First record of anamorphic Leveillula taurica on Vasconcellea goudotiana (Caricaceae) in Brazil

Powdery mildew fungi (Erysiphaceae: Ascomycota) in the subfamily Phyllactinioideae have hemiendophytic (partly external and partly internal) mycelium (Braun 1987). The Phyllactinioideae contains the genera Phyllactinia Lév. (anamorph Ovulariopsis Pat. & Har.), Leveillula Arnaud (anamorph Oidiopsis Scalia), Pleochaeta Sacc. & Speg. (anamorphs Streptopodium R.Y. Zheng & G.Q. Chen emend. Liberato & R.W. Barreto) and the monotypic Queirozia Viégas & Cardoso emend. Liberato & R.W. Barreto (Zheng and Chen 1978; Braun 1987; Liberato et al. 2004, 2006).

The family Caricaceae contains five genera of plants, namely Carica L., Vasconcellea A. St.-Hil., Jacaratia A. DC., Jarilla Rusby and Cylicomorpha Urb. (Tropicos.org. Missouri Botanical Garden. 8 Nov. 2010, available at http://www.tropicos.org). Carica papaya L. (papaya, pawpaw) is the most important cultivated plant in this family and has been reported as host of four powdery mildew species belonging to the subfamily Phyllactinioideae, namely Ovulariopsis papayae Van der Byl in South Africa (van der Bijl 1921), Phyllactinia caricaefolia Viégas in Brazil (Viégas 1944), Oidiosis haplophylli (Magnus) Rulamort, which is the anamorph of Leveillula taurica (Lév.) G. Arnaud, in Australia, India and Portugal (Clare 1964; Simmonds 1965; Ullasa and Sohi 1978; Sequeira 1992; Liberato et al. 2004) and Streptopodium caricae Liberato & R.W. Barreto in Brazil (Liberato et al. 2004).

In Brazil, S. caricae and P. caricaefolia have been reported (Viégas 1944; Liberato et al. 2004). A specimen reported as L. taurica (Nogueira et al. 1997) was re-examined and identified as S. caricae (Liberato et al. 2004). A report of the occurrence of O. papayae (Ribeiro et al. 1988) cannot be confirmed as a specimen was not retained and deposited in a herbarium. Liberato et al. (2004) examined published pictures of the specimen and concluded that the fungus was probably S. caricae.

In November 2008, powdery mildew was observed on 1-year-old potted plants of Vasconcellea goudotiana Triana & Planch. growing under shade in Campos dos Goytacazes-RJ, Brazil. A fresh specimen was collected and examined in the Plant Pathology Laboratory of the North Fluminense State University. The origin of the conidiophores was determined by a technique commonly used for the examination of stomata, that is, a thin layer of clear nail varnish was painted onto the lower leaf surface, on areas with signs of the fungus and left drying for 10 min. A strip of transparent adhesive tape (sellotape) was placed over the dried varnish and light pressure applied for 1 min to obtain an imprint. The sellotape with varnish imprint was peeled off the leaf and mounted in lactoglycerol on a glass microscope slide (Ferris et al. 1996). The conidiophores were examined by light microscopy and found to originate from internal mycelium through the stomata, which is characteristic of the genus Oidiopsis. The specimen was identified as O. haplophylli and is described below.

Fig. 1.  Oidiopsis haplophylli on Vasconcellea goudotiana (Vic. 30735). (a, b) Hyphae (h) and conidiophores (c) arising from stomata (st); (c) primary (pc) and secondary conidia (sc); (d) primary lanceolate conidium.

Mycelium hypophyllous, hemiendophytic (partly external and partly internal), Superficial hyphae entering the leaves through stomata, branched, septate, hyaline, smooth. Conidiophores hypophyllous, produced from the internal mycelium, arising through the stomata, rarely branched, up to 227 μm long, cylindrical, hyaline, smooth. Conidia single, dimorphic: primary conidia lanceolate, apically pointed, base rounded, 61–85 × 12–22 μm, l/w ratio 3.0–5.4; secondary conidia subcylindrical to cylindrical with rounded ends, 49–73 × 12–20 μm, l/w ratio 2.8–5.2, aseptate, hyaline, smooth. Teleomorph: not found.

Material examined: Brazil: Rio de Janeiro: Campos dos Goytacazes, 12 Nov. 2008, M. Vivas (VIC 30735) on Vasconcellea goudotiana Triana & Planch. (≡Carica goudotiana (Triana & Planch.) Solms).

Morphological measurements corresponded to those given for L. taurica by Braun (1987) and Palti (1988). The primary conidium of Oidiopsis is apically pointed or lanceolate, whereas secondary conidia are usually ellipsoid to cylindrical with rounded to truncate apices. The conidiophores of Oidiopsis originated from the internal mycelium, emerging through the stomata, which is a unique characteristic among the powdery mildews (Braun 1987). This feature is well observed under scanning electron microscopy or using a leaf-clearing technique (Liberato et al. 2005) with a light microscope. The technique used in this study was considered very practical to determine the origin of the conidiophores.

Ullasa et al. (1983) observed infection on Vasconcellea cauliflora (Jacq.) A. DC., V. monoica (Desf.) A. DC., V. goudotiana (referred to as Carica cauliflora Jacq., C. monoica Desf. and C goudotiana, respectively), and C. papaya when 5-months old plants in the field were inoculated with L. taurica. In the same study, Vasconcellea quercifolia A. St.-Hil. (referred to as Carica quercifolia (A. St.-Hil.) Hieron.) was resistant, showing no symptoms. Franceschini et al. (1989) described the occurrence of anamorphic L. taurica on babaco (Vasconcellea × heilbornii (V.M. Badillo) V.M. Badillo (≡ Carica × heilbornii V.M. Badillo, = Carica pentagona Heilborn)) in greenhouses in Sardinia, Italy.

Oidiopsis haplophylli is a collective species with worldwide distribution and more than 1000 host plant species (Braun 1987; Palti 1988). In Brazil, it was first reported in 1987 (Kurozawa 1987) and since then it has driven the attention of many plant pathologists as it has gradually spread through many regions and hosts causing important diseases in pepper (Capsicum annuum L.) and tomato (Solanum lycopersicum L. = Lycopersicon esculentum Mill.) (Liberato et al. 1998, 2000), particularly in greenhouse crops (Café Filho et al. 2001). This is the first report of the occurrence of O. haplophylli on Caricaceae in Brazil.