BOITEUX, L. S.

LOPES, C. A.

PAZ-LIMA, M. L.

REIS, A.

SILVA, P. P.

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New host of Oidiopsis haplophylli in the solanaceae family in Brazil.

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New hosts of Oidiopsis haplophylli in the SolanaceaeFamily in BrazilAilton Reis1, Leonardo S. Boiteux1*, Milton L. Paz-Lima2, Patrícia P. Silva1 & Carlos A. Lopes11Embrapa Hortaliças, Cx. Postal 218, CEP 70359-970, Brasília, DF, Brazil, e-mail: boiteux@cnph.embrapa.br;2Universidade de Brasília, Depto. Fitopatologia, Cx. Postal 4457, CEP 70910-900, Brasília, DF(Accepted for publication in 12/11/2004)Corresponding author: Leonardo S. BoiteuxMany field and vegetable crops of economic importanceare members of the Solanaceae family including tobacco(Nicotiana spp.), tomato (Lycopersicon esculentum Mill.),sweet pepper (Capsicum annuum L.), potato (Solanumtuberosum L.), eggplant (S. melongena L.) and gilo (S. giloRaddi). The genomes of the plant species within the Solanaceaefamily are highly conserved in relation to chromosome number,gene order, and gene repertoire (Doganlar et al. 2002).Therefore, it is not surprising that a number of commondiseases occur in species of this family caused by the samevirus, bacteria, nematodes or fungi (Zambolim et al. 2000).Oidiopsis haplophylli Rulamort (syn. O. sicula Scaliaor O. taurica Salmon), is an unusually polyphagous powderymildew-causing fungus able to infect a broad range ofherbaceous plants in different taxa, including several generaand species within the Solanaceae (Palti, 1988; Cook et al.1997; Mendes et al. 1998). Infection by O. haplophylli maycause economic losses to tomato and sweet pepper during theREIS, A., BOITEUX L.S., PAZ-LIMA, M.L., SILVA, P.P. & LOPES, C.A. New hosts of Oidiopsis haplophylli in the Solanaceaefamily in Brazil. Fitopatologia Brasileira 30:195-198. 2005.ABSTRACTA powdery mildew disease was observed on leaves of Solanum gilo, S. melongena, S. tuberosum S. chacoense,Nicotiana rustica and N. tabacum in Brasília (Federal District), Brazil. Symptoms were mainly characterized by adaxialyellow areas in the leaves corresponding to white fungal colonies on the abaxial surface. Profuse sporulation was oftenobserved. Light microscopy of the fungal colonies revealed the presence of conidiophores emerging through stomata withsome having two or three branches. Ellipsoidal, subhyaline conidia were predominantly  born singly and terminally on theconidiophore. All morphometrical characteristics agreed with those of Oidiopsis haplophylli (Syn. O. sicula). The teleomorph(Leveillula taurica) was not observed. Inoculation tests indicated that O. haplophylli isolates obtained from S. gilo, S.melongena, S. tuberosum, S. chacoense, Nicotiana rustica and N. tabacum were also pathogenic to sweet pepper (Capsicumannuum) and tomato (Lycopersicon esculentum). This is apparently the first report of these Solanaceae species as hosts of O.haplophylli in Brazil. This disease may become important in these crops, especially in greenhouses, and in hot and dry areaswhere drip irrigation is employed.Additional keywords: etiology, Solanum gilo, S. melongena, S. tuberosum, S. chacoense, Nicotiana tabacum, N.rustica, powdery mildew, Leveillula taurica.RESUMONovas solanáceas hospedeiras de Oidiopsis haplophylli no BrasilA ocorrência natural de oídio foi observada em plantas de jiló (Solanum gilo), berinjela (S. melongena), batata (S.tuberosum), batata silvestre (S. chacoense) e em duas espécies de fumo (Nicotiana rustica e N. tabacum) em Brasília, DistritoFederal. Os sintomas iniciais da doença incluíam manchas amarelas na face superior do limbo foliar correspondendo a colôniasfúngicas, esbranquiçadas com abundante produção de conídios, na superfície inferior. Com o desenvolvimento da doença, asmanchas amarelas passaram a necróticas com coloração marrom clara. Observações em lupa revelaram a presença de conidióforosemergindo através dos estômatos e alguns apresentavam duas a três ramificações. Conídios hialinos e com evidente dimorfismoforam observados, sendo os conídios primários de formato lanceolado e os secundários subcilindricos. As característicasmorfológicas e morfométricas dos dois tipos de conídios apresentaram um padrão similar àqueles descritos para Oidiopsishaplophylli. A forma perfeita do fungo (Leveillula taurica) não foi encontrada em nenhuma das hospedeiras examinadas. Esteé o primeiro relato destas seis espécies de solanáceas como hospedeiras naturais de O. haplophylli no Brasil. Inoculaçõescontroladas empregando os isolados de O. haplophylli obtidos destas hospedeiras indicaram que estes são também patogênicosao pimentão (Capsicum annuum) e tomate (Lycopersicon esculentum). Esta doença pode se tornar um problema para estasnovas hospedeiras especialmente em condições de cultivo protegido ou em áreas de clima seco com irrigação localizada viagotejamento.Palavras-chave adicionais: etiologia, oídio, Leveillula taurica, Oidiopsis sicula, Solanum gilo, S. melongena, S.tuberosum, Nicotiana rustica, N. tabacum.195Fitopatol. bras. 30(2), mar - abr 2005A. Reis et al.196 Fitopatol. bras. 30(2), mar - abr 2005FIG. 1 - Powdery mildew symptoms caused by Oidiopsis haplophylli isolates on eggplant (Solanum melongena), (A); Nicotianarustica (B); and potato (S. tuberosum) (C); morphological aspects of primary (a) and secondary (b) conidia of O. haplophylliobtained from infected gilo (S. gilo) leaves (D) and conidiophore with a terminal primary conidium (E).dry season in open-field plantings and during the entireyear under greenhouse and/or plastic house conditions.Currently,  powdery mildew (PM) caused by O. haplophylliis one of the most important fungal diseases affecting tomatoand sweet pepper under plastic cultivation in Central Brazil(Café Filho et al. 2001).Complexes of greenhouses for large-scale commercialproduction of transplants are now increasing in number andin economic importance in Brazil. A number of distinct speciesare cultivated in these large contiguous areas. It is commonto observe styrofoam trays (used for initial plant cultivation)with seedlings of distinct vegetable species in either the sameor in adjacent insect-proof greenhouses. The O. haplophyllispores are not trapped in the nets used in these seedlingproducing greenhouses and a relatively large number of plantspecies naturally affected by this disease has been observedin greenhouses located in Brasília (Distrito Federal). The PMsymptoms in those plants were mainly characterized by yellowspots on the upper leaf surface corresponding to fungalcolonies in the abaxial surface with profuse sporulation. Thesesymptoms were very similar to those formerly described asbeing caused by O. haplophylli in tomato and sweet pepper(Boiteux et al. 1994; Santos & Boiteux, 1994; Liberato et al.1998; 2000). However, similar PM symptoms were observedin several plant species previously not described as being hostsof O. haplophylli in Brazil. In this work, we describe for thefirst time, the occurrence of PM on six species of two generain the family Solanaceae, and provide the identification ofthe causal agent.Greenhouse-grown seedlings of potato, wild potato (S.chacoense Bitter) eggplant, gilo and two tobacco species (N.tabacum L. and N. rustica L.) were observed exhibiting typicalPM symptoms (Figure 1- A to C). Eggplant and gilo leaveswith PM symptoms were also found in experimental fields ofEmbrapa Hortaliças in Brasilia. Light microscopy of thefungal colonies on all these hosts revealed the presence ofconidiophores emerging through leaf stomata. Someconidiophores were divided into two to three branches.Ellipsoidal, light-pale conidia were predominantly bornesingly and terminally on the conidiophores (Figure 1-E). Themajor light microscopy and host range characteristics werein complete agreement with an O. haplophylli-induced PMdisease as described in the synoptic table elaborated by Cooket al. (1997) including: large size lanceolate shaped primaryconidia and secondary conidia with a somewhat cylindricalshape (Figure 1-D), absence of fibrosin bodies, conidia formedsingly (not in chains), presence of only endophytic mycelium,appressoria not lobed and able to infect a large number ofherbaceous hosts. Sexual stage [Leveillula taurica (Lev)Arnald] was not observed in any host plant throughout thepresent investigation.Measurements of length and diameter were performedusing 30 primary conidia and 30 secondary conidia (chosenrandomly) collected from each host described in thisNew hosts of Oidiopsis haplophylli in the Solanaceae family in Brazil197Fitopatol. bras. 30(2), mar - abr 2005LITERATURE CITEDBOESEWINKEL H.J. The morphology of the imperfect states ofpowdery mildews (Erysiphaceae). The Botanical Review 46:167-224. 1980.BOITEUX, L.S. Powdery mildew of potato caused by Erysiphecichoracearum in Brazil. Plant Disease 78:830. 1994. (Note)BOITEUX, L.S., SANTOS, J.R.M. & LOPES, C.A. First record ofpowdery mildew of sweet-pepper (Capsicum annuum) incited byLeveillula taurica in Brazil. Fitopatologia Brasileira 19:304. 1994.(Resumo)BRAUN, U. A monograph of the Erysiphales (powdery mildews).Nova Hedwigia. 89:1-700. 1987.CAFÉ FILHO, A.C., COELHO, M.V.S. & SOUZA, V.L. Oídios deHortaliças. In: Stadnik, M.J. & Rivera, M.C. (Eds.) Oídios.Jaguariúna: Embrapa Meio Ambiente, 2001. Cap. 11, pp.285-302.COOK R.T.A., INMAN A.J. & BILLINGS C. Identification andclassification of powdery mildew anamorphs using light and scanningelectron microscopy and host range data. Mycological Research101:975-1002. 1997.DOGANLAR, S., FRARY, A., DUANAY, M-C., LESTER, R.N. &TANKSLEY, S.D. A comparative genetic linkage map of eggplant(Solanum melongena) and its implications for genome evolution inthe Solanaceae. Genetics 161:1697-1711. 2002.LIBERATO, J.R. LOURO, R.P., SUZUKI, M.S. & BARRETO, R.W.Ocorrência de oídio do tomateiro causado por Oidiopsis no Estadodo Rio de Janeiro. Fitopatologia Brasileira 23:81. 1998. (Abstract)TABLE 1 - Length and diameter of primary and secondary conidia of Oidiopsis haplophylli from seven hosts of the Solanaceae family*Length and diameter, measured in µmPrimary Conidia* Secondary conidia*HostRange Average Range AverageS. melongena 36,0 -78,5 x 9,5 -21,4 66,3 x 15,8 31,8 -68,5 x 8,7 -17,9 65,0 x 15,8S. gilo 54,4 -71,2 x 12,6 -18,9 66,9 x 15,3 53,7 -71,6 x 13,1 -19,2 64,1 x 15,8S. tuberosum 60,6 -77,5 x 13,5 -19,6 67,2 x 15,5 55,6 -71,9 x 13,3 -19,5 64,1 x 15,8Solanum chacoense 59,6 -76,6 x 13,8 -19,5 67,1 x 14,9 56,8 -70,3 x 13,8 -18,7 65,1 x 15,2N. tabacum 54,1 -71,0 x 12,8 -18,2 65,3 x 16,2 53,8 -71,7 x 13,7 -19,3 63,2 x 15,7Nicotiana rustica 49,8 -73,1 x 14,3 -20,5 60,1 x 16,2 55,9 -71,3 x 15,0 -17,9 64,8 x 15,7Capsicun annuun (standard) 60,5 -76,4 x 13,7 -19,4 67,0 x 15,6 58,4 -71,2 x 13,3 -19,6 65,4 x 15,8investigation plus one O. haplophylli isolate of sweetpepper employed as standard (Table 1). Primary andsecondary conidia of the potato isolate were on average of67.2 µm long x 15.5 µm diameter and 64.0 µm x 15.8 µm,respectively, whereas the isolates from eggplant were onaverage 66.3 µm x 15.8 µm and 65.0 µm x 15.8 µm,respectively. The size of primary and secondary conidia fromgilo were very close to that of potato and eggplant, 66.9 µmlong x 15.3 µm diameter and [64.1 µm x 15.8 µm] and alsovery similar to that of S. chacoense, 67.1 µm long x 14.9µm diameter and 65.1 µm x 15.2 µm, N. rustica [60.1 x16.2] and [64.8 x 15.7], and N. tabacum [65.3 x 16.2] and[63.2 x 15.7]. The measurements taken from primary andsecondary conidia of the original O. haplophylli isolate fromsweet pepper cv. Margarita were in the following range: [67.0µm long x 15.6 µm diameter] and [65.4 µm x 15.8 µm],respectively. All these morphometrical characteristics werein the range reported for O. haplophylli (Yarwood, 1978;Boesewinkel, 1980; Braun, 1987; Cook et al., 1997; Liberatoet al., 1998 and 2000).Host range studies were conducted by inoculatingplants either via dusting dry conidia or by leaf-to-leaf contact.The inoculum was obtained from each new host andindividually placed on sweet pepper (‘Margarita’) and tomato(‘Santa Clara’) plants. Plants inoculated with each isolate werekept in separate growing chambers after inoculation. Thepresence of PM symptoms was assessed 15 days afterinoculation. The results confirmed that O. haplophylli isolatesfrom these new host species are pathogenic to sweet pepperand tomato. The pattern of symptom development was similarto that of O. haplophylli, characterized by chlorotic spots onthe upper leaf surface that gradually turned to light brownnecrotic lesions (Figure 1-A to C ).Our report confirms that O. haplophylli has an unusualhost range plasticity being able to infect a large number ofplant species from genetically unrelated plant taxa (Braun,1987; Mendes et al., 1998; Palti, 1988; Café Filho et al.,2001; Silva et al., 2003; Souza & Café Filho, 2003). Thehost range of O. haplophylli appears to be broadening in Brazilwithout any strong evidence of host specialization (Café Filhoet al., 2001; Paz Lima, et al. 2002; Silva et al., 2003; Souza& Café Filho, 2003). Previous work by Souza & Café Filho(2003) demonstrated that O. haplophylli could be pathogenicto gilo and egg plant when artificially inoculated. However,our report is apparently the first formal description of thesesolanaceous species as natural hosts of O. haplophylli inBrazil. On the other hand, this is not the first record of aPM disease on potato in Brazil. Erysiphe cichoracearumDe Candolle -like isolates have been previously reportedinfecting some S. tuberosum cultivars under greenhouseconditions (Boiteux, 1994). There is so far no report in theliterature describing N. tabacum and S. chacoense as hostsof O. haplophylli. These new PM diseases caused by O.haplophylli may become important to these solanaceous cropsespecially under plastic house cultivation and/or in hot anddry areas where drip irrigation is employed.A. Reis et al.198 Fitopatol. bras. 30(2), mar - abr 200504053LIBERATO, J.R. CUNHA, M., SUZUKI, M.S. & SILVEIRA, S.F.Ocorrência do oídio do pimentão causado por Oidiopsis sp. no Estadodo Espírito Santo. Fitopatologia Brasileira 25:110. 2000. (Abstract)MENDES, M.A.S., SILVA, V.L., DIANESE, J.C., FERREIRA,M.A.S.V., SANTOS, C.E.N., GOMES NETO, E., URBEN, A.F. &CASTRO, C. Fungos em plantas no Brasil. Brasília, Embrapa-SPI,Embrapa Cenargen, 1998.PALTI, J. The Leveillula mildews. The Botanical Review 54:423-535. 1988.PAZ LIMA, M.L., BOITEUX, L.S., REIS, A., COSTA, S.B. &LOPES, C.A. Alho porró: Hospedeiro de Oidiopsis taurica no Brasil.Fitopatologia Brasileira 27:S126. 2002. (Abstract)SANTOS, J.R.M.& BOITEUX L.S. Ocorrência de oídio (Leveillulataurica e Erysiphe cichoracearum) em tomateiro no Distrito Federal.Fitopatologia Brasileira 19:313. 1994. (Abstract)SILVA, P.P., LOPES, C.A., REIS, A., PAZ LIMA, M.L. &BOITEUX, L.S. Eryngium foetidum, Petroselinum crispum,Coriandrum sativum e Solanum tuberosum:Novas hospedeiras deOidiopsis taurica no Brasil. Fitopatologia Brasileira 28:S214.2003. (Abstract).SOUZA, V.L. & CAFÉ FILHO, A.C. Genetic resistance toLeveillula taurica in the genus Capsicum. Plant Pathology 52:613-619. 2003.YARWOOD, C.E. History and taxonomy. In: Spencer, D.M. (Eds.)The Powdery Mildews. London:Academic Press, 1978. Cap.1, pp.1-28.ZAMBOLIM, L., VALE, F.X.R. & COSTA, H. Controle de doençasde plantas: hortaliças. Viçosa:Universidade Federal de Viçosa, 2000.

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New host of Oidiopsis haplophylli in the solanaceae family in Brazil.

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