Biocontrol of Powdery Mildews

Powdery mildew fungi are obligate parasites of plants that derive nutrients and water from their host, thereby reducing growth and yield through the acquisition of photosynthates. The fungi penetrate into the epidermis directly and establish a parasitic relationship with the plant host through the formation of haustoria, the nutrient-absorbing structures. Mycelial growth and sporulation occur on the surface of leaves and stems, resulting in a white fuzzy mildew appearance.

Over the years, powdery mildew diseases have been managed through the use of chemical fungicides and genetic resistance, but recent reports have highlighted the potential of biological control methods. Fungal and yeast biological control agents have been described which can reduce sporulation and growth of mildew pathogens, thereby minimizing their damaging effects to host plants. The fungal biocontrol agents are mostly mycoparasites, while the yeasts produce antibiotics and hydrolytic enzymes that cause the mildew hyphae and conidia to collapse and be rendered nonviable.

4.3.1 Fungi As Biological Control Agents of Powdery Mildews

Verticillium lecanii has been described as a mycoparasite of powdery mildew fungi as well as a pathogen of insects and it has been developed as a biocontrol agent of insects on greenhouse crops. Strains of V. lecanii differed in their level of antagonism against the powdery mildew pathogen of cucumber, Sphaerotheca fuliginea, under laboratory conditions (Askary et al. 1998). Application to cucumber leaves prior to mildew infection and incubation under high (> 95%) relative humidity conditions reduced mildew development (Verhaar et al. 1997). The high humidity requirement for growth of this mycoparasite was reduced by the addition of an oil formulation (Verhaar et al. 1999). Infection of S.fuliginea by V. lecanii resulted in disorganized cytoplasm and plasmalemma disruption, possibly due to chitinase enzyme activity (Askary et al. 1997).

Another mycoparasite, Ampelomyces quisqualis, has been extensively studied as a biocontrol agent of powdery mildew of cucumber. The mycoparasite infects the mildew pathogen and forms pycnidia in association with colonized mycelium, reducing growth and sporulation of the pathogen. Cells of the mycoparasite grow inside the mildew hyphae, gradually causing them to degenerate. High levels of b-1,3-glucanase activity were reported in A. quisqualis (Rotem et al. 1999) and exposure of mildew hyphae to the enzymes caused them to degrade.

A commercially available formulation of A. quisqualis AQ10 has been extensively evaluated against powdery mildew development. On cucumbers grown in the greenhouse, AQ10™ was very effective in reducing mildew development (Elad et al. 1998). On field-grown cucurbits, AQ10™ also suppressed mildew development and increased yield when compared to the nontreated plants (McGrath and Shishkoff 1999).

Molecular techniques have been used to characterize strains of A. quisqualis. The RFLP analysis of the nuclear rDNA ITS region and sequence analysis among a worldwide collection of isolates revealed considerable intraspecific variation (Kiss 1997; Kiss and Nakasone 1998). Isolates of the same genetic background were found in widely different areas and genetically different isolates could be found in a given area.

4.3.2 Yeasts As Biological Control Agents of Powdery Mildew

Pseudozyma (Sporothrix) flocculosa is a yeast-like fungus with demonstrated biocontrol activity against powdery

Biological Control Powdery Mildew

Figure 2 Effect of Tilletiopsis pallescens on development of powdery mildew (S. fuliginea) on cucumber leaves. (A) A mildew-infected leaf showing chains of conidia and mycelium. (B) A mildew colony treated with a 3-day-old liquid culture of T. pallescens. Note collapsed conidia and mycelium. Photograph was taken 2 days following treatment. (C) Spore masses of Tilletiopsis adjacent to mildew conidia. Note intact mildew conidia on left and collapsed condia on the right.

Figure 2 Effect of Tilletiopsis pallescens on development of powdery mildew (S. fuliginea) on cucumber leaves. (A) A mildew-infected leaf showing chains of conidia and mycelium. (B) A mildew colony treated with a 3-day-old liquid culture of T. pallescens. Note collapsed conidia and mycelium. Photograph was taken 2 days following treatment. (C) Spore masses of Tilletiopsis adjacent to mildew conidia. Note intact mildew conidia on left and collapsed condia on the right.

mildew fungi, especially on cucumber and rose (Belanger and Benyagoub 1997; Belanger et al. 1994). Cytochemical investigations have shown that the yeast induces a rapid collapse of mildew spores and hyphal cells (Hajlaoui et al. 1992). Extracellular fatty acids with antifungal properties were produced by P. flocculosa and reported to be the principle mode of action in biological activity against powdery mildew (Benyagoub et al. 1996), by disrupting the cytoplasmic membrane in a range of fungi (Avis and Belanger 2001). A fungicide-tolerant strain of the yeast was selected which could be used in conjunction with chemical control methods to reduce powdery mildew development (Benyagoub and Belanger 1995). In a comparative study of three biological control agents against powdery mildew of cucumber, i.e., V. lecanii, A. quisqualis, and P. flocculosa, it was shown that P. flocculosa gave the best disease control (Dik et al. 1998).

Molecular techniques have been used to characterize strains of Pseudozyma flocculosa (Avis et al. 2001b). Ribosomal DNA sequences and random amplified microsatellites were used to distinguish among different strains of this species and to develop isolate-specific markers to monitor spread and confirm genetic fidelity of the strains. A strain of P. flocculosa has been formulated and produced commercially under the name Sporodex™ for use in control of powdery mildew on a number of crops grown under greenhouse conditions.

Species of Tilletiopsis are saprophytic yeast-like fungi that occur as epiphytes on the leaf surface of various plant species and which have been demonstrated to have biological control activity against powdery mildew diseases (Hijwegen 1992; Knudsen and Skou 1993; Urquhart et al. 1994). Scanning electron microscopic studies have revealed that mildew hyphae and spores appeared collapsed after treatment with Tilletiopsis (Figure 2) (Urquhart and Punja 1997). It was postulated that extracellular antifungal compounds were involved in biocontrol activity that included fatty acid esters and hydrolytic enzymes (Urquhart and Punja 2002). Various species of Tilletiopsis have demonstrated biological control activity, including T. albescens, T. minor, T. pallescens, and T. washingtonensis (Table 2). These species could be distinguished using RAPD analysis of PCR-generated DNA with random primers (Urquhart et al. 1997). Intraspecific variation was also noted and DNA fingerprints were generated for some isolates that could be useful for monitoring the distribution and spread of certain isolates.

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