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BOITEUX, L. S.

PAZ-LIMA, M.

REIS, A.

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Summa Phytopathol., Botucatu, v. 33, n. 4, p. 405-408, 2007 405Powdery mildew of ornamental species caused by Oidiopsis haplophylli  in BrazilAilton Reis1,3; Leonardo Silva Boiteux1,3 & Milton Luiz Paz-Lima21Embrapa Hortaliças, Centro Nacional de Pesquisa de Hortaliças (CNPH), CP 218, 70359-970, Brasília-DF; 2Universidade de Brasília, CampusDarcy Ribeiro, Departamento de Fitopatologia, CP 4457, 70910-900, Brasília-DF, Brazil; 3CNPq (MCT) Fellowship. E-mail:ailton@cnph.embrapa.brData da chegada: 18/01/2006. Aceito para publicação em: 17/04/2007.        1309ABSTRACTOidiopsis haplophylli (syn. Oidiopsis sicula) was identified as thecausal agent of powdery mildew diseases occurring on five ornamentalspecies in Brazil. This disease was observed in plastic house-grownlisianthus (Eustoma grandiflorum:  Gentianaceae), in nasturtium(Tropaeolum majus: Tropaeolaceae) cultivated under open fieldcondit ions and in greenhouse-grown calla l i ly (Zantedeschiaaethiopica :  Araceae),  impatiens (Impatiens balsamina :Balsaminaceae) and balloon plant (Asclepias physocarpa :Asclepiadaceae). Typical disease symptoms consisted of chloroticareas on the upper leaf surface corresponding to a fungal colony inthe abaxial surface. With the disease progression, these chloroticareas eventually turned to necrotic (brown) lesions. Fungi morphologyon all hosts was similar to that described for the imperfect stage ofReis, A.; Boiteux, L. S. & Paz-Lima, M. L. Powdery mildew of ornamental species caused by Oidiopsis haplophylli  in Brazil. SummaPhytopathologica, v.33, n.4, p.405-408, 2007.RESUMOO fungo Oidiopsis haplophylli (= O. sicula) foi identificado comosendo o agente causal de uma nova doença do tipo oídio em beijo-de-frade (Impatiens balsamina: Balsaminaceae), capuchinha (Tropaeolummajus :  Tropaeolaceae), copo-de-leite (Zantedeschia aethiopica :Araceae), lisianthus (Eustoma grandiflorum: Gentianaceae) e flor-borboleta (Asclepias physocarpa: Asclepiadaceae) em Brasília-DF,Brasil. Esta doença foi observada em condições de casa de vegetaçãoem beijo-de-frade, copo-de-leite, lisianthus e flor-borboleta e emcondições de campo na capuchinha. O sintoma típico é o aparecimentode uma área clorótica na superfície superior da lâmina foliar quecorresponde a uma colônia fúngica na superfície inferior. Com oprogresso da doença,  estas lesões tornavam-se necróticas eReis, A.; Boiteux, L. S. & Paz-Lima, M. L. Oídio em plantas ornamentais, causado por Oidiopsis haplophylli, no Brasil. Summa Phytopathologica,v.33, n.4, p.405-408, 2007.Palavras-chave adicionais: etiologia, Leveillula taurica, lisianthus, copo-de-leite, capuchinha, impatiens, Asclepias physocarpa.Leveillula taurica  (O. haplophylli). The Koch’s postulates werefulfilled by inoculating symptom-free plants via leaf-to-leaf contactwith fungal colonies. Additional inoculations using an isolate of O.haplophylli from sweet pepper (Capsicum annuum) demonstratedthat it is pathogenic to all five species belonging to distinct botanicalfamilies, indicating lack of host specialization. This is the first formalreport of a powdery mildew disease on lisianthus, calla lilly, impatiensand nasturtium in Brazil. It is, to our knowledge, the first report of O.haplophyllii infecting A. physocarpa, extending the host range ofthis atypical powdery mildew-inducing fungus. This disease mightbecome important on these ornamental crops especially in protectedcultivation and also under field conditions in hot and dry areas ofBrazil.Additional Keywords:  etiology, Leveillula taurica, lisianthus, calla lily, nasturtium, impatiens, Asclepias physocarpa.eventualmente coalesciam. As características morfológicas, observadasem microscopia de luz, corresponderam àquelas descritas para a faseimperfeita do fungo Leveillula taurica (O. haplophylli). Os testes depatogenicidade foram completados via inoculação por contato entrefolhas sadias e folhas apresentado colônias do fungo. Um isolado depimentão foi também patogênico a estas cinco espécies ornamentais(pertencentes a diferentes famílias botânicas) confirmando a ausênciade especialização por hospedeiro deste fungo. Este é o primeiro registrodeste patógeno nestas espécies ornamentais no Brasil  e,provavelmente, o primeiro relato de flor-borboleta como hospedeira.Este oídio pode se tornar importante para o cultivo destas espéciesem cultivo protegido ou condições de clima quente e seco.Ornamental pot plants and flowers (for both exporting andinternal markets) are among the fastest growing agribusinesssegments in Brazil. In the first half of 2005, total exports of thissector reached US$ 14 millions with an expansion of 19.5%compared to the same period of the year 2004. In Brazil, due to thelarge number of microclimate conditions, many ornamental plantspecies can be cultivated throughout the year. In addition, manyornamental plants are now being cultivated under greenhouse andplastic house. Cultivation under open field conditions using drip-irrigation is also increasing in the Northeast and Central Brazil,especially during the hot, dry season. In these circumstances, plantpathogens that are dependent upon high humidity and free waterfor infection and/or dissemination become minor problems. On theother hand, this novel cultivation system has favored a whole newset of pathogens that were not formerly reported as major diseasesin the country. One group of pathogens that became prevalentunder these conditions comprises fungi belonging to theErysiphaceae, which are able to induce powdery mildew diseases406 Summa Phytopathol., Botucatu, v. 33, n. 4, p. 405-408, 2007in many plant species. Oidiopsis haplophylli Rulamort (= Oidiopsissicula Scalia or Oidiopsis taurica Salmon) is one of the mosteconomically important fungal species reported infecting a widerange of vegetables and ornamental plants throughout the world(4, 9). In Brazil, powdery mildew outbreaks caused by O.haplophylli have been reported on processing tomatoes, fresh-market tomatoes and sweet peppers in several Brazilian States(3, 8, 11, 12, 13). The host range of O. haplophylli is expandingin the country with several new reports on distinct vegetableand ornamental hosts (10, 11, 13). Oidiopsis haplophylli hasnot been reported as seed-transmissible, therefore, it is morelikely that this fungus was introduced in Brazil via infectedornamental pot plants (11).In recent years, novel powdery mildew diseases have beenobserved affecting a range of ornamental species in distinct growingregions in Brasília (Federal District, Brazil). Powdery mildewdiseases were noticed on impatiens or touch-me-not (Impatiensbalsamina L.: Balsaminaceae), balloonplant [Asclepias physocarpa(E. Mey.) Schlechter: Asclepiadaceae] and white arum lily or callalily [Zantedeschia aethiopica (L.) Spreng.: Araceae] cultivated underglasshouse conditions. Plastic house Lisianthus [Eustomagrandiflorum (Raf.) (Shinners): Gentianaceae] in São Sebastião(Federal District) and open field-grown nasturtium (Tropaeolummajus L.: Tropaeolaceae) in Ponte Alta (Federal District) werealso found to be affected by a new powdery mildew disease. In thepresent work, we report that all diseases were caused by a singleagent, O. haplophylli.Leaf samples of impatiens, balloon plant and calla lily collectedin a glasshouse in Brasília (Federal District) showed diseasesymptoms characterized by yellow spots on upper surface of leavescorresponding to the establishment of a fungal colony in the abaxialsurface. As disease progressed the yellow spots developed a lightbrown color. Similar symptoms were also observed in leaf samplesof field-grown nasturtium in Gama (Federal District). Lisianthusplants collected in São Sebastião (Federal District) displayed similarsymptoms (Figure 1A-C).The affected areas were visualized under stereomicroscope,symptomatic leaf sections were removed and the fungal structureswere visualized in microscope slides prepared by mounting thinhost tissue slices in lactophenol. Measurements of length and widthwere done using 50 primary and 50 secondary conidia that werecollected from each host described in the present investigation.Other morphological aspects of the fungal structures associatedwith the imperfect stages of powdery mildew fungi (2, 4, 9) wereobserved including color of conidia, vacuoles and type ofgermination tube. Pathogenicity tests were performed by inoculatingsymptom-free plants via leaf-to-leaf contact with fungal colonies.A group of test plants was separately inoculated with each of theFigure 1.  Symptoms ofpowdery mildew, caused byOidiopsis haplophylli, inornamental species:  A =nasturtium, B = balloonplant, C = lisianthus and D= structures of theimperfect state of O.haplophylli (pc = primaryconidium, sc = secondaryconidium and cd =conidiophores). Arrows areindicating necrotic lesionsinduced by the fungus.A BCDcdpcSCSumma Phytopathol., Botucatu, v. 33, n. 4, p. 405-408, 2007 407five isolates obtained from each host and also with one isolatefrom pepper.Observations on the light microscope revealed that myceliumis predominantly endophytic with the presence of conidiophoresemerging through leaf stomata. Some conidiophores were dividedinto two to three branches. Ellipsoidal, light pale conidiospores(conidia) were borne predominantly single and terminally on theconidiogenic cell. The main light microscopy and host rangediagnostic characters of O. haplophylli were in complete agreementwith that described by Braun (4) and Palti (9): large primary conidiawith lanceolate shape and secondary conidia with a cylindricalshape (Figure 1D), presence of endophytic mycelicum and not-lobed appressorium. The presence of the sexual stage (Leveillulataurica) was not observed in the leaf samples of any host plantthroughout this investigation.The length and diameter measurements taken from primaryand secondary conidia of the impatiens, balloon plant, calla lilyand nasturtium isolates as well as the standard O. haplophylli isolatefrom sweet pepper (Capsicum annuum L.) cv. Ikeda are shown inTable 1. All morphometrical characteristics (including their ranges)are in agreement with the ones reported in the literature for O.haplophylli (2, 4, 9).Koch’s postulates were fulfilled for all five ornamental species.The host range studies indicated that O. haplophylli isolate fromsweet pepper is also virulent on these five ornamental plants,belonging to five distinct botanical families. Therefore, there wasno clear indication of host specialization of these isolates. Thissuggests that sweet pepper could be a potential source of inoculumof O. haplophylli once there is a large amount of fields of thisvegetable crop in Federal District area. Furthermore, plants ofimpatiens, balloon plant and calla lily, infected by this funguswere initially collected in a glasshouse with sweet pepper plantspresenting powdery mildew symptoms. This promiscuous hostrange clearly indicates that these ornamental plant species mightserve as alternative hosts of both tomato and sweet pepperpowdery mildews.Severe outbreaks of powdery mildew on sweet pepper andtomato caused by O. haplophylli were  initially restricted to plastichouse conditions in Brazil. This powdery mildew disease is noweconomically important for tomato and sweet pepper under bothplastic house and open-field conditions (8, 11, 13). This is thefirst formal report of a powdery mildew disease on lisianthus,greenhouse calla lilly, I. balsamina, A. physocarpa and nasturtiumin Brazil. Powdery mildew caused by O. haplophylli was alreadyreported elsewhere for lisianthus (5, 6), greenhouse calla lily (7,14), I. balsamina (9) and nasturtium (1). However, to ourknowledge, it is the first report of O. haplophyllii infecting A.physocarpa, extending the host range of this powdery mildew-inducing fungus. These hosts belong to five botanical families,which is in agreement with the current notion that O. haplophylli isan atypical powdery mildew since it has a wide host range usuallynot observed for obligate parasites of the Erysiphaceae family (4,9, 10, 11).These powdery mildew diseases might become important on theseornamental crops especially in protected cultivation and under fieldconditions in hot and dry areas such as those in the Central andNortheast regions of Brazil. The wide host range of O. haplophyllicould have important epidemiological implications when establishingdisease control strategies for these ornamental crops.LITERATURE CITED1. Besri, M.; Hormattallah, A. Manifestation et mode de conserva-tion de Leveillula taurica, agent de l’oidium de la tomate au Ma-roc. Phytopathologische Zeitschrift, Berlin, v.112, n.4, p.348-354, 1985.2. Boesewinkel, H.J. The morphology of the imperfect states ofpowdery mildews (Erysiphaceae). The Botanical Review, NewYork, v. 46, p.167-224, 1980.3. Boiteux, L.S.; Santos, J.R.M.; Lopes, C.A. First record of pow-dery mildew of sweet-pepper (Capsicum annuum) incited by Le-veillula taurica  in Brazil. Fitopatologia Brasileira, Brasília,v.19, supl., p.304, 1994.4. Braun, U.  A monograph of the Erysiphales (powdery mildews).Nova Hedwigia, Stuttgart, v.89, p.1-700, 1987.5. Garibaldi, A.; Rapetti, S.; Aloi, C.; Gullino, M.L.; Bozzano, G.Malattie delle piante da fiore ornamentali recentemente osserva-te in Italia. Informatore Fitopatologico, Turim, v.40, n.5, p.9-15, 1990.6. Koike, S.T.; Tjosvold, A.S.; Greene, I.D. Powdery mildew of Eus-toma caused by Leveillula taurica in California. Plant Disease,St. Paul, v.79, n.4, p.426, 1995.7. Koike, S.T.; Beckman, P. Characterization of powdery mildewcaused by Leveillula taurica on calla lily in California. PlantDisease, St. Paul, v.86, n.2, p.187, 2002.8. 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.  Fungosem Plantas no Brasil. Brasília; Embrapa, 1998. 555p.9. Palti, J. The Leveillula Mildews. The Botanical Review, NewYork, v. 54, n.4, p.423-535, 1988.10. Reis, A., Boiteux, L.S., Paz-Lima, M.L., Silva, P.P., Lopes, C.A. Pow-dery mildew of Allium species caused by Oidiopsis taurica in Brazil.Horticultura Brasileira, Brasília, v.22, n.4, p.758-760, 2004.11. Reis, A.; Boiteux, L.S.; Henz, G.P.; Lopes, C.A. Oidiopsis haplo-phylli (Leveillula taurica):  um patógeno polífago e amplamente*Length and diameter, measured in µm.  **Standard host plant.HostImpatiensNasturtiumCalla lilyLisianthusBalloon plantSweet pepper**Range57.6-68.2 x 16.3-21.149.0-71.0 x 15.0-18.051.7-73,2 x 14.2-18.954.2-71.4 x 13,6-18.551.2-71.1 x 14.3-18.359.6-74.4 x 14.3-19.1Average62.8 x 19.060.0 x 16.558.5 x 15.460.1 x 15.758.2 x 15.362.4 x 15.2Range52.8-70.1 x 11.5-21.144.0-64.0 x 11.0-23.055.3-69.0 x 15.6-17.954.5-70.6 x 13.8-18.756.0-68.8 x 14.7-17.857.2-71.1 x 13.7-18.9Average59.6 x 17.156.6 x 16.256.8 x 15.458.9 x 15.256.5 x 14.862.1 x 14.9Primary Conidia*Secondary conidia*Table 1. Length and diameter of primary and secondary conidia of Oidiopsis haplophylli obtained from impatiens (Impatiens balsamina: Balsaminaceae),nasturtium (Tropaeolum majus: Tropaeolaceae) calla lily (Zantedeschia aethiopica: Araceae), lisianthus (Eustoma grandiflorum: Gentianaceae), balloonplant(Asclepias physocarpa: Asclepiadaceae), and sweet pepper (Capsicum annuum).408 Summa Phytopathol., Botucatu, v. 33, n. 4, p. 405-408, 2007distribuído no Brasil. Comunicado Técnico, Embrapa Hortali-ças, Brasília, n. 26, 2005. 13p.12. Santos, J.R.M.; Boiteux L.S. Ocorrência de oídio (Leveillula tau-rica e Erysiphe cichoracearum) em tomateiro no Distrito Fede-ral. Fitopatologia Brasileira, Brasília, v.19, supl., p.313, 1994.13. Souza, V.L.; Café Filho, A.C.  Resistance to Leveillula taurica inthe genus Capsicum .  Plant Pathology, London, v.52. p.613-619, 2003.14. YuhKun, C., ChingChung, C. LungChung, C. Occurrence of pow-dery mildew on golden calla lily in Taiwan. Annals of the Phyto-pathological Society of Japan , Tokyo, v.62, n.6, p.580-583,1996.

Powdery mildew of ornamental species caused by Oidiopsis haplophylli in Brasil.

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Powdery mildew of ornamental species caused by Oidiopsis haplophylli in Brasil.

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