Regīna Rancāne1,2
Alma Valiuškaitė
Arne Stensvand- 1Institute of Horticulture, Lithuanian Research Centre for Agriculture and Forestry, Babtai, Lithuania
- 2Institute for Plant Protection Research “Agrihorts”, Latvia University of Life Sciences and Technologies, Jelgava, Latvia
- 3Division of Biotechnology and Plant Health, Norwegian Institute of Bioeconomy Research (NIBIO), Ås, Norway
This review summarizes and discusses the geographical distribution, overwintering, dissemination, and management of the asexual stage of Venturia inaequalis, the fungal pathogen causing apple scab. The asexual overwintering of V. inaequalis has primarily been described as wood scab, superficial scab, or bud scab, and more rarely, it is mentioned as overwintering on infected leaves and fruits still attached to the trees. Wood scab is fungal pustules found on new and 1-year-old shoots, but it is also found on 2-year-old wood. It has been reported in many apple-growing countries throughout the world; however, most reports of wood scab being an important source of primary inoculum, as well as the most in-depth studies, are from the UK. Reports from some countries describe what is named superficial scab, which are symptomless infections of the pathogen on shoot surfaces. Overwintering of V. inaequalis on the inner or outer bud scales has also been reported in some countries. Infections may appear as small lesions on the bud scales, but numerous conidia have also been found in buds without symptomatic fungal tissue. The incidence and quantity of overwintering in the asexual stage are dependent on the amount of scab in the previous season, growth characteristics, and cultivar susceptibility. In orchards with limited options for fungicide control and/or in orchards with loss of scab control in the preceding season, conidia of V. inaequalis should not be underestimated as a source of primary inoculum.
Introduction
Apple scab, caused by the ascomycete Venturia inaequalis (Cooke) Wint., is one of the most common diseases of apple (Malus × domestica Borkh.) worldwide. Overwintering as mycelium and conidia of V. inaequalis in shoots or buds is reported in many countries where apples are produced (Tables 1, 2). In 1855, Berkley in the UK was wondering why twigs of apple and pear were cracking, thus indicating the appearance of scab in the wood (Marsh and Walker, 1932). Bagenal et al. (1925) claimed that until 1924, the only stage of V. inaequalis known in the UK, in which the fungus persisted through the winter, was on the 1-year-old wood of certain apple cultivars. However, no solid evidence for this statement was put forward.
Table 1 Publications that report on Venturia inaequalis overwintering on apples in its asexual stage in wood pustules, and/or superficially on shoots.
Table 2 Publications that report on Venturia inaequalis overwintering in its asexual stage in apple buds.
Asexual overwintering of V. inaequalis has most commonly been described as dark pustules consisting of fungal stroma with conidial spores under the bark on twigs (Table 1). Such symptoms have been named shoot scab, twig scab, and wood scab and are designated as wood scab below. The fungus can also be symptomless as conidia or hyphae on the surface of shoots, and this is named superficial scab (Table 1). On both the inner and outer bud scales, the fungus may overwinter as visible fungal lesions or asymptomatically, both with conidia present. This is named bud scab (Table 2). Finally, shoot base scab are scab lesions expanding from the surface of 1-year-old shoots onto new emerging leaves and shoot tissues (Kennel, 1990). Leaves and non-detached fruits may stay on trees throughout winter and into the early spring and can potentially be sources of inoculum of apple scab (e.g., Young and Curtis, 1927; Shabi et al., 1981; Kennel, 1990; Washington et al., 1998; Von Diest et al., 2015), but this is not further discussed below. Asexual overwintering as conidia in twig lesions in wood is reported also for other Venturia spp. (e.g., Saccas, 1944; Kienholz and Childs, 1951; Umemoto, 1992; Scherm et al., 2008). This review reports on the geographical distribution, overwintering, and dissemination of V. inaequalis in its asexual stage in wood and bud tissue, and briefly also on management.
Geographical distribution and importance
The occurrence of wood scab of V. inaequalis has been known for a long time (e.g., Cuboni, 1892; Sorauer, 1890; Stewart and Blodgett, 1899). In Europe, wood scab has especially been reported from the northwestern parts, including Ireland, Scandinavia, and the UK (Table 1). It was not detected in a survey in Finland (Hårdh, 1955). In Germany, Switzerland, and Poland, most reports describe symptomless superficial scab. In the Netherlands, it was concluded that the conidial inoculum of V. inaequalis from wood tissue was of minor importance (Holb et al., 2004; Holb et al., 2005). Wood scab has been reported in several states in northern regions of the USA (Table 1); however, with few exceptions (e.g., Morse and Darrow, 1913), it has not been considered important. Wood scab has been reported in Australia (McAlpine, 1902), New Zealand (Cunningham, 1925), India (Gupta and Lele, 1980), and South Africa (Louw, 1951) but as of minor importance. In a survey in Chile, wood scab was not detected (Montealegrale and González, 1982). Winter survival of V. inaequalis in buds has been reported in Australia, South Africa, and the USA, as well as in several countries in Europe and Asia (Table 2).
Pathogen development on shoots
Green, succulent tissue of shoots of apple trees may become infected by V. inaequalis (Marsh and Walker, 1932; Dillon Weston and Petherbridge, 1933; Hockey, 1953; Swinburne, 1965). Both vigorously growing terminal shoots and water sprouts (rapidly emerging shoots from dormant buds) are susceptible to wood infections (Morse and Darrow, 1913). Marsh and Walker (1932) and Swinburne (1965) in the UK and Saccas (1944) in France provided detailed descriptions and illustrations of the infection process of V. inaequalis in apple shoots. The fungus forms a lens-shaped parenchymatous tissue, forcing the epidermis and the cuticle apart. The epidermal cells in contact with the fungal tissue will collapse, and these cells are invaded by the fungus. New infections may take place at any time during the shoot growth, but only in the green apical regions. The time of infection determines the final position of the lesion on the shoot, i.e., early infections appear closer to the base, while later infections are further up along the shoots (Cook, 1974). In winter, the fungus may grow between the collenchyma and bark tissues to form subsidiary pustules, and this new extension of fungal growth remains covered until spring (Marsh and Walker, 1932). The fungal stroma is eventually stopped by the formation of cork barriers in the host tissue (Marsh and Walker, 1932; Saccas, 1944; Swinburne, 1965).
During late winter and early spring, the subsidiary stromata become thicker, with layers of radially arranged rows of fungal cells (Marsh and Walker, 1932; Cook, 1974). Conidiophores and conidia are formed under the bark although the bark is still unbroken. Eventually, the bark gives way to the pressure and is ruptured, and the formation of conidia begins in the central portions and spread toward the margins (Marsh and Walker, 1932). In late spring or early summer, further cork barriers are formed, and eventually, the infected tissue is sloughed off. Infections on apple shoots are predominantly found on new and 1-year-old wood (e.g., Marsh and Walker, 1932; Wiesmann, 1935; Saccas, 1944; Stensvand et al., 1996) but have been found on 2-year-old wood in early spring (Swinburne, 1965).
In the UK, the release of conidia on new shoots of cv. Cox Orange Pippin was observed from August to November, with a peak in October (Hill, 1975). There were low releases from December to February, high releases from March to May, and they ceased in June. Another study in the UK found conidia in wood pustules on 1-year-old wood from 2-3 weeks prior to bud burst, with the highest numbers in April and May (Cook, 1974). Yet another study from the UK found the first conidia of V. inaequalis on wood pustules in early March (Dillon Weston and Petherbridge, 1933), and in Switzerland, conidia on wood pustules were recorded before mid-March (Müller-Thurgau, 1902). Conidia were produced in wood pustules from November to early July in Ireland but were most abundant from March to June (McKay, 1938). In Germany, the first conidia in wood pustules were found in late February and early March (Voges, 1910; Winkelmann et al., 1937). Conidia on new shoots were found in August and on 1-year-old shoots from March to September in Norway (Stensvand et al., 1996), and in France, conidia were produced in 1-year-old wood from February to April (Saccas, 1944). In New York, high numbers of conidia were observed in new infections on green shoots in July, while numbers and viability declined in October (Becker and Burr, 1992). Wood pustules of new apple shoots in Australia had conidiophores and conidia of V. inaequalis in early autumn (March) (Washington et al., 1998).
The viability of conidia from scab pustules of 1-year-old wood was 50 to 70% in April and May in the UK (Marsh and Walker, 1932). In Maine, high amounts of viable conidia in scab pustules were found in March and April, in the time before or around bud break (Morse and Darrow, 1913). In Norway, the viability of conidia was low in February, high in March to August, and low in September (Stensvand et al., 1996). Conidia on the surface of apple shoots in the Netherlands had a viability of less than 1.5% (Holb et al., 2004; Holb et al., 2005). In New York, very few viable conidia were found on wood in an unsprayed orchard in April (Becker and Burr, 1992).
Superficial scab on shoots
Shoot base scab is lesions appearing superficially on the surface of 1-year-old shoots and growing directly onto the new apple tissue (Kennel, 1990; Stensvand et al., 1996). However, superficial scab was described in Germany as asymptomatic scab overwintering as individual hyphae and/or conidia on the bark surface or on the trichomes (epidermal hairs) (Kennel, 1981a; Moosherr and Kennel, 1986; Moosherr and Kennel, 1995). It was speculated that the fungus could overwinter inside trichomes (Moosherr and Kennel, 1995), but this could not be confirmed by Portz (2002). In France, trichomes were also mentioned as retaining conidia of V. inaequalis during winter (Saccas, 1944). Superficial scab was commonly observed if trees started regrowth after summer pruning, thus providing a tissue highly susceptible to V. inaequalis (Kennel, 1981a; Moosherr and Kennel, 1995).
In spring, an average of 12% of the conidia would germinate from superficial scab, but occasionally, more than 50% were viable (Moosherr and Kennel, 1995). High numbers of overwintering conidia were found on apple wood in early spring in Poland, especially on trees with much scab the preceding autumn (Rogaś and Grabowski, 2005). In South Australia, no superficially overwintered conidia of V. inaequalis remained viable after mid-winter (Jeffrey, 1953).
Scab in apple buds
Bud scales can be infected by V. inaequalis when buds start to form (Saccas, 1944; Olsson, 1960), and both in Ireland (McKay, 1938) and New York (Becker, 1990), new buds were infected in July. On immature newly infected bud scales, conidiophores and conidia were formed in dark lesions, and later, a more developed stroma was developed that was mostly less than 1 mm in diameter in February (McKay, 1938). In New York, scab lesions on bud scales were up to 2 mm in diameter (Becker and Burr, 1992). The formation of stroma in bud scales in autumn and winter was also described by Salmon and Ware (1931) and Dillon Weston et al. (1952) in the UK and by Saccas (1944) in France. Both external and internal bud scales can carry mycelial stroma, and it was stated that vegetative and generative buds constituted a source of inoculum as important as wood scab (Saccas, 1944). A mean viability of conidia of 77% was found in New York just before bud break, and viability was lowest for conidia of outer bud scales (Becker and Burr, 1992). Scab lesions were found in bud scales in several apple orchards in South Australia at the time of bud burst (Jeffrey, 1953).
Both in the Netherlands and New York, viable conidia were present in buds without any apparent lesion formation (Becker and Burr, 1992; Holb et al., 2004; Holb et al., 2005). It was speculated that conidia may remain ungerminated from the previous season, or that non-visible lesions had formed. Saccas (1944) indicated that conidia of V. inaequalis may themselves produce a conidiophore identical to the one normally formed by the hyphae. Most conidia were found on the outer bud scales, with a mean viability of only 2%, while viability from inner bud scales was up to 11% (Holb et al., 2004; Holb et al., 2005). In South Africa, the viability of conidia of V. inaequalis from inner bud tissue varied from 0 to 29% (Von Diest et al., 2015).
Although conidia of V. inaequalis from apple buds were found in February in Ireland, the majority were produced from mid-April to June (McKay, 1938). The reason why inoculum from bud scales was present until June may be because the lowermost part of the scab-infected scales remained attached to the shoots, as described by Salmon and Ware (1931). In Japan, scab pustules were observed on overwintering outer and inner bud scales of apple, and conidia in buds were formed before the ascospores in leaf litter (Kudo et al., 1976). In Sweden, scab pustules on infested bud scales were exposed and produced conidia in April (Olsson, 1960). Indications have been provided that new leaves can be infected prior to bud break, before they emerge (Bagenal et al., 1925; Saccas, 1944; Portz, 2002).
Factors influencing overwintering in the asexual stage
Numerous authors have concluded that overwintering in the asexual stage of V. inaequalis on wood or in the buds is associated with high inoculum in the orchards the preceding autumn (e.g., Morse and Darrow, 1913; Soenen et al., 1957; Siegfried et al., 1989; Van der Scheer and Grabowski, 1991; Becker and Burr, 1992; Holb et al., 2004; Holb et al., 2005; Rogaś and Grabowski, 2005; Von Diest et al., 2015). It has also been speculated that specific strains of the fungus may be more aggressive on wood (Cook, 1974).
Holb et al. (2004) concluded that conidia were unlikely to overwinter on the surface of apple tissues if they were exposed to fluctuating environmental conditions as in the Netherlands. Moosherr and Kennel (1995) speculated that insufficient winter hardiness and part death of shoots that had emerged after summer pruning was a less favorable environment for superficial scab. In experiments under controlled conditions, conidia of V. inaqualis survived repeated temperature fluctuations around 0°C, with minor losses in viability (Portz, 2002). Another study showed minimal loss of viability of conidia if kept at -5°C for 150 days or -10°C for one month (Saccas, 1944).
The amount of trichomes may vary with the genotype and stage of development of the apple tree. It has been speculated that trichomes may be barriers preventing spores from reaching the cuticle of the shoot surface, or contrary, that trichomes may prevent drying and thus create a better environment for fungal infection (Marsh and Walker, 1932). In a study in Germany, it was concluded that dense growth of trichomes on the shoots prevents infection by V. inaequalis (Portz, 2002).
In older literature from the UK and Ireland, cultivars reported as susceptible to wood scab included Bramley’s Seedling, Cox Orange Pippin, Egremont Russet, and Worcester Pearmain (Bagenal et al., 1925; Salmon and Ware, 1931; Marsh and Walker, 1932; Dillon Weston and Petherbridge, 1933; McKay, 1938; Preece, 1961; Swinburne, 1965), while cv. Blenheim Orange was mentioned as slightly to moderately susceptible (Salmon and Ware, 1931; Dillon Weston and Petherbridge, 1933; Preece, 1961). Cvs. Bramley’s Seedling and Cox’s Orange Pippin were mentioned as susceptible to wood scab also in Germany (Ahrens, 1985). In Canada and USA, cv. McIntosh was considered susceptible to wood scab (Morse and Darrow, 1913; Morris, 1914; McCurry and Hicks, 1926), as well as cv. Fameuse (Morse and Darrow, 1913). In Norway, wood scab was detected on all seven apple cultivars examined, including five with high susceptibility to scab (Gravensteiner, Lobo, Quinte, Summerred, and Vista Bella), and two with moderate to low susceptibility (Ingrid Marie and Torstein) (Stensvand et al., 1996). In Germany, Moosherr and Kennel (1995) reported that cvs. Gloster, Golden Delicious, and Jonagold frequently developed superficial scab. Medium to less susceptible cultivars were Cox Orange, James Grieve, and Jonathan, and the least susceptible was Gravensteiner. In Poland, cv. McIntosh was highly susceptible to superficial scab but was also found on cvs. Idared and Jonagold (Rogaś and Grabowski, 2005).
Control measures
Saccas (1944) suggested chemical treatments in the autumn when infections of the young twigs start to occur, as well as one or more treatments at the beginning of vegetation when overwintering conidia are released. Holb et al. (2004) indicated that a fungicide spray at bud break may protect against overwintered conidia. Marsh and Walker (1932), and Wiesmann (1935) considered that fungicide application in spring would likely not control scab in wood pustules because fungicides would only kill the outer layer of the exposed stroma, and lower portions would remain unharmed. They claimed that the prevention of new shoot infections during the summer and autumn would be more appropriate. The application of urea in autumn or spring reduced the formation of conidia in wood lesions (Cook, 1974), and the use of lime sulfur or copper compounds killed conidia and parts of the stroma in wood scab pustules of apple (Morse and Darrow, 1913; Weber, 1934).
Holb et al. (2004) found the most overwintered conidia in the upper third part of the shoots of the tree, and they, therefore, suggested pruning out that portion of the 1-year-old shoots combined with a fungicide spray at bud break. Moosherr and Kennel (1995) strongly recommended avoiding improper summer pruning since it promotes late shoot growth, thus providing a substrate for superficial scab infection.
Discussion
In reports from many apple-growing regions of the world, it has been shown that V. inaequalis can overwinter either as fungal stroma, inconspicuous hyphae, or conidia on apple shoot tissue and serve as sources of primary inoculum in spring. It seems evident that the asexual stage is associated with the presence of a high inoculum from the previous growing season; however, in most orchards with good scab control, primary inoculum from conidia is likely to be of minimal importance.
Historically, overwintering in scab pustules in shoots (wood scab) was frequently reported and considered more important in the UK than anywhere else. It may be speculated that predominant cultivars and the cool and wet weather during parts of the growing season when the green shoot and bud tissue is susceptible may be reasons for this. It is known that there can be significant genetic variations in strains of V. inaequalis within and between orchards, and among regions in a country (e.g., Xu et al., 2013; Koopman et al., 2017; Passey et al., 2017). Further speculation may thus be that the presence of specific strains of the fungus could explain a higher frequency of asexual overwintering in the UK, as indicated by Cook (1974).
Reports on wood and bud scab are commonly found in early reports when fungicide use was less intense, and at that time, the inoculum was likely higher. However, in organic production with strong restrictions on the use of chemicals or in integrated production with insufficient scab control, e.g., due to fungicide resistance, the risk of heavy scab attacks in autumn and asexual overwintering may occur. In an unsprayed research orchard in the UK, 20-50% of primary infections originated from conidia (Passey et al., 2017), clearly indicating that if scab control is lost, asexual overwintering of V. inaequalis may be important the following year. If overwintered conidial inoculum appears, it is ready to infect already at bud break and may cause early infections of the flower and fruit sepals and, thereby, be a source for severe fruit infections later in the season (Kennel and Moosherr, 1983; Kennel, 1987; Becker and Burr, 1992). To avoid overwintering in the asexual stage, attention must be drawn to avoid the build-up of the disease late in the season, and also following harvest, which is a time growers are often not focused on scab control.
Author contributions
RR and AS surveyed the literature, planned, and wrote the manuscript, and AV critically revised the manuscript. All authors contributed to the article and approved the submitted version.
Funding
The work was partly financed by funding from a PhD scholarship at Lithuanian Research Centre for Agriculture and Forestry.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Ahrens P. G. (1985). Die Möglichkeiten einer Bekämpfung des Apfelschorfes im Rahmen des integrieten Pflanzenschutzes. Erwerbsobstbau 27, 90–95.
Bagenal N. B., Goodwin W., Salmon E. S., Ware W. M. (1925). Spraying experiments against apple scab. J. Mineral Agric. 32, 137–149.
Becker C. M. (1990). Overwintering of the anamorph of Venturia inaequalis (Spilocaea pomi) in apple buds and the viability of conidia as affected by discontinuous wetting. PhD thesis. Ithaca (NY): Cornell Univ. 86.
Becker C. M., Burr T. J. (1992). Overwintering of conidia of Venturia inaequalis in apple buds in New York orchards. Plant Dis. 76, 121–126. doi: 10.1094/PD-76-0121
Cass Smith W. P., Harvey H. L., Goss O. J. (1948). Apple scab outbreaks season 1947-48, with special reference to the introduction of the disease by infected buds on imported nursery stock. W. Aus. J. Agric. 25, 129–135.
Cook R. T. A. (1974). Pustules as sources of inoculum in apple scab and their responses to chemical treatments. Ann. Appl. Biol. 77, 1–9. doi: 10.1111/j.1744-7348.1974.tb01381.x
Cuboni G. (1892). Sulla Forma ibernante del Fusicladium dendriticum. Bull. Soc. Bot. Ital. 1, 287–288.
Cunningham G. H. (1925). Fungous diseases of fruit trees in New Zealand and their remedial treatment (Auckland, New Zealand: Brett Printing and Publishing Co.).
Dillon Weston W. A. R., Petherbridge F. R. (1933). Apple and pear scab in East Anglia. J. Pomol. Hortic. Sci. 11, 185–198. doi: 10.1080/03683621.1933.11513417
Dillon Weston W. A. R., Storey I. F., Ives J. V. (1952). Apple scab in the Wisbech area. Garden. Chron. 132, 195.
Eriksson J. (1911). Die rote Farbe der Fruchtschale und die Schorfkrankheit der Obstsorten. Z. f. Pflanzenkrankh. 21, 129–131.
Gjærum H. B. (1962). Skurv på frukttrær. [In Norwegian]. Landbruksdepartementets opplysningstjeneste Småskrift 1/62, 8.
Goossens J. (1934). Onderzoek naar de erste infectiebron van appel- en peerenschurft. T. Pflantenziekten 40, 174–176.
Griffen E., Maublanc A. (1908). Note sur diverses maladies des branches du pommier. Bull. Séances Soc. Natl. Agric. 8.
Gupta G. K., Lele V. C. (1980). Morphology, physiology and epidemiology of the apple scab fungus, Venturia inaequalis (Cke.) Wint., in Kashmir Valley. Indian J. Agric. Sci. 50, 51–60.
Hårdh J. E. (1955). Omenarupi ja sen torjunta suomessa. [In Finnish, English summary]. Publ. Finnish State Agric. Res. Board 144, 43.
Hill S. A. (1975). The importance of wood scab caused by Venturia inaequalis (Cke.) Wint. as a source of infection for apple leaves in spring. Phytopathol. Z. 82, 216–223. doi: 10.1111/j.1439-0434.1975.tb03486.x
Hirst J. M., Storey I. F., Ward W. C., Wilcox H. J. (1955). The origin of apple scab epidemics in the Wisbech area in 1953 and 1954. Plant Pathol. 4, 91–96. doi: 10.1111/j.1365-3059.1955.tb00749.x
Hockey J. F. (1953). Studies in fruit diseases IX. Apple scab. Dept. Agric., Ottawa, Canada 519, 1–8.
Holb I. J., Heijne B., Jeger M. J. (2004). Overwintering of conidia of Venturia inaequalis and the contribution to early epidemics of apple scab. Plant Dis. 88, 751–757. doi: 10.1094/PDIS.2004.88.7.751
Holb I. J., Heijne B., Jeger M. J. (2005). The widespread occurrence of overwintered conidial inoculum of Venturia inaequalis on shoots and buds in organic and integrated apple orchards across the Netherlands. Eur. J. Plant Pathol. 111, 157–168. doi: 10.1007/s10658-004-1883-z
Jeffrey M. W. (1953). Preliminary investigations into the life cycle of Venturia inaequalis (Cooke) Wint. in South Australia. Aust. J. Aric. Res. 4, 415–422. doi: 10.1071/AR9530415
Jeger M. J., Alston F. H. (1986). Resistance in apple to shoot infection by Venturia inaequalis. Ann. Appl. Biol. 108, 387–394. doi: 10.1111/j.1744-7348.1986.tb07660.x
Kennel W. (1981a). Integrierte Bekämpfung des Apfelschorfes (Venturia inaequalis). Erwerbsobstbau 23, 132–135.
Kennel W. (1981b). Zum auftreten von Schorfkonidien auf äußerlichunversehrter Rinde von Apfelzweigen. Mitt. BBA Heft 203, 117.
Kennel W., Moosherr W. (1983). Kelchblattschorf, eine gefährliche aber wenig bekannte Erscheinungsform des Apfelschorfs. Obstbau 8/83, 470–472.
Kienholz J. R., Childs L. (1951). Pear scab in Oregon. Agric. Exp. Stn. Oregon State Coll. Corvallis Stn. Techn. Bull. 21, 31.
Koopman T. A., Meitz-Hopkins J. C., Bester-van der Merwe A. E., Tobutt K. R., Bester C., Lennox C. L. (2017). Genetic diversity and gene flow of four South African Venturia inaequalis (apple scab) populations. Phytopathology 107, 455–462. doi: 10.1094/PHYTO-07-16-0279-R
Kudo T., Takahashi S., Mizuno N. (1976). Studies on scab disease (Venturia inaequalis (Cooke) Winter) of apple. 1. Overwintering of apple scab fungus on the bud scales. Bull. Akita Fruit Tree Exp. Stn. 8, 19–29.
Louw A. J. (1951). Studies on the influence of environmental factors on the overwintering and epiphytology of apple scab [Venturia inaequalis (Cke.) Wint.] in the winter-rainfall area of the Cape Province. Union S. Afr. Dep. Agric. Sci. Bull. 310, 47.
Marsh R. W., Walker M. M. (1932). The scab fungus (Venturia inaequalis) on apple shoots. J. Pomol. Hortic. Sci. 10, 71–90. doi: 10.1080/03683621.1932.11513393
McAlpine D. (1902). The apple scab fungus causing black spot of apple and pear. Victoria Agric. Dept. J. 1, 703–708.
McCurry J. B., Hicks A. J. (1926). Sixth annual report on the prevalence of plant diseases in the Dominion of Canada. Canada Expt. Farms, Div. Bot. Ann. Rpt., Canad. Plant Dis. Survey 6, 1–47.
McKay R. (1938). Conidia from infected bud-scales and adjacent wood as a main source of primary infection with the apple scab fungus Venturia inaequalis (Cooke) Wint. Sci. Proc. R. Dublin Soc. 21, 623–640.
Mills W. D., Dewey J. E. (1947). Control of diseases and insects in the orchards. Cornell Ext. Bull. 711, 89.
Montealegrale J. A., González S. M. (1982). Prospeccion de invernacion de Fusicladium dendriticum (Wallr.) Fckl. en ramillas de manzano durante la prima-vera de 1979 en la provincia de Valdivia, Chile. Agro Sur. 10, 47–48.
Moore M. H. (1930). The incidence and control of apple scab and apple mildew at East Malling. J. Pomol. Hortic. Sci. 8, 283–304. doi: 10.1080/03683621.1930.11513365
Moosherr W., Kennel W. (1986). Zur epidemiologischen Bedeutung von superfiziellem Zweigschorf bei Apfelbäumen. Mitt. BBA Heft 232, 212.
Moosherr W., Kennel W. (1995). Investigations on superficial apple scab on apple shoots. Z. Pflanzenk. Pflanzen 102, 171–183.
Morris H. E. (1914). A contribution to our knowledge of apple scab. Montana Agric. Coll. Exp. Stn. Bull. 96, 65–102.
Morse W. J. (1916). Spraying experiments and apple diseases in 1915. Maine Agric. Exp. Stn. Bull. 252, 190–192. doi: 10.5962/bhl.title.86714
Morse W. J., Darrow W. H. (1913). Is apple scab on young shoots a source of spring infection? Phytopathology 3, 265–269.
Müller-Thurgau H. (1902). Die Schorfkrankheit der Obstbäume. Jahresb. D. deutsch-schweizerischen Versuchsstation und Schule F. Obst. Wein- und Gartenbau Wädenswil 9, 60–65.
Nichols L. P., Petersen D. H. (1969). Occurrence of the apple scab fungus on twigs of flowering crab apples and one cultivar of commercial apple. Plant Dis. Rep. 53, 974.
Nichols L. P., Petersen D. H. (1971). Overwintering of Fusicladium dendriticum, the imperfect stage of the apple scab fungus on twigs of flowering crab apples. Plant Dis. Rep. 55, 509–510.
Olsson K. (1960). En inventering av gren- og knoppskorv på äpple. [In Swedish]. Väkstskyddsnotiser Statens Växtskyddsanstalt 23, 5–9.
Passey T. A. J., Robinson J. D., Shaw M. W., Xu X. (2017). The relative importance of conidia and ascospores as primary inoculum of Venturia inaequalis in a southeast England orchard. Plant Pathol. 66, 1445–1451. doi: 10.1111/ppa.12686
Portz C. (2002). Venturia inaequalis (Cke.) Wint. beim Apfel: Bedeutung der Konidien als Primärinokulum, Einfluss auf die Knospenentwicklung und Alternativen zum Kupfereinsatz bei der Kontrolle des Blatt- und Fruchtschorfbefalls. PhD thesis at Hohen Landwirtschaftlichen Fakultät der Rheinischen Friedrichs-Wilhelms-Universität, 158.
Rogaś K., Grabowski M. (2005). The effect of autumn infection of apple leaves on the occurrence of the conidial stage of fungus Venturia inaequalis (Cooke) Aderh. on one-year-old shoots. Acta Sci. Pol. Hortorum Cultus 4, 21–26.
Saccas A. (1944). Étude morphologique et biologique des Fusicladium des Eosacees (Librairie Le François), 317.
Salmon E. S., Ware W. M. (1931). A new fact in the life-history of the apple scab fungus. Gard. Chron. 89.
Scherm H., Savelle A. T., Boozer R. T., Foshee W. G. (2008). Seasonal dynamics of conidial production potential of Fusicladium carpophilum on twig lesions in southeastern peach orchards. Plant Dis. 92, 47–50. doi: 10.1094/PDIS-92-1-0047
Schøyen W. M. (1907). Æbleskurv. [In Norwegian]. Fra Landbrugsdepartementet. Meddelelser fra Statsentomologen 3, 1–4.
Shabi E., Elisha S., Zelig Y. (1981). Control of pear and apple diseases in Israel with sterol-inhibiting fungicides. Plant Dis. 65, 992–994. doi: 10.1094/PD-65-992
Siegfried W., Bosshard E., Schüepp H. (1989). Das Schorjahr 1988. Schweiz. Z. Obst- und Weinbau 125, 175–182.
Stensvand A., Amundsen T., Semb L. (1996). Observations on wood scab caused by Venturia inaequalis and V. pirina in apple and pear in Norway. Norw. J. Agr. Sci. 10, 533–540.
Stewart F. C., Blodgett F. H. (1899). A fruit disease survey of the Hudson Valley in 1899. New York Agric. Exp. Stn. Bull. 167, 283.
Swinburne T. R. (1965). Apple scab infection of the young wood of Bramley’s Seedling trees in Northern Ireland. Plant Pathol. 14, 23–25. doi: 10.1111/j.1365-3059.1965.tb00614.x
Umemoto S. (1992). A simple method for estimating conidial numbers of Japanese pear scab in suspension. JARQ 26, 34–40.
Van der Scheer H. A., Grabowski M. (1991). Ascosporen meestal dader van schurftinfecties in het voorjaar. Fruitteelt 16, 28–29.
Von Diest S. G., Meitz-Hopkins J. C., MacHardy W. E., Lennox C. L. (2015). Overwintering of Venturia inaequalis conidiospores in South African apple orchards. IOBC/WPRS Bull. 110, 123–124.
Washington W. S., Villalta O. N., Ingram J., Bardon D. (1998). Susceptibility of apple cultivars to apple scab and powdery mildew in Victoria, Australia. Austral. J. Exp. Agric. 38, 625–629. doi: 10.1071/EA98073
Weber A. (1934). Undersøgelser over æbleskurvens (Venturia inaequalis) overvintring. [In Danish]. Tidsskrift Planteavl 40, 754–758.
Weber A., Jorgensen H. A. (1953). Forsøg med bekæmpelse af æbleskurv efter løvfald samt undersøgelse over skurvens modningstid. [In Danish]. Beretning fra Statens Forsøgsvirksomhed i Plantekultur 469, 443–469.
Wiesmann R. (1932). Untersuchungen über die Überwinterung des Apfelschorf – Pilzes Fusicladium dendriticum (Wallr.) Fckl. im toten Blatt sowie die Ausbreitung der Sommersporen (Konidien) des Apfelschorfpilzes. Landw. Jahrb. Schweiz 46, 619–679.
Wiesmann R. (1935). Untersuchungen über die Bedeutung des Ascosporen (Wintersporen) und der Konidien an den schorfigen Trieben für die Entstehung der Primärinfektionen des Apfelschorfpilzes Fusicladium dendriticum.. Landw Jahrb. Schweiz. 49, 147–175.
Winkelmann A., Holz W., Jaenichen H. (1937). Beiträge zur Biologie und Bekämpfung des Apfelschorfes (Fusicladium dendriticum (Wallr.) Fckl.). III. Zbl. für Bakt. 96, 177–191.
Xu X., Harvey N., Roberts A., Barbara D. (2013). Population variation of apple scab (Venturia inaequalis) within mixed orchards in the UK. Europ. J. Plant Pathol. 135, 97–104. doi: 10.1007/s10658-012-0068-4
Keywords: bud scab, Malus × domestica, shoot scab, superficial scab, twig scab, wood scab
Citation: Rancāne R, Valiuškaitė A and Stensvand A (2023) Primary inoculum of Venturia inaequalis (Cooke) Wint. in its asexual form in apple – a review. Front. Hortic. 2:1175956. doi: 10.3389/fhort.2023.1175956
Received: 28 February 2023; Accepted: 27 April 2023;
Published: 18 May 2023.
Edited by:
Cheryl Lennox, Stellenbosch University, South AfricaReviewed by:
David Gadoury, Cornell University, United StatesJulia Christine Meitz-Hopkins, Stellenbosch University, South Africa
Copyright © 2023 Rancāne, Valiuškaitė and Stensvand. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Arne Stensvand, arne.stensvand@nibio.no