich bisher dem Pilz gegenüber am widerstandsfähigsten gezeigtPomol. Monatsh.XLV266272

  • BaggaH.S.BooneD.M.1968aGenes in Venturia inaequalis controlling pathogenicity to crabapplesPhytopathology5811761182

  • BaggaH.S.BooneD.M.1968bInheritance of resistance to Venturia inaequalis in crabapplesPhytopathology5811831187

  • BelfantiE.Silfverberg-DilworthE.TartariniS.PatocchiA.BarbieriM.ZhuJ.VinatzerB.GianfranceschiL.GesslerC.SansaviniS.2004The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated varietyProc. Natl. Acad. Sci. USA101886890

  • BooneD.M.1971Genetics ofVenturia inaequalisAnnu. Rev. Phytopathol.9297318

  • BooneD.M.KeittG.W.1957Venturia inaequalis (Cke.) Wint. XII. Genes controlling pathogenicity of wild-type linesPhytopathology47403409

  • BusV.G.M.2006Differential host–pathogen interactions of Venturia inaequalis and Malus. Thesis, Doctor of Philosophy in Biological SciencesUniversity of Auckland

  • BusV.G.M.LaurensF.N.D.Van deWegW.E.RusholmeR.L.RikkerinkE.H.A.GardinerS.E.BassettH.C.M.PlummerK.M.2005The Vh8 locus of a new gene-for-gene interaction between Venturia inaequalis and the wild apple Malus sieversii is closely linked to the Vh2 locus in Malus pumila R12740-7ANew Phytol.16610351049

  • ButtnerR.GeibelM.FischerC.2000The genetic potential of scab and mildew resistance in Malus wild speciesActa Hort.5386770

  • ChadwickL.C.1965Ornamental crabapples. Lawn and ornamentals researchOhio Agricultural Research and Development CenterWooster, OH

  • ChatfieldJ.A.DraperE.A.HermsD.A.CochranK.A.2005Apple scab on crabapple at Secrest Arboretum: 2005. The Ohio Agricultural Research and Development Center11712111 Mar. 2009<http://ohioline.osu.edu/sc197/pdf/sc197.pdf>.

  • ChengF.S.WeedenN.F.BrownS.K.AldwinckleH.S.GardinerS.E.BusV.G.1998Development of a DNA marker for Vm, a gene conferring resistance to apple scabGenome41208214

  • Crandall C.S. 1926. Apple breeding at the University of Illinois. Bulletin No. 275.

  • CroxallH.E.GwynneD.C.JenkinsJ.E.E.1952The rapid assessment of apple scab on leavesPlant Pathol.13941

  • CrosbyJ.A.JanickJ.PecknoldP.C.KorbanS.S.O'ConnonP.A.RiesS.M.GoffredaJ.VoordeckersA.1992Breeding apples for scab resistance: 1945–1990Fruit Varieties Journal46145166

  • DaytonD.F.WilliamsE.B.1968Independent genes in Malus for resistance to Venturia inaequalisProc. Amer. Soc. Hort. Sci.928994

  • den BoerJ.H.GreenT.L.1995Disease and aesthetic ratingsMalus9858

  • DirrM.1990Manual of woody landscape plants4th EdStipes PublishingChampaign, IL

  • FialaJ.L.1994Flowering crabapples. The genus MalusTimber PressPortland, OR

  • FlorH.H.1956The complementary genic systems in flax and flax rustAdv. Genet.82954

  • ForslineP.L.AldwinckleH.DicksonE.LubyJ.HokansonS.2003Collection, maintenance, characterization, and utilization of wild apples of central AsiaHort. Rev. (Amer. Soc. Hort. Sci.)29160

  • GesslerC.PatocchiA.SansaviniS.TartariniS.GianfranceschiL.2006Venturia inaequalis resistance in appleCrit. Rev. Plant Sci.25473503

  • GuerinF.Le CamB.2004Breakdown of the scab resistance gene Vf in apple leads to a founder effect in populations of the fungal pathogen Venturia inaequalisPhytopathology94364369

  • GygaxM.GianfranceschiL.LiebhardR.KellerhalsM.GesslerC.PatocchiA.2004Molecular markers linked to the apple scab resistance gene Vbj derived from Malus baccata jackiiTheor. Appl. Genet.10917021709

  • Hammond-KosackK.E.JonesJ.D.G.1997Plant disease resistance genesAnnu. Rev. Plant Physiol. Plant Mol. Biol.48575607

  • HoughL.F.1944A survey of the scab resistance of the foliage on seedlings in selected apple progeniesProc. Amer. Soc. Hort. Sci.44260272

  • HoughL.F.ShayJ.R.DaytonD.F.1953Apple scab resistance from Malus floribunda SiebProc. Amer. Soc. Hort. Sci.63341347

  • HoughL.F.WilliamsE.B.DaytonD.F.ShayJ.R.BaileyC.H.MowryJ.B.JanickJ.EmersonF.H.1970Progress and problems in breeding apples for scab resistanceProc. Angers Fruit Breeding Symposium14–18 Sept. 1970217230INRAVersailles, France

  • JacobsK.SpravkaM.1996High- and low- performing crabapples during abnormally severe apple scab conditionsHortTechnology6140

  • JanickJ.2002History of the PRI apple breeding programActa Hort.5955560

  • JeffersonR.M.1970History, progeny, and location of crabapples of documented authentic originUS Department of AgricultureWashington, DC

  • KeittG.W.LangfordM.H.1941Venturia inaequalis (Cke.) Wint. I. A groundwork for genetic studiesAmer. J. Bot.28805820

  • KeittG.W.PalmiterD.H.1938Heterothallism and variability in Venturia inaequalisAmer. J. Bot.25338345

  • LespinasseY.1989Breeding pome fruits with stable resistance to disease: 3 genes, resistance mechanisms, present work and prospectsIOBC WPRS Bull.12100115

  • LubyJ.2003Taxonomic classification and brief history114FerreeD.C.WarringtonI.J.Apples: Botany production and usesCABI PublishingCambridge, MA

  • MacHardyW.E.1996Apple scab: Biology, epidemiology, and managementAPS PressSt. Paul, MN

  • McDonaldB.LindeC.2002Pathogen population genetics, evolutionary potential and durable resistanceAnnu. Rev. Phytopathol.40349379

  • MattisonH.NybomH.2005Application of DNA markers for detection of scab resistant apple cultivars and selectionsIntl. J. Hort. Sci.115963

  • ParisiL.FouilletV.SchoutenH.J.GroenwoldR.LaurensF.DidelotF.EvansK.FischerC.GennariF.KempH.LateurM.PatocchiA.ThissenJ.TsipouridisC.2004Variability of the pathogenicity of Venturia inaequalis in EuropeActa Hort.663107113

  • ParisiL.LespinasseY.1996Pathogenicity of Venturia inaequalis strains of race 6 on apple clones (Malus sp.)Plant Dis.8011791183

  • ParisiL.LespinasseY.GuillaumesJ.KruegerJ.1993A new race of Venturia inaequalis virulent to apples with resistance due to the Vf genePhytopathology83533537

  • PatocchiA.WalserM.TartariniS.BrogginiG.GennariF.SansaviniS.GesslerC.2005Identification by genome scanning approach (GSA) of a microsatellite tightly associated with the apple scab resistance gene VmGenome48630636

  • RichterK.PeilA.HöferM.FischerC.2005Identification of resistance donors for fire blight in MalusZellerW.Proc. of the 1st International Symposium on Biological Control of Bacterial Plant Diseases

  • RobertsA.L.CruteI.R.1994Apple scab resistance from Malus floribunda 821 (Vf) is rendered ineffective by isolates of Venturia inaequalis from Malus floribundaNorw. J. Agr. Sci. Suppl.17403406

  • RobinsonJ.P.HarrisS.A.JuniperB.E.2001Taxonomy of the genus Malus Mill. (Roseaceae) with emphasis on the cultivated apple, Malus domestica BorkhPlant Syst. Evol.2263538

  • RomerJ.P.IlesJ.K.HaynesC.L.2003Selection preferences for crabapple cultivar and speciesHortTechnology13522526

  • SandskarB.LiljerothE.2005Incidence of races of the apple scab pathogen Venturia inaequalis in apple growing districts in SwedenActa Agr. Sc. Section. B-Soil Plant Sci.55143150

  • SchmidtM.1938Venturia inaequalis (Cooke) Aderhold. VIII. Weitere Untersuchungen zur Zuchtung schorfwiderstandsfaÅNhiger ApfelsortenDer Zuchter10280291

  • ShayJ.R.HoughL.F.1952Evaluation of apple scab resistance in selections of MalusAmer. J. Bot.39288297

  • ShayJ.R.WilliamsE.B.1956Identification of three physiological races of Venturia inaequalisPhytopathology46190193

  • ShayJ.R.WilliamsE.B.JanickJ.1962Disease resistance in apple and pearProc. Amer. Hort. Soc.8097104

  • WilliamsE.B.BrownA.G.1968A new physiological race of Venturia inaequalis, incitant of apple scabPlant Dis. Rpt.52799801

  • WilliamsE.B.ShayJ.R.1957The relationship of genes for pathogenicity and certain other characters in Venturia inaequalis (Cke.) WintGenetics42704711

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Contributor Notes

To whom reprint requests should be addressed; e-mail janna@purdue.edu.

Headings

References

AderholdR.1899Auf welche Weise konnen wir dem immer weiteren Umsichgreifen des Fusicladiums in unseren Apfelkulturen begegnen und welche Sorten haben sich bisher dem Pilz gegenüber am widerstandsfähigsten gezeigtPomol. Monatsh.XLV266272

BaggaH.S.BooneD.M.1968aGenes in Venturia inaequalis controlling pathogenicity to crabapplesPhytopathology5811761182

BaggaH.S.BooneD.M.1968bInheritance of resistance to Venturia inaequalis in crabapplesPhytopathology5811831187

BelfantiE.Silfverberg-DilworthE.TartariniS.PatocchiA.BarbieriM.ZhuJ.VinatzerB.GianfranceschiL.GesslerC.SansaviniS.2004The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated varietyProc. Natl. Acad. Sci. USA101886890

BooneD.M.1971Genetics ofVenturia inaequalisAnnu. Rev. Phytopathol.9297318

BooneD.M.KeittG.W.1957Venturia inaequalis (Cke.) Wint. XII. Genes controlling pathogenicity of wild-type linesPhytopathology47403409

BusV.G.M.2006Differential host–pathogen interactions of Venturia inaequalis and Malus. Thesis, Doctor of Philosophy in Biological SciencesUniversity of Auckland

BusV.G.M.LaurensF.N.D.Van deWegW.E.RusholmeR.L.RikkerinkE.H.A.GardinerS.E.BassettH.C.M.PlummerK.M.2005The Vh8 locus of a new gene-for-gene interaction between Venturia inaequalis and the wild apple Malus sieversii is closely linked to the Vh2 locus in Malus pumila R12740-7ANew Phytol.16610351049

ButtnerR.GeibelM.FischerC.2000The genetic potential of scab and mildew resistance in Malus wild speciesActa Hort.5386770

ChadwickL.C.1965Ornamental crabapples. Lawn and ornamentals researchOhio Agricultural Research and Development CenterWooster, OH

ChatfieldJ.A.DraperE.A.HermsD.A.CochranK.A.2005Apple scab on crabapple at Secrest Arboretum: 2005. The Ohio Agricultural Research and Development Center11712111 Mar. 2009<http://ohioline.osu.edu/sc197/pdf/sc197.pdf>.

ChengF.S.WeedenN.F.BrownS.K.AldwinckleH.S.GardinerS.E.BusV.G.1998Development of a DNA marker for Vm, a gene conferring resistance to apple scabGenome41208214

Crandall C.S. 1926. Apple breeding at the University of Illinois. Bulletin No. 275.

CroxallH.E.GwynneD.C.JenkinsJ.E.E.1952The rapid assessment of apple scab on leavesPlant Pathol.13941

CrosbyJ.A.JanickJ.PecknoldP.C.KorbanS.S.O'ConnonP.A.RiesS.M.GoffredaJ.VoordeckersA.1992Breeding apples for scab resistance: 1945–1990Fruit Varieties Journal46145166

DaytonD.F.WilliamsE.B.1968Independent genes in Malus for resistance to Venturia inaequalisProc. Amer. Soc. Hort. Sci.928994

den BoerJ.H.GreenT.L.1995Disease and aesthetic ratingsMalus9858

DirrM.1990Manual of woody landscape plants4th EdStipes PublishingChampaign, IL

FialaJ.L.1994Flowering crabapples. The genus MalusTimber PressPortland, OR

FlorH.H.1956The complementary genic systems in flax and flax rustAdv. Genet.82954

ForslineP.L.AldwinckleH.DicksonE.LubyJ.HokansonS.2003Collection, maintenance, characterization, and utilization of wild apples of central AsiaHort. Rev. (Amer. Soc. Hort. Sci.)29160

GesslerC.PatocchiA.SansaviniS.TartariniS.GianfranceschiL.2006Venturia inaequalis resistance in appleCrit. Rev. Plant Sci.25473503

GuerinF.Le CamB.2004Breakdown of the scab resistance gene Vf in apple leads to a founder effect in populations of the fungal pathogen Venturia inaequalisPhytopathology94364369

GygaxM.GianfranceschiL.LiebhardR.KellerhalsM.GesslerC.PatocchiA.2004Molecular markers linked to the apple scab resistance gene Vbj derived from Malus baccata jackiiTheor. Appl. Genet.10917021709

Hammond-KosackK.E.JonesJ.D.G.1997Plant disease resistance genesAnnu. Rev. Plant Physiol. Plant Mol. Biol.48575607

HoughL.F.1944A survey of the scab resistance of the foliage on seedlings in selected apple progeniesProc. Amer. Soc. Hort. Sci.44260272

HoughL.F.ShayJ.R.DaytonD.F.1953Apple scab resistance from Malus floribunda SiebProc. Amer. Soc. Hort. Sci.63341347

HoughL.F.WilliamsE.B.DaytonD.F.ShayJ.R.BaileyC.H.MowryJ.B.JanickJ.EmersonF.H.1970Progress and problems in breeding apples for scab resistanceProc. Angers Fruit Breeding Symposium14–18 Sept. 1970217230INRAVersailles, France

JacobsK.SpravkaM.1996High- and low- performing crabapples during abnormally severe apple scab conditionsHortTechnology6140

JanickJ.2002History of the PRI apple breeding programActa Hort.5955560

JeffersonR.M.1970History, progeny, and location of crabapples of documented authentic originUS Department of AgricultureWashington, DC

KeittG.W.LangfordM.H.1941Venturia inaequalis (Cke.) Wint. I. A groundwork for genetic studiesAmer. J. Bot.28805820

KeittG.W.PalmiterD.H.1938Heterothallism and variability in Venturia inaequalisAmer. J. Bot.25338345

LespinasseY.1989Breeding pome fruits with stable resistance to disease: 3 genes, resistance mechanisms, present work and prospectsIOBC WPRS Bull.12100115

LubyJ.2003Taxonomic classification and brief history114FerreeD.C.WarringtonI.J.Apples: Botany production and usesCABI PublishingCambridge, MA

MacHardyW.E.1996Apple scab: Biology, epidemiology, and managementAPS PressSt. Paul, MN

McDonaldB.LindeC.2002Pathogen population genetics, evolutionary potential and durable resistanceAnnu. Rev. Phytopathol.40349379

MattisonH.NybomH.2005Application of DNA markers for detection of scab resistant apple cultivars and selectionsIntl. J. Hort. Sci.115963

ParisiL.FouilletV.SchoutenH.J.GroenwoldR.LaurensF.DidelotF.EvansK.FischerC.GennariF.KempH.LateurM.PatocchiA.ThissenJ.TsipouridisC.2004Variability of the pathogenicity of Venturia inaequalis in EuropeActa Hort.663107113

ParisiL.LespinasseY.1996Pathogenicity of Venturia inaequalis strains of race 6 on apple clones (Malus sp.)Plant Dis.8011791183

ParisiL.LespinasseY.GuillaumesJ.KruegerJ.1993A new race of Venturia inaequalis virulent to apples with resistance due to the Vf genePhytopathology83533537

PatocchiA.WalserM.TartariniS.BrogginiG.GennariF.SansaviniS.GesslerC.2005Identification by genome scanning approach (GSA) of a microsatellite tightly associated with the apple scab resistance gene VmGenome48630636

RichterK.PeilA.HöferM.FischerC.2005Identification of resistance donors for fire blight in MalusZellerW.Proc. of the 1st International Symposium on Biological Control of Bacterial Plant Diseases

RobertsA.L.CruteI.R.1994Apple scab resistance from Malus floribunda 821 (Vf) is rendered ineffective by isolates of Venturia inaequalis from Malus floribundaNorw. J. Agr. Sci. Suppl.17403406

RobinsonJ.P.HarrisS.A.JuniperB.E.2001Taxonomy of the genus Malus Mill. (Roseaceae) with emphasis on the cultivated apple, Malus domestica BorkhPlant Syst. Evol.2263538

RomerJ.P.IlesJ.K.HaynesC.L.2003Selection preferences for crabapple cultivar and speciesHortTechnology13522526

SandskarB.LiljerothE.2005Incidence of races of the apple scab pathogen Venturia inaequalis in apple growing districts in SwedenActa Agr. Sc. Section. B-Soil Plant Sci.55143150

SchmidtM.1938Venturia inaequalis (Cooke) Aderhold. VIII. Weitere Untersuchungen zur Zuchtung schorfwiderstandsfaÅNhiger ApfelsortenDer Zuchter10280291

ShayJ.R.HoughL.F.1952Evaluation of apple scab resistance in selections of MalusAmer. J. Bot.39288297

ShayJ.R.WilliamsE.B.1956Identification of three physiological races of Venturia inaequalisPhytopathology46190193

ShayJ.R.WilliamsE.B.JanickJ.1962Disease resistance in apple and pearProc. Amer. Hort. Soc.8097104

WilliamsE.B.BrownA.G.1968A new physiological race of Venturia inaequalis, incitant of apple scabPlant Dis. Rpt.52799801

WilliamsE.B.ShayJ.R.1957The relationship of genes for pathogenicity and certain other characters in Venturia inaequalis (Cke.) WintGenetics42704711

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