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Home , Apple scab, Pleosporales, Venturiaceae, Venturia inaequalis

Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182

International Journal of Current Microbiology and Applied Sciences ISSN: 2319-7706 Volume 8 Number 01 (2019) Journal homepage: http://www.ijcmas.com

Review Article https://doi.org/10.20546/ijcmas.2019.801.019

Studies on Biology and Management of Scab Incited by inaequalis

Annu1*, Rinku Rani2 and J.R. Sharma2

1Department of Plant Pathology, 2Department of Horticulture, CCS HAU, Hisar, Haryana, India

*Corresponding author

ABSTRACT

Apple ( × domestica) is an important fruit crop cultivated worldwide. Apple orchards are exposed to a diverse set of environmental and biological factors that affect the productivity and sustainability of the apple cultivation. Many of the efforts for apple production rely on reducing the incidence of fungal diseases, and one of the main diseases

K e yw or ds is caused by the (Cooke) Wint. Apple scab is the most devastating important disease of cultivated apple causing economic losses in terms of

Biology and fruit quality and yield in many apple growing areas. Apple scab attacks foliage, blossoms Management , and fruits, resulting in the defoliation of trees and making the fruits unmarketable. If the Apple scab, disease is not controlled effectively, more than 80 percent fruits of susceptible cultivars Venturia inaequalis can be damaged. Depending on the severity of disease, 10 to 15 or even more fungicidal applications are usually needed for efficient control. The uncontrolled disease may result Article Info in almost devastation of whole crop. The main strategy used for scab control is still the

Accepted: frequent application of throughout the season. However, selection pressure has 04 December 2018 lead to the evolution of -resistant strains of scab that represent a threat to the Available Online: apple industry. Therefore, all the research work in apple growing regions will be focus on 10 January 2019 identifying and creating commercial varieties with long lasting resistance characteristics and develop alternative strategies to manage apple scab. Main strategies for effectively managing apple scab includes use of resistant cultivars, tolerant rootstock, effective control of primary and secondary through use of an integrated crop management system, biological control, use of biotechnological approaches that maximizes yield and quality of apple.

Introduction 84.6 million tons (FAOSTAT, 2014). Apple is a industrial fruit and millions of people Apple (Malus x domestica Borkhausen) is an are associated with it. However like any other important fruit widely cultivated in crop species many diseases cause huge the temperate regions of the world (Harris et economic losses to the growers. Usually, al., 20002). It ranks third in terms of are consumed fresh or after storage for production with annual production of about up to 6 months or even longer. It can be also

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Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182 an important raw material for many fields of fungicides and biological disease control are processing industry like juice, sauce, slices, among the tools used to control apple scab vinegar and (Vejl et al., 2003; Folta and disease (Jonsson, 2007; Dewasish and Amal, Gardiner, 2009). Apple is attacked by several 2010). Since the late nineteenth century, apple pathogens for example fungi, bacteria, scab has been extensively investigated, and viruses, mycoplasmas and nematodes. Among substantial information covering all key fungal diseases is the main problem for aspects of the biology and genetics of the commercial apple production in temperate fungus and the epidemiology and control of and humid regions. It has been reported that the disease has been published and reviewed apple is host to over 70 infectious diseases; by Machardy (1996) and Bowen et al., most of these diseases are caused by (2011). In contrast to the efforts devoted to pathogenic fungi. They cause root rots, leaf investigating Venturia inaequalis, little work blights, leaf spots, blossom blights, fruit has been conducted on Venturia spp. affecting decay, fruit spots, canker and post-harvest other fruit trees. This difference in research decay. Among the common fungal diseases, effort and number of publications, however, apple scab is the major fungal disease in does not directly reflect the importance of the commercial apple production in temperate host crop worldwide. The difference might be and humid regions of the world (Sandskar, explained by (i) minor investments in these 2003). Apple scab is caused by Venturia non-apple crops, (ii) less specialized inaequalis (Cooke) Wint. The first report on management directed at the non-apple crops, scab was published by Fries in Sweden in and (iii) the common use of the information 1819 (Fries, 1819), but the oldest clue to the developed for Venturia inaequalis for existence of scab dates from 1600, in a managing the other fruit scabs. Concerning painting by Michelangelo Caravaggio („The the last point, researchers generally assume Supper at Emmaus‟), held at the National that infection of any scab fungus may occur Gallery, London (MacHardy et al., 2001). under environmental conditions similar to Venturia inaequalis has a wide geographical those required by Venturia inaequalis. The range and is found in almost all region in Mills and Laplante‟s (1954) table, which is which apples are grown commercially. the most popular system for scheduling However, the disease is more severe in fungicides against apple scab, has been temperate region with cool, moist climates broadly recommended for management of during early spring (MacHardy, 1996). Direct pear scab (Sobreiro and Mexia, 2000; infection of fruits and pedicels results in yield Mitcham and Elkins, 2007; Travis et al., losses. In addition, severe leaf damage can 2012; Elkins et al., 2016), cherry scab lead to a weakened tree with reduced flower (Schweizer, 1958), peach scab (Keitt, 1917; bud formation (Verma and Sharma, 1999). If Pineau et al., 1991), and loquat scab (Ramos, the apple scab is chemically controlled losses 2008). However, there is no clear evidence can be minimized, but the production costs that the environmental conditions conducive increase together with increasing health and for infection are similar for all of these ecological concerns (Patrascu et al., 2006). A Venturia species. In fact, recent studies have well-integrated approach is usually needed to revealed important differences concerning the achieve successful disease management, for environmental requirements for infection by example improve the environment and F. eriobotryae and F. oleagineum vs. selection of a suitable site for the orchard, Venturia inaequalis (Viruega et al., 2011; selection of resistant or tolerant rootstocks Gonzalez-Dominguez et al., 2013). In and grafts (scion) varieties, application of addition, substantial differences exist in the

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Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182 ecophysiologies and the life cycles of their Living tissues are infected by heterothallic hosts. Objectives of this review are: to fungus Venturia inaequalis (Jha et al., 2009). summarize the review and simplify the use of different disease control measures in an Apple scab physiological races integrated management program, and different defense mechanisms of apple to The concept of race as a fixed genetic unit is Venturia inaequalis. not valid for an obligatory sexually reproducing organism. The terminology „race‟ used for Venturia inaequalis indicate an isolate capable of infecting and sporulating on Apple scab is caused by a pathogen fungus a particular host resistant to other isolates; as including two different states: Venturia such it should be called physiological race as inaequalis, the perfect (sexual) or saprophytic in the early literature. In other words, in the state and Spilocaeapomi Fr., the imperfect case of an obligatorily sexually reproducing (asexual) or parasitic state (Jamar, 2011). pathogen like Venturia inaequalis, the word Venturia inaequalisis belongs to „race‟ indicates nothing more than the Venturia (Lepoivre, 2003). It can be classified presence or lack of virulence traits with it to the subdivision of , class respect to specific hosts on which the isolate Loculoascomyctes, order and is tested. Eight physiological races of scab are family (MacHardy, 1996). currently defined according to their virulence Spilocaeapomi Fr. is placed in the subdivision on „specific host‟ varieties as shown in table of Deuteromycota, class Hyphomycètes, order 1. The first three of these were identified by Moniliales (Lepoivre, 2003). Basically, Shay and Williams (1956) Race 1 is taken as Venturia inaequalis only infects Malus a well sporulating isolate on popular domestic species. It is a non-pathogen to all non Malus cultivars and eliciting flecks or necrotic plants. However, pathogens responsible for lesions without sporulation on Malus clones scab on Malus sp. And sp. are Dolgo, R12740- 7A and Geneva (Shay and considered as two formae speciales belonging Williams, 1956). Race 2 can sporulate on to Venturia inaequalis (Cam et al., 2002). „Dolgo,‟ „Geneva‟ and certain offspring of Yet, while the genus Malus is the main host „R12740-7A.‟ Race 3 is characterized as of Venturia inaequalis, not all Malus being able to sporulate on „Geneva,‟ genotypes are susceptible. otherwise being the same as race 1, and race 4 differs from 1 by sporulating on those Venturia inaequalis was one of the first offspring of „R12740-7A‟ that race 2 is not studied ascomycetes and remains to be a able to sporulate on. Race 5 has the ability to practical implementation for numerous sporulate on carriers of the Vm resistance and genetic studies, for example, its sexual can thus circumvent the resistance of Malus compatibility and the heritability of micromalus. Race 6 first appeared at pathogenicity. This is caused by similarity to Ahrensburg, in Germany, in the nineteen- other parasites that infect young living tissues eighties (Bus et al., 2005). It is virulent on without obvious damage for a long period as most of the varieties containing the Vf , well as its ability to be cultivated and mate in but not on clone. vitro (Vaillancourt and Hartman, 2000). Among the characteristics that make Venturia Symptoms of the disease and host range inaequalis so acceptable to genetic studies include its genotype and phenotype stability The most visible and severe symptoms of for many years and large diversity in nature. apple scab occur on leaves and fruits. It also 164

Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182 visible on sepals and petals, young shoots and are in storage. This is referred to as “pin-point bud scales (Sandskar, 2003; Daniels, 2013; scab”. The term “storage scab” refers to Turechek, 2004; Giraud et al., 2011). The incipient that were too small to see earliest symptoms of the apple scab are prior to fruit storage or may be the result of usually appearing on the underside of infections during storage that occur as a result emerging cluster leaves. However, symptoms of sporulation from older scab lesions. may first develop on the upper side of these leaves in cases where significant infection Life cycle and epidemiology of apple scab was delayed. Young lesions are velvety brown to olive green and have feathery, The ascomycete Venturia inaequalis infects indistinct margins. Lesions expand with time members of the subfamily Maloideae, and and may coalesce with other leaf lesions. The causes the disease apple scab. Venturia number of lesions can vary from very few to inaequalis is a hemibiotrophic fungus. It several hundred per leaf. Young leaves with overwinters mostly in dead fallen leaves, in significant infection often curl, shrivel and which microscopic flask-formed black fall from the tree. However, it is not atypical fruiting bodies, called pseudothecia, are for infected leaves to remain on the tree for formed. In the early spring, the the entire season. The term “sheet scab” refers inside pseudothecia start to mature and in to the condition when the entire leaf surface is suitable weather conditions, when leaves covered with the disease; when this occurs, become wet after the rain, are forcibly leaves typically shrivel and fall to the ground. ejected into the air (Sandskar, 2003; Jamar, Eventually, fungal growth stops and the 2011). The life cycle of Venturia inaequalis lesions develop distinct margins. The infected can be subdivided into two phases: primary or leaf tissue around lesions often becomes sexual phase and secondary or asexual phase thickened and lead to bulging of the infected (Figure 1). The primary phase mainly occurs area and a corresponding cupping of the area in winter and the secondary in summer underneath the leaf lesion. (MacHardy, 1996; Verma and Sharma, 1999). Primary phase/ phase Lesions on the petiole (leaf stem) extend generally creates primary infection. The along the length of the petiole and are similar fungus over winters remains as pseudothecia in appearance to those on the leaf. Severe (sexual fruiting bodies) that develop in apple infection of the petiole typically leads to a leaf litter following a short phase (maximum yellowing of the infected leaf and eventual of four weeks) of saprophytic vegetative leaf drop. On the fruit, young lesions appear growth after leaf abscission. As most similar to those on leaves. Although the entire ascomycetes, Venturia inaequalis is surface of the fruit is susceptible to infection, anisogamous: the sex organs are differentiated lesions often cluster around the calyx end of into ascogonia in the female and antheridia in the fruit (Fig. 1). As lesions get older they the male haploid parent. Also, it is become brown and corky and take on a heterothallic: plasmogamy of the two “scabby” appearance. Early infections kill the gametangia can only proceed if the expanding tissue which often results in antheridium and the ascogonium originate deformed fruit. As lesions age, they typically from parents of opposite mating type, i.e. crack and provide sites that may serve as an carry different mating type alleles on the opening to invasion by secondary pathogens. mating type (MAT) locus. The mating type is Infections late in the season are usually not the result of a complex interaction between detectable until after harvest when the fruit the gene products encoded by the different

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Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182 which are situated on MAT locus (Gisi periods. These criteria have become a et al., 2002; Billiard et al., 2011). The standard tool, in combination with electronic ascospores are produced in the asci which are weather monitoring, for identifying when in turn carried by the pseudothecium (Daniels, conditions favourable for infection occur, so 2013). The optimal temperature for the that fungicide applications can be targeted development of ascogonia and maturation of effectively. Infection risk is greatest early in the ascospores is 8-12° C and 16-18° C, the growing season when leaves and fruit are respectively (Turechek, 2004). The primary young and at their most susceptible inoculum is released by rainfall in spring developmental phase (Xu and Robinson, whithin five to nine weeks and mainly 2005). The germ tubes arising from consists of ascospores (Sandskar, 2003). The ascospores penetrate through the cuticle not sexual spores have inner and outer cell wall. through stomata via an appressorium and The outer cell wall is fragile and thin. The differentiate to form sub cuticular runner inner cell wall is elastic and thick that protects hyphae. At regular intervals, from these sub the ascospores from winter conditions (Jha et cuticular hyphae, multilayered, pseudo al., 2009). The asci also have a double cell parenchymatous structures, termed stromata, wall. The release of ascospores takes place if formed. Stromata are made up of laterally the inner and outer cell walls of the asci dividing cells and these are presumed to break. During rainfall, a thin water film is obtain nutrients from the sub cuticular space developed around the pseudothecia due to (Lepoivre, 2003; Jha et al., 2009). Secondary asci adsorb water and expand. Because of the phase/ of Venturia building pressure first the outer cell wall inaequalis starts by producing conidia, these breaks and, after some time, also the inner. conidia responsible for secondary infection. The release of ascospores is mainly takes Spilocae apomi is known as the conidial stage place during the day favoured by sunlight of the Venturia inaequalis. The conidia are (Biggs and Stensvand 2014; Rossi et al., olive/brown colored single-cells with width of 2001). The spores are spread up to 200 m 6-12μm and length of 12- 22μm. They are from the source by the wind (Turechek, produced one after the other at the tip of 2004). The primary inoculum lands on the hyphae termed as conidiophores. The conidia host plant surface (inoculation) after which an and conidiophores give a distinctive velvety infection can take place when conditions are exterior to the newly formed lesions of scab favourable. Free moisture on the leaf surface as mass produced on the thick mat of is necessary for germination. Once (Vaillancourt and Hartman, 2000). initiated, the germination will continue as Once distributed by wind and flopping rain, long as the relative humidity (RH) is more conidia land on an apple blossom or fruit and than 95% (Turechek, 2004). Spore leaves, and stick to the surface and germinate. germination does not guarantee infection. The The hyphae germination breaks through the further development of the fungus is cuticle and develops a new infection (Fig. 2). dependent on the temperature, the duration of leaf wetness and the susceptibility of the plant The conidia of Venturia inaequalis are able to itself and of the inoculated plant organ such adhere and germinate also on non-host plants. as leaves vs. sepals and petals, age of the leaf. Like in the case of ascospores, the Meteorological criteria defining the duration discharging of conidia depends on of (leaf) wetness required for infection at temperature as well as moisture and humidity, different temperatures were first proposed by and may develop from few days to a couple of (Daniels, 2013), and are known as Mills‟ weeks after initial leaf infection. The

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Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182 favourable conditions for the development of wild Malus or certain cultivated genotypes secondary infection by conidia are wet and can break down if new scab races/forms cool days in spring, summer and fall (Biggs appear (Benaouf and Parisi, 2000). „Golden and Stensvand, 2014). Many cycles of Delicious‟ is good example which was conidial production and secondary infection regarded as relatively scab resistant at the take place during particular growing period beginning of 20 century and has now become under the suitable weather conditions. Late extremely susceptible (Carisse et al., 2006). infection in autumn may not be detected. But, Therefore, disease management practices on during storage, it can affect fruits (Sandskar, scab resistant cultivars, should take into 2003). consideration the development of new strains of Venturia inaequalis that may be virulent on Control measures of the disease the cultivars resistant to only one strain of the pathogen (Parisi et al., 1993). Commonly, Host plant resistance apple cultivars differ greatly in regard to their resistance and susceptible level to scab. For Besides considerations such as fruit quality, instance, in Europe and New Zealand, over 50 productivity, ease of tree management and scab-resistant cultivars have been released commercial criteria, it is also essential use based on apple breeding programs. Redfree, varieties that are more resistant to apple scab Prima and are good examples of diseases and other pest. Therefore, now a day resistant cultivars (Table 2) (Lepoivre, 2003; there is more than 100 apple cultivars are Benaouf and Parisi, 2000; Shane, 2016) (Fig. released with reaction to Venturia. inaequalis 3). (Table 2) (Beckerman, 2006). To reduce fungicide applications, apple breeders are Resistant varieties currently introgressing disease resistance from wild Malus accessions into commercial There are a number of apple varieties that lines. The first attempts were made 100 years have high levels of resistance to apple scab ago. Genetic resistance to the apple scab disease (Carisse and Dewdney, 2002). pathogen was originally found in a crab apple, Currently, there are six major genes that 821 and therefore most of impart resistance to apple scab: Vf (Malus today‟s scab-resistant cultivars rely on a floribunda), Vr (Russian apple seedling), Vbj single introduction of scab resistance (Malus baccata Jackii), Vb (Hansen‟s from Malus floribunda 821, referred to as Vf baccata), Va (), and Vm (Malus (Gessler and Pertot, 2012). Currently cultivars micromalus susceptible to race 5). Each of with scab resistance incorporate several these genes, except for Vm, confer resistance dominant resistance genes, most of which are to all known races of the pathogen. Nearly all located at the Vf locus of the apple genome. resistant commercial varieties contain the Vf Generally, in apple scab disease management, gene. Resistant varieties include „Prima‟, resistance breeding is the most efficient and „Priscilla‟, „Macfree‟, „‟, „Liberty‟, effective method. But, this has been „Jonafree‟, and „Pioneer‟ to name a few. complicated by the presence of several races These varieties are planted primarily in or forms of the fungus, and the fact that plants organic orchards and not widely planted in resistant to one race may be susceptible to many commercial orchards. The role of another, because of the scab strains‟ ability to cultivar susceptibility has received little adapt to a specific host plant (Carisse et al., attention in disease management, particularly 2006). So, the immunity of some species of in forecasting. The original Mills curves were

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Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182 developed for the highly susceptible cultivar role against apple scab disease causing „McIntosh‟. Aldwinckle (Aldwinckle, 1974) pathogen. Cuticle is one of the outer structural ranked 51 varieties but made no attempt to defence mechanisms of plants. It is a adjust Mills‟ curves based on his findings. protective film cover the epidermis of leaves, Olivier (1984) also ranked cultivars into young shoots and other aerial plant organs susceptibility groups for the selection of an without periderm (Kolattukudy, 1996). It appropriate infection curve but does not seem consists of lipid and a three dimensional to have verified his results to confirm his hydrocarbon polymer impregnated with classification. Schwabe (1980) in South cuticular wax Beisson et al., 2012). The Africa tested commercial varieties for physical and chemical properties of cuticular differences in leaf wetness required for waxes have role in vital functions for plants infection and reported that all cultivars i.e. limits water loss, inhibits the growth and required between 3-6 hrs of wetness for development of disease causing pathogens infection but made no mention of such as bacteria and fungi (Dominguez et al., the relative susceptibility of the cultivars. In a 2011). The pathogen Venturia inaequalis 3 year study, Ellis et al., (1998) evaluated the needs certain amount of free water on surface efficacy and economics of using an inorganic of leave in order to survive and the (primarily sulfur) and conventional spray composition, the thickness and robustness of program to manage apple scab on the scab- cuticle also determine the speed with which resistant variety „Liberty‟ and the scab- the Venturia inaequalisis able to penetrate the susceptible variety „McIntosh‟ in Ohio. host plant. Generally, the properties of the During the three year period, an average of 5 cuticle and the hydrophilicity of the leaf and 9 applications of fungicide were applied change during development. This would play under the conventional program and 7 and a role in ontogenic resistance (Jha et al., 12.6 applications under the inorganic program 2009). The role of a number of PR proteins on „Liberty‟ and „McIntosh‟, respectively. has been demonstrated in apple scab defence. The reduction in the number of sprays on A comparative study by (Gau et al., 2004) „Liberty‟ was associated with the elimination between the apoplastic protein accumulation of all pre-petal fall applications which are of the Rvi6 resistant cultivar „Remo‟ and the usually targeted for apple scab. This resulted susceptible cultivar „‟ found that, the in a cost savings of 73% and 57% for the apoplast is formed by the continuum of cell inorganic and conventional, respectively, for walls of adjacent cells as well as the extra- apple scab disease management on „Liberty‟ cellular matrix. It is important for all the compared to „McIntosh‟. Despite the savings, plant‟s interaction with its environment. By apple scab resistant varieties are not widely means of two-dimensional gel electrophoresis grown as there is virtually no consumer (2-DE) and mass spectrometry, differences in demand for these varieties. concentration of a number of PR proteins between both cultivars (resistant and Structural and biochemical defence susceptible)were detected. In the susceptible mechanisms of Apple for Venturia cultivar „Elstar‟ the number of detectable inaequalis apoplastic proteins more than doubled after infection. Most of the extra proteins detected Both structural (cuticle) and biochemical had an isoelectric point between 4 and 5 (Gau (relative oxygen species, enzymes, defence et al., 2004). The concentrations of the proteins, phytoalexins, phytoanticipins, respective PR-2, PR-3 and PR-8 proteins β- hormones, etc.) defence mechanisms have 1,3-glucanase (36-40 kDa), chitinase (27-28

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Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182 kDa) and endochitinase type III (27-28 kDa) relationship to scab resistance Phenolic are higher prior to infection in cv. „Remo‟ compounds would play important role in the than in „Elstar‟. After infection by Venturia defence of apple against Venturia inaequalis. inaequalis, the concentrations in „Elstar‟ For instance, the elimination of phenyl become similar to those in „Remo‟. This alanine ammonia-lyase (PAL), a very suggests a constitutive accumulation of these important enzyme in the phenol synthesis proteins only in the resistant cultivar. Β-1, 3- signal transduction pathway, turns the glucanase, chitinase and endochitinase are resistant cv. „Sir Prize‟ susceptible (Mayr et capable to hydrolyze the fungal cell wall. The al., 1997). PAL catalyzes the first step in the chito-oligosaccharides that are formed as a phenyl propanoid pathway and is therefore result of the endochitinase activity would involved in the biosynthesis of phenolic induce defense mechanisms through a yet compounds such as phenyl propanoids, uncharacterized pathway (Paris et al., 2009). flavonoids and lignin in plants. The activity of A thaumatin-like protein (PR-5) is PAL is known to be induced dramatically in constitutively present in higher concentrations response to various stimuli, including in the apoplast of the resistant cv. Remo. In pathogenic attack (MacDonald and D‟Cunha, the susceptible „Elstar‟, the accumulation 2007). The main phenolic compounds are increases upon infection. Thaumatin (21 kDa) present in both susceptible and resistant is a sweet-tasting protein and considered a cultivars. However, the absolute amounts and prototype for a PR protein (Gau et al., 2004). relative proportions of these compounds These authors also detected osmotin like differ. Rvi6 cultivars generally have higher proteins and a PR-1 protein (15-16 kDa). A total phenol contents, as well as greater possible explanation is that this protein would amounts of particular phenolic molecules, as play a role in the recognition of the pathogen compared with susceptible cultivars, even as and the onset of the defence response. It these levels vary over the course of the season would interact with pathogen‟s effectors and (Petkovsek et al., 2009) and are influenced by induce a non-specific, systemic resistance cultural practices (Petkovsek et al., 2010). An (Blein et al., 2002). The lipid transfer protein example of a phenolic compound that is also transfers phospholipids through present in higher amounts in older leaves and membranes and would play a role in the in resistant apple cultivars is chlorogenic acid formation of the cuticle and epicuticular wax (Petkovsek et al., 2009). Not only the phenols (Diaz-Perales et al., 2002). The reduced themselves, but also their degradation accumulation of the Mald3 gene that codes products also contribute to resistance for this lipid transfer protein was confirmed development. Phlorizin for example is the by Paris et al., (Paris et al., 2009). The most prominent phenolic glycoside in apple accumulation of a number of Mald1 proteins and has an inhibitory action on Venturia of the ribonuclease type (PR-10) is increased inaequalis (Gosch et al., 2009). It is mainly after infection in HcrVf2 transformed „‟ present in the cuticle and thus would (Paris et al., 2009). Besides, the expression of influence the most critical moment in the genes that code for defencing-like proteins survival of the fungus after inoculation: the (PR-12) is also increased after infection. Plant germination and penetration in the defences would exert their antifungal activity subcuticular space. Venturia inaequalis by altering fungal membrane permeability and converts phlorizin to phloretin. This by inhibiting fungal macromolecule compound has an antifungal action as well biosynthesis (Thevissen et al., 1999). (MacHardy, 1996). Gessler et al., (2006) Phenolic compounds of apple and their concluded from the studies that it is not the

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Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182 constitutive presence of phenols that causes planting in wet, low-lying areas (Corroyer and resistance, but rather a local accumulation and Petit, 2002). Kolbe (1983) found that orchards transformation activated by an elicitor. which promote circulation of air through the Infection of apple by Venturia inaequalis also rows and between the rows by means of leads to an accumulation of flavanols in the appropriate pruning have lower levels of scab region adjacent to the scab lesions (Mayr and in the long term. Holb (2005) compared three Treutter, 1998). Malusfuran and derivatives of pruning models (intense, moderate and none) dibenzofuran are produced upon fungal attack on two very susceptible cultivars (cv. and suppress the germination and growth of and cv. ), two susceptible Venturia inaequalis (Jha et al., 2009). cultivars (cv. Elstar and cv. ) and two resistant cultivars (cv. Liberty and cv. Prima) Cultural control methods in an organic apple orchard. He concluded, notably, that intense pruning of susceptible Standard cultural and sanitary practices are cultivars results in significantly less scab on used to reduce scab infection such as leaf the leaves and fruit as compared to other two shredding, burning or burying leaves in the models. Simon et al., (2006) showed the soil, and application of 5% urea favourable effects of centrifugal as training (approximately 40 pounds urea in 100 gallons compared to conventional solaxetraining on of water) onto leaves on the floor, which help scab control, interpreting these results as to reduce the development of Venturia being due to better ventilation within the tree inaequalis (Giraud et al., 2011; Ziems, 2009). and, therefore, a microclimate which is However, these inoculum reduction practices unfavourable to scab. may be expensive and impractical for some commercial operations, and never fully Inoculum reduction eradicate all sources of primary inoculum (Sutton et al., 2000; Merwin et al., 1994). In Scab over winters mainly on dead leaves general, to prevent spread of inoculum from fallen on the ground and these are therefore crab apple trees to apple trees, crab apple the main source of the primary inoculum that trees at the edges of the apple orchard should causes contamination the following spring be removed. Regular pruning is also (MacHardy et al., 2001). The two main ways necessary for the proper sunlight penetration of discouraging the primary inoculum are (i) and air circulation in the canopy and between to reduce the mass of scabbed leaf litter and trees for the prevention of scab development. (ii) to prevent Venturia inaequalis developing Selecting sites that provide more than six in the litter that remains (MacHardy et al., hours of sunlight per day, spacing trees 2001). Several other studies have also shown adequately, and following proper pruning the effects of sanitary practices such as practices to open the tree canopy can be also burning or burying leaves in the soil (Gomez minimize or even prevented the disease et al., 2004), leaf shredding (Vincent et al., (Beckerman, 2006a). 2004; Holb et al., 2006) and a combination of shredding and using urea (Sutton et al., 2000) Pruning on reducing scab inoculum. These studies found that an ascosporic inoculum reduction To reduce apple scab, it is necessary to keep of between 40 and 95% and a correlated scab the leaves as dry as possible, in other words, reduction of 45 to 85%.Collecting leaves from to avoid planting too close together, to the ground in the inter-rows in autumn along ventilate the canopy by pruning and to avoid with burying the leaves left along the row has

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Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182 a positive effect in discouraging primary reported that a high level of potassium contamination (Gomez et al., 2004). Gomez fertilizers increased resistance of apple tree to et al., (2004) reported that for two scab but a similar effect was not obtained consecutive years the practice of „raking and with high levels of phosphorus fertilization. ridging‟ reduced the severity of scab on the fruit by 68 to 74%, depending on the year. Biological control methods Burchill et al., (1965) first showed that application of 5% urea to English orchards in Biological control is the method of the autumn completely suppressed ascospore controlling or suppressing of plant disease by production the following spring. Burchill using other microorganisms (Pal and (1968) treated Bramley‟s Seedling trees at Gardener, 2006) Several studies have two sites in Kent with a post-harvest, pre- leaf identified different antagonistic agent to fall application of 5% urea; scab lesions on manage Venturia inaequalis. Such as, blossom- spur leaves were reduced by 59% ochracea, which occurs and 46%, respectively, the following spring naturally on dead leaves and isolated, as a compared to the untreated control. Mitre et good antagonist of Venturia inaequalis when al., (2012) studied the effect of applications of applied in August and September resulting in urea 5% after harvest but before leaf-fall, as a 95 to 99% reduction in spring ascospore foliar application, in order to restrict production as compared to untreated perithecial production by Venturia inaequalis treatments (Carisse and Rolland, 2004). This in a commercial super intensive apple orchard potential biological control method is not situated near Cluj-Napoca, Romania. The solely sufficient for management of apple results found that large reductions in spore scab to commercially acceptable level. production, often as high as 70 to 80%, Therefore, cultural and potential biological following application of 5% urea. Spraying practices would have to be used in the surface of the leaves on the ground with combination with a fungicide spray program urea 5% reduced primary infection by about (MacHardy, 1996). MacHardy (1996) 60%. identified two antagonistic fungi, Athelia bombacina and Chaetomium globosum which Fertilization are potentially useful as biological control agents for Venturia inaequalis. Chaetomium Professional fruit grower requires regular globosum applied during the secondary supplement of minerals to warrant fruit set infection season could be beneficial, it and quality. Heavy nitrogen fertilization decreases the size and number of lesions, the supports tree and fruit growth ie. it is a conidial density and the conidial germ tube prominent controlling tool for yield. An germination rate and elongation. Vincent et enhanced vegetative growth of apple trees, al., (1986) observed a reduction in spring however, is often correlated with an ascospore production of about 81 and 85% increasing susceptibility to pathogens such as following autumn application of Athelia Venturia inaequalis (Leser and Treutter, bombacina and Microsphaeropsis ochracea, 2005). This may be result of the concomitant respectively. Several studies showed that decrease of phenolic compounds by high some fungi such as Auerobasidium botrytis, nitrogen uptake (Leser and Treutter, 2005), Cladosporium spp. and several epiphytic indicating that environmental conditions yeast strains from the apple tree favouring plant growth reduce investment of plyllosphereare capable to inhibit Venturia carbon for defence. Kumar and Gupta (1986) inaequalis germination and mycelial growth

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Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182 on apple tree plantlets by up to 80%. Some infection (Daniels, 2013; Beckerman, 2009). strains of Trichoderma longibrachiatum also Preventing early or initial infection of apple found antagonistic towards Venturia scab produced by ascospores is the most inaequalis, decreasing ascospore production critical step toward successful control of later from naturally infected leaves (Fiss et al., leaf and fruit infections, on which chemical 2003; Palani and Lalithakumari, 1999) The control of apple scab is concentrated. Later earthworms, Lumbricus terrestris are the fungicide sprays are targeted at other fungal main natural biological agents for removing diseases as well as against secondary dead fallen leaves from orchard floors in infection of apple scab. The strategies of winter and early spring (Holb et al., 2006). In using fungicides are formed on the base of grassed-down orchards the number and studies of apple scab epidemiology and weight of leaves buried are directly related to biology throughout the years (Alaniz et al., the weight of Lumbricus terrestris in the soil. 2014; Cova et al., 2015). In general, growers In some orchards containing between 275 and apply preventive and curative chemical 367 kg of Lumbricus terrestris per hectare, fungicides together for good efficiency that the earthworms can bury up to 184 kg of are capable of stopping fungus development leaves per hectare, which is equivalent to 90% (Vaillancourt and Hartman, 2000; Chapman of the total autumn leaf fall (MacHardy, et al., 2011). Even though, regular and well- 1996). At the same time, this is a major timed fungicide sprays have proven to be the contribution to the turnover and redistribution most commercially practical means of of organic matter in the soil. controlling scab for susceptible apple trees, but the first line of defense is to consider Chemical control method scab-resistant apples (Ziems, 2009) and at present, to reduce fungicide applications, On susceptible apple cultivars, apple scab is enhanced strategies are developed based on a primarily managed through the application of better understanding of the airborne spreading fungicides (Diaz-Perales et al., 2002). At the of ascospores, host foliage and fruit area, and end of 19th century first chemical fungicides, the host defenselessness against infection. In especially protective fungicides based on addition, repeated application of fungicide for copper against pathogen Venturia inaequalis, apple scab management result in high costs in were discovered. However, in some countries, terms of money and for the fungicide sprays the use of copper as fungicides in apple fruit and in the time dedicated to scab is totally prohibited. These constraints drive management. Because of increasing pressure growers to use large quantities of sulphur- on apple growers to reduce pesticide use and based fungicides, which may have other reduce production costs, while maintaining a drawbacks. Recently based on high level of crop quality, we believe it is epidemiological trainings, mineral fungicides crucial and timely to simplify and optimize like sulfur with less toxicity were developed apple scab management (Gessler et al., 2006). (Jamar, 2011). Farmers have to treat apple Therefore, this is indicating that researchers cultivars, which are vulnerable for scab, many or growers will focus into new strategies for times with fungicides per season (Soriano et controlling apple scab in apple production. al., 2009). Also in organic apple production, Generally, selection pressure has resulted in applications of mineral substances like sulfur, the evolution of fungicide-resistant strains of lime sulfur, and copper salts are essential for scab that represent a threat to the industry. For effective scab management to preserve the example, dodine was first released in 1959 to resistance of cultivars and to prevent initial control scab, and 10 years later resistance was

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Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182 first recorded (MFPMG, 2017; Szkolnik and methods are used in combination and more Gilpatrick, 1969). In addition, resistance of likely to be effective to managing disease as Venturia inaequalis to demethylation compared to reliance on a single technique, inhibitors fungicides was documented in such as calendar-based pesticide spraying practice (Braun 1994). Strategies to delay the (Trumble, 1998; Shumann. and D‟Arcy, development of resistance to the different 2006). IDM programs for scab control usually classes of fungicides under field conditions focus on reduction of primary inoculum, or rely on restricting the number of applications reducing fungicidal sprays using predictive per season of fungicides in each class and models. The pathogen, Venturia inaequalis mixing or alternating fungicides of different has high pathogenic variability and new races classes (Lepoivre, 2003). Therefore, the use of the pathogen are evolved frequently. of compounds or fungicides, acting via elicitation or priming for plant defense Therefore, IDM is the most effective enhancement, and the development of new, approach to minimize the yield losses due to durable scab-resistant apple cultivars will scab. Malavolta and Cross (2009) stated that, most likely gain importance in future apple IDM has made tremendous progress in terms scab management strategies. of tree nutrition, plant protection product spraying quality, restriction on post-harvest Integrated disease management Integrated treatments, soil management, selection and Disease Management (IDM) rate of application of active substances used in disease and pest control and timing of pest IDM is a multidisciplinary strategy for treatments, based on an assessment of the disease management that seeks to achieve actual risk they pose. Pruning in combination long-term effectiveness, affordability, and with fungicide use has been shown to minimal environmental disruption (Fadamiro significantly reduce leaf scab because it et al., 2003). IDM tactics include host plant improved spray deposition in the tree canopy resistance, cultural practices, biological (Holb, 2005). controls and chemical application. All these

Table.1 Physiological races of Venturia inaequalis (Bus et al., 2005; MacHardy, 1996)

Races Pathological characteristics on apple cultivars Race 1 Non sporulating lesion on Dolgo, R 12740-7A (a Russian cultivar) and Geneva Race 2 Sporulating lesions on Dolgo, Geneva and some progenies of R 12740-7A Race 3 Sporulating lesions on Geneva, and non sporulating lesion on Dolgo, R 12740- 7A Race 4 Non sporulating lesion on Dolgo, Geneva and sporulating lesion on those progenies of R12740-7A on which race 2 isolates cannot sporulate Race 5 Sporulating lesions on Vm R gene containing cultivars Race 6 Sporulating lesions on Vf hybrids but cannot infect Malus floribunda 821 containing Vfh R gene Race 7 Can infect cultivars having Vf and Vfh R gene but cannot infect which contains Vg gene Race 8 Can infect Golden delicious, Royal gala, and cultivars containing Vh8 R gene

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Table.2 List of apple cultivars reaction to apple scab

Apple Apple Apple Apple Apple Apple Apple Apple Apple Apple cultivar scab cultivar Scab cultivar Scab cultivar Scab cultivar Scab Adam’s MR Crimson VR Golden VS Jonamac S Murray R Permain Crisp Delicious R Delicious S Gold Rush VR S Mutsu VS (Red) (Crispin) VS Dayton VR Granny S Julyred VS Newtown S Smith Pippon Ashmead’s MR Early S S S NJ90 MR Kerne McIntosh S VS Grimes R Macfree R Northern S Golden Spy S Enterpris VR MR Macoun VS Nova VR e Easygrow Belmac R Florina R Honey MR McIntosh VS Novamac VR (Querina) Crisp S Freedom VR Honey R VS Nova Spy R Gold Britegold R S Idared S Milton S R

Cameo S Gala VS Jerseymac VS Moira R Pink Lady VS

Cortland VS Ginger VS Jonagold S Mollies S R Gold Delicious (Corrail) Prima VR Roxbury S Starkspur S Trent VR VS Russet Earliblaze Priscilla VR Runkel R Stark S Viking S Winter VS Splendor Banana Pristine VR Scarlet VR VS Wayne S Wolf R O‟Hara River Puritan S Silken VS Summer S S Yellow MR red Transpare nt Redfree R Sir Prize VR Suncrisp MS Wellingto S York S n Imperial R.I. S Spijon S Sundance VR William‟s VR Zestar MS Greening Pride Rome VS Stark S Beauty Bounty Abbr: Where, VR=Very Resistant; VS=Very Susceptible; R= Resistant S=Susceptible; MR=Moderately Resistant and MS=Moderately Susceptible) (Jamar, 2011; Jha et al., 2009; Ziems, 2009; Shane, 2016)

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Figure.1 (a) Apple scab lesion in the early stage of development; (b-c) secondary scab lesions on leaves; (d-e) scab lesions on fruits; and (f) pin-point scab (Gessler et al., 2006; Carisse et al., 2006)

Figure.2 Apple scab disease cycle (Cornell University, NYSAES, Geneva, NY.).

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Figure.3 Three reproductive strategies and practices for controlling each reproductive strategy (Jamar, 2011)

In conclusion, apple scab is economic inaequalis is also a prerequisite for breeding importance and if not managed, the disease program aimed at obtaining durable resistance can cause extensive losses following humid to apple scab. Further studies on ecology and cool weather conditions during the spring of Venturia inaequalis and its epidemiology months. Direct losses result from fruit are required to improve current disease infections and indirect losses from management strategies. Both innovative and defoliation, which can reduce tree vigour, conventional approaches should be used to winter hardiness, and subsequent yield. investigate the host-pathogen relationship Fungicidal control is generally considered the between Malus×domestica and Venturia sole economically feasible control measure inaequalis. Intensive research on the against apple scab disease. However, this may management of apple scab using bio-agents, change due to the high costs of new improved cultural practices and developing fungicides, increased fungicide resistance in resistance varieties should be emphasized in populations of Venturia inaequalis, and the future to enhance the overall efficacy of increasing concerns of environmental both organic and conventional apple pollution and consumers negative perceptions production. Generally, integrated disease of fungicide use. Therefore, new strategies for management (IDM), which combines development of a durable management of biological, resistance, cultural and chemical apple scab are clearly necessary. The use of control strategies in a holistic way rather than fungicides or compounds, acting via using a single component strategy proved to elicitation or priming for plant defense be more effective and sustainable for apple enhancement, and the development of new, scab disease management. Therefore, every durable scab-resistant apple cultivars will country will give a propriety on research in most likely gain importance in future apple order to: identify and create commercial scab management strategies. Knowledge of varieties with lasting resistance the biology and variability of Venturia characteristics, improve the effectiveness of 176

Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182 phyto-sanitary practices aimed at reducing the scab: Compendium of Apple and Pear inoculum and develop knowledge of the Diseases and Pests. American potential of such practices in order to reduce Phytopathological Society Press, T.B. demand for fungicides, find alternative St. Paul, MN, USA. fungicides to sulfur and copper, refine Billiard S., Lopez-Villaviciencio M., Devier strategies and protection schemes, optimize B., Hood M.E. and Fairhead C. (2011) treatment timing, improve plant protection Having sex, yes, but with whom? product application techniques and develop Inferences from fungi on the evolution specific cultural practices that are less of anisogamy and mating types. Biol favourable to the development of the disease. Rev Camb Philos Soc., 86: 421-442. Blein J., Coutos-Thevenot P., Marion D. and References Ponchet M. (2002) From elicitins to lipid-transfer proteins: a new insight in Alaniz S., Leoni C., Bentancur O. and cell signaling involved in plant Mondino P. (2014) Elimination of defence mechanisms. Trends Plant summer fungicide sprays for apple Sci., 7: 293-296. scab (Venturia inaequalis) Bowen J., Mesarich C., Bus V., Beresford R. management in Uruguay. Sci Hortic., and Plummer K. (2011) Venturia 165: 331-335. inaequalis: the causal agent of apple Aldwinckle H.S. (1974) Field susceptibility of scab. Mol Plant Pathol., 12: 105-122. 51 apple cultivars to apple scab and Braun P.G. (1994) Development and decline apple . Plant Disease of a population of Venturia inaequalis Reporter, 58: 625-629. resistant to sterol-inhibiting Beckerman J. (2006) Disease Susceptibility of fungicides. Norweg J Agric Sci., 17: Common Apple Cultivars, Fruit 173- 184. Diseases. Perdue Extension, Perdue Burchill R.T. (1968) Field and laboratory University, USA. studies of the effect of urea on Beckerman J. (2006a) Apple Scab on Tree ascospore production of Venturia Fruit in the Home Orchard: Fruit inaequalis (Cke.) Wint. Ann Appl Diseases. Perdue Extension, Perdue Biol., 62: 297–307. University, USA. Burchill R.T., Hutton K.E., Crosse J.E. and Beckerman J. (2009) Managing Scab- Garrett C.M. (1965) The inhibition of Resistant Apples, Disease the perfect stage of Venturia Management Strategies for inaequalis (Cooke) Wint. by urea. Horticultural Crops. Perdue Extension, Nature, 205: 520 Perdue University, USA. Bus V. G. M., Laurens F. N. D. and van de Beisson K.F., Li-Beisson Y. and Pollard M. Weg W. E. (2005) The Vh8 locus of a (2012) Solving the puzzles of cutin new gene-for- gene interaction and suberin polymer biosynthesis. between Venturia inaequalis and the Curr Opin Plant Biol., 15: 329-337. wild apple is closely Benaouf G. and Parisi L. (2000) Genetics of linked to the Vh2locus in Malus the host-pathogen relationship pumila R12740-7A. New Phytol., 166: between Venturia inaequalis races 6 1035–1049. and 7 and Malus species. Cam B.L., Parisi L. and Arene L (2002) Phytopathology, 90: 236-242. Evidence of two formae speciales in Biggs A.R. and Stensvand A. (2014) Apple Venturia inaequalis, responsible for

177

Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182

apple and pyracantha. Phytopathology, belonging to the lipid-transfer protein 92: 314-320. family. Clin Exp Allergy, 32: 87-92. Carisse O, Jobin T, McFadden-Smith W, Dominguez E., Heredia-Guerrero J.A. and Meloche C, Lasnier J (2006) Apple Heredia A. (2011) The biophysical Scab: Improving Understanding for design of plant cuticles: an overview. Better Management. Agriculture and New Phytol., 189: 938-949. Agri- Food Canada, Canada. Elkins B., Gubler W.D. and Adaskaveg J.E. Carisse O. and Dewdney M. (2002) A review (2016) UC IPM Pest Management of non-fungicidal approaches for the Guidelines: Pear. UC ANR control of apple scab. Phytoprotection, Publication, 3455. 83: 1-29. Ellis M.A., Ferree D.C., Funt, R.C. and Carisse O. and Rolland D. (2004) Effect of Madden L.V. (1998) Effect of an timing of application of the biological apple scab-resistant cultivar on use control agent Microsphaeropsis patterns of inorganic and organic ochracea on the production and fungicides and economics of disease ejection pattern of ascospores by control. Plant Dis., 82: 428-433. Venturia inaequalis. Phytopathology. Fadamiro H., Ciborowski J. and Hock H. 94: 1305-1314. (2003) Integrated pest management Chapman K.S., Sundin G.W. and Beckerman manual for Minnesota apple orchards. J.L. (2011) Identification of resistance A scouting and management guide for to multiple fungicides in field key apple pests. Minnesota populations of Venturia inaequalis. Department of Agriculture. St. Paul. Plant Dis., 95: 921-926. FAOSTAT (2014) FAO statistics division. Corroyer N. and Petit J.L. (2002) Le Fiss M., Barckhausen O., Gherbawy Y., pommier. pp. 230-261. In Produire des Kollar A. and Hamamoto M. (2003) fruits enAgriculture Biologique. Characterization of epiphytic yeasts of ITAB. 253 p. apple as potential biocontrol agents Cova V., Bandara N., Liang W., Tartarini S. against apple scab (Venturia and Patocchi A. (2015) Fine mapping inaequalis). J Plant Dis Prot., 110: of the Rvi5 (Vm) apple scab resistance 513-523. locus in the „Murray‟ apple genotype. Folta K.M. and Gardiner S.E. (2009) Plant Mol Breed., 35: 200. genetics and genomics: Genetics and Daniels B (2013) Response of apple (Malus × genomics of . (6th edtn), domestica) to Venturia inaequalis, the Springer Science Business Media, causal agent of apple scab: a real-time New York, USA. PCR and proteomics study. PhD Fries E. (1819) Spilocacea pomi, Fr Nov Fl thesis. Catholic University of Leuven, Suec 5: 79. Belgium, 199p. Gau A., Koutb M., Piotrowski M. and Dewasish C. and Amal M. (2010) Fruit crops. Kloppstech K. (2004) Accumulation (3rd edtn), Oxford book company of pathogenesis-related proteins in the publisher, Jaipur, India. apoplast of susceptible cultivar of Diaz-Perales A., Garcia-Cassado G., Sanchez- apple (Malus domestica cv. Elstar) Monge R., Garcia-Selles F. and after infection by Venturia inaequalis Barber D. (2002) cDNA cloning and and constitutive expression of PR heterologous expression of the major genes in the cultivar Remo. Eur J allergens from peach and apple Plant Pathol., 110: 703-711.

178

Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182

Gessler C. and Pertot I. (2012) Vf scab Plant Dis., 89: 611-618. resistance of Malus. Trees, 26: 95- Holb I.J., Heijne B. and Jeder M. (2006) 108. Effects of integrated control measures Gessler C., Patocchi A., Sansavini S., on earthworms, leaf litter and Venturia Tartarini S. and Gianfranceschi L. inaequalis infection in two European (2006) Venturia inaequalis Resistance apple orchards. Agric. Ecosyst. in Apple. Crit Rev Plant Sci., 25: 473- Environ., 114: 287-295. 503. Jamar L (2011) Innovative strategies for the Giraud D.D., Elkins R.B. and Gubler W.D. control of apple scab (Venturia (2011) Apple and Pear Scab. Plant inaequalis [Cke.] Wint.) in organic Pathology. University of California. apple production. PhD thesis, Statewide Integrated Pest University of Liege-Gembloux Agro- Management. Program Agriculture Bio Tech, Belgium. and Natural Resources. Jha G., Thakur K. and Thakur P (2009) The Gisi U., Sierotzki H., Cook A. and McCaffery Venturia apple pathosystem: A. (2002) Mechanisms influencing the pathogenicity mechanisms and plant evolution of resistance to Qo inhibitor defense responses. J Biomed fungicides. Pest Manag Sci., 58: 859- Biotechnol., 28: 1-10. 867. Jonsson A. (2007) Organic apple production Gomez C., Brun L., Chauffour D., De Le in Sweden, cultivation and cultivars. Valee D. and Dumont E. (2004) Effet PhD thesis, Swedish University of de la reduction de l‟inoculum Agricultural Sciences, Sweden. d‟automne sur le développement des Keitt G. (1917) Peach scab and its control. épidémies de tavelureen verger de Bull. Dep. Agric. U.S.A. 395: 1–64. pommiers biologiques. Dans: Journées Kolattukudy P.E. (1996) Biosynthetic techniques fruits et legumes pathways of cutin and waxes, and their biologiques. Saint- Pierre-des- Corps, sensitivity to environmental stresses: les 30 nov. & 1er déc. 2004: pp 45-52, Plant Cuticles an integrated functional ITAB. approach. BIOS Scientific publishers Gonzalez-Dominguez E., Rossi V., Ltd., Oxford, pp. 83-108. Armengol, J. and Garcia-Jimenez J. Kolbe W. (1983) Effects of different pruning (2013) Effect of environmental factors systems and chemical retardants on mycelial growth and conidial compared with no pruning on apple germination of trees on yield fruit quality and disease eriobotryae and the infection of loquat incidence in the long term trial at leaves. Plant Dis., 97: 1331–1338. Hofchen (1959-1982). Erwersobstbau, Gosch C., Halbwirth H., Kuhn J., Miosic S. 25: 246-255. and Stich K. (2009) Biosynthesis of Kumar J. and Gupta G.K. (1986) Influence of phloridzin in apple (Malus domestica host response and climatic factors on Borkh.). Plant Sci., 176: 223-231. the development of conidial stage of Harris S.A., Robinson J.P. and Juniper B.E. apple scab fungus (Venturia (2002) Genetic clues to the origin of inaequalis). Indian J Mycol Plant the apple. Trends in Genetics, 18(8): Patho., l16: 123- 135. 426-430. Lepoivre P (2003) Phytopathologie. De Boek Holb I.J. (2005) Effect of pruning on apple University. Bruxelles. 427p. scab in organic apple production. Leser C. and Treutter D. (2005) Effects of

179

Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182

nitrogen supply on growth, contents of Mitre V., Mitre L., Adriana F., Petrisor C. and phenolic compounds and pathogen Sestras R. (2012) Reducing primary (scab) resistance of apple trees. inoculum of apple scab using foliar Physiologia Plantarum, 123: 49-56 application of urea in autumn. Bulletin MacDonald M.J. and D‟Cunha G.B. (2007) A of the University of Agricultural modern view of phenylalanine Sciences & Veterinary, 69: 415-420. ammonia lyase. Biochem Cell Biol., Olivier J.M. (1984) Evolution de la lutte 85: 273-282. contre la tavelure du pommier. La MacHardy W. (1996) Apple Scab Biology, Défense des Végétaux, 225: 22-35. Epidemiology and Management. Pal K.K. and Gardener B.M. (2006) American Phytopathological Society Biological Control of Plant Pathogens. Press, St. Paul, MN. The Plant Health Instructor. MacHardy W., Gadoury D. and Gessler C. Palani P.V. and Lalithakumari D. (1999) (2001) Parasitic and Biological Fitness Antagonism of Trichoderma of Venturia inaequalis: Relationship longibrachiatum strains to fungicide to Disease Management Strategies. sensitive and resistant strains of Plant Dis, 85: 1036-1051. Venturia inaequalis. J Plant Dis Prot., Malavolta C. and Cross J.V. (2009) Technical 106: 581-589. Guideline III: IOBC. WPRS Bulletin. Paris R., Cova V., Pagliarani G., Tartarini S. (4th edtn), 47, 21p. and Komjanc M. (2009) Expression Mayr U. and Treutter D. (1998) Flavanols as profiling in HcrVf2-transformed apple defence barriers in apple leaves plants in response to Venturia against the apple scab fungus inaequalis. Tree Genet Genomes, 5: (Venturia inaequalis). Acta Hortic., 81-91. 466: 79-82. Parisi L., Lespinasse Y., Guillaumes J. and Mayr U., Michalek S., Treutter D. and Feucht Kruger J. (1993) A new race of W. (1997) Phenolic compounds of Venturia inaequalis virulent to apples apple and their relationship to scab with resistance due to the Vf gene. resistance. J Phytopathol., 145: 69-75. Phytopathology, 83: 533-537 Merwin I.A., Brown S.K., Rosenberger D.A., Patrascu B., Pamfil D., Sestras R., Botez C. Cooley D.R. and Berkett L.P. (1994) and Gaboreanu I. (2006) Marker Scab resistant apples for the assisted selection for response attack Nort1heastern United States: new of Venturia inaequalis in different prospects and old problems. Plant apple genotype. Not Bot Horti Dis., 78:4-10. Agrobot Cluj Napoca, 34: 121-133. MFPMG. Midwest Fruit Pest Management Petkovsek M.M., Slatnar A., Stampar F. and Guide (2017) Perdue Extension, Veberic R (2010) The influence of Perdue University, USA. organic/integrated production on the Mills W.D. and LaPlante A.A. (1954) Apple content of phenolic compounds in scab: Disease and insects in the apple leaves and fruits in four orchard. Cornell Extension Bulletin, different varieties over a 2-year 711: 20-28. period. J Sci Food Agric., 90: 2366- Mitcham E. and Elkins R. (2007) Pear 2378. Production and Handling Manual. Petkovsek M.M., Stampar F. and Veberic R. California, CA: University of (2009) Seasonal changes in phenolic California Publications. compounds in the leaves of scab-

180

Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182

resistant and susceptible apple Phytopathology, 46: 190-193. cultivars. Can J Plant Sci., 89: 745- Shumann G.L. and D‟Arcy C.J. (2006) 753. Essential Plant Pathology. American Pineau R., Raymondaud H. and Schiavon M. Phytopathological Society Press. St. (1991) Elaboration d‟un modèle de Paul, Minnesota USA. prévision des risques d‟infection du Simon S., Lauri P. E., Brun L., Defrance,H. mirabellier (Prunus domestica L var and Sauphanor B. (2006) Does insititia) parl‟ agent delatavelure manipulation of fruit tree architecture (Cladosporium carpophilum Thumen). affect the development of pests and Agron. EDP Sci., 11: 561–570. pathogens? A case study in an organic Ramos N. (2008) Relatório de Aplicação de apple orchard. J. Hortic. Sci. Modelos de Previsão de Ocorrencia de Biotechnol., 81: 765-773. Inimigosdas Culturas. Casodo Modelo Sobreiro J. and Mexia A. (2000) The Paraa Cochonilhade S.José– simulation of pear scab (Venturia Resultados preliminares. Algarve pirina) infection periods and (Portugal): Direcção Regional de epidemics under field conditions. Acta Agricultura e Pescas do Algarve, Hortic., 525: 153–160. Patacão. Julho. Soriano J., Joshi S., van Kaauwen M., Rossi V., Ponti I., Marinelli M., Giosue S. and Noordijk Y. and Groenwold R. (2009) Bugiani R. (2001) Environmental Identification and mapping of the factors influencing the dispersal of novel apple scab resistance gene Vd3. Venturia inaequalis ascospore in Tree Genet Genomes, 5: 475-482 orchards air. J Phytopathol., 149: 11- Sutton D.K., MacHardy W.E. and Lord W.G. 19. (2000) Effects of shredding or treating Sandskar B. (2003) Apple Scab (Venturia apple leaf litter with urea on ascospore inaequalis) and Pests in Organic dose of Venturia inaequalis and Orchards. PhD Thesis, Swedish disease build up. Plant Dis., 84:1319- University of Agricultural Sciences, 1326. Alnarp, 39. Szkolnik M. and Gilpatrick J.D. (1969) Schwabe W.F.S. (1980) Wetting and Apparent resistance of Venturia temperature requirements for apple inaequalis to dodine in New York leaf infection by Venturia inaequalis apple orchards. Plant Dis Reports, 53: in South Africa. Phytophylactica, 12: 861-864. 69-80. Thevissen K., Terras F. and Broekaert W. Schweizer H. (1958) Contributions to the (1999) Permeabilization of fungal biology of the pathogen of cherry and membranes by plant defensins inhibits peach scab (Fusicladium cerasi fungal growth. Appl Environ (Rabh.) Sacc. Venturia cerasi Ad. and Microbiol., 65: 5451-5458. Cladosporium carpophilum v. Thum). Travis J.W., Rytter J. and Yoder K. (2012) J. Phytopathol., 33: 55–98. Pear Scab (Venturia pirina). Extension Shane B (2016) Apple Varieties with Service, West Virginia University. Significant Scab Resistance, Michigan Trumble J.T. (1998) IPM: overcoming State University Extension. conflicts in adoption. Integra Pest Shay J.R. and Williams E.B. (1956) Manage Rev., 3: 195-207. Identification of three physiologic Turechek W.W. (2004) Apple diseases and races of Venturia inaequalis. their management: Diseases of fruits

181

Int.J.Curr.Microbiol.App.Sci (2019) 8(1): 162-182

and vegetables. Diagnosis and 604 management. (1st edtn), Kluwer Viruega J. R., Roca L. F., Moral J. and Academic Publishers, Dordrecht. Trapero A. (2011) Factors affecting Vaillancourt L. and Hartman J. (2000) Apple infection and disease development on scab. The Plant Health Instructor olive leaves inoculated with Vejl P., Skupinoval S., Blazek J., Sedlak P. Fusicladium oleagineum. Plant Dis., and Bardova M. (2003) PCR markers 95: 1139–1146. of apple resistance to scab (Venturia Xu X.M. and Robinson J. (2005) Modelling inaequalis CKE.) controlled by Vf the effects of wetness duration and gene in Czech apple breeding. Plant fruit maturity on infection of apple Soil Environ, 49: 427-432. fruits of Cox‟s Orange Pippin and two Verma L.R. and Sharma R.C. (1999) Diseases clones of Gala by Venturia inaequalis. of horticultural crops: fruits. Indus Plant Pathol., 54:347-356. Publishing Company, New Delhi. Ziems A.D. (2009) Apple scab: Plant disease. Vincent C., Rancourt B. and Carisse O. Lincoln Extension, Institute of (2004) Apple leaf shredding as a non- Agriculture and Natural Resources, chemical tool to manage apple scab University of Nebraska, USA. and spotted tentiform leaf miner. Agric. Ecosyst. Environ., 104: 595-

How to cite this article:

Annu, Rinku Rani and Sharma, J.R. 2019. Studies on Biology and Management of Apple Scab Incited by Venturia inaequalis. Int.J.Curr.Microbiol.App.Sci. 8(01): 162-182. doi: https://doi.org/10.20546/ijcmas.2019.801.019

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