Apples - Chap 18 21/3/03 3:03 pm Page 459

18 Diseases of

Gary G. Grove1, Kenneth C. Eastwell1, Alan L. Jones2 and Turner B. Sutton3 1Irrigated Agriculture Research and Extension Center, Washington State University, Prosser, Washington, USA; 2Department of Botany and Plant Pathology, Michigan State University, East Lansing, Michigan, USA; 3Department of Plant Pathology, North Carolina State University, Raleigh, North Carolina, USA

18.1 Introduction 460 18.2 Diseases Caused by Bacteria 460 18.2.1 Fire blight 460 18.3 Diseases Caused by Fungi 468 18.3.1 468 18.3.2 Powdery mildew 470 18.3.3 Brown-rot diseases 472 18.3.4 Summer diseases 473 18.3.5 crown and root rot 476 18.3.6 European or Nectria canker 477 18.4 Postharvest Diseases 477 18.4.1 Blue mould 478 18.5 Diseases Caused by Viruses, Viroids, Phytoplasmas and Other Virus-like Agents 478 18.5.1 Chlorotic leaf spot 479 18.5.2 Apple decline (on ‘Virginia Crab’) 480 18.5.3 Flat apple 480 18.5.4 Apple mosaic 481 18.5.5 Stem pitting 481 18.5.6 Union necrosis 481 18.6 Diseases Caused by Phytoplasmas 482 18.6.1 Proliferation 482 18.6.2 Chat fruit 482 18.7 Diseases of Apple Caused by Viroids 482 18.7.1 Blister bark 482 18.7.2 Dapple apple 483 18.7.3 Dimple fruit 483 18.7.4 Fruit crinkle 483 18.8 ’Virus-like’ or Graft-transmissible Diseases of Apple with No Known Causal Agents 483 18.8.1 Green crinkle 484 18.8.2 Rubbery wood 484 18.8.3 Dead spur 485 18.9 Control Measures 485

© CAB International 2003. : Botany, Production and Uses (eds D.C. Ferree and I.J. Warrington) 459 Apples - Chap 18 21/3/03 3:03 pm Page 460

460 G.G. Grove et al.

18.1 Introduction Blister bark has been described from South Africa but the pathogen P. s. pv. syringae van Apples are host to over 70 infectious dis- Hall is found as a common epiphyte on eases, the vast majority of which are caused apple foliage worldwide. Crown gall and by pathogenic fungi (Table 18.1). Apples are hairy root are soil-borne diseases caused by also susceptible to diseases caused by bac- two species of Agrobacterium; crown gall is teria, phytoplasma and virus/virus-like the most common of the two problems. agents. The authors discuss several but not In areas where these bacterial pathogens all economically important pre- and posthar- either are not established or are rare, bacter- vest apple diseases in this chapter. Readers ial diseases are often avoided by planting should keep in mind that some of the dis- pathogen-free nursery stock. Where these eases discussed might be in some diseases are established, they are managed areas and minor in others. Others (e.g. fire through orchard sanitation, wound mini- blight) are of importance or potential impor- mization, the use of resistant rootstocks and tance wherever apples are grown. In most cultivars, site selection, cultural practices apple-producing regions, disease control is a that promote air movement and drying of major annual expense for the grower. For plant surfaces and, in some cases, the use of example, in the eastern USA, the manage- copper and antibiotic sprays. ment of apple scab can require eight to ten protective fungicide applications annually. In those areas, the apple grower must manage 18.2.1 Fire blight early-season diseases, such as apple scab and cedar apple rust, as well as a group of dis- Fire blight is of major concern in all countries eases termed ‘summer diseases’. Conversely, where apples are grown including countries in the arid production regions of the Pacific that are currently free of this disease Northwest, these diseases are non-existent or (Vanneste, 2000). When fire blight is epi- sporadic in nature and powdery mildew is demic, it can cause serious tree loss in nurs- much more problematic. eries and orchards (Plate 18.1), even leading Successful disease management usually to orchard removal. In high-risk areas, fire results from the integration of several meth- blight is limiting the planting of some highly ods of disease control. The use of resistant susceptible apple cultivars and rootstocks. rootstocks and scions, fungicides, bacteri- Strict quarantines and restrictions are main- cides, biological control agents, environmen- tained in countries where the disease does tal modification and site selection are some not currently occur; enforcing quarantine of the means used to control apple diseases. regulations and restrictions and, if necessary, The precise combination and order of control eradicating the disease are very costly. measures are usually disease-specific. The fire blight pathogen kills fruit-bear- ing spurs, branches and entire trees. Infected blossoms are initially water-soaked and 18.2 Diseases Caused by Bacteria darker green; spurs with infected blossoms (Table 18.2) turn brown to dark brown and collapse after 4–5 days. Infected shoots turn brown to Fire blight, blister spot, blister bark, crown black from the tip and bend near the tip to gall and hairy root are diseases of apple resemble a shepherd’s crook (Plate 18.2). caused by bacteria. Fire blight is the most When shoots are invaded from the base, the important of these diseases and is described basal leaves and stem turn brown to black. in more detail below. Blister spot, caused by Leaves may exhibit discoloration of the Pseudomonas syringae pv. papulans (Rose) midrib, followed shortly by a darkening of Dhanvantari, occurs in North America and the lateral veins and surrounding tissues. Europe. It causes a fruit spot on Bark on infected branches and scaffold ‘’/‘Crispin’, ‘’, ‘Redcort’, ‘Sun limbs is darker than normal. When the outer Crisp’, ‘Smoothee’ and a few other cultivars. bark is peeled away, the inner tissues are Apples - Chap 18 21/3/03 3:03 pm Page 461

Diseases of Apple 461 Continued ms and damage Main control method b wood Borkh.) A.L. Jones, primary collator (last update 3/12/93). Borkh.) domestica Conidia in pycnidia, Spots on leaves and fruit, Sanitation, fungicides Conidia in pycnidia; Cankers on wood, decay Fungicides Conidia/conidiophores Leaf spots, defoliation Fungicides, (Penz.) Berg. Conidia/conidiophores Spots on fruit and leaves Fungicides (Peck) ascospores in apothecia of fruit (P) De Not. (syn. (Fr.) Pouzar (Fr.) Conidia in a sclerotia-like Cankers on branches Removal of infected branches J.H. Simmons (Schwein.) Tul. & C. Tul. (Schwein.) stroma, ascospores in Berk. [anamorph] ascospores in pseudothecia defoliation, cankers on (Schwein.) Shoemaker Nose) ascospores in pseudothecia of fruit (Stoneman) Spauld. Conidia in acervuli; Decay of fruit Fungicides, sanitation (H. Jacks.) Nannf Conidia in acervuli; Cankers on wood, decay Fungicides (Pers.:Fr.) Grev. Grev. (Pers.:Fr.) (Cooke) G. Wint. Ascospores in pseudothecia; Leaf spots, scabs on fruit, resistant fungicides, Sanitation, (Fr.:Fr.) Keissl(Fr.:Fr.) Conidia/conidiophores Decay of fruit None (G. Wint.) Honey Conidia in sporodochia; Decay of fruit (P) preharvest injury to fruit Avoid Fr.:Fr. [anamorph]Fr.:Fr. conidia/conidiophores defoliation cultivars (Vahl:Fr.) P. Kumm. P. (Vahl:Fr.) Basidiospores in basidiocarps Decay of roots None, avoid problem sites Roberts; = Fromme Ascospores in perithecia Decay of roots None (Fr.:Fr) Kessl apple pathotype (Fr.:Fr) cultivar selection Nummularia discreta Colletotrichum gloeosporioides Cryptosporiopsis curvispora Spilocaea pomi Sphaeropsis malorum Biscogniauxia marginata perithecia Tul. Helminthosporium papulosum Xylaria mali Xylaria polymorpha Botryosphaeria obtusa & H. Schrenk Penz. & Sacc. in [anamorph] Colletotrichum acutatum ascospores in perithecia Armillaria mellea Glomerella cingulata Pezicula malicorticis [anamorph] inaequalis Venturia Botryosphaeria berengeriana Physalospora piricola alternata Alternaria alternata Monilinia fructicola ) Fungal pathogen Reproductive stage Common symptoms a Fungal diseases of apples, names the asexual and sexual stages causal fungi their reproductive stages, sympto blotch (A, rot (W) (shoestring) ; W) (AF, E, NA, SA, O) (AF, leaf spot and canker Blister canker (nail- head canker) (NA) = Black pox (NA) Black root rot (NA for X. mali Black rot, frog-eye Armillaria root rot (W) Bitter rot (W) (mushrooms); rhizomorphs (A, AF, NA,O)AF, (A, Anthracnose canker rot (E, and bull’s-eye NA, O) Apple scab (W) Apple ring rot and Gremmen in Boerema & ascospores in apothecia canker (A) Table 18.1. Table most likely to be encountered and general methods of control. ( Disease (distribution Alternaria NA) AF, Alternaria American brown rot Apples - Chap 18 21/3/03 3:03 pm Page 462

462 G.G. Grove et al. Main control method fungicides b spots, blisters in bark spur dieback and ß spores) in Cankers on 1- and Sanitation Basidiospores in basidiocarps Decay of roots None often in the same stroma branches et al (Penz.) et al. Shear E. Mason spots on fruit Shoemaker Pycnidia and pseudothecia; Cankers on branches Pruning out of infected (Lév.) Bres. (Lév.) basidiospores in culture (Lib.) de Bary Ascospores in apothecium Decay of fruit None C. Brooks ascospores in pseudothecia calyx end (Scop.) Bres. (Pass.) Lindau Conidia/conidiophores; Spots on fruit, often at Fungicides Kobayashi & Sakuma pycnidia; ascospores in 2-year-old shoots (Stoneman) Spauld. & Conidia in acervuli; Spots on leaves, Fungicides (Scop.) Dennis Ellis & Everh. Conidia in pycnidia Blotches on fruit, leaf Fungicides (Mont.:Fr.) Arx (Mont.:Fr.) Conidia in pycnidia Small, superficial, dark Cultural practices, fungicides Honey in Whetzel Conidia in sporodochia; Blossoms and spur Sanitation, fungicides Weresub & Illman Weresub Basidiomycete, may produce Decay of fruit (P) None Pers.:Fr. [anamorph]Pers.:Fr. ascospores in apothecia blight, decay of injured Kobayashi & Sakuma Conidia ( (Fr.: Fr.) Mont. [anamorph] Fr.) (Fr.: (Aderh. & Ruhl.) Honey Conidia in sporodochia Blighting of blossoms, Fungicides (Aderhold & Ruhland) fruit Link spp. Conidia/conidiophores Decay of fruit (P) Packing-house sanitation, Clitocybe tabescens Physalospora malorum Diplodia mutila Cylindrosporium pomi Phomopsis tanakae Monilia fructigena Zygophiala jamaicensis Colletotrichum gloeosporioides Phyllosticta solitaria Penicillium expansum P. Mycosphaerella pomi [anamorph] Monilinia laxa Sclerotinia sclerotiorum Armillaria tabescens = [anamorph] perithecia Diaporthe tanakae Monilinia laxa Honey Butlerelfia eustacei = Corticium centrifugum Schizothyrium pomi [anamorph] Glomerella cingulata Botryosphaeria stevensii Penz. & Sacc. in [anamorph] Monilinia fructigena ) Fungal pathogen Reproductive stage Common symptoms a Continued. leaf spot canker (A) root rot (NA) canker (E, Clitocybe Table 18.1. Table Disease (distribution Blotch (NA) Blue mould (W) Brooks fruit spot (NA) Brown-rot blossom E, NA, AF, blight (A, SA) Calyx-end rot (NA) Diplodia Diaporthe Fish-eye rot (A, E, NA) Fly-speck (W) (A, E, AF) (A, E, Glomerella (NA, SA) H. Schrenk ascospores in perithecia defoliation NA, O) = European brown rot Apples - Chap 18 21/3/03 3:03 pm Page 463

Diseases of Apple 463 Continued Sanitation and chemical control spp. around the fruit core (Berk. & ascospores in perithecia occasional fruit decay spp. spp. (Fuckel) Sacc. spp.; Conidia of various types Discoloration and decay Packing-house sanitation (Nitschke) Hohn. (Pers.) Rabenh. (Fuckel) Barr Leaves (Ellis & J.J. Davis) conidia in acervuli spots on surface of fruit Fr. [anamorph] Fr. (de Bary) Whetzel nature) of fruit; nest rot fruit in fungicides Sacc. [anamorph] (Nattras et al.) H.J. Tode:Fr. [anamorph]Tode:Fr. ascospores in perithecia and trunk (Ellis & Everh.) Sacc. small twigs Penicillium Ulocladium (Tode:Fr.) Fr. Fr. (Tode:Fr.) Conidia on sporodochia; Cankers on branches branches Removal of affected (Fr.:Fr.) Hohn. (Fr.:Fr.) Perithecial stroma with a Cankers on branches branches Removal of affected (Cooke & Ellis) Sutton Cankers in wounds on None Sacc. [anamorph] central pycnidium Nitschke Bres. in Strass. Conidia on phialides; Cankers on branches, Fungicides Harada & Sawamura Ascospores in apothecia; Leaf spots, defoliation, Sanitation, fungicides Coniothyrium Pers. Fr. Pers. Fr. Conidia and sclerotia (rare in Decay often at calyx end Packing-house sanitation and Stemphylium spp.; (Takahashi) Whetzel (Takahashi) Ascospores in apothecia; Blossom and spur blight, E. Fischer zygospores fruit (P) spp.; spp.; spp. [anamorph] conidia with disjunctors decay of young fruit spp. Sporangiospores and Soft, watery decay of Packing-house sanitation Pleospora herbarum Leucostoma auerswaldii Leptosphaeria coniothyrium Monochaetia mali Lepteutypa cupressi Coniothyrium fuckelii Cytospora personata Cylindrocarpon heteronemum vulgaris Tubercularia Cytospora cincta Marssonina coronaria Botryotinia fuckeliana Monilia Cladosporium Epicoccum Swart [teleomorph] Mucor M. piriformis Nectria galligena [anamorph] Broome) Wollenweb. Nectria cinnabarina J.J. Davis [anamorph] Alternaria Leucostoma cincta auerswaldii Valsa = Diplocarpon mali and Diapleella coniothyrium wet core rot, mainly Botrytis cinerea Seiridium unicorne Monilinia mali canker twig canker blotch (A, canker (A, AF, AF, canker (A, twig blight leaf blight (A) rot (AF, NA, rot (AF, rot (W) Mucor O) Nectria NA, SA, O) Nectria = coral spot (E, O, NA) and dieback (E, NA) Mouldy core and Leucostoma Marssonina NA, E) blossom-end rotLeptosphaeria and fruit rot (W) [teleomorph] = storage (P) = dry-eye rot, Grey-mould rot (W) Monochaetia canker (NA) = Monilia Apples - Chap 18 21/3/03 3:03 pm Page 464

464 G.G. Grove et al. or postharvest treatments Main control method b LeavesSpots on leaves, Removal of alternative host, Removal of alternative host, and ß spores) in Cankers on wood, fruit None Pycnia and aecidia on apple; on cedar Pycnia and aecidia on apple; on cedar of fruit Duggar (Farl.) Farl. (Zeller & ascospores in apothecia decay of fruit (Duggar) Hyphae with conidia on Decay of roots None Corda storage (Ellis & Everh.) Conidia/conidiophore; Powdery spots on leaves, Cultivar selection, fungicides . R. Hartig pycnidia on synnemata (Lebert & Cohn) See above Rotting of fruit Late-season fungicide sprays (Kleb.) Kleb. (Pers.:Fr.) Link(Pers.:Fr.) Conidia Decay of fruit (P) Prevented by refrigerated cold Em. Marchal pycnidia, ascospores in decay (P) Kienholz Conidia in acervuli; Cankers on branches, Sanitation, fungicides G.H. Cunn. Basidiomycete with crust-like Infected roots with Resistant rootstocks and Prill. Ascospores in perithecia; Decay of roots Cultural practices, solarization Drechs Roberts Conidia ( (Petr.) Buisman(Petr.) germinating oospores or Pethybr. & Lafferty & Lafferty Pethybr. chlamydospores spp. Zoospores produced in Decay of crown and root Cultural practices, host (Lebert & Cohn) J. Schröt. sporangia from hyphae or tissues resistance, chemical treatment (Kleb.) Kleb. Cephalothecium roseum Phymatotrichum omnivorum Dematophora necatrix Diaporthe perniciosa Cryptosporiopsis perennans P. cactorum P. cambivora P. cryptogea P. megasperma P. syringae P. [anamorph] Gymnosporangium globosum Gymnosporangium juniperi-virginianae Schwein telentospores in telial horns defoliation and distortion fungicides Phymatotrichopsis omnivora Phytophthora syringae roseum Trichothecium = Podosphaera leucotricha E.S. Salmon Rosellinia necatrix ascospores in cleistothecia fruit russeting Childs) Wollenweb. [anamorph] Childs) Wollenweb. Phomopsis mali Phytophthora Phytophthora cactorum Peniophora sacrata Neofabrae perennans ) Fungal pathogen Reproductive stage Common symptoms a root root rot crown, fruit rot Continued. root canker canker, fruit canker, root rot (W) Dematophora Rust, American hawthorne (NA)Rust, cedar apple (NA) telentospores in telial horns fungicides = decay and rough bark (A, E, NA)Phymatotrichum [teleomorph]Pink mould rot (W) Powdery mildew (W) perithecia Rosellinia Phomopsis rot = cotton root rot (NA) = (sprinkler rot) (W) Hennebert (E, NA) J. Schröt.; conidiophores and sclerotia Phytophthora collar and root rot; Phytophthora (O) fruiting-bodies characteristic crackssanitation Peniophora (O) fruiting-bodiesPerennial canker (NA) characteristic Table 18.1. Table Disease (distribution Apples - Chap 18 21/3/03 3:03 pm Page 465

Diseases of Apple 465 fungicides America; W, worldwide. America; W, on the surface of fruit fungicides Root decay Soil sterilization Juniperus chinensis Libocedrus decurrens telentospores in telia on cedar Basidiospores decay Wood Cultural practices conidia Basidiospores in basidiocarps et al. Miyabe ex Pycnia and aecidia on apple; Leaves Removal of alternate host, (C.Henn.) F. (C.Henn.) F. Aecidia on apple; (Cooke & Peck) Pycnia and aecidia on apple; Distortion of fruit Removal of alternative host, (Pers.:Fr.) Pouzar (Pers.:Fr.) Noack (Fr.) Donk (Fr.) Basidia on a resupinate Decay of roots None (Moug.) Ces. & De Conidia in pycnidia; Decay of fruit, cankers Fungicides and sanitation M. Cline Tanaka Tanaka (Fr.) Burt (Fr.) hymenium Cooke basidia with basidiospores (Hino) Redhead Ascospores in apothecia; Leaf spot, defoliation Sanitation (M.N. Kidd & A. (M.N. Kidd & Conidia at the apex of Decay of fruit (P) Cultural practices, postharvest (Schwein.) Gvritischvili stroma (Schwein.) Colby) (Tode:Fr.) Maire (Tode:Fr.) Pycnidia and perithecia in a Cankers on branches Sanitation Corda [anamorph] Leptodontium Burt Rhizomorphs and sclerotia; Blighting of branches Fungicides (Johnson, Sutton, Conidia in pycnidia Blotches of various size Cultural practices and Sacc. Sclerotia Decay at base of trunk Cultural practices (Curzi) Tu & Kimbrough Tu (Curzi) Geastrumia polystigmatis (G. Mangenot) (De Hoog); and Pellicularia koleroga Hypochnus ochroleucus Corticium galactinum Athelia rolfsii Cytospora sacculus Grovesinia pyramidalis Gymnosporangium yamadae Gymnosporangium libocedri Gymnosporangium clavipes Cooke & Peck in Phialophora malorum Beaumont) McColloch Chondrostereum purpureum Peltaster fructicola Batista & M.L. Farr; elatius Gloeodes pomigena Sclerotium rolfsii phialides[teleomorph] Corticium stevensii treatments Valsa ceratosperma Valsa [anamorph] Helicobasidium mompa [teleomorph] Cristulariella moricola Scytinostroma galactinum = Botryosphaeria dothidea Fusicoccum aesculi leaf blight = canker(A) Hypochnus Approximate geographical distribution of the disease: A, Asia; AF, Africa; E, Europe; NA, North America; O, Oceania; SA, South Africa; E, Europe; NA, North AF, Asia; A, Approximate geographical distribution of the disease: postharvest disease problem. P, Rust, Japanese apple (A) pear (NA) Yamada Kern (W) Hodges); telentospores in telia on telentospores in telia on fungicides a b Rust, Pacific Coast Rust, quince (NA) Side rot (E, NA) Silver leaf (W) Sooty-blotch complex Southern blight (AF, NA, SA) Thread blight = (NA) = Valsa root rot (O) Violet Zonate leaf spot (A) White root rot (NA) NA, White rot (AF, SA, O) Not. ascospores in pseudothecia on limbs and twigs Apples - Chap 18 21/3/03 3:03 pm Page 466

466 G.G. Grove et al.

Table 18.2. Bacterial diseases of apple, scientific name of the pathogen, symptoms and main control method.

Disease Common (distributiona) Pathogen symptoms Main control method

Fire blight (E, NA, Erwinia amylovora Blight, cankers, Resistant cultivars and New Zealand) dead trees rootstocks, sanitation, antibiotics Blister spot (E, NA) Pseudomonas syringae pv. Spots on fruit Avoiding susceptible papulans (Rose) Dhanvantari cultivars, antibiotics Blister bark (AF) Pseudomonas syringae pv. Terminal dieback, None syringae van Hall blossom blight, Crown gall (W) Agrobacterium tumefaciens Galls on roots Sanitation, biocontrol but (E.F. Smith & Townsend) Conn often less effective than on Prunus species Hairy root (W) Agrobacterium rhizogenes Excessive production Sanitation (Riker et al.) Conn of fibrous roots

aApproximate geographical distribution of the pathogen: A, Africa; E, Europe; NA, North America, W, worldwide.

water-soaked with reddish streaks when and LB media (see Bereswill et al., 1998, for first invaded; later the tissues are brown. As the composition of these media), patho- lesion expansion slows, the bark sometimes genicity tests performed on immature fruit, cracks, delineating a canker. Infected fruit seedlings or vigorous plants, and molecular develop a brown-to-black decay. During assays (Bereswill et al., 1995; McManus and wet, humid weather, droplets of whitish to Jones, 1995). reddish-brown, sticky liquid (known as The pathogen overwinters in cankers ooze) seeps from the surface of infected tis- located on branches and tree trunks (Fig. sues (Plate 18.3). Infected rootstocks may 18.1). Ooze can begin to appear on the sur- show bleeding or ooze from rootstock tissue face of these cankers at or just before the early in summer and internal necrosis of the onset of bloom. Bacteria are disseminated to bark and the leaves of the scion turn reddish flowers by splashing rain and, occasionally, early in the autumn. flies and other insects that visit both bacterial Fire blight is caused by Erwinia amylovora ooze and blossoms. Eventually, honey bees (Burrill) Winslow et al., a Gram-negative, visit infected blossoms and pick up pollen or rod-shaped, non-fluorescent bacterium with nectar contaminated with bacteria. Spread of peritrichous flagella. More than 130 species bacteria from flower to flower by bees is in 39 genera of the Rosaceae are hosts. rapid. Bacteria colonize the stigmatic surface Important hosts include apple, pear, orna- of the pistils of healthy apple and pear flow- mental Pyrus and Malus species, quince ers, resulting in epiphytic populations of (Cydonia oblonga), loquat (Eriobotrya japon- bacteria (Thomson, 1986). Climatic condi- ica), hawthorn (Crataegus spp.), Cotoneaster tions govern the rate of spread and severity spp., Sorbus spp., Pyracantha spp. and Rubus of blossom blight and even the infection spp. Most strains of E. amylovora from Rubus process itself. Temperatures between 18.3 do not infect apple and are therefore consid- and 30°C (accompanied by rain or high ered to be pathologically distinct. Primary humidity during the day) favour infection. isolation of the bacteria is by culturing on Although bacteria invade the flowers pri- Luria–Bertani (LB) agar or some semi-selec- marily through natural openings, storms tive medium. They are distinguished from containing wind-driven rain or hail are other plant pathogenic bacteria based on important in spreading bacteria during the colony colour and morphology on MM2Cu summer months, which under some condi- Apples - Chap 18 21/3/03 3:03 pm Page 467

Diseases of Apple 467

Fig. 18.1. The fire blight disease cycle. The pathogen overwinters in cankers. At the onset of bloom, bacteria begin to ooze on to the surface of cankers; splashing rain, along with flies and other insects, moves the bacteria to open flowers. Then, honey bees spread the bacteria from flower to flower on contaminated pollen and nectar. The bacteria multiply on the stigmatic surface of the pistils to produce high epiphytic populations. Favourable combinations of moisture and temperature govern infection of the flowers. Summer storms with wind-driven rain spread the bacteria, leading to sudden and severe outbreaks of diseases. Inoculum for secondary infection originates from droplets of ooze produced on infected flowers, fruit and shoots. (Figure courtesy A.L. Jones.)

tions lead to sudden and severe outbreaks of to prevent the importation of plant material disease. Inoculum for secondary infection that may harbour the pathogen. originates from droplets of ooze produced In countries where fire blight is a prob- on infected flowers, fruits and shoots. lem, sanitation – the removal of infected por- Temperature, as measured by the accumu- tions of the tree – is critical to the success of lation of degree-days (DD), governs the rate other control measures and is effective pro- of symptom development. Symptoms are vided it is done during the early stages of an expressed when 55 DD (base 12.5°C) are epidemic. New orchards should be planted accumulated following the infection date. on blight-resistant rootstocks if available. A The susceptible rootstocks M.9 and M.26 are realistic plan for controlling fire blight is infected by systemic movement of bacteria needed before making large plantings of through symptomless scion tissue or through blight-susceptible cultivars. Antibiotics have infected rootstock shoots (Momol et al., 1998). been highly effective for preventing the blos- Although the rootstock Bud.9 is blight-sus- som-blight stage of fire blight, but in some ceptible, rootstock blight has not developed regions or orchards control with antibiotics is on many Bud.9/scion combinations. Losses no longer possible, due to the development from rootstock blight can be avoided by of streptomycin-resistant strains of E. using resistant rootstocks, such as G.16, G.30, amylovora. Predictive models, particularly G.65 and other blight-resistant rootstocks Maryblyt and Cougarblight in the USA and from the US Department of Agriculture– Billings’ integrated system and Firescreens in Agricultural Research Service (USDA- Europe, help growers identify potential ARS)/Cornell apple-rootstock programme. infection periods (Billings, 2000). Such infor- Many practices help to prevent or reduce mation is helpful in timing antibiotic treat- the severity of fire blight. In countries where ment and for avoiding unnecessary E. amylovora is not established, only trees pro- treatment. Bacterial antagonists that sup- duced in fire-blight-free regions should be press fire blight may be integrated with used when establishing new orchards. These antibiotics to control flower infections countries may already have strict quarantines (Stockwell et al., 1996). Apples - Chap 18 21/3/03 3:03 pm Page 468

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18.3 Diseases Caused by Fungi symptoms are found on both sides of leaves. Conidia are produced abundantly in new Within this diverse group of plant pathogens lesions; therefore, lesions appear as velvety are the causes of most apple diseases (Table brown to olive spots that turn black with age 18.1). Fungi pathogenic to apple can cause (Plate 18.4). Severe infection can cause leaves root rots, leaf spots, leaf blights, blossom to abscise, resulting in defoliated trees. Return blights, fruit decay, fruit spots, defoliation bloom on trees defoliated in midsummer is and trunk, branch and twig cankers. The often reduced due to a lack of flower-bud for- fungal diseases discussed in this chapter are mation the previous summer. Fruit infections caused by fungi belonging to the general tax- resemble leaf infections when young but turn onomic groups represented by the mush- brown and corky with age (Plate 18.5). Early- rooms (Basidiomycetes) and morels season infections are often associated with the (Ascomycetes). The phylum Oomycota also blossom end of the fruit; later they can occur contains the water moulds, an important anywhere on the surface. Scab infections group of plant pathogens formerly classified result in uneven growth of fruit and even as fungi. Fungi in the ascomycete group cracking of the skin and flesh. Rough, black have scientific names for the anamorph and circular lesions develop in cold storage on teleomorph. The anamorph is the asexual fruit infected close to harvest. The latter phase form (also called the imperfect stage) of the is known as pinpoint scab. Infection of blos- and produces asexual spores (such as soms and bud scales may be observed in conidia) or no asexual spores. The teleo- high-inoculum orchards when infection peri- morph is the sexual form (also called the per- ods occur at critical times. Lesions on blos- fect or sexual state) and produces sexual soms and bud scales resemble those on leaves spores (ascospores) in various fruiting bodies but are seldom observed because these tissues (pseudothecia, perithecia, apothecia, etc.). normally drop to the ground before the symp- These fungi generally reproduce by spores toms are well developed. that are dispersed by air currents or splash- Venturia inaequalis (Cooke) G. Wint., ing water. Fungal diseases are prevented or anamorph Spilocea pome Fr., causes apple managed by using resistant cultivars and scab. It has one sexual cycle and a series of rootstocks, site selection, sanitation, cultural asexual cycles per year. Flask-shaped, ascus- practices and fungicide practices. Specific bearing fruiting bodies (pseudothecia) management measures vary according to develop in overwintering infected leaves. disease and geographical location. Pseudothecia form as a result of the interac- tion of two strains of opposite mating types (heterothallic fungus). Asci in pseudothecia 18.3.1 Apple scab are eight-spored. Mature ascospores are two- celled, with the upper cell shorter and wider Scab occurs in virtually all apple-producing than the lower cell, yellowish green to tan regions worldwide (MacHardy, 1996). The and with smooth walls. Conidia are one- disease is an annual threat in cool, humid celled, yellowish-olive and pointed. regions with frequent rainfall in spring and From late autumn to spring, microscopic, early summer. In semiarid regions, scab is a black, pimple-like pseudothecia develop in threat in years with above-normal rainfall or leaves on the orchard floor (Fig. 18.2). in orchards where artificial wetting periods Normally, pseudothecia contain mature are created from the improper use of over- ascospores when the blossom buds start to head irrigation. open in spring. Maturation and discharge of Scab attacks the leaves and fruit through- ascospores lasts about 5–9 weeks. When out most of the growing season; blossoms and leaves on the orchard floor become wet from bud scales are attacked for short periods in rain, spores are ejected into the air. Air cur- spring and late summer, respectively. rents carry them to the emerging tissues, Symptoms first appear on the undersides of where infection occurs. Young leaves and fruit leaves, the side exposed as buds open. Later, are highly susceptible to infection, but their Apples - Chap 18 21/3/03 3:03 pm Page 469

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Fig. 18.2. The apple scab disease cycle. The fungus Venturia inaequalis overwinters in leaves on the orchard floor and sometimes in apple buds. Pseudothecia with ascospore-bearing asci in dead leaves discharge their ascospores when the leaves become wet from rain. Ascospores produce the first, or primary, infections on the young fruit and leaves. Conidia produced on the inner surface of apple-bud scales can also cause primary infections. Depending on temperature, 9–17 days are required before new scab lesions appear on the infected tissues. Conidia, formed in continual crops of new lesions, produce secondary infections. Secondary cycles are repeated many times until leaf fall in autumn. (Figure courtesy A.L. Jones.)

susceptibility declines with maturity. Spore but fails to develop until after the fruit has germination begins soon after ascospores been held in cold storage for several months. land on wet leaves or fruit. Prevailing temper- Infections can also build up in leaves after atures govern the infection rate, provided a harvest and prior to normal leaf abscission. continuous film of moisture is present for ger- The fungus overwinters in these leaves and mination of the spores. Depending on the they are often the source of very high levels average temperature after penetration, 9–17 of inoculum the following spring. days are required before the appearance of Basic studies on the biology and epidemi- the olive-green, velvety scab lesions. In some ology of apple scab from the 1920s to the apple-producing regions and on some culti- 1940s established a rational basis for scab vars, the fungus also overwinters in lesions control and these concepts continue to be on twigs and bud scales (Becker et al., 1992); refined. The initial ascosporic inoculum is conidia produced in these lesions are a second usually present in large amounts; therefore, form of primary inoculum. However, the estimating the risk of the initial ascosporic number of conidia available from overwinter- inoculum and forecasts of its efficiency are ing lesions at bud break is low compared with very important for determining when to ini- the number of ascospores potentially avail- tiate scab-control programmes and the able from leaf litter. application frequency. Inoculum risk is Secondary infections are initiated by coni- determined by monitoring pseudothecia dia produced in primary and secondary from early spring to midsummer to deter- lesions. Conidia can be produced in new mine whether ascospores are mature and lesions beginning as soon as 7–9 days after available for discharge and by detecting infection and these lesions can produce coni- ascospore release in orchards during wetting dia in continuous crops for several weeks. periods. Statistical models have been devel- Conidial germination and infection occur oped to predict ascospore maturity based under about the same conditions as germina- on DD accumulations and these models tion and infection by ascospores. Secondary are replacing ascospore-monitoring pro- infection on fruit can occur in the autumn grammes. Inoculum risk forecasts assume Apples - Chap 18 21/3/03 3:03 pm Page 470

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high inoculum levels, an assumption that is fungal antagonists to the foliage just prior to usually incorrect for orchards where scab leaf fall (Carisse et al., 2000), but this strategy was well controlled the previous season. alone is not adequate for season-long scab Therefore, methods for assessing differences control. This approach may be more feasible in inoculum among orchards based on a in areas with lower amounts of overwinter- potential ascospore density (PAD) system ing inoculum and mild winters. were developed (Gadoury and MacHardy, Scab is controlled primarily with fungi- 1986). It was found that in low-inoculum cides applied in predetermined schedules, orchards spray programmes in spring could beginning at green tip. The fungicides are be delayed until about the tight-cluster stage applied on a 7–14-day interval with eight to of bud development, rather than green tip in ten applications per season. Several classes the normal spray schedule for high-inocu- of fungicides are available for apple-scab lum orchards. Integrating inoculum risk control. They are often rotated during the with environmental risk is accomplished by season or applied as mixtures because of the the identification of ‘infection periods’. high potential of the scab fungus to develop Rainfall is necessary for the discharge of fungicide-resistant strains. ascospores – free water for the germination of ascospores and penetration of tissues. The rate of this infection process is temperature- 18.3.2 Powdery mildew dependent, and the duration of wetness required for successful infection across a Powdery mildew is circumglobal and a wide range of temperatures is well known potentially serious disease wherever apples (Jones, 1998). Therefore, temperature and are grown. The disease is particularly prob- wetness measurement can be used to fore- lematic in the western and mid-Atlantic cast the success or failure of each ascospore- regions of the USA. Severe infections reduce discharge event. These events can be tree photosynthesis and transpiration (Ellis monitored with environmental sensors et al., 1981) and may result in partial defoli- linked to small computers placed in the ation (Ogawa and English, 1991). Chronic orchard or with automated weather stations infections can result in reduced tree vigour, connected directly to computers. Fungicides poor return bloom and yield reduction. with post-infection efficacy are applied after Fruit infection can result in the rejection of predicted but unprotected infection periods. fruit for fresh-market sale. Apple cultivars Apple-breeding programmes aiming for vary in their susceptibility to powdery high-quality, disease-resistant cultivars are in mildew. ‘’, ‘’, ‘’, progress in New Zealand and some ‘Mutsu’ (Crispin), ‘’, ‘’, European and North American countries. ‘Monroe’, ‘’, ‘’, ‘’, Over 50 scab-resistant cultivars have been ‘’, ‘Ginger Gold’, ‘Rome released and are gaining in commercial Beauty’, ‘’ and ‘Pink Lady®’ are acceptance as fruit quality and other horti- particularly susceptible. ‘Delicious’ and cultural characteristics are improved. ‘’ are less susceptible. Guarding against races of the scab pathogen Leaves, flowers and fruit are susceptible that can overcome the resistance sources to infection by the powdery mildew fungus. used by apple breeders is a high priority in The foliage of new terminal growth is these breeding programmes (Bénaouf and extremely susceptible to infection. The ini- Parisi, 2000). tial signs of powdery mildew consist of Prevention of pseudothecia formation in white to grey felt-like patches on the lower overwintering leaves would probably elimi- leaf surface. These patches are comprised of nate scab. Unfortunately, complete elimina- masses of fungal mycelia and spores (coni- tion of pseudothecia is not possible under dia). As disease progresses, mildew signs orchard conditions using current methods. may also appear on the upper leaf surface Spring ascospore production can be reduced and eventually cover the entire leaf. Infected by making autumn applications of urea or foliage may curl, blister and eventually Apples - Chap 18 21/3/03 3:03 pm Page 471

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become brittle and necrotic (Plate 18.6). are therefore primary inocula, which initiate Internodal shortening may occur on additional new infections. This cycle of severely infected shoots. Infected flower sporulation and foliar infection can continue petals are distorted, stunted and light yel- as long as susceptible foliage is being pro- low to light green. Fruit infection typically duced. This secondary phase of powdery results in stunting accompanied by the pres- mildew can cycle many times during the ence of a fine network of rough lines (russet- growing season. Temperature is the most ing) (Plate 18.7). important factor affecting disease develop- Powdery mildew is caused by Podosphaera ment. Conidia germinate at temperature leucotricha (Ell. & Ev.) E.S. Salmon. The fun- between 10 and 25ºC; the optimum tempera- gus is superficial on the host surface but tures for germination are 20–22ºC. The sex- withdraws water and nutrients from host tis- ual stage (ascocarps) of P. leucotricha sue, using a structure called a haustorium. occasionally forms on infected twigs. The fungus produces barrel-shaped conidia Ascocarps are minute, brown to black, spher- in chains, which are dispersed by air cur- ical fruiting bodies that contain eight unicel- rents and initiate subsequent infections of lular ascospores. Various researchers have foliage and fruit (Fig. 18.3). P. leucotricha suggested that this stage is insignificant in survives through winter as mycelium in the epidemiology of the disease. Fruits are infected buds. This mode of perennation especially susceptible to infection during the results in the production of ‘flag shoots’ bloom period (Daines et al., 1984). (shoots covered with powdery mildew) Powdery-mildew epidemics are favoured when shoots emerge in the spring. Winter by high humidity; therefore problems with temperatures are the most important factor mildew can often be avoided or reduced affecting the amount of carry-over inoculum. with cultural practices that promote air Temperatures colder than 12ºC kill the fun- movement and light penetration. On suscep- gal mycelium in buds; temperatures lower tible cultivars, effective disease management than 24ºC may kill the infected buds usually depends on a fungicide-spray pro- (Spotts et al., 1981). Conidia produced on flag gramme. Benzimidazole, sulphur, horticul- shoots initiate the first spring infections and tural mineral, oils, demethylation-inhibiting

Fig. 18.3. The apple powdery mildew disease cycle. The fungus overwinters as mycelium in infected buds. Mildew conidia, produced on leaves arising from the infected buds, become wind-borne and cause primary infections on healthy leaves and fruit. Secondary infections are produced from conidia produced in both primary and other secondary infections and are repeated until shoot growth stops in late summer. (Figure courtesy A.L. Jones.) Apples - Chap 18 21/3/03 3:03 pm Page 472

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(DMI) and strobilurin fungicides are effec- pathogen present. M. laxa causes blossom tive against powdery mildew. Spray pro- blight, spur dieback and cankering of grammes should commence at tight cluster branches; M. fructigena causes fruit rot and and continue until the production of new sometimes cankers when the fungus foliage ceases. Because powdery mildews spreads into branches from the fruit; and can develop resistance to benzimidazole, M. fructicola causes a fruit rot. Monilia leaf DMI and strobilurin fungicides, rational blight infects young apple leaves; resistance-management strategies usually mycelium invading from leaves kills flower require the inclusion of two or more fungi- clusters, young fruits and fruiting spurs. cide classes in a season-long programme. The species of Monilinia can be differenti- DMI fungicides applied in apple-scab-man- ated by microscopic observation of conidia agement programmes generally provide the formed in chains in culture or on infected tis- added benefit of mildew control. sue. M. mali can be differentiated by disjunc- A predictive system has been developed tors present within the conidial chains. M. for aid in managing infections caused by P. fructicola, M. fructigena and M. laxa can be leucotricha. Podem© (Xu, 1999) is a system differentiated based on cultural characteris- developed in the UK that simulates epi- tics, isozyme variation, vegetative interac- demics of secondary mildew on vegetative tions and PCR assays. shoots. The effects of weather on conidial The life cycles of these pathogens differ production, dispersal and germination are only in the role that the perfect stage used to calculate a favourability index. The (apothecia) plays in the overwintering of the model itself is driven by hourly ambient fungi. M. mali and occasionally M. fructicola temperature, relative humidity, shade tem- produce apothecia on mummified fruit on perature and the total daily duration of rain- the ground. All species overwinter in fall. The model has been incorporated into infected parts of the tree. Secondary spread an integrated apple disease warning system is by conidia produced on infected host tis- (ADEM) and successfully used to time sue within the tree and on trees of neigh- fungicide applications and in some cases has bouring hosts, particularly Prunus species. resulted in improved disease control, with a Losses due to fruit decay caused by M. 40% reduction in fungicide usage (Berrie fructigena and M. fructicola increase gradu- and Xu, 1999). ally up to harvest time and are usually asso- ciated with injuries to the fruit. Cultivars prone to fruit cracking, such as ‘Cox’s 18.3.3 Brown-rot diseases Orange Pippin’ and ‘’, are especially susceptible to infection. Infection Several brown-rot fungi attack apple in dif- also occurs through wounds caused by ferent parts of the world. The species and birds pecking at fruit, insects infesting fruit their distribution are: Monilinia fructicola and hail. Fruit decay is prevented by avoid- (Wint.) Honey in most regions except ing cultivars prone to fruit cracking, by lim- Europe, where it is a European Union-listed iting the damage caused by birds and other quarantine pest (Smith et al., 1992); Monilinia wounding agents and by orchard sanitation laxa (Aderh. & Ruhl.) Honey in Asia, Europe, methods aimed at reducing the build-up of North and South America and South Africa; inoculum. and Monilinia fructigena (Aderh. & Ruhl.) Blossom infections from M. laxa, M. fructi- Honey in Europe and Asia (Byrde and gena and Monilia leaf blight are controlled by Willetts, 1977). A related species, Monilinia orchard sanitation, combined with the appli- mali (Takahashi) Whetzel, causes Monilia leaf cation of fungicides. Blighted spurs and blight of apple in Asia. cankers are removed and destroyed during The brown-rot fungi cause blossom wilt, the dormant period and in the growing sea- spur dieback, cankering and fruit rot (Plate son. Fungicides applied as the flowers begin 18.8); the incidence and severity of these to open and one or two times 5–7 days later symptoms depend on the species of should prevent blossom blight. Apples - Chap 18 21/3/03 3:03 pm Page 473

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18.3.4 Summer diseases has enormous potential for secondary spread and is very difficult to control when the Summer diseases refer to a collection of nine weather is warm and wet. diseases that tend to be most severe from 2–3 G. cingulata also survives from year to weeks after petal fall until harvest. They are year on dead wood and mummified apples. most prevalent in warm and moist growing There appear to be several strains, which regions of the world, where they can cause produce somewhat different symptoms. A extensive losses if not controlled. They are serious leaf-spot disease, Glomerella leaf spot, relatively minor problems in arid and cooler occurs on ‘Gala’ in Brazil, which is associ- growing regions. ated with G. cingulata (Sutton and Sanhueza, Of all the summer diseases, rot diseases 1998). It causes small irregular lesions are most destructive and can cause losses of 3–12 mm in diameter on leaves and can 50% or more if not controlled. These diseases result in significant defoliation when severe. tend to be most severe in the south-eastern It also causes small corky lesions on fruit. USA but cause problems in other areas as This strain overwinters in leaves on the well. The life cycles of the pathogens that orchard floor, much like apple scab, and cause these diseases are similar, as is the infection is initiated in the late spring by air- overall strategy for managing them. borne ascospores, which are discharged dur- ing periods of rain. Perennation also occurs in twig cankers and mummified apples. 18.3.4.1 Bitter rot Glomerella leaf spot has been observed in the Bitter rot is the most destructive of the three south-eastern USA (Gonzalez and Sutton, rot diseases and is the most difficult of the 1999). Another strain of G. cingulata produces three to control once an epidemic has begun. a large, firm, brown lesion on the fruit, It is caused by Colletotrichum gloeosporioides which is not sunken, and few spores are pro- (Penz.) & Sacc. in Penz. and Colletotrichum duced on the surface of the lesion (Shane acutatum J.H. Simmons. These pathogens and Sutton, 1981b). It is not known whether coexist in many orchards, whereas in others this strain causes a leaf-spot symptom. one or the other species predominates. Management of bitter rot is based on sani- Glomerella cingulata (Stoneman) Spauld & H. tation and a preventive spray programme. In Shrenk is often listed as the sexual stage of C. warm, rainy, growing regions, the disease gloeosporioides but may be a distinct taxon cannot be successfully managed without (Shane and Sutton, 1981a; TeBeest et al., 1997). pruning to remove inoculum sources and The Colletotrichum spp. that cause bitter facilitate drying in the tree canopy. Current- rot survive from one growing season to season fire blight strikes need to be removed another in mummified apples, twig cankers because they can be colonized by the bitter- and other dead wood in the tree. In the late rot fungi and serve as an inoculum source spring when temperatures begin to warm, late in the season. The ethylenebisdithiocar- conidia are released, initiating infections on bamate (EBDC) fungicides are most effective, fruit. Fruit is susceptible throughout the sea- but restrictions on their application after son (Shane and Sutton, 1981b; Noe and petal fall in the USA have limited their use- Starkey, 1982). Lesions begin as small, circu- fulness. Captan, ziram and thiram (applied lar, light tan to brown spots, sometimes sur- on a 10–14-day schedule from petal fall to rounded by a red halo. As the lesions enlarge, harvest) are the most effective fungicides they become brown and sunken (Plate 18.9) currently registered in the USA. The benzim- and extend into the flesh of the apple in a V- idazole fungicides are ineffective. shaped pattern, which is a good diagnostic technique. Fruiting structures on the surface 18.3.4.2. Black rot and bot (white) rot of the lesion, called aecidia, produce copious amounts of salmon-coloured conidia, which Black rot and bot rot are caused by can be splash-dispersed to other fruit, initiat- Botryosphaeria obtusa (Schwein.) Shoemaker ing new infections. Consequently, the disease and Botryosphaeria dothidea (Moug.) Ces. & Apples - Chap 18 21/3/03 3:03 pm Page 474

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DeNot., respectively. Although caused by the and mushy (Plate 18.11). Under cooler tem- same fungal genus, the diseases caused by peratures, the rot tends to be darker in the two species are different in many ways. colour and firmer, making it more difficult Both overwinter in dead wood, mummified to separate from black rot. Infected fruit apples and cankers in the tree canopy and may fall or may remain attached to the tree produce ascospores and conidia through and mummify. most of the growing season. Both cause a Control of the black rot and bot rot is fruit rot and cankers, but only B. obtusa based on sanitation and preventive fungicide causes a leaf spot. Infections by B. obtusa can sprays. Colonized dead wood and mummi- begin as early as silver tip and occur fied apples can both serve as inoculum throughout the season, whereas infections by sources. Wood infected by the fire blight B. dothidea occur mainly during the warm pathogen can become colonized by these summer months. B. obtusa infections develop fungi and produce spores during the current into firm brown lesions on the fruit and growing season. This wood should be B. dothidea infections develop into light removed during the early summer. Prunings brown, soft, watery rots. should be chopped by a flail mower or B. obtusa infections can occur on the sepals pushed out of the orchard and burned. as soon as the buds begin to open. These Fungicides should be applied every 10–14 infections spread into the fruit as they begin days from petal fall to harvest. Captan and to mature, resulting in a firm brown rot on the benzimidazole fungicides are most effec- the calyx end (Plate 18.10). Other fruit infec- tive; the dithiocarbamate fungicides are not tions can occur from soon after petal fall until especially efficacious. harvest during favourable weather (Arauz and Sutton, 1989). Infections that occur soon 18.3.4.3 Sooty blotch and fly-speck after petal fall first appear as small, dark pim- ples. As lesions enlarge, they become dark Sooty blotch and fly-speck are two of the and irregular in shape and are often sur- most common diseases in humid growing rounded by a red halo. Eventually the entire areas. While they do not reduce yield, fruit may become rotten and shrivel, remain- affected fruit are usually downgraded from ing attached to the tree. Leaf spots (known as fresh-market to processing or juice grades. frog-eye leaf spot) begin as small purple to Sooty blotch is a disease complex caused by brown necrotic lesions, which enlarge to several fungi and is characterized by dusty 4–5 mm in diameter and are often sur- to dark colonies of fungi growing epiphyti- rounded by a purple halo. When infections cally on the surface of the fruit (Williamson are numerous, leaves may turn yellow and and Sutton, 2000; Plate 18.12). They range abscise. from small discreet colonies to large, amor- B. dothidea infections can occur from soon phous ones. Each colony has a characteristic after petal fall until harvest (Parker and appearance, depending on the fungus Sutton, 1993). Infections that occur early in involved. Fly-speck colonies are character- the season often remain quiescent and do ized by numerous thyrothecia, which are not begin developing until the soluble scattered throughout the thallus, giving it an solids in the fruit begin increasing. This appearance of ‘fly-specks’ (Plate 18.13). often leads growers to think that their late- Colonies range from several to many mil- season spray programme is ineffective, limetres in diameter. when in actuality the disease increase that Sooty blotch is a disease complex caused they are observing is more closely related to by Peltaster fructicola Johnson, Sutton & their spray programme earlier in the season. Hodges, Leptodontium elatius (G. Mangenot) As lesions begin to develop on the fruit, De Hoog, Geastrumia polystigmatis Batista & they extend in a cylindrical manner towards M.L. Farr and probably other fungi. These the core. Once the core is invaded, the entire fungi grow superficially on the cuticle of apple becomes infected. Rotten fruit are affected fruit. All have numerous reservoir often light tan in colour and are very soft hosts in the wooded areas in close proximity Apples - Chap 18 21/3/03 3:03 pm Page 475

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to orchards and most inoculum comes from for timing sprays of benzimidazole fungi- outside the orchard. Conidia of P. fructicola cides to manage sooty blotch and fly-speck. and G. polystigmatis are primarily water- They found that sprays of benzimidazoles borne and are spread by wind-blown rain; could be omitted in the cover-spray pro- conidia of L. elatius are airborne. Infection gramme until 225 h of wetting had accumu- can occur as early as several weeks after lated. In dry years, using the model could petal fall. Symptom expression is closely save three to five spray applications. associated with the hours of wetting that Rosenberger (Agnello et al., 1999) and occur in the spring. Brown and Sutton (1995) Hartman and Smigell (Hartman, 1995; found that the first symptoms of sooty blotch Smigell and Hartman, 1998) have modified (and fly-speck) appeared after an average of this model for their growing regions. 273 h of leaf wetting of 4 h duration or greater accumulated following the first rain 18.3.4.4 Brooks fruit spot which occurs 10 days after petal fall. P. fructicola, G. polystigmatis and L. elatius all Brooks fruit spot caused by Mycosphaerella produce conidia on fruit, which serve as pomi (Pass.) Lindau affects apples primarily secondary inoculum. All apple cultivars are in the south-eastern and mid-Atlantic apple- equally susceptible, but the colonies are growing regions of the USA (Sutton et al., more visible on light-skinned cultivars. 1987). Symptoms on fruit appear as small, Washing and brushing in the packing line slightly sunken, superficial lesions on the can often remove small colonies with lightly fruit (Plate 18.14). Lesions resemble cork pigmented thalli. spot, but there is no corky tissue beneath Fly-speck is caused by Schizothyrium pomi them. Leaf spots appear as small purple (Mont.: Fr.) Arx (anamorph Zygophiala flecks on leaves (Plate 18.15). Affected fruit jamaicensis E. Mason). Ascospores of S. pomi, are often downgraded from fresh-market to which are produced in thyrothecia on reser- processing or juice grades. voir hosts, provide the primary inoculum for M. pomi overwinters in apple leaves and infections. While some infections occur on ascospores are discharged from pseudothe- fruit, the most important infections occur on cia during rainfall. The ascospores are pro- reservoir hosts, which serve as a source of duced during a distinct period, about 6 inoculum (conidia) throughout the growing weeks in duration, beginning about 2 weeks season. Moisture and temperature require- after petal fall (Sutton et al., 1987). Symptoms ments for colony development are similar to do not appear on fruit and leaves until 6–8 those of the fungi causing sooty blotch. While weeks after infection. There is no secondary the fungi that cause sooty blotch grow super- spread. There are some differences among ficially on the cuticle, Z. jamaicensis metabo- cultivars; ‘Golden Delicious’, ‘Rome Beauty’, lizes the cuticle and the incipient thyrothecia ‘’ and ‘Idared’ are quite susceptible; become firmly attached to it, making the ‘Delicious’ is relatively resistant. A preven- colonies difficult to remove during washing tive fungicide program that includes a and brushing in the packing line. There are dithiocarbamate or benzimidazole fungicide no differences in susceptibility among culti- controls the disease. vars to either fly-speck or sooty blotch. Control of sooty blotch and fly-speck is 18.3.4.5 Alternaria blotch based on sanitation to remove reservoir hosts, pruning to open the canopy and facili- Alternaria blotch, caused by Alternaria mali tate drying, thinning fruit clusters to Roberts (= Alternaria alternata apple patho- improve drying, and fungicide sprays. The type), was first reported in the USA in the benzimidazole and dithiocarbamate fungi- late 1980s (Filajdic and Sutton, 1991). The cides are most effective; captan is not very disease affects ‘Delicious’ and cultivars with effective. The benzimidazole fungicides have ‘Delicious’ as a parent (e.g. ‘’) and is some eradicant activity against the diseases. characterized by circular, necrotic spots on Brown and Sutton (1995) developed a model the leaves (Plate 18.16), which, when abun- Apples - Chap 18 21/3/03 3:03 pm Page 476

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dant, can cause extensive defoliation. lesions, often bounded by veins. Mid-shoot Defoliation by the fungus is exacerbated by leaves are most severely affected. Lesions are mite injury. A. mali and the European red initially pale green, over a few hours turn mite act synergistically to increase defolia- chocolate brown and, as they age, often tion (Filajdic et al., 1995). When defoliation is appear tan (Plate 18.18). Severely affected extensive, fruit size and soluble solids are leaves turn yellow in a few days and abscise. reduced. Fruit symptoms are usually limited The disorder appears following periods of to small, corky, dark lesions, often associated cloudy, cool weather during the summer and with the lenticels. can result in 50% or more defoliation. It has The fungus overwinters in leaves on the been associated with an increase in the pro- orchard floor and to a lesser extent in leaf duction of gibberellins, which is triggered by buds. Infection by airborne conidia occurs environmental factors. Necrotic leaf blotch within a month of petal fall if temperature can be controlled by applications of heavy and moisture conditions are favourable. The metal-containing fungicides, such as ziram, numerous secondary cycles that can occur thiram, mancozeb and Bordeaux, or foliar throughout the growing season may result in nutrient sprays (e.g. zinc oxide). extensive defoliation. Control of the disease is based primarily on preventive control of mites to minimize 18.3.5 Phytophthora crown and root rot defoliation. Most fungicides currently regis- tered for apples in the USA, with the excep- Phytophthora crown and root rot is a poten- tion of the strobilurins, have little effect on tially serious soil-borne disease wherever Alternaria blotch. apples are grown. The disease is prevalent when susceptible rootstocks are planted in heavy soils or in areas of poor soil drainage. 18.3.4.6 Black pox Infected trees exhibit a variety of symptoms. Black pox, caused by Helminthosporium papu- During summer, foliage on infected trees losum Berg., is a problem, especially on may appear light green. As the season pro- ‘Golden Delicious’ in the south-eastern USA. gresses, leaves on infected trees turn a red- It is characterized by small, black, slightly dish-bronze. Branches on infected trees sunken lesions, 3–9 mm in diameter on the typically have stunted leaves and poor ter- fruit (Plate 18.17). Leaf spots begin as red minal growth. Fruit on infected trees is haloes with light green centres, enlarge to smaller than normal and colours prema- 1.5–11.0 mm and turn tan to brown with pur- turely. Accurate diagnosis of Phytophthora ple borders (Taylor, 1963). H. papulosum over- crown and root rot frequently requires dig- winters in twig lesions. Conidia produced in ging in order to expose the upper portions these lesions initiate infections during the of the root system. Infected tissue is reddish summer. Black pox is one of the least-studied brown and delineated from healthy tissue summer diseases, and conditions favouring by a definite margin (Plate 18.19). Diseased infection are not known. Preventive fungicide trees are often randomly distributed sprays of dithiocarbamate or benzimidazole throughout a planting. The disease is some- fungicides provide effective control. times confused with the rootstock phase of fire blight. The Phytophthora species present, soil 18.3.4.7 Necrotic leaf blotch of ‘Golden moisture and temperature, relative resistance Delicious’ of the rootstock and contamination of nursery Necrotic leaf blotch is a physiological disor- stock all affect the incidence and severity of der that affects primarily ‘Golden Delicious’ the disease (Welsh, 1942; Sewell and Wilson, and its progeny (Sutton and Sanhueza, 1998) 1959; Browne, 1984; Jeffers and Aldwinckle, and is a particular problem on the new culti- 1986; Ogawa and English, 1991). The disease var ‘Pacific Rose’. It is characterized by the can result from infection by any of several sudden appearance of large, irregular species in the genus Phytophthora: P. cactorum, Apples - Chap 18 21/3/03 3:03 pm Page 477

Diseases of Apple 477

P. cryptogea, P. cambivora, P. megasperma, P. 18.3.6 European or Nectria canker syringae, P. citricola and P. drechsleri. These fungi can persist in soil for extended periods Nectria or European canker is circumglobal of time as thick-walled sexual spores, called in distribution and particularly problematic oospores. When soil becomes saturated and in northern Europe and parts of South temperatures are conducive for sporulation, America (Grove, 1990). The disease is consid- oospores germinate to produce sporangia. ered minor in most of North America, but Within sporangia are numerous unicellular can be a serious problem in the production motile spores that are liberated into the soil areas of coastal California. The disease is water. The spores, known as zoospores, swim characterized by zonate cankers located on short distances in the soil pore spaces or can the main trunk or scaffold limbs (Plate be transported longer distances by runoff or 18.20). Young infected tissue is darker than irrigation water. When zoospores contact surrounding healthy tissue. Limb or tree roots of susceptible hosts, they germinate and death can occur from girdling, which results establish new infections. Zoospores are liber- from canker enlargement. A layer of callus ated only when soil is saturated. Prolonged tissue is formed annually around each flooding favours the production of sporangia canker. The fungus invades callus tissue and and dissemination of zoospores and may also spreads to healthy tissue outside the callus predispose the host to infection. The majority layer. Over a period of years this results in of new infections are initiated between the cankers with characteristic zonate appear- pink stage of blossom development and the ances. In some areas nurseries are important beginning of shoot elongation. The optimum sources of infected trees. temperature for disease development The disease is caused by Nectria galligena depends upon the Phytophthora species pre- Bres. The fungus produces ascospores and sent, but in general soil temperatures between conidia in orange-red fruiting-bodies pro- 20 and 30°C favour the disease. duced in twig, branch or trunk cankers. Spores Phytophthora crown and root rot is man- are produced in a gelatinous matrix and dis- aged through the integration of chemical and persed by the impaction of water droplets. cultural practices. Two of the most important The disease can be aggravated by over-the- decisions of the producer are to plant canopy irrigation. Infection occurs through pathogen-free nursery stock and to avoid the leaf scars and pruning wounds. Nectria canker use of susceptible rootstocks. Rootstocks is favoured by cool, moist weather. vary in their susceptibility to the various An integrated approach is required for species of Phytophthora. The vast majority of successful disease management. Diseased rootstock-susceptibility evaluations have wood should be removed from the orchard been conducted using P. cactorum. The and destroyed. Young infected trees should be MM.104 and MM.106 rootstocks are particu- severely pruned or removed. In some areas larly susceptible to the disease, while M.9 is diseased bark is removed to prevent spore relatively resistant. During planting, orchard production. Copper fungicides (e.g. Bordeaux managers should ensure that the graft union mixture) are sometimes applied prior to is not in contact with soil. Heavy or poorly autumn rains in order to protect leaf scars. drained soils should be avoided. In irrigated areas, water should be managed to avoid prolonged flooding and the presence of 18.4 Postharvest Diseases standing water around the base of trees. Plantings are sometimes established on Apples are also host to a multitude of raised beds in order to facilitate drainage postharvest diseases and disorders. The for- around the base of trees. Acylalanine and mer are caused exclusively by pathogenic ethyl phosphonate fungicides available for fungi. Two of the more serious postharvest control of this disease are applied as soil diseases are blue mould and grey mould, drenches or foliar sprays, respectively which are the first and second most impor- (Jeffers and Wilcox, 1990). tant postharvest diseases of apple, respec- Apples - Chap 18 21/3/03 3:03 pm Page 478

478 G.G. Grove et al.

tively. Most postharvest pathogens invade ties or severe tree decline and even death. fruit wounded during harvest, shipping or The degree of affliction depends greatly on handling. Therefore, the management of the rootstock and scion selection, pathogen postharvest diseases begins with very careful isolate and climate. Viruses or virus-like fruit harvest, bin sanitation and transport. agents that incite severe symptoms on some Fruit bins used for transport should be free apple selections will cause no obvious symp- of soil, leaves and rotten fruit debris. Fruit toms on others. However, even in the latter should be picked individually and placed case, significant yield reductions have been very gently into bins. Orchard access roads documented in the few studies undertaken should be smooth and free of ruts and major to study such effects (van Oosten, 1983). bumps. Bins should be transported at speeds Thus, infections by viruses and virus-like that will not result in shifting or bouncing. agents are important to the commercial pro- Additional means of postharvest disease duction of apples. management include packing-house sanita- Although most of these agents do not tion, rapid immediate postharvest cooling, spread naturally, many are common in com- fungicide drenches and the provision of ade- mercial orchards. The universal presence of quate tree nutrition. many of these agents is due to collecting grafting material from infected but appar- ently symptomless trees while preparing for 18.4.1 Blue mould vegetative propagation of new trees. The propagation of trees from infected sources Blue mould, which is caused by fungi in the ultimately affects yield and, under certain genus Penicillium, is the most common environmental circumstances or clone com- postharvest disease of apple (Rosenberger, binations, results in orchards that are not 1990; Plate 18.21). Decayed flesh is soft and economically productive due to fruit-quality watery and separates readily from healthy issues or tree decline. The only reasonable tissue. Infected epidermal tissue is light to method for controlling these diseases is the dark brown. Infected fruit are malodorous. initial use of virus-tested propagation The causal organism produces blue or blue- materials. green conidia on the surface of infected fruit. Quick and reliable diagnostic assays are Penicillium spp. are present in orchard soils available for a few of the viruses and virus- and on decayed fruit in the orchard and like agents that infect apple. However, for packing-house and in postharvest drench the most part, detection of such infections is solutions and flume water. Fruit infection a cumbersome and laborious proposition. typically occurs through wounds. Wounding Furthermore, only a few of the agents that should be prevented during harvest, ship- incite these diseases have been identified. ping and processing. Infested fruit bins and The use of modern laboratory diagnosis is warehouses should be disinfested before precluded until such identifications are processing fruit. made. Most assays for these agents are con- ducted by inoculative assays on sensitive woody indicator selections; these tests 18.5 Diseases Caused by Viruses, require 2 months to 3 years to complete. Viroids, Phytoplasmas and Other Virus- Aetiological studies of viruses that infect like Agents woody plants are greatly enhanced if the virus is first transmitted to a herbaceous Viruses or virus-like agents incite over 50 host. Unfortunately, many of the virus-like described diseases of apple. These agents agents that elicit disease in apple trees have include viruses, viroids and phytoplasmas not been successfully transmitted to herba- and several graft-transmissible agents that ceous plants and therefore are called ‘non- have yet to be identified. Some of these dis- sap-transmissible’. This may simply mean eases have great economic consequences in that the correct combinations of host plants that they are associated with fruit deformi- and transfer conditions have not yet been Apples - Chap 18 21/3/03 3:03 pm Page 479

Diseases of Apple 479

found. The significance of this limitation is share many important qualities, we may be that progress towards characterization of able to predict the behaviour of that these pathogens has been dramatically pathogen based on the epidemiology of a slowed. Nevertheless, the non-sap-transmis- few well-studied pathogens in the same sible viruses of fruit trees present a very group. interesting and challenging group of viruses, The caused by since relatively little is known about them. ‘virus-like’ agents is alarming in its length. Contemporary methods in molecular biol- However, many of these disease names were ogy have accelerated investigation of these applied locally to a particular symptom and pathogens. thus many of the names are duplicative. Pathogens are frequently referred to as Also, many of these diseases have very lim- viruses based on the ability to transmit the ited distribution. Only diseases that remain pathogen by grafting and/or budding and of a more general importance will be dis- the absence of any other obvious pathogens. cussed in detail. For an expanded list of This simplistic distinction is often incorrect. reported diseases of apple that are induced Many disease-causing agents are more cor- by virus-like agents, see Németh (1986). rectly referred to as ‘virus-like’ agents since no direct association between a pathogen and disease has been established – that is, 18.5.1 Chlorotic leaf spot Koch’s postulates have not been fulfilled. The disease names commonly used in the Relatively few well-characterized viruses literature are descriptive of the disease and are routinely found in the Malus of com- host but provide little information about the merce (Table 18.3). Each of these viruses pathogen. Consequently, a pathogen or vari- incites disease with major characteristics on ant thereof may be associated with different selected host cultivars that help identify the disease names, depending on the symptom disease agent. produced, the latter frequently affected by The causal agent apple chlorotic leaf- cultivar and environment. With advances in spot trichovirus (ACLSV) is one of the most our ability to isolate and characterize fruit- widely distributed viruses of fruit trees. tree pathogens at the molecular level, this Although first described as a virus in complicated structure of nomenclature is apples, it was subsequently found to be evolving to reflect more accurately the very widespread in stone fruits, where it nature of the pathogen, rather than the can cause severe losses in production. symptoms that they elicit. This is of practical Although the interaction of ACLSV with as well as academic importance. By relating many commercial apple cultivars is latent, it a pathogen to other members of a group that was first discovered associated with the

Table 18.3. Diseases of apple with known virus aetiology and their vectors.

Known means of Disease Causal agent transmission

Apple chlorotic leaf spot Apple chlorotic leaf-spot trichovirus Grafting Apple decline Apple stem-grooving capillovirus Grafting (on Virginia crab) Apple mosaic Apple mosaic ilarvirus Grafting Apple mosaic (Tulare) Tulare apple-mosaic ilarvirus Grafting Apple stem grooving Apple stem-grooving capillovirus Grafting Apple stem pitting Apple stem-pitting foveavirus Grafting Apple union necrosis Tomato ringspot nepovirus Nematodes and grafting Flat apple Cherry rasp-leaf nepovirus Nematodes and grafting Spy decline Apple stem pitting foveavirus Grafting Apples - Chap 18 21/3/03 3:03 pm Page 480

480 G.G. Grove et al.

decline and death of new Malus breeding cultivars, but appears on rootstocks with lines in an apple-scab-resistance breeding crab apple in their heritage. programme. Over the past few decades, ASGV can be diagnosed by herbaceous there have been several examples where the indexing on C. quinoa, although this method interaction of the virus with specific root- is not very reliable. Woody indexing on stocks is not latent. The top-working dis- Malus micromalus GMAL273.a or M. sylvestris ease of Japan is believed to be a cv. ‘Virginia Crab’ (Howell et al., 1995) or hypersensitive reaction of rootstocks (Malus detection by RT-PCR is the preferred method prunifolia var. ringo) to isolates of ACLSV of testing (Kummert et al., 1995; Kinard et al., found in contaminated apple scions from 1996). North America. This resulted in significant failure of mature trees (reviewed in Mink, 1989). The death of cells at the graft union 18.5.3 Flat apple results in weakened trees with reduced vigour and productivity and which are very This disease is caused by cherry rasp-leaf susceptible to wind damage. nepovirus (CRLV) (Parish, 1977), a virus ACLSV is diagnosed by serological test- that is believed to be native to western ing, indexing on herbaceous hosts North America, ranging from Utah to (Chenopodium quinoa) or budding to Malus southern British Columbia. CRLV is indicator species, usually Malus sylvestris cv. believed to have originated in one or two R12740-7A (also known as ‘Russian’). In the species of native vegetation and subse- latter case, chlorotic leaf symptoms appear quently been transmitted into horticultur- soon after new leaves develop unless the ally important crop plants, such as apple ambient temperature rises above 20°C. Low and cherry. The symptoms in apple are virus titre and inhibitors in Malus often limit most striking on the fruit of ‘’ the use of serology or indexing on herba- and related cultivars. The length of the fruit ceous plants. Molecular techniques of diag- is significantly reduced to produce a fruit nosis, such as RT-PCR, are becoming more that is squat, and the stem cavity is almost common methods of diagnosis (Kummert et absent (Plate 18.22). At first, only a few fruit al., 1995; Kinard et al., 1996). The extreme will be affected, but eventually the entire strain variation of ACLSV has limited the tree will be involved. widespread acceptance of serological and CRLV is transmitted by the nematode molecular methods. Xiphinema americanum (sensu lato) (Wagnon et al., 1968). Therefore, secondary spread of the disease is relatively slow. Apple trees 18.5.2 Apple decline (on ‘Virginia Crab’) planted on sites previously planted to rasp- leaf-diseased cherry trees can become Infection of most apple trees with apple infected. In addition to fruit trees, many stem-grooving capillovirus (ASGV) is latent orchard weeds, such as dandelions and plan- – that is, there are no acute symptoms visi- tains, are hosts, although they exhibit no ble. However, when infected scion material symptoms of the disease. This makes elimi- is grafted on to sensitive rootstocks, such as nation of the virus from an infected orchard M. sylvestris cv. ‘Virginia Crab’, growth and very difficult. The alternative hosts and/or development of the ‘Virginia Crab’ wood the nematode vectors would have to be elim- cylinder is impaired and deep grooves inated to protect replanted trees. appear under the bark. The vascular tissue Since CRLV achieves high concentration of the ‘Virginia Crab’ often becomes in young shoots, it can be readily detected necrotic, resulting in weakness and a visible by serology and by mechanical inoculation brown line at the graft union. The trees of C. quinoa with extracts from young leaves often break at this necrotic union (Németh, in early spring. Leaf symptoms and tip 1986). Stem grooving caused by ASGV is necrosis on C. quinoa usually develop 3 days not seen on current commercial apple after inoculation. Apples - Chap 18 21/3/03 3:03 pm Page 481

Diseases of Apple 481

18.5.4 Apple mosaic used to detect ASPV. Epinasty and decline may be observed after 1 year when ‘Spy227’ is Apple mosaic ilarvirus (ApMV) induces dra- the recipient. ‘Radiant’ crab apple is a more matic white bands or patterns on leaves of reliable detection host. It is sensitive to a wide many apple cultivars (Plate 18.23). Affected range of ASPV isolates and displays severe leaves may have irregular distribution epinasty and decline within 6 weeks under through the tree or even on individual limbs. controlled greenhouse conditions. The devel- The severity of the symptoms can vary dra- opment of stem-pitting symptoms on matically from year to year, with symptoms ‘Virginia Crab’ is also reliable, but at least two being almost undetectable in seasons with growing seasons are required for trustworthy high temperatures during the growing sea- results. Fruit with ridges and flutes are pro- son. This disease can result in significant duced if the ‘Virginia Crab’ is allowed to bear. production losses (ranging up to 40%) Molecular methods are also available for the depending on the cultivar, virus isolate and detection of ASPV. RT-PCR (Nemchinov et al., environment (Posnette and Cropley, 1956). 1998) is sensitive and offers faster diagnosis ApMV is detected by serological assays relative to woody indexing. but results (when apple tissue is tested) are variable. Therefore, serological testing is best limited to confirming the identity of the 18.5.6 Union necrosis pathogen in herbaceous indexing. ApMV can also be detected by inoculating field-grown Union necrosis is caused by tomato ringspot trees of ‘Golden Delicious’ apple. Herbaceous nepovirus (TmRSV) (Stouffer and Uyemoto, indexing on C. quinoa is possible but quite 1976). Symptoms of infection generally do unreliable. Molecular methods of detection, not appear until the tree reaches bearing age, such as RT-PCR (Rowhani et al., 1995), are at which time the tree assumes an unthrifty becoming more widely accepted, as the growth habit. The leaves and bark are red- methods are evaluated with more and varied dish in colour, and bloom and fruit set are isolates of the virus. abnormally high. Depending on the root- stock/scion combination, the results of infec- tion may range from very mild to a rapid 18.5.5 Stem pitting decline in tree health, resulting in death. In severe reactions (‘Red Delicious’ on MM.106), The viral nature of apple stem pitting was the union of rootstock and scion will reveal a discovered soon after the Second World War dark necrotic line spanning the union, with in mid-western North America (Guengerich soft, spongy, orange bark flanking the union. and Millikan, 1956). Production of crab This disease is common in several locales apples had become uneconomic and old crab along the east coast of North America, and apple rootstocks were budded over to stan- has been reported sporadically in the Pacific dard cultivars, such as ‘Delicious’. Two or Northwest of the USA. TmRSV is transmitted three years after budding, the crab apple by dagger nematodes, X. americanum (sensu rootstocks became pitted and severely weak- lato), which are abundant in eastern fruit- ened. This is an example where the ‘latent’ growing areas of North America (Stouffer virus in the ‘Delicious’ scion resulted in sig- and Powell, 1989). Other species belonging to nificant economic damage when the variety this nematode group, Xiphinema revesi and was budded on to rootstocks with crab apple Xiphinema californicum, are also known to be in their heritage. Apple stem-pitting fovea- vectors of TmRSV in orchards. virus (ASPV), the causal agent of apple stem- TmRSV is easily transmitted from young pitting disease, is thought to have been leaves to C. quinoa by mechanical inoculation distributed worldwide in contaminated with crude extracts. Prunus tomentosa is a diag- apple and pear propagation material. nostic woody host for this virus. Alternatively, Woody indexing on any one of a variety of serological and RT-PCR (Griesbach, 1995) Malus species is the method most frequently assays can be used to detect it. Apples - Chap 18 21/3/03 3:03 pm Page 482

482 G.G. Grove et al.

18.6 Diseases Caused by Phytoplasmas 18.6.2 Chat fruit (Table 18.4) Apple chat fruit is believed to be caused by 18.6.1 Proliferation phytoplasma infection. Sensitive cultivars develop undersized fruit, many of which Apple proliferation occurs throughout much drop in June. The remaining fruit do not of Europe, but has not been reported in the develop colour properly and may exhibit western hemisphere. The disease is caused dark water-soaked spots. Many of the cur- by an apple proliferation phytoplasma. The rent commercial cultivars do not express any pattern of occurrence in European orchards symptoms of apple chat fruit. The pathogen suggests that the pathogen is harboured in is detected by budding on to ‘Lord the native weed population, from which it Lambourne’. An incubation period of up to 3 moves into the orchards. The vector of this years is required for reliable detection. Until pathogen is at least one species of leafhop- a firm association of a biological agent with per, Fieberiella florii. This disease reduces fruit apple chat-fruit disease can be established, size by up to 30–70% and fruit have longer the use of biological indicators remains the than normal peduncles. However, the most only means of detection. striking symptom, for which the disease is named, is the proliferation of vegetative shoots, otherwise known as witches’-broom. 18.7 Diseases of Apple Caused by Viroids In addition, apple leaves exhibit greatly (Table 18.5) enlarged stipules. Because the disease is debilitating and insect-vectored, apple prolif- Viroids are sub-virus particles that are diffi- eration disease has important quarantine sig- cult to detect. Since proteins are not part of nificance in the western hemisphere. their structure, serological methods are not The most widely accepted detection method for apple proliferation phyto- useful. Woody indexing and molecular plasma has been woody indexing in the detection methods are commonly used to field. Bark patches from roots of the test diagnose these pathogens. plant are budded on to ‘Golden Delicious’ and the tree is observed for 2 years for the appearance of witches’-broom and the 18.7.1 Blister bark enlarged stipules. However, the long obser- vation period and concern about reliable Apple blister bark is characterized by areas transmission of the pathogen encouraged of the bark taking on the appearance of the development of alternative detection orange tissue-paper. The disease can be methods. Detection by PCR (Lorenz et al., induced by apple fruit-crinkle viroid 1995) is becoming widely accepted and the (AFCVd) (Ito et al., 1993). As the underlying techniques are becoming increasingly tissue becomes desiccated, the bark cracks refined to improve the reliability of molecu- and peels. Scarring of the underlying tissue lar methods (Carraro et al., 1998; occurs. Several mineral deficiencies can Skrzeczkowski et al., 2001). PCR is now the mimic infection by AFCVd, so proper diag- preferred test method. nosis is important.

Table 18.4. Diseases of apple suspected to be caused by phytoplasma.

Known means of Disease Causal agent transmission

Apple chat fruit Phytoplasma Grafting Apple proliferation Apple-proliferation phytoplasma Leafhoppers and grafting Apples - Chap 18 21/3/03 3:03 pm Page 483

Diseases of Apple 483

Table 18.5. Diseases of apple known to be caused by viroids.

Known means of Disease Causal agent transmission

Apple blister bark Apple fruit-crinkle viroid (AFCVd) Grafting Apple dimple fruit Apple dimple-fruit viroid (ADFVd) Grafting Apple fruit crinkle Apple fruit-crinkle viroid (AFCVd) Grafting Apple scar skin Apple scar-skin viroid (ASSVd) Grafting Dapple apple Apple scar-skin viroid (ASSVd) Grafting

18.7.2 Dapple apple than fruit from uninfected trees. Diagnosis is performed as described for dapple-apple dis- Dapple apple aptly describes one of the dis- ease. The dapple and scar-skin diseases eases caused by apple scar-skin viroid (ASSVd). evoked by ASSVd appear to be dependent Affected fruit, especially near the calyx end, upon climatic and cultivar differences. The bear small circular spots, which enlarge and original isolates of each produce similar dis- increasingly contrast with the background eases on fruiting trees of ‘Scarlet Pimpernel’ colour as the fruit matures (Plate 18.24). Larger (W.E. Howell, Washington State University, spots may coalesce to produce dappling or a unpublished data). broad zone of discoloration. There are no pro- nounced leaf or bark symptoms. Since many commercial cultivars do not express symptoms, 18.7.3 Dimple fruit this disease has been particularly problematic when old orchards are top-worked to change Apple dimple fruit caused by apple dimple- cultivars. The original cultivar may not express fruit viroid (ADFVd) has been observed in symptoms, whereas the new cultivar does. Pear several commercial cultivars of southern also appears to be a symptomless carrier of Italy (DiSerio et al., 1996). The disease ASSVd; the role of pear as a symptomless car- induces depressions on the fruit surface as it rier of this pathogen in apple-disease aetiology matures. Under the depression will be an is unknown. ‘Stark’s Earliest’ (‘Scarlet area of necrotic tissue. Pimpernel’) or ‘Delicious’ can be used for woody indexing, and three crops must be observed for accurate assessment of viroid sta- 18.7.4 Fruit crinkle tus. ‘Scarlet Pimpernel’ grown at 18ºC under constant light for 2 months will yield diagnostic Apple fruit-crinkle disease is caused by iso- symptoms on its foliage (Skrzeczkowski et al., lates of AFCVd (Ito et al., 1993). The viroid 1993). Molecular techniques are preferred for was described in Japan, where fruit symp- their speed and reliability. Both RT-PCR toms are most severe on the cultivar ‘Ohrin’. (Hadidi and Yang, 1990) and hybridization This pathogen can be detected by woody (Hadidi et al., 1991) assays are used for ASSVd. indexing on the apple cultivars ‘Delicious’ Apple scar-skin disease is a more severe or, preferably, ‘NY5822’, where it induces disease caused by ASSVd, as compared with symptoms of blister bark (Ito et al., 1993). the milder one referred to as dapple apple. Symptoms usually begin at the distal portion of the fruit and the severity increases as the 18.8 ’Virus-like’ or Graft-transmissible fruit matures. Small discoloured circles merge Diseases of Apple with No Known Causal to form large green-brown to brown patches Agents (Table 18.6) (Plate 18.25). Eventually, the brown patches become necrotic and fissures appear on the There are many diseases of apple for which fruit. Diseased fruit are significantly smaller no pathogen has been identified. The disease Apples - Chap 18 21/3/03 3:03 pm Page 484

484 G.G. Grove et al.

Table 18.6. Graft-transmissible diseases of apple for which there are no known causal agents.a

Apple blister bark Apple green crinkle Apple ringspot Apple dead spur Apple horseshoe wound Apple rosette Apple decline Apple internal bark necrosis Apple rough skin Apple false sting Apple leaf pucker Apple rubbery wood Apple flat limb Apple ring pustule canker Apple freckle scurf Apple ring-line pattern

aThere are many more described but rare graft-transmissible diseases of apple (Németh, 1986).

names are generally descriptive of the symp- may appear on only one or two limbs of an toms. Some may be caused by pathogens infected tree, and there are no acute foliar described above but, until more information symptoms associated with the disease is obtained about their aetiology, the causal (Thomsen, 1989). Budding and grafting of agents remain an enigma. Since the agents for contaminated propagation material is the these diseases have not been identified, con- major mechanism by which apple green- firmation of the pathogen depends on symp- crinkle disease is spread. If field spread tom expression on susceptible cultivars. All occurs, it is very slow and possibly by root are graft-transmissible. Furthermore, as most grafting only. of these diseases are spread primarily through the use of infected propagation material, the creation of virus-certification 18.8.2 Rubbery wood programmes over the past 40 years has essen- tially eliminated many of these diseases from Apple rubbery wood affects 2-year-old wood commercial apple production. Still a few con- of apple and pear trees. On sensitive culti- tinue to cause concern. vars, branches develop that are very pliable and droop under their own weights (Waterworth and Fridlund, 1989). Affected 18.8.1 Green crinkle limbs are also very sensitive to cold and frost damage. The disease originated in Europe Apple green-crinkle disease, a severely and was later introduced to North America debilitating disease of some apple cultivars, with infected rootstock. Many older root- is always associated with trees infected with stocks introduced from Europe were uni- ASGV, ASPV and ACLSV. The individual formly infected with rubbery wood. In viruses have not been separated to deter- countries with active certification pro- mine if this disease symptom is induced by a grammes, this disease has become increas- mixture of viruses, by a particular isolate of ingly rare. The degree of symptom one of the viruses or by another as yet development is dependent on climate. The uncharacterized pathogen. Apple green-crin- pliable limbs and poor growth are more kle disease is diagnosed by woody indexing extreme in moderate climates, relative to on the apple indicator ‘Golden Delicious’. warmer environments. No obvious symp- The trees are observed for the development toms are associated with many commercial of fruit symptoms during the following three cultivars. Nevertheless, fruit yield and qual- crops. Symptoms begin to appear after the ity can be adversely affected (van Oosten, fruit reaches 1–2 cm in diameter. Fruits 1983). The pathogen has been assumed to be develop deep depressions and distortions, a phytoplasma, based on electron- which become more severe as the fruits microscopic examination of affected tissues, mature. Cracks may develop in pits and but attempts to confirm this association by crevices (Plate 18.26). Depressions are linked molecular techniques have been contradic- through the flesh to the vascular system by tory (Poggi Pollini et al., 1995; Bertaccini et discoloured tissue. Severe fruit symptoms al., 1998). The disease is detected by indexing Apples - Chap 18 21/3/03 3:03 pm Page 485

Diseases of Apple 485

on ‘’, followed by 3 years of 18.9 Control Measures observation for the development of limbs lacking normal lignification. Very few viruses or virus-like agents of apple Apple flat limb is believed to be caused disease spread naturally in the orchard. This by the same agent that causes apple rubbery means that the most efficient and cost-effec- wood (see above). Apple flat limb is only tive control measure for apple virus diseases observed in those areas where sensitive culti- is the use of propagation material and plants vars, such as ‘’, are grown. The that are certified to be free from viruses. Once disease results in flattening of the shoots and the trees are planted in the orchard, they branches on limbs that are 2–3 years old and should, for the most part, remain virus-free. eventually leads to deep furrows that Still, some spread of these pathogens occurs become more severe as the branches become in orchards via tree-to-tree root grafts. Such older (Fridlund and Waterworth, 1989). In root grafts provide effective means by which addition to reduced vigour and production, pathogens can move from an infected tree to the weak limbs are susceptible to easy break- the next. However, this process is relatively ing. Severely affected limbs are also more slow and involves spread only to adjacent susceptible to winter or frost damage. The trees. Thus, if a diseased tree is detected in an disease is detected by woody indexing on established orchard, it may be prudent to ‘Gravenstein’ or ‘Lord Lambourne’, followed remove adjacent trees to eliminate the virus. by 3 years of observation. In those cases where some form of natural field transmission exists, diseases can be much more difficult to control. Again, initial planting of certified virus-free material is the 18.8.3 Dead spur first step in maintaining a healthy orchard. In European countries, where apple prolifer- Apple dead spur was originally observed in ation phytoplasma is prevalent, regular the western USA, but has since been insecticide applications to control the reported throughout North America and in leafhopper vector can significantly reduce Europe and Asia (Parish, 1989). The charac- the incidence of this disease (Kunze, 1976). teristic symptom is death of fruiting spurs, The two diseases of apple whose causal with the resulting development of long seg- agents are known to be transmitted by nema- ments of blind wood. This is most pro- todes, flat apple and union necrosis, can be nounced on the interior of the tree, so the very difficult to control. Exclusion of the virus canopy in the centre of the tree is sparse, initially is crucial since, once the virus is pre- with fruiting spurs at the shoot tips. The dis- sent, it is very difficult to eliminate it from an ease is spread through the use of infected orchard. Dagger nematodes, Xiphinema spp., propagation material. No natural spread has are nearly universal and difficult to eradicate. been observed. The only means by which the Fumigation and soil pretreatment before plant- diagnosis based on symptoms can be con- ing will reduce but not eliminate these nema- firmed is bud-inoculating spur-type todes from soil. Leaving the ground planted in ‘Delicious’ trees. Symptoms will develop in plants that are not virus hosts for 1–2 years the third or fourth year after inoculation. before replanting will help prevent transmis- Since this disease is difficult to diagnose, it sion of these viruses to the young trees. The may be overlooked in virus-testing pro- nematodes lose the ability to transmit these grammes. Like green-crinkle disease, dead viruses with each moult. Since many weed spur has not been observed in the absence of plants common in the orchard floor, such as ACLSV, ASPV or ASGV. Therefore, although dandelion and plantain, act as reservoirs of the dead-spur agent poses a concern for the these two nepoviruses, intense weed control is safe propagation of healthy apple trees, elimi- required during this period of fallow. If these nation from propagation programmes of trees viruses and their nematode vectors are present with these three ‘sentinel’ viruses may well in an area, it is best to select rootstock/scion indicate freedom from this and other graft- combinations that offer protection against the transmitted diseases of unknown aetiology. nematode and/or virus disease. Apples - Chap 18 21/3/03 3:03 pm Page 486

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