Preformed Antimicrobial Compounds and Plant Defense against Fungal Attack.

Plants produce a diverse array of secondary metabolites, many of which have antifungal activity. Some of these compounds are constitutive, existing in healthy plants in their biologically active forms. Others, such as cyanogenic glycosides and glucosinolates, occur as inactive precursors and are activated in response to tissue damage or pathogen attack. This activation often involves plant enzymes, which are released as a result of breakdown in cell integrity. Compounds belonging to the latter category are still regarded as constitutive because they are immediately derived from preexisting constituents (Mansfield, 1983). VanEtten et al. (i994) have proposed the term “phytoanticipin” to distinguish these preformed antimicrobial compounds from phytoalexins, which are synthesized from remote precursors in response to pathogen attack, probably as a result of de novo synthesis of enzymes. In recent years, studies of plant disease resistance mechanisms have tended to focus on phytoalexin biosynthesis and other active responses triggered after pathogen attack (Hammond-Kosack and Jones, 1996, in this issue). In contrast, preformed inhibitory compounds have received relatively little attention, despite the fact that these plant antibiotics are likely to represent one of the first chemical barriers to potential pathogens. The distribution of preformed inhibitors within plants is often tissue specific (e.g., Price et ai., 1987; Poulton, 1988; Davis, 1991; Fenwick et ai., 1992; Bennett and Wallsgrove, 1994), and r there is a tendency for these compounds to be concentrated in the outer cell layers of plant organs, suggesting that they may indeed act as deterrents to pathogens and pests. Some diffusible preformed inhibitors, such as catechol and protocatechuic acid (which are found in onion scales), may influence fungal growth at the plant surface. In general, however, preformed antifungal compounds are commonly sequestered in vacuoles or organelles in healthy plants. Therefore, the concentrations that are encountered by an invading fungus will depend on the extent to which that fungus causes tissue damage. Biotrophs may avoid the release of preformed inhibitors by minimizing damage to the host, whereas necrotrophs are likely to cause substantial release of these compounds. The nature and leve1 of preformed inhibitors to which a potential pathogen is exposed will also vary, depending on factors such as host genotype, age, and environmental conditions (Price et ai., 1987; Davis, 1991). There have been numerous attempts to associate natural variation in levels of preformed inhibitors in plants with resistance to particular pathogens, but often these attempts have failed to reveal any positive correlation. However, whereas preformed inhibitors may be effective against a broad spectrum of potential pathogens, successful pathogens are likely to be able to circumvent the effects of these antibiotics either by avoiding them altogether or by tolerating or detoxifying them (Schonbeck and Schlosser, 1976; Fry and Myers, 1981; Bennett and Wallsgrove, 1994; VanEtten et al., 1995; Osbourn, 1996). The isolation of plant mutants defective in the biosynthesis of preformed inhibitors would allow a direct genetic test of the importance of these compounds in plant defense. However, in most cases this approach is technically difficult because of the problems associated with screening for lossof the compounds. In the absence of plant mutants, a complementary approach involving the study of fungal mechanisms of resistance to preformed inhibitors, and of the contribution of this resistance to fungal pathogenicity to the relevant host plants, offers another route toward investigating the importance of these inhibitors in plant defense. A large number of constitutive plant compounds have been reported to have antifungal activity. Well-known examples include phenols and phenolic glycosides, unsaturated lactones, sulphur compounds, saponins, cyanogenic glycosides, and glucosinolates (reviewed in Ingham, 1973; Schonbeck and Schlosser, 1976; Fry and Myers, 1981; Mansfield, 1983; Ku6, 1992; Bennett and Wallsgrove, 1994; Grayer and Harborne, 1994; Osbourn, 1996). More recently, 5-alkylated resorcinols and dienes have been associated with disease resistance, in this case, resistance of subtropical fruits to infection by Collefotrichum gloeosporioides (Prusky and Keen, 1993). However, only a few classes of preformed inhibitor have been studied in detail to determine their possible roles in plant defense against fungal pathogens. This review focuses on three of these classes-saponins, cyanogenic glycosides, and glucosinolates-and summarizes our current knowledge of the role of these preformed inhibitors in determining the outcome of encounters between plants and phytopathogenic fungi.