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Allelochemicals: Biological Control of Plant Pathogens and Diseases, 157-175. © 2006 Springer. Printed in the Netherlands.

They also cause haemolysis, though are generally non-toxic when taken orally. Saponins are broadly categorised as being either triterpenoid- or steroid-derived, despite the common triterpenoid origin of both. Triterpenoid saponins are widely distributed in many dicot families, and are generally based on pentacyclic triterpene parent carbon skeletons (e.g., a- and P-amyrin), or tetracyclic parent compounds (e.g., the dammaranes). By contrast, steroidal saponins are commonly found in monocots, and are characterised by a spiroketal moiety at C-22. Plants of the Solanaceae contain steroidal glycoalkaloid saponins, which are nitrogen analogues of steroidal saponins.

In general, saponins are glycosylated at the C-3 hydroxyl group, typically with a glucose molecule. However, there are other potential glycosylation sites on the parent carbon skeletons, and multi-site glycosylation can occur. Accordingly, saponins are subdivided into monodesmosidic (one glycosylation site) and bisdesmosidic (glycosylation sites at both ends of the compound) categories. The majority of saponins, however, are monodesmosidic. While glucose is the most common sugar in saponins, arabinose, galactose, rhamnose and xylose, as well as sugar acids are also present. The glycosylation patterns of saponins can lead to small families of compounds based on the same parental carbon skeleton (i.e., sapogenin or aglycone), differing only in the composition and arrangement of sugars.

2.2. Saponins as Fungitoxic and Plant Defense Compounds

There are numerous reports in the literature that describe the anti-fungal activity of saponins (Zimmer et al., 1967; Levy et al., 1986; 1989; Marston et al., 1988; Takechi and Tanaka, 1990; Ohtani et al., 1993; Ouf et al., 1994; Favel et al., 1994; Escalante et al., 2002; Nicol et al., 2002). These reports coupled with molecular data (Bowyer et al., 1995; Papadopoulou et al., 1999) suggest that these phytochemicals are constitutive plant defenses against fungi (Osbourn, 1996; 2003), that is phytoanticipins (Van Etten et al., 1994). For example, the role that the triterpenoid saponin avenacin A-1 plays in conferring resistance to "take-all disease", caused by Gaeumannomyces graminis in oats, is well established (Turner, 1956; Burkhardt et al., 1964; Maizel et al., 1964; Bowyer et al., 1995; Papadopoulou et al., 1999).

While the molecular mechanism of saponin fungitoxicity is not known, avenacin A-1 as well as steroidal glycoalkaloid saponins such as a-tomatine and solanine have been demonstrated to form complexes with membrane sterols, thereby causing a reduction in membrane integrity (Roddick, 1979; Steel and Drysdale, 1988; Keukens et al., 1992; 1995; Armah et al., 1999). Two models have been proposed to explain the consequences of saponin-sterol aggregation in target membranes (Morrissey and Osbourn, 1999). One suggests that the deleterious effects of saponins are related to the formation of transmembrane pores (Armah et al., 1999), whereas the other suggests that membrane integrity is compromised due to the extraction of sterols (Keukens et al., 1992; 1995). Regardless of the exact mechanism, saponins probably disrupts fungal membranes through complexation with ergosterol, the major membrane sterol in higher fungi (Evans and Gealt 1985; Weete 1989; Griffiths et al., 2003).

Saponins may act as host chemical defenses, but because fungi successfully attack plants containing these defenses, there must be means of tolerating or avoiding saponin toxicity. Fungal resistance to defensive chemicals in general can either involve enzymatic detoxification of antifungal compounds or the more ambiguous "innate resistance" (Morrissey and Osbourn, 1999). Some fungi are able to detoxify phytoalexins (Van Etten et al., 1995) as well as phytoanticipins such as saponins (Osbourn et al., 1995a; Van Etten et al., 1995; Weltring et al., 1997). Although saponin detoxification generally occurs via enzymatic cleavage of the saccharides to form the aglycone parent compound, different fungi employ different strategies and enzymes. For example, fungal detoxification of a-tomatine by Botrytis cinerea (Quidde et al., 1998) Septoria lycopersici (Arneson and Durbin, 1967) and Verticillium albo-atrum (Pegg and Woodward, 1986) involves cleavage of one terminal monosaccharide from the tetrasaccharide chain at carbon three of the sapogenin, whereas Fusarium oxysporum f. sp. lycopersici removes the entire tetrasaccharide (Ford et al., 1977). The saponin-detoxifying enzymes tomatinase from S. lycopersici and avenacinase from G. graminis exhibit high sequence similarity (Osbourn et al., 1995b), whereas the tomatinase from F. oxysporum f. sp. lycopersici appears to be more related to a different family of glycosyl hydrolases (Roldan-Arjona et al., 1999). The ability to efficiently detoxify host chemical defenses determines virulence and host range in fungal pathogens such as G. graminis, Rhizoctonia solani and Phoma lingam (Bowyer et al., 1995; Pedras et al., 2000a,b). Efficient detoxification is taken an extra step by S. lycopersici as the hydrolysis products of the saponin-based defense subsequently inhibit inducible defenses of the host by interfering with signal transduction pathways (Bouarab et al., 2002).

Transformation of secondary metabolites (e.g., cleaving sugars from saponins) has been suggested as a way of providing fungi with a carbon source in addition to achieving detoxification (Van Etten et al., 1995; Roldan-Arjona et al., 1999). Since some fungal detoxification enzymes are repressed by glucose (Straney and Van Etten, 1994; Roldan-Arjona et al., 1999) they may have a dual function. This would be analogous to non-pathogenic fungi that obtain carbon from phenolic monomers produced during lignin decomposition (Henderson and Farmer, 1955; Rahouti et al., 1989). Presumably it would be advantageous for pathogens to circumvent host defenses and simultaneously derive nutrition.

Pathogens in the Pythiaceae (Oomycota) appear to possess an innate resistance to the toxic effects of saponins. Members in this family are reported to be relatively unaffected by aescin (Olsen, 1971) and other saponins (Assa et al., 1972) in vitro, and probably the lack of ergosterol in these species (Olsen, 1973a; Weete, 1989) allows them to avoid saponin toxicity (Arneson and Durbin 1968; Olsen, 1971; Weltring, 1997). Although Pythium spp. appear to be unaffected by saponins, saponin toxicity can be induced through the addition of sterols to the growth medium (Olsen, 1973b; Steel and Drysdale, 1988). Members of the Pythiaceae can incorporate sterols by the binding and transport action of small protein carriers called elicitins (Mikes et al., 1997; Panabieres et al., 1997; Capasso et al., 2001) and this uptake of exogenous sterols could be the cause of the observed increase in the deleterious effects of sa-ponins on these organisms.

2.3. Criteria for Saponins as Allelochemicals

Allelopathy is the study of those interactions between and among plants and microbes that are mediated by secondary compounds i.e., allelochemicals (Rice, 1984). The concept of allelopathy is most frequently applied within the context of plant-plant chemical interactions. Allelochemicals can act as a form of chemical interference between competing species (Rice, 1984) as well as conspecific plants (Singh et al., 1999). However, it has recently been argued that allelochemicals are unlikely to reach phytotoxic levels in the soil and therefore plant-microbe allelopathy may be more likely to occur (Schmidt and Ley, 1999). It has been suggested that slow diffusion rates and complexation reactions in soil, coupled with degradation/utilization by microbes would generally prevent allelochemicals from accumulating to phytotoxic concentrations (Schmidt and Ley, 1999). Microbes are expected to metabolize allelochemicals because soil is generally considered to be low in available carbon (Sparling et al., 1981; Scow, 1997) and these organisms are known to utilize a wide range of molecules as carbon sources (Henderson and Farmer, 1955; Black and Dix, 1976; Campbell et al., 1997).

Two related but unintegrated lines of evidence suggest that plants do in fact influence specific soil microbes via secondary chemicals. First, both plant species and genotype are known to affect the rhizosphere species composition of mycorrhizal fungi (Johnson et al., 1992) and actinomycetes and some bacteria (Azad et al., 1987; Miller et al., 1989; Larkin et al., 1993). Recently, results obtained using molecular (Miethling et al., 2000) and physiological (Grayston et al., 2001) methods have confirmed the primary importance of plant species on the composition of soil microbial communities. Second, of the carbon fixed by photosynthesis in plants, an estimated 10 to 20% is released into the rhizosphere (Bowen and Rovira, 1991) and in some instances this amount may exceed 20% (Shepherd, 1994). The potential effects of soil-deposited carbon may extend a distance from the root, as carbon fixed by the aerial portions of maize plants has been found over 3 cm away from the roots (Helal and Sauerbeck, 1984). A diverse array of organic secondary compounds from plants (e.g., alkaloids, phenolics, quinones, saponins, stilbenes) are potent antifungal agents (Grayer and Harborne, 1994), and various species/pathovars of fungi can be differently susceptible to these chemicals (Zimmer et al., 1967; Arneson and Durbin, 1968; Suleman et al., 1996; Sandrock and Van Etten, 1998). It then follows that if secondary compounds are present in the rhizosphere, they could influence the growth and/or species composition of the soil microbial community and therefore have to be considered allelochemicals. However, with the exception of the flavonoids identified in tree-mycorrhizal interactions (Becard et al., 1992; Lagrange et al., 2001) and legume-nodulating bacteria interactions (D'Arcy Lameta and Jay, 1987; Peters and Long, 1988) and the determination of chemicals in Arabidopsis thaliana root exudates (Narasimhan et al., 2003), these "root exudates" are not well characterized. In order to establish whether specific compounds or groups of compounds such as saponins are allelochemicals, therefore, they first must be shown to be present in the rhizosphere (i.e., to determine their ecologically relevant concentration), and second, be shown to be biologically active at their ecologically relevant concentration. Lastly, the allelopathic role of the compounds has to be demonstrated at the field level.

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