The Influence Of Pathogens On Interference And Allelopathy

Natural plant populations increase in production and number of individuals until constrained by environmental limitations (Burdon, 1987). The constraint of plant growth by the environment is often mediated through plant interference. Therefore, the ability of plants to interfere with their neighbours is important in determining their abundance in a community. Plant pathogens generally reduce the development, production and longevity of their hosts. In plant communities, this 'burden of a parasite' may result in a partly unoccupied niche that resistant plants re-inhabit. Overall, pathogens play a significant role in the ecology of plant communities by maintaining (Peters and Shaw, 1996) or reducing (Burdon, 1991) species diversity, driving succession (Van der Putten et al., 1993), ensuring plants do not establish under their parents (Augsberger, 1984) and help determine the long-term composition of plant communities (Dobson and Crawley, 1994).

3.1. The Impact of Pathogens on Competition

Several pioneering publications on plant competition suggest that pathogens might alter the balance of competition in mixed communities in favour of the resistant components (de Wit, 1960; Harper, 1977). Since then, there have been numerous reviews and theoretical interpretations of the impact of pathogens in natural communities and on competition (Chilvers and Brittain 1971; Burdon, 1982; 1987; 1991; Dinoor and Eshed, 1984; Gates et al., 1986; Alexander, 1990; Ayres and Paul, 1990; Clay, 1990; Paul, 1990; Dobson and Crawley, 1994; Jarosz and Davelos, 1995; Alexander and Holt, 1998; Mattner 1998), but empirical experimentation is less extensive. Empirical studies have usually involved binary mixtures of a host and a non-host, grown under optimal conditions of nutrient and water availability, and inoculated with a single, copious and homogenous dose of inoculum. With few exceptions, these studies show that the influence of a host-specific pathogen reduces the vigour of the host, rendering it less able to compete with a neighbouring non-host species (Burdon, 1987; Ayres and Paul, 1990; Mattner, 1998). As such, the combination of the 'burden of a parasite' and competition can have a devastating effect on a plant. For example, Groves and Williams (1975) demonstrated that the combined effects of competition from subterranean clover (Trifolium subterraneum) and rust infection (Puccinia chondrillina) reduced the yield of skeleton weed (Chondrilla juncea) by 94%. This combined effect was more marked than the action of either the competitor (yield was reduced by 70%) or the rust (yield was reduced by 51%) alone. Similarly, Friess and Maillet (1996) found that infection by cucumber mosaic virus reduced the vegetative yield of its host purslane (Portulaca oleracea), with this effect intensifying when infected plants were in competition with healthy plants. In mixtures of common lambsquarters (Chenopodium album) and corn (Zea mays) or beetroot (Beta vulgaris), foliar infection by Ascochyta caulina reduced the competitiveness of its host (lambsquarters) and increased the yield of non-host crops. In corn, infection negated the effects of competition from lambsquarters altogether, highlighting its potential as a biological control agent (Kempenaar et al., 1996). Despite pathogens reducing the competitiveness of their hosts, the effect of infection is often greater on a neighbouring non-host than on the host itself. For example, in mixtures of groundsel (Senecio vulgaris) and lettuce (Lactuca sativa), rust (Puccinia lagenophorae) increased the biomass of lettuce (the non-host) markedly, while only reducing that of its host groundsel marginally (Paul and Ayres, 1987a).

Competitive stress for limited resources intensifies as plant density increases (Shinozaki and Kira, 1956). Consequently, the effect of a pathogen on the competitiveness of its host is most devastating at high densities. For example, rust reduced the competitive ability of groundsel in mixtures with healthy groundsel (Paul and Ayres, 1986) or with lettuce (Paul and Ayres, 1987a) more so at high densities than at low densities. Similarly, Ditommaso and Watson (1995) demonstrated that anthracnose (Colletotrichum coccodes) was more detrimental to the growth of velvetleaf (Abutilon theophrasti) in mixtures with soybean (Glycine max) at high plant densities. Conversely, the performance of the non-host, relative to the infected host, generally increases as density increases. For example, the ability of lettuce to compete with rusted groundsel was greater at high densities than at low densities (Paul and Ayres, 1987a).

Considering that competition occurs for shared resources that are in limited supply, it is not surprising that resource availability influences the interaction between competition and infection by pathogens. Paul and Ayres (1987b) examined the effect of rust on competition between infected and healthy groundsel under conditions of drought. They found that rust reduced the competitiveness of groundsel, however, this was more so in droughted plots than in well-watered plots. They concluded that water stress is important in determining the impact of rust in mixed populations in the field. Owing to the effects pathogens can have on nutrient uptake, Paul and Ayres (1990) also studied the effect of nutrient supply on the interaction between rust and competition. Under high nutrition, groundsel was more competitive than shepherd's purse (Capsella bursa-pastoris). This superiority was lost, however, following the inoculation of groundsel with rust. In contrast, shepherd's purse had a greater competitive ability than groundsel under nutrient-poor conditions. Despite this, it did not increase its advantage when groundsel was rusted.

While most studies show that pathogens decrease the competitiveness of their hosts and increase that of neighbouring non-hosts, there are several exceptions. For example, Catherall (1966) found that for most of the year, barley yellow dwarf virus reduced the competitive ability of its host, perennial ryegrass (Lolium perenne), when grown with white clover (Trifolium repens). During spring, however, the virus stimulated tillering in ryegrass and increased its competitiveness. In another example, the rust Puccinia pulsatillae sterilises its host, Pulsatilla pratensis, by inhibiting flowering. Yet, infected plants are more vigorous and produce more leaves than healthy plants. In a natural community, Wennstrom and Ericson (1991) found that diseased plants had a greater survival rate than healthy plants, which they postulated was due to their greater competitiveness. The effects of pathogens on allelopathy may also mediate their influence on competition.

3.2. The Impact of Pathogens on Allelopathy

The term allelopathy is seldom used in plant pathology (Rice, 1984) even though, by definition, allelopathy includes chemical interactions involving microorganisms. Furthermore, the same or similar secondary metabolites implicated in allelopathy between plants are also important in plant pathology in: enhancing the germination of fungal spores (Odunfa, 1978); antibiosis between microorganisms (Di Pietro, 1995); regulating fungal growth and development (Calvo et al., 2002); pathogen/host recognition (Nicol et al., 2003); the development of disease symptoms (Daly and Deverall, 1983); the promotion of infection through the suppression of the host (Toussoun and Patrick, 1963); the breaking of fungistasis (Mol, 1995); and host resistance to pathogens. Similarly, some authors do not consider chemical interactions by microorganisms as part of allelopathy (Putnam and Duke, 1978; Putnam and Tang, 1986; Pratley, 1996). Rice (1984) explained that this reluctance is due to the chemicals involved not always escaping to the environment. This rationale seems invalid, however, because the chemicals involved do enter the environment of the pathogen or the plant. Moreover, microorganisms can mediate allelopathy between plants (Rice, 1992; Bremner and McCartey, 1993). Such difficulties may have hindered the study of the impact of pathogens on plant allelopathy in the past.

Both Rice (1984) and Einhellig (1995) hypothesised that pathogens enhance their host's allelopathic ability, but few studies have observed such a relationship (Tang et al., 1995). This is despite several investigations on the effects of pathogens on plant competition (Burdon, 1987; Ayres and Paul, 1990; Section 3.1), all of which could potentially include allelopathic interactions. However, competition may have obscured allelopathy in these experiments (Trenbath, 1974), since competition is usually the dominant process of interference (Joliffe, 1988; Tilman, 1988). This is particularly so considering that many experiments studying the effect of pathogens on competition have utilised high plant densities, where competitive effects are most intense. Evidence supporting the hypothesis that pathogens can increase allelopathy between plants occurs in at least two forms: (i) pathogens can stimulate secondary metabolite production in their hosts, and (ii) field, glasshouse and bioassay experiments signifying an increased allelopathic ability of infected plants.

3.2.1. Effect of Pathogens on Secondary Metabolite Production

Numerous studies document the ability of plant pathogens to stimulate the metabolic activity (Daly, 1976) and increase the production of secondary metabolites (Stoessl, 1982, 1983; Goodman et al., 1986; Kuc, 1997) by their hosts. Müller and Börger (1941) first proposed that plants produce defensive substances called phytoalexins in response to infection, which are important to host resistance. Phytoalexins are 'low molecular weight; antimicrobial compounds that are both synthesised by and accumulated in plant cells after exposure to microorganisms' (Paxton, 1981). As such, phytoalexins fit the definition of allelochemicals. Like allelochemicals that act against plants, phytoalexins are secondary compounds that belong to a wide range of different chemical classes (Stoessl, 1982), with more than 300 distinct phytoalexins already characterised (Smith, 1996). They are mostly synthesised via the acetate and shikimic acid pathways (Bailey, 1982; Bennett and Wallsgrove, 1994), as are allelochemicals that act against plants. Notwithstanding their similarities, allelopathy between plants and phytoalexin research has developed almost independently.

Many compounds with phytoalexin activity are also implicated in allelopathy between plants (Rice, 1984). For example, isoflavonoids are important phytoalexins (Ingham, 1982; Paxton, 1981; Dakora and Phillips, 1996) and allelochemicals (Tamura et al. 1967; 1969) from the Leguminosae. Parbery et al. (1984) found that the isoflavonoids biochanin A, formononetin and genistein increased in subterranean clover by 62%, 123% and 75% respectively following infection by pepper spot (Leptosphaerulina trifolii). In comparison, Tamura et al. (1967; 1969) isolated a succession of isoflavonoids (including biochanin A, formononetin and genistein) from the shoots of red clover (Trifolium pratense) that inhibited its own germination by 50% at concentrations of 50 ppm.

As expected, most studies concerned with the toxicology of phytoalexins concentrate on their effects on microorganisms. Increasingly, however, studies show that phytoalexins are also toxic to plants. Despite this, they are seldom referred to as allelochemicals. Pisatin and phaseollin, pterocarpans produced by pea (Pisum sativum) and bean (Phaseolus vulgaris) respectively, were the first phytoalexins characterised (Perrin and Bottomly, 1962; Cruickshank and Perrin 1963). Skipp et al. (1977) noted that phaseollin inhibited the respiration and growth of cell cultures of bean and tobacco (Nicotiana tabacum), eventually causing cell death. Similarly, pisatin reduced the growth of callus cultures of pea (Bailey, 1970) and inhibited the root growth of wheat (Cruickshank and Perrin, 1961). The phytoalexin rishitin (a sesquiterpene) accumulates in potato cells challenged by incompatible isolates of Phytophthora infestans (Tomiyama et al., 1968). Studies show that the compound also inhibits pollen germination in three Solanum species (Hodgkin and Lyon, 1979); causes lysis of potato and tomato protoplasts (Lyon and Mayo, 1978); and cell death in tubers and epidermal strips of potato (Ishiguri, et al., 1978; Lyon, 1980). Other studies show that phytoaxelins may inhibit seed germination (Chang et al., 1969), growth (Glazener and VanEtten, 1978) and cellular metabolism and function (Lyon, 1980; Boydston et al., 1983; Kurosaki et al., 1984; Giannini et al., 1990; Spessard et al., 1994) of plants. The ability of pathogens to stimulate secondary metabolite production in their hosts and for these to affect plant growth provides strong circumstantial evidence for the hypothesis that pathogens can increase plant allelopathy.

Many studies have established that pathogens can increase the production of phenolic acids in their hosts, which are perhaps the most important group of plant allelochemicals. For example, when challenged by a range of different pathogens, concentrations of phenolics often associated in allelopathic interactions have increased in a variety plants, including carrot (Daucus carota) (Phan et al., 1991), chickpea (Cicer arietinum) (Singh et al., 2002); date palm (Phoenix dactylifera) (Daayf et al., 2003); potato (Solanum tuberosum) (Kuc et al., 1956); sorghum (Sorghum bicolor) (Woodhead, 1981); sugar cane (Saccharum officinarum) (Legaz et al., 1998); sunflower (Helianthus anuus) (Spring et al., 1991); and wheat (Triticum aestivum) (Siranidou et al., 2002), amongst many others. This increase in phenolics post-infection is one of the most important methods of disease resistance in plants. For example, inoculation with crown rust (Puccinia coronata f.sp. avenae) induced the production of three phenolic compounds (avenalumins I, II and III) by resistant oats (Avena sativa). Purified preparations of these chemicals inhibited the germination and germ tube growth of crown and stem rust (Puccinia graminis) at concentrations as low as 200 |xg/mL (Mayama, 1981; 1982). Similarly, Mandavia et al. (2000) found that varieties of cumin (Cuminum cyminum) tolerant of Fusarium wilt (Fusarium oxysporum f.sp. cumini) contained higher concentrations of salicylic acid, hydroquinone and umbelliferone in their root, stem and leaf tissues than susceptible varieties. These phenolics inhibited fungal spore germination and mycelial growth of F. oxysporum. However, to this author's knowledge, the effect of the increased phenolic concentrations in infected plants on plant allelopathy has not been investigated empirically.

The production of glucosinolates by plants in the Capareles and their subsequent hydrolysis to toxic isothiocyanates, thiocyanates, and nitriles has been one of the most intensively studied systems in allelopathy, due partly to the similarity of these breakdown products to some synthetically produced soil fumigants (and therefore termed biofumigation; Kirkegaard et al., 2000). Glucosinolates are important in plant defence against insects, pathogens and nematodes. Jay et al. (1999) showed that infection of Brassica napus with beet western yellows virus increased glucosinolate concentration in tissues by 14%. Similarly, Li et al. (1999) found that infection of B. napus by Sclerotinia sclerotiorum increased glucosinolate content in resistant, but not in susceptible varieties. Exposure to the pathogenic bacterium, Erwinia carotovora, triggered the production of glucosinolates in Arabidopsis thaliana (Brader et al., 2001). The hydrolysis products from these glucosinolates inhibited the growth of E. carotovora in culture. Furthermore, Tierens et al. (2001) demonstrated that a range of pathogens were more aggressive in infecting an A. thaliana mutant that did not produce glucosinolates than the wild type, suggesting the importance of glucosinolates in protecting against infection. However, the role of glucosinolates in disease resistance may be species specific, since Andreasson et al. (2001) found that infection of B. napus by Leptosphaeria maculans had no effect on glucosinolate concentration in the resistant or susceptible host. Despite the ability for at least some pathogens to increase glucosinolate production in the Capareles, no one has investigated whether this directly translates to an increased allelopathic effect against neighbouring plants.

3.2.2. The Effect of Rust on Ryegrass Allelopathy

Perennial ryegrass (Lolium perenne) and white clover (Trifolium repens) are important components of improved pastures grown in temperate regions worldwide. The ability of ryegrass to become dominant in pastures has led to numerous investigations that demonstrate its potential to interfere with companion plants through allelopathy (Naqvi, 1972; Naqvi and Muller, 1975; Newman and Rovira, 1975; Newman and Miller, 1977; Gussin and Lynch, 1980; Buta et al., 1987; Quigley et al., 1990; Sutherland and Hoglund, 1990; Wardle et al., 1991; Prestidge et al., 1992; Chung and Miller, 1995; Mattner, 1998; Mattner and Parbery, 2001). For example, in a study investigating the allelopathic ability of nine pasture species, Takahashi et al. (1988) found that leachate from soil surrounding ryegrass was the most inhibitory to the growth of the target species, including clover. In a subsequent experiment, they circulated nutrient solution between the roots of ryegrass and clover to eliminate competition effects. They found that the growth of clover declined in the system, particularly when the proportion of ryegrass was high. When they incorporated XAD-4 resin into the system (which selectively traps organic hydrophobic compounds) clover grew normally. Moreover, ryegrass became yellow and stunted when grown alone in the system, but this was prevented by the presence of the resin or clover (Takahashi et al., 1991). In a further experiment, root exudate from ryegrass not only inhibited the growth of clover, but also lettuce seedlings. The phytotoxic fraction of the extract contained p-methoxybenzoic, lauric, myristic, pentadecanoic, palmitoleic, palmitic, oleic and stearic acids. Sodium salts of myristic, palmitic, oleic and stearic acids suppressed the growth of clover at concentrations as low as 5 ppm (Takahashi et al., 1993). Similarly, in a study examining the allelopathic effects of a number of crop and pasture species, Halsall et al. (1995) found that aqueous extract from the dried shoots of perennial ryegrass suppressed the germination, radicle elongation, nodulation and seedling root elongation of subterranean and white clover. The magnitude of this inhibition increased as the concentration of the extract increased.

Crown rust, caused by Puccinia coronata f.sp. lolii, is the most devastating fungal disease of ryegrass, with epidemics regularly occurring between spring and autumn in temperate regions worldwide (Mattner and Parbery, 2001). Severe epidemics reduce ryegrass tillering by 20-38% (Lancashire and Latch, 1966; Mattner, 1998), leaf emergence by 60%, leaf area by 62%, root growth by 75% (Mattner, 1998), and increase the rate of leaf senescence by up to 184% (Lancashire and Latch, 1966; Trorey, 1979; Plummer et al., 1990; Mattner, 1998). Losses of herbage yield in ryegrass from rust have been as great as 94% (Critchett, 1991), with seed yield losses ranging from 1236% (Hampton, 1986; Mattner 1998). Furthermore, rust infection reduces forage quality (Isawa et al., 1974; Trorey, 1979; Potter, 1987) and palatability to grazers (Cruickshank, 1957; Heard and Roberts, 1975).

As would be expected by the devastating effect that rust has on ryegrass growth, most studies show that rust reduces the competitiveness of ryegrass with non-host plants such as clover. For example, in mixed swards of ryegrass and clover, Lancashire and Latch (1970) found that rust reduced ryegrass yield by 84% and increased the yield of clover by 87%. Furthermore, the proportion of clover in the rusted sward increased from 24% at the beginning to 80% at the termination of their experiment. Thus, their study pointed to a lowered competitiveness of rusted ryegrass. In mixtures of rust resistant and susceptible ryegrass, Potter (1987) found that rust reduced the yield of the susceptible cultivar and increased that of the resistant one, concluding that rust reduced ryegrass competitiveness. Similarly, crown rust infection in swards of ryegrass and cocksfoot (Dactylis glomerata) reduced ryegrass composition from 30% to 15%, and was more marked in rust susceptible than resistant cultivars (Trorey, 1979). However, in a series of experiments, Mattner (1998) reported an anomaly to the results of this previous research.

In pot studies consisting of 50:50 mixtures of ryegrass and clover grown over a range of plant densities, Mattner (1998) found that rust reduced the yield of ryegrass by an average of 41%. However, interference from rusted ryegrass suppressed clover biomass by up to 47% compared with interference from the more productive, healthy ryegrass. The onset of the suppression of clover by rusted ryegrass was rapid, occurring as early as 6-13 days after inoculation, which according to some growth parameters was earlier than the effects of rust on ryegrass itself. The suppression of clover by rusted ryegrass was greatest at low plant densities and diminished or disappeared as density increased. In a separate trial, rusted ryegrass again suppressed clover growth, even after the removal of infected tissue by cutting and after the death of the ryegrass. In this instance, ryegrass killed by infection, with a competitive ability of virtually zero, inhibited the growth of clover more than living plants of healthy ryegrass. In further trials, high rust severity and high soil moisture contents increased the suppression of clover by rusted ryegrass.

The ability of rust to directly inhibit or infect clover could not explain the results from these studies, since clover is a non-host of P. coronata and inoculation with this rust did not reduce the yield of clover monocultures. Under some conditions, infection by rusts can increase the scavenging ability of some hosts for water and nutrient resources (Ahmad et al., 1982; Paul and Ayres, 1988), potentially increasing their competitive ability. For this to explain the results from Mattner's studies, however, the suppression of clover by rusted ryegrass should have been greatest at high plant densities where competition for resources was most intense. Instead, the suppression of clover by rusted ryegrass was greatest at low densities where resources were plentiful and competition was low. Furthermore, the ability of rusted ryegrass to suppress clover continued even beyond the death of the plant, when it had no capacity to scavenge resources. For these reasons, Mattner (1998) posed the hypothesis that rust reduces the competitiveness of ryegrass, while simultaneously increasing its allelopathic ability. In this way, it was expected that the expression of allelopathy by rusted ryegrass was greatest at low densities, where there was little competition and the effects of rust in reducing ryegrass competitiveness did not obscure its effects on increasing allelopathy. Furthermore, high plant densities may detoxify or dilute the action of allelochemicals (Thijs et al., 1994).

To test the validity of this hypothesis and to separate the effects of competition and allelopathy, four bioassays for allelopathy were conducted (Mattner, 1998; Mattner and Parbery, 2001). Each bioassay highlighted the potential for extracts, leachate, or residues from ryegrass to inhibit the yield of clover through allelopathy, and for rust to enhance this potential. For example, soil previously growing rusted ryegrass suppressed clover biomass by 36% compared with soil previously growing healthy ryegrass. similarly, leachate from soil supporting rusted ryegrass suppressed clover biomass by 27% compared with that from healthy ryegrass (Mattner and Parbery, 2001). Although some bioassays have confounding and interpretational problems (Stowe, 1979; Inderjit and Weston, 2000), the conformity of results between these different bioassays provides strong evidence for the hypothesis that rust infection increases the allelopathic ability of ryegrass. Furthermore, in the field, the proportion of prickly lettuce (Lactuca serriola) reduced in areas of a depleted pasture dominated by rusted ryegrass, compared with areas dominated by non-rusted ryegrass (Mattner, 1998). Further bioassays provided evidence that this association potentially related to an enhanced allelopathic ability of ryegrass rather than to differences in soil chemistry. Thus, this study highlighted the potential for rust to increase ryegrass allelopathy in the field.

Mattner (1998) suggested two mechanisms by which rust may increase ryegrass allelopathy. Firstly, rust may directly stimulate the production of allelochemicals by ryegrass in a defensive response to infection. Alternatively, or additionally, the increased rate of tissue senescence in ryegrass induced by rust may result in a higher concentration of plant residues reaching the soil. These residues may then form an allelochemical source - either directly or following their decomposition. Most evidence gathered from his studies supported the first hypothesis. For example, when ryegrass residues were incorporated into soil, their ability to suppress clover growing in that soil depended on the residues being rusted and not their overall concentration. Furthermore, the knowledge that pathogens stimulate secondary metabolite formation in their hosts and the rapid effect rusted ryegrass had in suppressing clover, supported rust directly stimulating allelochemical production in ryegrass.

Mattner's findings appear to contradict those of Lancashire and Latch (1970) who studied the identical biological system in the field, and found that the proportion of clover in the sward more than doubled following infection of the ryegrass component by rust. However, Lancashire and Latch (1970) conducted their study under conditions that favoured the expression of the reduced competitiveness rusted ryegrass, i.e. at higher plant densities (2150 plants/m2) than those of Mattner (1998) (57 plants/m2). More importantly, however, their results only occurred in the highly susceptible ryegrass cultivar, Ruanui. In a more resistant cultivar, Ariki, rust reduced ryegrass yield by 18%, but clover was unable to take advantage of this reduction, producing the same dry weight when grown with rusted ryegrass as when grown with healthy ryegrass. Furthermore, rusted Ariki ryegrass actually suppressed the growth of clover at some harvests. Perhaps rust infection increased the production of defensive chemicals by Ariki, thereby increasing its resistance to rust and its allelopathic ability against clover. Lancashire and Latch (1970) disregarded these results because, overall, the yield of Ariki was abnormally poor in their experiment compared with several previous studies. Nonetheless, the poor yield of Ariki ryegrass occurred in both rusted and non-rusted treatments and does not explain the inability of clover to compensate for the reduced yield of rusted ryegrass, or the suppression of clover by rusted ryegrass. Rather, the hypothesis that rust increases the allelopathic response of ryegrass while also reducing its competitiveness fits their results.

Although there is strong circumstantial evidence from field, glasshouse and bioassay studies that rust increases the allelopathic ability of ryegrass, many questions remain. An important next step is to identify the allelochemicals concerned. Also, do rusted plants simply produce allelochemicals in higher concentrations or do they produce entirely different allelochemicals to healthy plants? Also, what is the allelochemical source in the plant and the mechanism of release to the environment? This information will provide a clearer understanding of the influence of pathogens on allelopathy.

3.2.3. The Effect of Neotyphodium lolii on Ryegrass Allelopathy

The endophytic fungus Neotyphodium lolii commonly infects perennial ryegrass forming a mutualistic relationship with its host. Apart from obtaining nutriment, the host provides the endophyte with a relatively exclusive niche and a vehicle for its transmittance through infected seed (Clay, 1987). The host benefits in several ways, including: (i) increased seed germination, dry matter production and tillering compared with non-infected ryegrass (Latch et al., 1985; Quigley, 2000); (ii) resistance to plant diseases caused by nematodes (Stewart et al., 1993), fungi (Latch, 1993) and viruses (Lewis and Day, 1993); (iii) increased tolerance of drought stress (Ravel et al., 1997), (iv) increased nitrogen use efficiency (Arachevaleta et al., 1989); and (v) increased competitiveness (Sutherland and Hoglund, 1989). Additionally, the fungus produces various alkaloids (e.g. peramine, ergovaline, and lolitrem) that protect the host against herbivory (Clay, 1996).

There is much speculation as to the role of the endophyte on the allelopathic ability of its host. This speculation originated with the observation that endophyte-infected ryegrass suppressed the growth of companion clovers to a greater extent than endophyte-free ryegrass (Stevens and Hickey, 1990). In order to explore several hypotheses on how this relationship might arise, Sutherland and Hoglund (1989) grew swards of endophyte-infected and endophyte-free perennial ryegrass in plots with white clover. Endophyte-infected ryegrass produced 16% more dry matter and suppressed the yield of clover by 72% compared with endophyte-free ryegrass. Neither mowing nor grazing by sheep affected the relationship. This demonstrated that selective grazing pressure on clover following a decline in the palatability of endophyte-infected ryegrass was not responsible for the reduction in clover yield. Rather, they suggested that the suppression was due to an increased competitiveness and allelopathic ability of endophyte-infected ryegrass. They implicated allelopathy in this effect because endophyte-infected ryegrass of a comparable yield to endophyte-free ryegrass, suppressed the yield of clover to a greater extent than endophyte-free ryegrass.

In a subsequent experiment, Sutherland and Hoglund (1990) surrounded individual plants of white clover with zero to seven endophyte-infected or endophyte-free perennial ryegrass plants. This experiment failed to demonstrate that endophyte-infected ryegrass suppressed clover more than endophyte-free ryegrass. They explained that this might be due to the cutting regime imposed on ryegrass and the non-return of these clippings to the soil, which possibly contained allelochemicals. A bioassay experiment, which showed that aqueous extracts from the shoots of endophyte-infected ryegrass inhibited the shoot growth of clover seedlings by 8%, supported their explanation. In a similar experiment, Quigley et al. (1990) found that aqueous extracts from endophyte-infected ryegrass depressed the root length of four germinating legumes (including white clover), by an average of 10% compared with extract taken from endophyte-free ryegrass. In contrast, after conducting several bioassays for allelopathy, Prestidge et al. (1992) found little evidence to suggest that the presence of endophyte in ryegrass enhanced its allelopathic effect. Field trials also failed to show that clover yield declined when grown with endophyte-infected ryegrass. Similarly, Watson et al. (1993) and Mattner (1998) failed to substantiate an increased allelopathic effect of endophyte-infected ryegrass. Furthermore, there was no apparent interaction between endophyte and rust infection in increasing the allelopathic ability of ryegrass (Mattner, 1998).

Applebee et al. (1999) found that the toxicity of tall fescue (Festuca arundinacea) infected with Neotyphodium coenophialum increased at elevated concentrations of C02 in the atmosphere. In a bioassay study conducted in sterile sand, Sutherland et al. (1999) applied aqueous extracts from ryegrass to potted clover seedlings. Extracts from three ryegrass cultivars infected with three different strains of endophyte, all inhibited the growth of clover, by up to 27% compared with extracts from endophyte-free ryegrass. Both ryegrass cultivar and endophyte strain influenced the degree that ryegrass extracts inhibited clover, but this did not relate to the type of alkaloids produced by the different endophyte strains. These studies suggest that both environmental and genetic influences may moderate the triggers for enhanced allelopathy by endophyte infected grasses, and this may explain the discrepancy in results between individual studies. Nonetheless, the majority of evidence suggests that endophyte infection has the capacity to increase ryegrass allelopathy, which is a further added benefit conferred by this mutualist to its host. Although the endophyte is a non-pathogenic organism, its ability to stimulate plant allelopathy adds further weight to the hypothesis that infection increases the allelopahtic ability of host plants.

3.2.4. Other Systems

The ability of rusts to stimulate allelopathy in their hosts may not be limited to ryegrass, as the rusts Puccinia hordei and Uromyces troflii-repentis increased the suppression of white clover by barley grass (Hordeum leporinum) and subterranean clover (Trifolium subterraneum), respectively (Mattner, 1998). Yet, the effect was not universal since Puccinia coronata in wild oat (Avena fatua), Puccinia graminis in cocksfoot (Dactylis glomerata) and Puccinia recondita in soft brome (Bromus mollis) all failed to increase their host's allelopathic ability.

Kong et al. (2002) studied the allelopathic potential of goatweed (Ageratum conyzoides) under different environmental stresses, including infection by powdery mildew (Erysiphe cichoracearum). Infection stimulated the production of 17 of the 24 volatile chemicals produced by goatweed that they investigated, with total volatile production increasing by 50%. Exposure to the volatiles released by infected goatweed stimulated the growth of peanut (Arachis hypogaea), redroot amaranth (Amaranthus retroflexus), Italian ryegrass (Lolium multiflorum) and cucumber (Cucumis sativus) compared with volatiles from healthy goatweed. In contrast, volatiles from infected plants inhibited the growth of three fungal pathogens (Rhizoctonia solani, Botrytis cinerea, and Sclerotinia sclerotiorum). For this reason, they postulated that the allelochemicals stimulated by fungal infection in goatweed are more important in the defence of the plant against infection, rather than against competition from neighbouring plants. Nonetheless, this study currently provides the clearest demonstration of the ability of pathogens to influence the allelopathic ability of plants.

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