Characteristics and host range of tomato powdery mildew

Characteristics and host range of tomato powdery mildew

J. M. Whippsa*†, S. P. Budgea and J. S. Fenlonb

aPlant Pathology and Microbiology Department; and bBiometrics Department, Horticulture Research International, Wellesbourne,Warwick, CV 35 9EF, UK

The anamorphic state of a powdery mildew, which first appeared on tomato in the UK in 1987, currently listed asErysiphe orontii (anamorph Oidium violae), was examined microscopically on both tomato and alternative hosts.Host range studies were also carried out. In 1993–95, species and cultivars of plants from 26 of the 30 families listed ashosts of E. orontii were inoculated with tomato powdery mildew in the glasshouse and assessed for susceptibility on a0–3 scale based on degree of sporulation and growth. Thirteen families contained species or varieties that weresusceptible and a total of 80 varieties, including many economically important Cucurbitaceae and Solanaceae,supported sporulation to some extent (susceptibility score 1–3). Necrosis was not a constant feature of plantsexhibiting resistance, as it could accompany sporulation on some susceptible varieties. Microscopic measurementsshowed that conidial size, conidiophore length, conidiophore foot-cell length and width, and the number of cells distalto the foot-cell were remarkably constant between samples of powdery mildew taken from tomato each year and fromthe various alternative hosts. Based on the production of conidia singly, the presence of nipple-shaped to moderatelylobed appressoria, and occurrence of straight conidiophores, it is concluded that this fungus on tomato should morecorrectly be named Oidium lycopersicum until the sexual stage is discovered. The highly polyphagous nature of thispowdery mildew would suggest that it represents a potential risk to UK agriculture and horticulture, but the failure torecover any powdery mildew from 120 samples of potato, including varieties Cara and Maris Piper, on which thetomato powdery mildew could sporulate in the glasshouse, suggests that environmental factors may play a key role inpreventing establishment of this powdery mildew on alternative hosts on a commercial scale in the field.

Introduction

In 1987 a new powdery mildew was observed in England(Fletcher et al., 1988) and it has since spread throughoutthe UK (Cook & Fox, 1992; Whipps & Helyer, 1994).Several other recent reports from Australia, Canada,France, Germany, Greece, Hungary, the Netherlands,Sweden and the USA (Blancard, 1988; Paternotte, 1988;Forsberg, 1989; Noordeloos & Loerakker, 1989; Gableret al., 1990; Vakalounakis & Papadakis, 1992; Belanger,1994; Arredondo et al., 1996; Karasevitz & Zitter,1996; Kiss, 1996; Smith et al., 1997; I. Pascoe, 1994,private communication) have suggested that the same, orsimilar, novel powdery mildew has spread to infecttomatoes around the world. In all cases, cleistotheciawere not observed and so, based on morphologicalcharacteristics of an Oidium asexual stage, the fungushas been considered to be a member of the genusErysiphe.

Fletcher et al. (1988) discussed the unsatisfactory

taxonomic position of this novel powdery mildewfungus. Based on UK microscopic studies (Fletcheret al., 1988; Cook & Fox, 1992; Whipps & Helyer,1994), the lack of long conidial chains would suggestthat the fungus is neither the Oidium consideredidentical to Erysiphe cichoracearum reported ontomato in several countries including Australia, Franceand Japan (Abiko, 1978; Price, 1981; Wicks & Clare,1981) nor a novel Erysiphe sp. found on aubergine in theUK (Whipps & Helyer, 1994). Similarly, the lack offibrosin bodies in conidia would rule out the possibilitythat the novel tomato powdery mildew pathogen wasSphaerotheca fuliginea, also reported on tomato in theNetherlands (Stolk & Cools, 1983). The fungus was alsoclearly not Leveillula taurica, which is present in warmerclimates and has branched conidiophores that emergethrough stomata.

Although several attempts at a detailed classificationof powdery mildew fungi have been made using onlyanamorphic characteristics (Boesewinkel, 1977, 1979,1980; Braun, 1980; Ialongo, 1993; Shin & La, 1993),these are generally considered inferior to the use ofsexual stage characteristics for identification (Zeller,1995). Consequently, it is by no means certain that thenovel powdery mildew pathogens reported from around

Plant Pathology (1998) 47, 36–48

Q 1998 BSPP 36

*E-mail: [email protected]

†To whom correspondence should be addressed.

Accepted 28 August 1997.

the world as Erysiphe sp. are the same species. There-fore, some care must be exercised in applying the generallabel of Erysiphe sp. to the novel agent of powderymildew on tomato, for which only the anamorph isavailable, particularly when conidiophore and conidialcharacteristics are known to be affected to varyingdegrees by environmental conditions and host (Yar-wood, 1978; Fletcher et al., 1988).

The apparent rapid spread of the new tomatopowdery mildew fungus raises the questions of itsorigin, host range, taxonomic position and variability.Preliminary host range studies have been carried out inthe UK (Fletcher et al., 1988; Foster, 1992), butcommercial concern over the role of alternative hostsin the spread of the disease indicates a need for a largersurvey to help understand its aetiology and thusfacilitate its control. The most recent checklist ofpowdery mildew fungi in the UK (Ing, 1990a,b,c,d;1991a,b,c) and the existing UK host range studiessuggest that Erysiphe orontii, previously Erysiphepolyphaga (Hammarlund, 1945; Braun, 1987), is themost appropriate name for the powdery mildew patho-gen present on tomato.

Based on this premise, this paper reports an examina-tion of species and cultivars of plants from 26 of the 30families listed as hosts of E. orontii worldwide (Braun,1987) for potential to act as hosts of the tomato powderymildew fungus. Particular emphasis has been placed onmembers of the Cucurbitaceae and Solanaceae, whichare widely grown on a commercial basis and couldprovide a suitable reservoir for rapid disease cycling anddissemination. Microscopic studies of conidia andconidiophores produced by the pathogen on tomatoand, following cross-inoculation, on alternative hostswere also carried out to determine the stability of thesecharacters and their diagnostic value.

Materials and methods

Production and maintenance of inoculum on tomatoplants

Tomato seed (var. Moneymaker) was sown on a weeklybasis into 12.5-cm plastic pots containing peat/sand(4 :1, v/v) compost. Plants at the four leaf stage weretransferred onto benches in a glasshouse maintained at198C minimum night temperature, 208C minimum daytemperature, with vents opening at 238C. The glasshousealready contained tomato plants infected with powderymildew, originally obtained from a natural infection in atomato crop at HRI Littlehampton. Aphid and whiteflyinfestations were controlled using the biological controlagents Aphidius and Encarsia, respectively. Normally,newly introduced tomato plants developed powderymildew infection after one week. If the level of infectionappeared low or inconsistent (less than 25% on fullyexpanded leaves), plants were given an additionalinoculation by tapping heavily infected leaves fromolder plants over them. Diseased tomato plants used for

inoculation of each group of test plants were derivedfrom a single sowing batch and were used whenapproximately 80 cm high.

Host range studies

Plant cultivationPotatoes used for the host range studies were grownfrom seed tubers supplied by ADAS Wolverhampton. Allother test plants were grown from seed obtained fromThompson & Morgan (Poplar Lane, Ipswich, UK) andChiltern Seeds (Bortree Stile, Ulverston, UK), or wereavailable from an HRI collection.

In February 1993, seed tubers of 45 potato varietieswere chitted in trays in a glasshouse at HRI Littlehamp-ton. Subsequently, tuber pieces containing a single shootwere placed individually into 12.5-cm pots containing thesame peat/sand compost as before with five replicate potsper cultivar. Three weeks after planting, the pots weretransferred from the propagation glasshouse intothe glasshouse containing tomato infector plants andinoculated as described below. No powdery mildew wasobserved on plants during growth in the propagationglasshouse.

Seeds of the other test plants were sown (betweenFebruary and May 1994 at HRI Littlehampton and inJuly 1995 at HRI Wellesbourne) in 5-cm plastic potscontaining the same peat/sand compost as before andpropagated according to the supplier’s recommenda-tions. Two to six seedlings, sufficiently developed(between four true leaves for larger leaved plants suchas cucurbits and 10 true leaves for very small leavedplants such as Linum spp.), were transferred from thepropagation area into the glasshouse containing tomatopowdery mildew infector plants and inoculated withpowdery mildew. Twelve species of plants were tested inboth 1994 and 1995 to check consistency of response.No powdery mildew was observed on any plant duringgrowth in the propagation glasshouse.

Inoculation and evaluation of powdery mildew on testplantsWith potatoes, immediately after plant transfer, theterminal leaflet of a leaf 15–30 cm from the pot surfacewas inoculated on both surfaces with powdery mildewconidia. These were applied using three completerevolutions of a cotton bud which had previously beenrolled once on a heavily sporulating leaf of an infectorplant. The leaflets were marked with small tie-on labelsand the whole plants were enclosed in polyethylene bagsfor 24 h. After two weeks, all plants were examined forsymptoms of powdery mildew infection. Necrosis wasnoted and susceptibility assessed visually on a 0–3 scalewhere 0 ¼ no conidiophore production, 1 ¼ very limitedconidiophore production (<30 conidiophores perinoculation site) with no spread from inoculation site,2 ¼ greater level of conidiophore production(>30 conidiophores per inoculation site) with somespread from the inoculation site, and 3 ¼ conidiophore

Host range of tomato powdery mildew 37

Q 1998 BSPP Plant Pathology (1998) 47, 36–48

production throughout the fungal colony with extensivespread from the inoculation site. Samples of the powderymildew pathogen were taken for microscopic observa-tion from all cultivars that developed infection, andcompared with similar samples collected from infectedtomato plants. In addition, conidia were transferredfrom four relatively susceptible cultivars (Dundrum,Minerva, Pentland Squire and Rocket), which developeda natural infection of powdery mildew, to tomato cv.Moneymaker plants maintained in separate perspexboxes in a growth room at 258C with a 16-h day length.The transfers were made using separate fine sable artists’brushes. After 7 days, the plants were examined for thepresence of powdery mildew as before.

Either on the day of transfer to the glasshouse con-taining tomato infector plants or one day later, testplants grown from seed were arranged so that up to sixpots of any single variety were surrounded by infectorplants, and inoculated by gently tapping a heavilyinfected tomato leaf over them. After one week, testplants were assessed for infection and necrosis. If no orvery little infection occurred, two leaves of each testplant were marked and re-inoculated by applying aheavy load of conidia from an infected tomato leaf witha fine sable artists’ brush and enclosing in plastic bags for24 h. After a further week, plants were re-examined forsymptoms of infection and necrosis. Susceptibility wasassessed on a 0–3 scale similar to that used for potatoexperiments but modified to consider the methods ofinoculation. In this modified scale, 0 ¼ no conidiophoreproduction after both inoculations, 1 ¼ very limitedconidiophore production (< 30 conidiophores per inocu-lation site), often only appearing as a result of the secondbrush inoculation, with no spread of infection from theinitial site of infection, 2 ¼ greater level of conidiophoreproduction (> 30 conidiophores per inoculation site)with some spread from the inoculation site, usually as aresult of the first tap inoculation, 3 ¼ conidiophoreproduction throughout the fungal colony with extensivespread from the inoculation site, always resulting fromthe initial tap inoculation. Test plants that did notdevelop infection after the second inoculation were keptin the glasshouse for a further 2 weeks to check for anyvery slow development of powdery mildew. Samples ofpowdery mildew were taken for microscopic observa-tion from all test plants that developed infection in orderto determine the stability and diagnostic value of a rangeof morphological characteristics, especially those ofconidia and conidiophores.

Microscopic observationsSmall pieces of clear adhesive tape (maximum 1 cm2)were gently applied to infected leaves, then transferredinto lactophenol/aniline blue on a glass slide. A coverslip was applied before the preparation was sealed withclear nail varnish. Using a light microscope equippedwith an eyepiece graticule, measurements of sixcharacters (length and width of conidia and foot-cells,length of conidiophores, and number of cells distal to

the foot-cell) were made on random transects across atleast two slide preparations. Thirty measurements ofeach character were normally made, except for tomatovar. Moneymaker controls, where 50, 91 and 60measurements were made in 1993, 1994 and 1995,respectively, and for six plants where sporulation wasinsufficient (Cucumis melo (water melon var. GoldenCrown) and the five potato varieties Ailsa, Ausonia,Cara, Navan and Picasso). The shape of foot-cells andappressoria were also noted.

In addition, for powdery mildew on tomato var.Moneymaker only, the process of conidial germinationwas observed from adhesive tape preparations, andhaustorial complexes were measured on whole leafpieces cleared in 70% ethanol and mounted and stainedas before. The presence of fibrosin bodies in conidia wasassessed by mounting fresh conidia in 30 g L¹1 potas-sium hydroxide. Scanning electron microscopy was alsocarried out on fresh material to complement theobservations made by light microscopy.

Statistical analyses of microscopic dataMeans and standard deviations were determined foreach of the six characters measured, and analysis ofvariance was also made, comparing between- andwithin-sample variation. For each pair of charactersmeasured on conidia, foot-cells and conidiophores, a bi-analysis using the method of canonical variates wasperformed (Krzanowski, 1988) to observe the variationbetween samples. This method allows for the variationbetween observations within samples to affect thesample discrimination rather than simply reflectingspatial variation due to means, as in principal compo-nent analysis (Krzanowski, 1988). Given that the patternof sample variation differed among the three sets ofobservation pairs, a further canonical analysis was alsoperformed on the three length measurements to identifythose samples that were most distinct from the generalgrouping. Details of further specific tests used to clarifythe statistical data are given in the results.

Potato powdery mildew survey

In August and September 1993, 54 samples of 20 leavesof five cultivars of potato (Cara, Estima, King Edward,Maris Piper and Record) from 20 counties in the UK(supplied by ADAS) were examined under a binocularmicroscope for presence of powdery mildew. In 1994,the survey was repeated with 64 samples from through-out the UK but with the omission of cultivar KingEdward.

Results

Host range studies

Thirteen of the 26 plant families tested contained speciesor varieties that developed symptoms when infected bythe tomato powdery mildew fungus and a total of 80

J. M. Whipps et al.38




Table 1 Host range tests of tomato powdery mildew

Type or YearFamily Species common name Variety tested Necrosisa Susceptibilityb

Acanthaceae Acanthus mollis 1994 – 0Thunbergia alata Susie Mixed 1994 – 0

Apocynaceae Catharanthus sp. Catharanthus Pretty in Soft Pink 1994, 1995 þ 1Asteraceae (Compositae) Aster alpinus 1994, 1995 – 0

Aster sp. Aster Pompom Splendid 1994 – 0Chrysanthemum carinatum Court Jesters Mixed 1994 – 0Chrysanthemum coronarium Golden Gem 1994 – 0Chrysanthemum indicum Incurved Mixed 1994 – 0Chrysanthemum multicaule Gold Plate 1994 – 0Chrysanthemum segetum Prado 1994 – 0Doronicum cordatum Finesse 1994 – 0Dahlia sp. Dahlia Coltness Mixed 1994 – 0

T & M Octopus Series 1994 – 0Helianthus annuus Italian White 1994 – 0Solidago canadensis Golden Baby 1995 – 0

Begoniaceae Begonia hortensis All Round Series Mix 1994 – 0Bignoniaceae Incarvillea sinensis Cheron 1994 – 0Brassicaceae (Cruciferae) Brassica napus Swede Best of All 1994 – 0

Brassica oleracea Kohl Rabi Rowel 1994 – 0Cauliflower All the year round 1994 – 0Brussels Sprout Dolmic F1 Hybrid 1994 – 0Cabbage Perfect Ball F1 Hybrid 1994 – 0

Brassica rapa Chinese Cabbage Mariko F1 Hybrid 1994 þ 0Turnip Snowball 1994 – 0

Cardamine pratensis 1995 – 0Eruca sp. Eruca Rocket/Italian Cress 1994 – 0Erysimum wheeleri 1994 – 0Raphanus sativus Radish Cherry Belle 1994 – 0

Campanulaceae Campanula isophylla Kristal Mixed 1994 – 0Campanula latifolia Mixed 1994 þ 1Specularia speculum 1994 – 0

Cistaceae Helianthemum sp. Helianthemum × Hybrids Mixed 1994 þ 1Crassulaceae Cotyledon orbiculata 1995 – 0

Echeveria peacockii 1994 – 0Kalanchoe blossfeldiana Pot Gold Hybrids 1994 – 0Sedum spurium Coccineum 1994 þ 3Sempervivum sp. Sempervivum × New American Hybrid 1994 – 0

Cucurbitaceae Cucumis anguria Gherkin Liberty F1 1994, 1995 þ 2Cucumis melo Melon Amber Nectar 1994 – 2

T & M Gaylia F1 Hybrid 1994 – 3Watermelon Golden Crown F1 Hybrid 1994, 1995 þ 1

Cucumis sativus Cucumber Corona 1994 – 3Rebella 1994 – 3

Cucurbita pepo Marrow Long G Stripe 1994 þ 2Green Bush 1994 þ 2

Cucurbita pepo Squash Cream of the Crop 1994, 1995 þ 2Winter Squash 1994 þ 1

Cucurbita pepo Courgette Sardane 1994 – 3Accefle 1994 – 3

Cyclanthera pedata 1994 – 3Lagenaria siceraria Gourd T & M Large Bottle 1994 – 3

Turks Turban 1994 – 2Choose the Weapon 1994 þ 1Ornamental 1994 þ 2

Luffa cylindrica Luffa 1994 – 0Ericaceae Calluna vulgaris Heather 1995 – 0

Erica mammosa 1995 – 0Erica terminalis 1995 – 0Erica tetralix 1995 – 0

Euphorbiaceae Ricinus communis Impala 1994 – 0



Table 1 continued


Gesneriaceae Sinningia speciosa 1995 – 0Hydrangeaceae Hydrangea quercifolia 1995 – 0Lamiaceae Hyssopus officinalis 1994 – 0Linaceae Linum grandiflorum Bright eyes 1994 – 0

Linum perenne Blue Saphyr 1994 þ 3Malvaceae Abelmoschus moschatus Hybrid Mischief 1994, 1995 þ 1

Althaea rosea Hollyhock Nigra 1994 – 0Hibiscus manihot Cream Cup 1994 þ 3Hibiscus trionum Sunny Day 1994, 1995 þ 2

Myrtaceae Eucalyptus macrocarpa 1994 þ 0Papaveraceae Papaver bracteatum 1994, 1995 þ 0

Papaver rhoeas Mother of Pearl 1994 – 3Papaver trinifolium 1994 þ 0

Pedaliaceae Sesamum indicum 1994, 1995 þ 3Scrophulariaceae Antirrhinum majus Nanum Liberty Mixed F1 Hybrid 1994 – 0

Monarch Mixed 1994 – 0Digitalis grandiflora 1994 þ 0Hebe hulkeana 1995 – 0Hebe raoulii 1995 – 0Linaria marroccana Fairy Lights Mixed 1994 þ 3Linaria nevadensis Elfin Delight 1994 þ 3Penstemon palmeri 1994 – 0Penstemon strictus 1994 – 0Scrophularia nodosa 1995 – 0Veronica teucrium Crater Lake Blue 1994 þ 1

Solanaceae Capsicum annuum Pepper Summer Salad F1 Hybrid 1994 – 0Chilli Seranadon 1994 – 0Big Bertha 1994 – 0

Cestrum nocturnum 1995 – 0Datura metaloides Evening Fragrance 1994 þ 1Datura suaveolens 1994 – 0Lycopersicon esculentum Tomato Ailsa Craig 1994 – 3

Calypso 1994 – 3Counter 1994 – 3Criterium 1994 – 3Liberto 1994 – 3Marathon 1994 – 3Mercator 1994 – 3Sonatine 1994 – 3Spectra 1994 – 3Sweet 100 1994 – 3

Nicotiana alata Fragrant Cloud 1994, 1995 þ 3Nicotiana langsdorffii 1994, 1995 þ 3Nicotiana sylvestris 1994 þ 3Petunia sp. Petunia Rainbow 1994 – 2

Mirage 1994 þ 2Physalis gigantia Chinese Lantern 1994 – 2Salpiglossis sinuata Bolero F2 Mixed 1994 – 1Schizanthus sp. Schizanthus Dwarf Bouquet Mixed 1994 þ 3Solanum capsicastrum 1994 þ 0Solanum melongena Aubergine Black Prince F1 Hybrid 1994 – 3

Elondo F1 Hybrid 1994 – 3Bambino 1994 – 2Black Enorma F1 Hybrid 1994 – 2

Solanum sisymbrifolium 1994, 1995 þ 3Solanum seaforthianum 1994 þ 1Solanum tuberosum Potato 1993

Accent 1993 þ 0Ailsa 1993 þ 1Ausonia 1993 þ 1



Table 1 continued


Balmoral 1993 þ 1Belle de Fontana 1993 þ 0Burber 1993 þ 0Cara 1993 þ 1Carlingford 1993 þ 0Colmo 1993 þ 0Concorde 1993 þ 0Desiree 1993 þ 0Diana 1993 þ 1Dundrum 1993 þ 2 (3)c

Estima 1993 þ 0Fambo 1993 þ 0Fresco 1993 þ 0Heather 1993 þ 0Javelin 1993 þ 1King Edward 1993 þ 0Kondor 1993 þ 0Lady Rosetta 1993 þ 0Marfona 1993 þ 0Maris Bard 1993 þ 0Maris Peer 1993 þ 0Maris Piper 1993 þ 1Minerva 1993 þ 2 (3)c

Morene 1993 þ 0Nadine 1993 þ 0Navan 1993 þ 1Ostala 1993 þ 0Penta 1993 þ 0Pentland Dell 1993 þ 1Pentland Javelin 1993 þ 1Pentland Squire 1993 þ 2 (3)c

Picasso 1993 þ 1Record 1993 þ 0Rocket 1993 þ 2 (3)c

Romano 1993 þ 0Sante 1993 þ 0Shula 1993 þ 1Stroma 1993 þ 0van Gogh 1993 þ 0Wilja 1993 þ 0Winston 1993 þ 0

Trichosanthes cucumeroides 1995 – 0Valerianaceae Valerianella Corn Salad Cavallo 1994 þ 2Verbenaceae Verbena x. hybrida Blaze 1994 – 0

Verbena rigida (vernosa) 1994 – 0Violaceae Viola x. wittrockiana Pansy Clear Crystal Mixed 1994 þ 2Vitaceae Cissus antarctica 1995 – 0

Cissus juttae 1995 – 0

(a) þ, necrosis present as a result of inoculation with powdery mildew on at least 1 plant; ¹, no necrosis.(b) 1993 tests with potato; 0, no conidiophore production; 1, very limited conidiophore production (< 30 per inoculation site) with no spread frominoculation site; 2, greater level of conidiophore production (>30 per inoculation site) with some spread from the inoculation site; 3 ¼ conidiophoreproduction throughout the fungal colony with extensive spread from the inoculation site.1994 and 1995 tests: 0, no conidiophore production after both inoculations; 1, very limited conidiophore production (< 30 with other species: perinoculation site) often only as a result of the second brush inoculation, with no spread from inoculation site; 2, greater level of conidiophore production(> 30 per inoculation site) with some spread from the inoculation site, usually as a result of the first tap inoculation; 3, conidiophore productionthroughout the fungal colony with extensive spread from the inoculation site.(c) Natural infection of powdery mildew subsequently developed.

varieties supported sporulation to some extent (suscept-ibility score 1–3) (Table 1). Although not all susceptiblevarieties exhibited macroscopic symptoms typical of thehighest level of susceptibility (3), sporulation was alwaysconfirmed microscopically.

Susceptibility was not universal within families at thegenus or species level, although no susceptible specieswere found in some families, such as the Asteraceae(Compositae) and Brassicaceae (Cruciferae) which weretested in detail (Table 1). For example, families such asthe Crassulaceae and Scrophulariaceae contained speciesthat were either fully susceptible (3) (Sedum spurium andLinaria spp., respectively) or resistant (0) (Cotyledonorbiculata and Antirrhinum majus, respectively) (Table 1).Some families contained a higher proportion of suscep-tible species than other families. For instance, of the ninespecies of Cucurbitaceae tested, only Luffa cylindrica wasresistant (0). Even so, in the Solanaceae, which containsthe original host (Lycopersicon esculentum), five of the 18species tested were resistant to fungus. Of the five speciesof Solanum tested, one (S. capsicastrum) was resistant,another (S. seaforthianum) was susceptible at a low level(1), S. melongena and S. tuberosum had varieties thatexhibited a range of susceptibility (2–3 and 0–3, respec-tively) and S. sisymbrifolium was fully susceptible (3).Sixteen of the 45 potato varieties tested were susceptible,and only four of these (Dundrum, Minerva, PentlandSquire and Rocket) were fully susceptible when a naturalinfection developed subsequent to the initial challenge.

Generally, the most susceptible reactions, such as thosedeveloping on all tomato varieties, did not involve necrosisin response to inoculation (Table 1). Necrosis was not aconstant feature of resistance as some resistant species(e.g. Acanthus mollis) showed a complete absence ofmacroscopic symptoms, but it was observed in manypotato varieties with high levels of resistance. Irrespectiveof the presence of necrosis, the conidia formed on the fourmost susceptible potato varieties were able to infecttomato to give a fully susceptible reaction again (data notshown).

Microscopic observations

Tomato powdery mildewThe morphological characteristics of the tomato pow-dery mildew pathogen observed over three years aregiven in Table 2. Conidia germinated from one end andthe short germ tube terminated in an appressorium(Fig. 1). The mycelium then continued to develop bothfrom the appressorium and from further germ tubesarising from the conidium. Single or pairs of nipple-shaped to moderately lobed appressoria were associatedwith the generally straight, superficial hyphae (Fig. 2).Conidiophores arose from unbranched, mainly straightfoot-cells with 2–3 distal cells (Figs 3 and 4). Theproximal cell acted as the generative cell, elongatingand dividing each day in synchrony with the dailydevelopment and abscission of a terminal conidium.Rarely, short chains of 1–3 conidia were observed underrelatively humid conditions with little air movement.



Figure 1 Photomicrograph showing the germination of conidia oftomato powdery mildew on tomato. Note the germ-tube formation atthe end of the conidia and the production of appressoria. Barlength ¼ 20 mm.

Figure 2 Scanning electron micrograph of the edge of a 6-day-oldcolony of tomato powdery mildew on tomato. Note the straightsurface hyphae and the nipple-shaped or moderately lobedappressoria, present singly (1) or in pairs (2). Bar length ¼ 50 mm.

Figure 3 Scanning electron micrograph (back-scatter image)towards the centre of a 6-day-old colony of tomato powdery mildewon tomato. Note the erect conidiophores with a straight basal foot-cell (FC) with distally, a generative cell (GC), a first-stage conidium(C1) and a second-stage conidium (C2), which has been lost insome cases. No chains of conidia are present. Bar length ¼ 50 mm.



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Conidia did not contain fibrosin bodies. In each yearof study, the mean values of all the features measured(conidial length and width, foot-cell length, conidio-phore length and width, and number of cells distal tothe foot-cell) were similar, with their ranges over-lapping (Table 2).

Alternative hostsMean conidial length measured on samples from allhosts including tomato, varied from 24.6 to 33.5 mm(SED (standard error of difference between any twomeans) ¼ 0.975 mm), while conidial width varied from12.58 to 16.68 mm (SED ¼ 0.385 mm). Conidial lengthand width were highly significantly correlated(r ¼ 0.729; d.f. ¼ 71; P< 0.001) (Fig. 5). The averageratio of length to width, taken across all 73 samples, was2.06 (SE ¼ 0.012), with the range varying from 1.9 to2.43. Analysis of variance of both length and width datarevealed significant (P ¼ 0.001) differences betweenmeans, although bi-variate analysis (canonical variates)indicated a continuum with four isolated samples withlarger, broader spores (Fig. 5). One of these consisted ofonly three observations (potato, variety Navan) and

another was the 1993 tomato var. Moneymaker controlfrom Littlehampton. The two remaining samples (Valer-ianella sp., Mixed Corn and Solanum seaforthianum)gave longer, thinner spores than all other samples. Nodistinct pattern was apparent between samples collectedfrom members of the same family, genus or species,suggesting that the variation among all host species maybe random.

Mean foot-cell length varied between 33.25 and60.75 mm (SED ¼ 2.130 mm), and width means variedbetween 5.88 and 8.25 mm (SED ¼ 0.265 mm). Nosignificant correlation was found between length andwidth (r ¼ 0.182; d.f. ¼ 71; P ¼ 0.05). All six incompletesamples were peripheral to the main grouping of thesamples, and three (watermelon var. Golden Crown andpotato varieties Ailsa and Cara) were very distinctoutliers (Fig. 6). The samples with the eight largest meanfoot-cell lengths were all from 1993, with five beinginoculated sites on potato (varieties Ailsa, Balmoral,Navan, Pentland Dell and Rocket) and three comingfrom tomato cross-inoculated from potato (varietiesMinerva, Pentland Squire and Rocket). However, noparticular significance can be assigned to this observa-tion, as only one of the tomato sample cross-inocula-tions yielding longer foot-cells came from a potato(variety Rocket) with long foot-cells. Canonical variateanalysis for foot-cell length and width confirmed thispattern.

The mean length of conidiophores ranged between



Figure 4 Scanning electron micrograph (back-scatter image) show-ing details of the conidiophore of tomato powdery mildew on tomato.FC, foot-cell; GC , generative cell; C1, first-stage conidium; C2,second-stage conidium. Bar length ¼ 10 mm.

Figure 5 A bi-variate plot of mean conidial length (mm) against meanconidial width (mm) of all species and varieties with a susceptibilityscore of 1 or above (see Table 1) with outliers specifically named onthe figure based on analysis of variance and bi-analysis usingcanonical variates. W, tomato var. Moneymaker controls for 1993,1994 and 1995; B, species or varieties with < 30 observations (water-melon var. Golden Crown and potato varieties Ailsa, Ausonia, Cara,Navan and Picasso); P, Solanum seaforthianum; O, Valerianella sp.;X, all other species and varieties.

65.75 and 108.25 mm (SED ¼ 3.73 mm) with the averagenumber of distal cells varying between 1.87 and 2.97(SED ¼ 0.119). The pattern of means is shown in Fig. 7.The range of values for distal cell numbers was verylimited (2–3, rarely 4). Nevertheless, the number ofdistal cells does appear to be a potential discriminatorbetween powdery mildew developing on Cucurbitaceae(fewer cells) and Solanaceae (more cells), although thereis overlap. Further, samples from the four naturalinfections on potato were not distinct from samplescollected on other Solanaceae. The correlation betweendistal cell number and conidiophore length was highlysignificant (r ¼ 0.507; d.f. ¼ 71; P ¼ 0.001), and thecorrelation between conidiophore length and conidiallength was even greater (r ¼ 0.713; d.f. ¼ 71; P ¼ 0.001).

Potato powdery mildew survey

No powdery mildew was observed on any potato samplecollected from the field in 1993 or 1994.

Discussion

The morphological characteristics of the tomato pow-dery mildew fungus were stable within the rangesdescribed over a three-year period from tomato plantsgrown at Littlehampton and Wellesbourne, and agreedwith the description of these characters in earlier UKstudies (Fletcher et al., 1988; Cook & Fox, 1992;Whipps & Helyer, 1994) and recent reports fromelsewhere in Europe, North America and Australia(Noordeloos & Loerakker, 1989; Gabler et al., 1990;Vakalounakis & Papadakis, 1992; Kiss, 1996; Karase-vitz & Zitter, 1996; Smith et al., 1997; I. Pascoe, 1994,private communication). This would suggest that asingle novel powdery mildew taxon, particularly aggres-sive on tomato, has arisen fairly recently and spreadrapidly around the world.

From the host range studies, species from 13 of 26families reported to contain hosts of E. orontii wereinfected, which suggests that this taxon could beconsidered a new race, form or variety (sensu Hammar-lund, 1945; Braun, 1987) of this polyphagous species.However, somewhat surprisingly, Antirrhinum majus, aparticularly common host of E. orontii (Braun, 1987),was not infected, confirming observations of Fletcheret al. (1988) and questioning further the use of the nameE. orontii for this pathogen. Interestingly, although thecross-inoculation studies carried out by Fletcher et al.(1988) and Foster (1992) agreed in general with theresults found in this study, differences in susceptibilitywere observed. For example, Petunia was infected in thisstudy, confirming observations of Fletcher et al. (1988)but not those of Foster (1992); Valerianella andcucumber were infected in this study, but not in theexperiments of Fletcher et al. (1988); and the potatocultivar Desiree was infected in the work of Fletcher etal. (1988) and of Foster (1992), but not in this study.This could reflect differences in the environmental



Figure 6 A bi-variate plot of mean foot-cell width (mm) against meanfoot-cell length (mm) of all species and varieties with a susceptibilityscore of 1 or above (see Table 1) with outliers specifically named onthe figure based on analysis of variance and bi-analysis usingcanonical variates. W, tomato var. Moneymaker controls for 1993,1994 and 1995; B, species or varieties with <30 observations(watermelon var. Golden Crown and potato varieties Ailsa, Ausonia,Cara, Navan and Picasso); X, all other species and varieties.

Figure 7 A bi-variate plot of mean number of distal cells againstmean conidiophore length (mm) of all species and varieties with asusceptibility score of 1 or above (see Table 1). W, tomato var.Moneymaker controls for 1993, 1994 and 1995; B, species orvarieties with < 30 observations (watermelon var. Golden Crownand potato varieties Ailsa, Ausonia, Cara, Navan and Picasso);O, Valerianella sp.; X, all other species and varieties. There were nooutliers based on analysis of variance and bi-analysis usingcanonical variates.

conditions used for inoculation, the inoculation methodsthemselves, the cultivars of plants in some cases, or evenpathogenic differences within the tomato powderymildew fungus itself, as the culture was initiated froma mixed population of conidia. Contamination fromconidia from outside the glasshouse is also a possibility,but the fact that no powdery mildew was observed onplants grown in the propagation house and thatobservations were based only on the sites of inoculationlimit the significance of this problem. Some plantsclassed as hosts in this study were slow to produceconidiophores or exhibited necrosis at the same time asconidiophores were produced, and this could havebrought about different interpretations of susceptibilityby different workers. In some plants in this study,necrosis and infection could also have resulted as aresponse to the heavy conidial load applied and may notnecessarily reflect the natural response of the plant to thelow numbers of conidia likely to occur in the field.

The concept that the tomato powdery mildew fungusis a new race, form or variety of E. orontii was alsochallenged by microscopic evidence. First, conidia wereproduced singly in the same manner as Erysiphe pisi andErysiphe polygoni (Yarwood, 1936; Martin & Gay,1983). Short chains consisting of a maximum of threeconnected conidia were observed occasionally, but onlyunder relatively high humidity and in the absence ofrapid air movement in the glasshouse. After preparationfor microscopy, chains of conidia were never observed.This clearly places this taxon in the Pseudoidium group,as opposed to the Euoidium group where conidia areproduced in chains (Blumer, 1967). However, earlierdescriptions of E. orontii (then E. polyphaga) withconidia formed in ‘long chains’ (Hammarlund, 1945) orin ‘chains, with several immature and mature onespresent at the same time’ (Boesewinkel, 1980), place thisspecies in the Euoidium group. Nevertheless, thisargument might not be entirely conclusive, since Braun(1987) considered E. orontii to form ‘conidia in chains,chains not very long’ which largely contradicts theearlier descriptions of E. polyphaga and unfortunatelylays a way open for misinterpretation of the identity ofthe species. Confusion could exist if chains of conidiawere seen on fresh specimens under the binocularmicroscope without resort to examination of conidio-phores and conidia using a compound microscope todetermine the system of conidia production. Secondly,appressoria were nipple-shaped to moderately lobed,single or in opposite pairs; they were never inconspic-uous. In contrast, E. orontii has nipple-shaped, oftenpoorly developed or inconspicuous appressoria (Boese-winkel, 1980; Braun, 1987). Again, a compoundmicroscope must be used to examine this character.Finally, the foot-cells of our samples were straight andwere never seen to branch or be curved below asreported for E. orontii (Boesewinkel, 1980; Braun,1987). Because of these reservations, the use of E.orontii as the name of the new powdery mildew funguson tomato would seem inappropriate. In contrast, the

name Oidium lycopersicum, based on a redescription ofa powdery mildew fungus found on tomato in Australiain 1888 by Cooke and Massee (Noordeloos & Loer-akker, 1989), may be more acceptable (see Gabler et al.,1990; Braun, 1995). All characteristics of the newpowdery mildew pathogen on tomato fit with those ofthe holotype, and the objection by Vakalounakis &Papadakis (1992) that the conidiophore of O. lycopersi-cum is too long to fit with Greek samples of the tomatopowdery mildew fungus is clearly overcome from thegreater range of conidiophore lengths found in thisstudy. The view that the Oidium sp. found on tomato inCalifornia did not match the description of O. lycoper-sicum (Arredondo et al., 1996) requires a more detailedstudy, as the characteristics described by these authorsappear to satisfy the criteria for inclusion within O.lycopersicum except for the presence of short chains ofconidia, which might be explained as discussed earlier.Despite the current acceptance of describing powderymildews by the teleomorph, the novel powdery mildewon tomato should continue to be described as O.lycopersicum until the sexual stage is discovered.However, the proviso must be added that microscopicobservation should be carried out to determine whethera powdery mildew on tomato relates to E. orontii (withan anamorph of Oidium violae: Braun, 1987), or toOidium lycopersicum with an unknown teleomorph.

One of the main findings of this study was the relativestability of the morphological characters measured onalternative hosts. The statistical analysis of the micro-scopic measurements made on the 73 samples examinedrevealed very few significant differences for any of thecharacters investigated. For example, on hosts wheresporulation was poor, it could be expected that thefungus would be under stress, producing conidia andconidiophores of abnormal size. However, this was notfound for the majority of plants exhibiting low levels (1–2) of susceptibility. Even in the six samples where lessthan 30 observations were possible, all measurementswere not consistently out of the range determined fromthe remaining samples. The statistical analysis alsoprovided some evidence that foot-cell length and distalcell numbers could indicate differences in the develop-ment of the powdery mildew fungus on some groups ofplants, such as members of the Cucurbitaceae andSolanaceae, but there is considerable overlap in valuesfor some varieties of these plants, and the differences aresmall in real terms. This is significant as anamorphmorphology of several powdery mildews is known tovary with environmental conditions and host (Yarwood,1978; Whipps & Helyer, 1994). It may well be that theuse of such a large number of samples from alternativehosts has provided enough data to overcome problemswith variation, observed in relatively small samples ofpowdery mildew material often examined. Fletcher et al.(1988) also found that, in general, size of conidia,conidiophores and foot-cells varied little on alternativehosts, except that powdery mildew from tomatoinoculated onto Petunia hybrida and Nicotiana tabacum



resulted in the production of long chains of conidia. Noexplanation is available for the difference in conidialproduction on petunia and tobacco in this study incomparison with Fletcher et al. (1988), unless perhapscontamination with another species occurred in theirstudy.

This work has highlighted considerable problems withthe identification and classification of this new tomatopathogen, and it is unclear from the host range studies ofdifferent UK workers and the disparate observations oftomatopowderymildewworldwide,whether the Erysiphesp. occurring on tomato is always the same organism. Amolecular approach, which has proven invaluable forresolving similar problems in other host–pathogenrelationships (e.g. Zimand et al., 1994; Matthew et al.,1995; Bowen et al., 1996; Parry & Nicholson, 1996),may well be the way forward for this situation.

Potentially, the polyphagous nature of the tomatopowdery mildew presents a risk to the UK horticultureand agriculture industry. Although many of the testplants infected were garden plants, hot-house plants orherbs, the large number of commercially grown mem-bers of the Cucurbitaceae and Solanaceae that weresusceptible is worrying, particularly with the routinetransfer of seedlings around the country and fromabroad. Currently, no resistant cultivars of tomato areavailable, and although specific off-label approval forbupirimate, fenamirol and sulphur is available forcontrol of powdery mildew on tomato, the potentialfor continual reinfection from conidia derived fromvolunteer plants (Caffier et al., 1996) or plants grown byamateurs must be considerable. It may also go some wayto explaining the rapid spread of this disease worldwide.Nevertheless, the fact that powdery mildew was neverrecovered from 120 samples of potato leaves taken overa two-year period throughout the UK, includingcultivars Cara and Maris Piper on which the tomatopowdery mildew could sporulate in the glasshouse,suggests that environmental factors may play a key rolein preventing establishment of this powdery mildew onalternative hosts in the field. The preliminary studies onenvironmental factors affecting germination alreadycarried out on this pathogen (Fletcher et al., 1988;Foster, 1992) need to be expanded to consider infectionand spread of this pathogen as well.

Acknowledgements

We thank the Ministry of Agriculture, Fisheries andFood (MAFF) and the Biological and BiotechnologySciences Research Council for financial support, andDr Ian Pascoe for many helpful discussions. We alsothank Peter Atkey for help with electron microscopy.

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Characteristics and host range of tomato powdery mildew

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