Developments in the Biological Control of Soil-borne Plant Pathogens

Developments in the Biological Control of Soil-borne Plant Pathogens

J. M. WHIPPS

Plant Pathology and Microbiology Department, Horticulture Research International, Wellesbourne, Warwick CV35 9EF, U K

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Ecological Considerations ........................................................... A. Suppressive Soils ................................................................ B. Monoculture Decline ............ C. Organic Amendments and Corn ..................................... D. Physical and Chemical Practices E. Role of Fauna in Natural Biolo

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1. Introduction 11.

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111. Modes of Action ........................ .............................. A. Direct Modes of Action ...................................................... B. Indirect Modes of Action ............ ................................. C. Rhizosphere Competence ...... ..............................

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IV. Application of Specific Antagonists .............................................. A. Selection and Screening .............................. B. Inoculum Production, For lication .................

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References

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INTRODUCTION

There has been a large upsurge in interest in biological disease control recently, reflecting increasing environmental concern over pesticide use. This interest has been further stimulated by the occurrence of fungicide resistance in some pathogens, and, for some soil-borne diseases, the lack of reliable Advances in Botanical Research Vol. 26 incorporating Advances in Plant Pathology ISBN 0-12-0059266

Copyright 0 1997 Academic Press Limited All rights of reproduction in any form reserved

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chemical controls or resistant plant varieties. The potential withdrawal of methyl bromide for soil fumigation in many countries (Noling and Becker, 1994) has added further impetus. Indeed, in The Netherlands, the multi-year crop protection plan was introduced in 1991 (Anonymous, 1991) with the aim of reducing pesticide usage by 50% by the year 2000. Until recently, there were relatively few commercially available biological disease control products but this seems to be changing, possibly reflecting a switch in the attitude of both researchers and industry. The commercial perceptions or requirements, including cost-effective control equivalent to, or better than, existing control treatments, long shelf-life, temperature stability, and integration with pesticides and existing crop management procedures (Powell and Faull, 1989; Renwick and Poole, 1989) may still stand, but the realization that several other key areas need to be examined before any biological disease control strategy can be developed commercially may finally have been appreciated. These areas include the aetiology and epidemiology of the pathogen; the growth and method of cultivation of the crop; the physical, chemical and microbiological environment where the biocontrol agent must act; and which biocontrol agents are available, their ecology and their modes of action. Such interdependent interactions can be expressed graphically in the form of an interaction template (Fig. 1) and form the basis of any holistic approach to biocontrol. Against this interaction template biocontrol agents and their method of use can be identified, inoculum production, formulation and application procedures can be considered, and methods for further selection or improvement in activity can be identified. Significantly, many of the problems routinely associated with variable and irreproducible results using biological methods of disease control, stem from a failure to address all the possible interactions as a whole. Failure to consider the ecology of the biocontrol agent in relation to the environment of use may be particularly important in this respect (Deacon, 1991, 1994; Deacon and Berry, 1993; Whipps, 1997a) and reflects the drive for the development of specific microbial inoculants which could be used as direct substitutes for chemicals rather than a potentially more realistic holistic approach. Thus, this review will concentrate on developments in three main areas: ecological considerations associated with natural biocontrol; modes of action of biocontrol agents; and, finally, use of specific microbial antagonists for biocontrol. Future approaches for biological control of soil-borne plant pathogens will also be examined in the concluding section. With the recent explosion in interest in biological disease control it is impossible to cite all the relevant publications that have appeared. Therefore, by necessity, this review will consider key topics using specific recent examples, wherever possible, to illustrate the main points of interest. For further information on earlier material, the reader is referred to the numerous in-depth reviews on specialized topics as well as books on biological control which have been published in the last few years (e.g. Cook and Baker, 1983;

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Hoitink and Fahy, 1986; Schippers et nl., 1987; Burge, 1988; Cook, 1988, 1993; Fravel, 1988; Weller, 1988; Baker. 1989, 1991; Kloepper et a / . , 1989; Whipps and Lumsden, 1989, 1991; Adams, 1990; Hornby, 1990; Taylor and Harman, 1990; Beemster et al., 1991; Deacon, 1991, 1994; Harman, 1991; Katan and DeVay, 1991; Keel et al., 1991; Keister and Cregan, 1991; Lewis and Papavizas, 1991; Nelson, 1091; Huang, 1992; Jensen et a [ . , 1992; Leatham, 1992; Lumsden, 1992; O’Sullivan and O’Gara, 1992; Tjamos et a l . , 1992; Whipps, 1992; Whipps and Gerlagh 1992; Alabouvette et al., 1993, Chet, 1993; Deacon and Berry, 1993; Lumsden and Vaughn, 1993; Powell and Jutsum, 1993; Whipps and McQuilken, 1993; Campbell, 1994; Dowiing and O’Gara, 1994; Goldman et nl., 1994a; Jeffries and Young, 1994; Ryder et al., 1994; Hatcher, 1995; Keel and Defago, 1997; Whipps, 1997a,b).

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ECOLOGICAL CONSIDERATIONS

When the interaction template (Fig. 1) is considered in terms of biological control, the biological control agent is generally the major feature examined. This is understandable, as the biocontrol agent is the most tangible part for

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Envi ronment !

Fig. 1. Ecological interactions associated with biological control.

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manipulation and development if the pathogen cannot be controlled directly by other means and there are no resistant plant varieties. However, there are clear examples where the extant environment or the resident microbial community provide natural biocontrol. This situation may occur naturally in disease-suppressive soils or develop with disease decline in monoculture, but is often produced directly through agricultural or horticultural practices. These practices include the use of organic amendments and composts, and physical and chemical treatments such as soil sterilization, flooding, crop rotations, tillage and use of fertilizers. Soil fauna may also play a key role in some cases. In addition, examination of the features of the interaction template when natural biocontrol exists may also aid in the selection, targeting, development and use of selected biocontrol agents; these aspects are considered later (section 1V.A). A.

SUPPRESSIVE SOILS

The occurrence of soils which are suppressive to the development of diseases caused by soil-borne plant pathogens is well documented (Table I). In these soils, disease severity is reduced in susceptible plants even when there is a large inoculum density of the pathogen present and environmental factors are conducive for disease (Cook and Baker, 1983). This disease suppression may be due to a direct effect of the soil on the pathogen (pathogensuppressive soils) or to an indirect effect mediated through the host plant (disease-suppressive soils). Only studies of the mechanisms of suppressiveness can distinguish between the two. Soil suppressiveness is related to both biotic and abiotic characteristics of the soil. For instance, for most Fusariurn-suppressive soils, biocidal treatments such as steam, gamma-irradiation and methyl bromide nullify the suppressive effect and convert a suppressive soil to a conducive one (Alabouvette et al., 1985). Further, transfer of even a small proportion (1-10%) of suppressive soil to a previously heated conducive soil confers suppressiveness to the mixture, indicating that soil suppressiveness is related to the activity of some or all of the soil microbiota. In contrast, suppressiveness in other soils, such as those suppressive to Thielaviopsis basicola causing black root rot of tobacco in North Carolina (Meyer and Shew, 1991a,b) and a forest soil suppressive to Phyfophfhora capsici in Hawaii (KO,1985), was not affected by autoclaving, suggesting abiotic factors alone were responsible for suppressiveness. However, in most cases, a specific combination of abiotic and biotic factors is required for soil suppressiveness to occur. Much work has been done to elucidate the key physicochemical components and microorganisms responsible for suppressiveness in many soils, as this information could form the basis for the development of reproducible biocontrol programmes in the future.

TABLE I Examples of disease-suppressive soils Pathogen

Disease

Location

Reference

Fusarium oxysporum

Vascular wilt of many crops

Central America, France, Israel, Japan, USA

Fusarium solani Gaeumannornyces graminis

Root rot of bean Dry rot of potatoes Take-all of cereals

Japan, USA France Australia, the Netherlands, USA

Phytophthora spp.

Root rot of many plants

France, Taiwan, USA

Plasmodiophora brassicae

Clubroot of crucifers

Taiwan

Pseudomonas solanacearum Pythium aphanidermatum Pythium spp.

Bacterial wilt Root rot of radish Damping-off of many plants

USA Mexico Finland, USA

Rhizoctonia solani Streptomyces scabies Thielaviopsis basicola

Root-rot of radish Potato scab Black root of tobacco

Colombia Japan Switzerland, USA

Stover (1962); Stotzky and Martin (1963); Yuen et al. (1985); Alabouvette (1986); Sneh, et al. (1987); Toyota et al. (1994) Burke (1965); Furuya and Ui (1981) Tivoli et al. (1990) Gerlagh (1968); Shipton et al. (1973); Cook and Rovira (1976); Rovira et al. (1990); Andrade et al. (1994) KO and Nishijima (1985); Benson (1993); Ann (1994); Andrivon (1995) Young et al. (1991); Osozawa et al. (1994) Nesmith and Jenkins (1985) Lumsden et al. (1987) Tahvonen (1982); Lifshifz et al. (1984a); Kao and KO (1986a,b); Martin and Hancock (1986) Chet and Baker (1981) Mizuno and Yoshida (1993) DCfago et al. (1990); Meyer and Shew (1991a,b)

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Many individual physicochemical factors have been identified with soil suppressiveness, but often unique combinations of physicochemical characteristics are related to suppression of specific diseases in specific environments. For example, low pH values, high levels of organic matter, calcium, potassium and magnesium were associated with suppression of Pythium aphanidermatum in a Mexican Chinampa agricultural system (Lumsden et af., 1987), but high calcium content was the single most important physicochemical characteristic related to suppressiveness towards Pythium splendens in Hawaii, although several other factors with some lesser effect were also identified (Kao and KO, 1986a,b). Some physicochemical factors, particularly clay type and pH, are consistently identified as playing a key role in soil suppressiveness, but are not always consistently associated in the same way for suppressiveness to the same or similar pathogens in different soils. Further, a soil which is suppressive towards one pathogen is not always suppressive to another. For example, in France, the level of suppressiveness of a soil towards Fusarium oxysporum f. sp. lini was associated with high montmorillonite clay levels (Amir and Alabouvette, 1993), but was subsequently shown to be related also to soil texture, pH, exchangeable calcium and magnesium, and EDTA-extractable iron (Hoper et al., 1995). In Central America, soil suppressiveness to Fusarium wilt of banana was also correlated with the presence of montmorillonite clay (Stotzky and Martin, 1963). However, in Switzerland, vermiculitic clays were important in suppression of black root rot of tobacco caused by Thielaviopsis basicola (DCfago et af., 1990). In contrast, in the USA, suppression to black root rot of tobacco was dependent on the interaction between pH, base saturation and exchangeable aluminium and not clay content at all (Meyer and Shew, 1991a,b). Generally, soils suppressive to Fusarium have a high pH (>7.0) and this is linked with high calcium content and low levels of available iron (Scher and Baker, 1980; Elad and Baker, 1985). Indeed, one of the proposed mechanisms for soil suppressiveness relates to the regulation of the availability of iron to pathogenic Fusarium spp. in suppressive soils by other soil microorganisms, particularly fluorescent pseudomonads (see later in this section). Similarly, a soil in Taiwan suppressive to clubroot of crucifers caused by Plasmodiophora brassicae was also characterized by a high pH and high calcium content (Young et al., 1991). In contrast, soils suppressive to other pathogens may be characterized by low pH. These include soils suppressive to Phytophthora spp. (KO and Nishijima, 1985; Benson, 1993; Andrivon, 1994, 1995), Thielaviopsis basicola (Meyer and Shew, 1991a,b), Streptomyces sp. (Mizuno and Yoshida, 1993) and, unusually, Fusarium solani f. sp. coeruleum (Tivoli et al., 1990). A direct effect of pH alone on these pathogens could be possible, but this is unlikely for T. basicola at least, as this pathogen grows in culture at pH values of 3.3-8 (Lucas, 1955) and causes disease in acid soil under high base saturation conditions (Meyer and Shew, 1991b).

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Certainly, evidence is now accumulating that under low pH conditions, aluminium toxicity may be the key controlling feature (Andrivon, 1994, 1995; Meyer et al., 1994). Other ions may play a role in disease suppression in some soils. For instance, in the San Joachim Valley of California, suppression of Pythium ultimum was associated with increased chloride levels (Martin and Hancock, 1986). Under these circumstances, Pythium digandrum, which was less affected by increased chloride levels than P. ultimum, was able to outcompete the pathogen. In turn, this suppressed the saprotrophic ability of P. ultimum and resulted in less disease. Indeed, NaCl has been applied to soil to control Fusarium crown and root rot of asparagus (Asparagus oficinalis) caused by Fusarium oxysporum and F. proliferatum. This suppression is related to changes in manganese (Mn) availability and an increase in antagonistic Mn-reducing strains of bacteria (Elmer, 1995). Such interactions between soil physicochemical characteristics and the microbial components involved with soil suppressiveness have been identified in numerous other soil-plant systems including the Mexican Chinampa System and Hawaiian soils suppressive to Pythium (Kao and KO, 1986a,b; Lumsden ef a f . , 1987) and in some Fusarium-suppressive soils (Alabouvette, 1986). The microbial component may be involved in general soil suppressiveness due to the presence of a highly metabolically active microbiota which outcompetes the pathogen for nutrients, particularly carbon and iron (Schneider, 1982; Alabouvette, 1986; Sivan and Chet, 1989a; Couteaudier, 1992; Lemanceau et al., 1993). Alternatively, specific components of the soil microbiota may antagonize the pathogen directly, by competition, parasitism or production of antibiotics, or indirectly by inducing resistance in the host plant (DCfago et al., 1990; Schippers, 1992; Alabouvette, 1993; Liu ef al., 1995a,b); these mechanisms are discussed later in section 111. Numerous microorganisms have been isolated and implied as causing or contributing to soil suppressiveness in a range of systems (Table 11). Non-pathogenic fusaria in Fusarium-suppressive soils and fluorescent pseudomonads in a range of systems are particularly frequently reported, reflecting the intensive studies of soils suppressive to Fusarium spp., to take-all of wheat (Triticum spp.) caused by Gaeumannomyces graminis var. tritici, and to black root rot of tobacco. However, it is likely that the numbers of species identified as being associated with suppressive soils are likely to increase as greater numbers of systems are examined in detail. Significantly, many of the organisms isolated from suppressive soils have been used individually, or more recently in combination, to provide or demonstrate biological control (DCfago et al., 1990; Ryder et al., 1990; Thomashow and Weller, 1990; Alabouvette et al., 1993; Duffy et al., 1996; Leeman ef al., 1996a). Indeed, several commercial products on the market or undergoing registration contain microorganisms isolated originally from suppressive soils. These include Mycostop, which contains a Streptomyces griseoviridis isolate which

TABLE I1

Examples of microorganisms implicated as causing or contributing to soil suppressiveness

Microorganism Bacteria

Actinomycete spp. Acaligenes sp. Arthrobacter sp. Bacillus sp. Hafnia sp. Pseudomonas spp.

Pathogen or disease suppressed

Reference

Serratia sp. Streptomyces sp.

Fusarium wilt of date palm Fusarium wilt of carnation Fusarium wilt of carnation Fusarium wilt of carnation Fusarium wilt of carnation Fusarium wilts in general Take-all of wheat Take-all of wheat and turf grass Thielaviopsis basicola on tobacco Fusarium wilt of carnation Several soil and seed-borne pathogens

Amir and Amir (1989) Yuen et al. (1985) Sneh (1981) Yuen et al. (1985) Sneh et aI. (1985) see Lemanceau and Alabouvette (1993) Weller and Cook (1983) Wong and Baker (1984) Stutz et al. (1986) Sneh (1981) Tahvonen (1982)

Fungi Coniothyrium minitans Fusarium spp. (non-pathogenic)

Sclerotinia on sunflower and oilseed rape Numerous Fusarium wilt pathogens

Huang and Kozub (1991); Whipps et al. (1993) Baker et al. (1978); Rouxel et al. (1979); Scbneider (1984); Ogawa and Komada (1985a); Paulitz et al. (1987); Garibaldi et al. (1990); Mandeel and Baker (1991); Alabouvette (1993) Marois et al. (1981) Lin and Cook (1979) Deacon (1973, 1974) Liftshitz et al. (1984a) Martin and Hancock (1986) Adams and Fravel (1993) Lin and Cook (1979) Marois et al. (1981) Liu and Baker (1980) van den Boogert and Velvis (1992) M a n (1975) Schonheck and Dehne (1977) Davis et al. (1979) Davis and Menge (1980)

Penicillium spp. Phialophora graminicola Pythium nunn Pythium oligandrum Sporidesmium sclerotivorum Trichoderma spp. Verticillium biguitatum Mycorrhizal fungi

Fusarium crown rot of tomato Fusarium avenaceum Take-all of grass pastures Pythium damping-off Pythium damping-off Sclerotinia on lettuce and other crops Fusarium avenaceum Fusarium crown rot of tomato Rhizoctonia solani Black scurf of potatoes Phytophfhora cinnamoni P. parasitica Verticillium wilt of cotton Thielaviopsis basicola

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originated from a Finnish sphagnum peat suppressive to many pathogens (Lahdenpera et al., 1991), Fusaclean, which contains a non-pathogenic strain of Fusarium oxysporum (Fo47) from a Fusarium-suppressive soil (C. Alabouvette, pers. comm.), and Biofox C, which also contains a nonpathogenic strain of F. oxysporum (251/2RB) from a Fusarium-suppressive soil (Aloi et al., 1992). B. MONOCULTURE DECLINE

Monoculture decline may be considered as a rapid development of a suppressive soil. It is typically expressed as a reduction in disease incidence when a susceptible crop is grown continually in the absence of rotation. Monoculture decline has been observed for many crops (Table 111). In the glasshouse, successive planting of radish (Raphanus sativus) in Rhizoctonia solani-infested soil led to decreased disease which was associated with the development of an active, antagonistic population of Trichoderma harzianum (Henis et al., 1978; Chet and Baker, 1980; Liu and Baker, 1980). Similarly, decline of Rhizoctonia root rot of sugar beet (Beta vulgaris) and Sclerotinia disease of sunflower (Helianthus annuus) caused by Sclerotinia sclerotiorum are related to increases in sclerotial antagonists (Hyakumachi et al., 1990; Huang and Kozub, 1991). However, with take-all decline, a complex interrelationship over time between antagonists, the wheat root and the pathogen, Gaeumanomyces graminis var. tritici, appears to be involved (Homma et al., 1979; Hornby, 1983; Cook, 1990; Simon and Sivasithamparam, 1990). Significantly, repeated plantings of potato (Solanum tuberosum) resulted in disease suppression of Verticillium wilt caused by Verticillium dahliae in some, but not all soils tested (Keinath and Fravel, 1992). Indeed, some became more conducive, again highlighting the complexity of the phenomenon of suppressive soils. Antagonistic pseudomonads, actinomycetes, fungi and amoebae may all contribute to the development of monoculture decline to different degrees in different soils. They may interact with the pathogen on the root and in infected crop residues, as well as perhaps inducing resistance to the pathogen in the roots, or depriving the pathogen of available nutrients. Nevertheless, in take-all decline situations where most research has been done, fluorescent pseudomonads antagonistic to G. graminis var. tritici are often dominant, and selected strains have given biological control of take-all when coated onto seeds and planted in naturally infested soil (Weller and Cook, 1983; Weller, 1988; Bull et al., 1991). Interestingly, reports of monoculture decline associated with Fusarium wilt diseases are rare, involving only decline of Fusarium oxysporum f. sp. melonis following continuous cropping of melon (Sneh et al., 1987) and decline of F. oxysporum f. sp. niveum with successive cropping of watermelon (Hopkins

TABLE 111 Examples of monoculture decline Pathogen

Crop

Fusarium oxysporum Gaeumannomyces graminis

Several crops including melon Wheat

Phymatotrichum omnivorum Rhizoctonia solani

Cotton Several crops including potato, radish, sugar beet and wheat

Sclerotinia sclerotiorum

Several crops including lettuce, and sunflower Potato Potato

Streptomyces spp. Verticillium dahliae

Reference

Sneh et al. (1987); Larkin ef a f . (I993a)

Shipton (1975); Cook and Rovira (1976); Hornby (1983) Cook and Baker (1983) Henis et al. (1978); Chet and Baker (1980); Liu and Baker (1980); Chern and KO (1989); Hyakumachi er al. (1990); van den Boogert and Velvis (1992); Lucas et at. (1993) Huang and Kozub (1991); Adams and Fravel (1993) Menzies (1959) Keinath and Fravel (1992)

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et a l . , 1987; Larkin et al., 1993a,b). In both cases suppression was associated with changes in the microbiota, but significantly, in contrast to other monoculture decline systems in which repeated plantings of susceptible cultivations are involved, disease suppression in these Fusarium systems was specifically associated with cropping of partially resistant cultures. This suggests that the host genotype is of considerable importance in the development of the suppressive rhizosphere microbiota. As size and composition of the rhizosphere microbiota may be plant dependent in general (Lemanceau e t a l . , 1995), in the future, it may be possible to select biocontrol organisms from disease-suppressive soils and incorporate them into soils with plants of a genotype that enhances the development of such biocontrol organisms. This could avoid the common problem of the introduced antagonist failing to establish and survive in the rhizosphere. C. ORGANIC AMENDMENTS AND COMPOSTS

Organic amendments are traditionally used to improve soil structure and plant nutrition but, there are numerous reports that their addition can also lead to control of pathogens such as Aphanomyces spp., Fusarium spp., Macrophomina phaseolina, Phymatotrichum omnivorum, Phytophthora spp., Pyrenochaeta lycopersici, Rhizoctonia solani, Sclerotinia spp., Sclerotium spp., Streptomyces spp., Thielaviopsis basicola and Verticillium spp. (Papavizas and Lumsden, 1980; Jarvis and Thorpe, 1981, Lumsden et a l . , 1983b; Hoitink and Fahy, 1986; Romero et al., 1986; Stirling et a l . , 1992; Asirifi et al., 1994; Workneh and van Bruggen, 1994; Rothrock et al., 1995; Sharma et al., 1995; Toyota et al., 1995). These amendments can take the form of crop residues, farmyard manure, mulches, composts and specially grown cover crops, often legumes, which are ploughed in as a green manure. These amendments commonly result in a highly metabolically active microbiota which can be antagonistic towards many pathogens (De Brito Alvarez el al., 1995; Liu et al., 1995c; You and Sivasithamparam, 1995). In some cases, dormant propagules such as sclerotia, chlamydospores and oospores are stimulated to germinate, but are unable to compete with the active saprotrophic microbiota in the absence of the host and are subject to nutrient stress. This leads to lysis due to starvation. An active microbiota may similarly prevent germination of propagules by continual removal of nutrients required for germination by the pathogen. In other cases, the saprotrophic microbiota may cause inhibition of germination or direct lysis of spores and hyphae through the release of antifungal metabolites per se, or through the action of volatile sulphur-containing compounds or ammonia released during decomposition of the organic material itself (Lewis and Papavizas, 1971; Lumsden et al., 1983b). Bacillus spp., Pseudomonas spp. and Streptomyces spp. as well as protozoa have all been implicated in this

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natural biocontrol (Old and Darbyshire, 1978; Malajczuk, 1979). Similarly, increases in chitinolytic organisms in soil following addition of chitin in the form of crushed shells has been associated with reductions in diseases caused by Fusarium oxysporum f. sp. phaseoli, F. oxysporum f. sp. lycopersici, Rhizoctonia solani and Sclerofium rolfsii (Mitchell and Alexander, 1962; Sneh et al., 1971; Rodriguez-Kabana ef al., 1987; Toyoda et al., 1993). Organic amendments may also serve as carriers of biocontrol agents. Grass-cuttings and rice hulls were reported to be colonized effectively by Gliocladium virens, Trichoderma harzianum and Pseudomonas spp. and were non-toxic to avocado (Persea americana) when used as a mulch for control of Phytophthora root rot caused by Phytophthora cinnamoni (Costa et al., 1994; Casale et al., 1995). However, there may sometimes be a risk associated with organic amendments. Pathogens such as Pythium spp. and Fusarium spp. may utilize the material as a food base, surviving competition or antagonism from the saprotrophic microbiota; this may lead to greater levels of disease. Also, there may be metabolites released from the decomposing organic material which are toxic to plants (Lumsden e f al., 1983b; Paulitz and Baker, 1987b; Asirifi et al., 1994). In other cases, organic amendments may have no effect upon target pathogens. For instance, incorporation of chitin, cellulose or a mixture of both materials failed to influence survival of sclerotia of Aspergillus fravus and A . parasificus in soil in the USA (Will et al., 1994). This emphasizes the need to examine each pathosystem and control measures independently. Some organic-based soil amendments have been developed recently in attempts to alter the soil environment such that specific pathogens are inhibited. For instance, addition of a series of inorganic materials to pine bark improved control of damping-off of seedlings of slash pine (Pinus elliottii var. elliottii) in soil caused by a complex of pathogens (Huang and Kuhlman, 1991a,b). In this novel mixture, control of Rhizoctonia solani was related to proliferation of Trichoderma harzianum and Penicillium oxalicurn whereas control of Pythium spp. was related to both inorganic and organic components of the mixture. This approach has been extended in Taiwan where a complex of materials based on bagasse, rice husks, oyster shell powder, urea, potassium nitrate, calcium superphosphate and mineral ash, termed S-H mixture, has been successfully used to control a range of pathogens (Lin ef al., 1990; Huang and Sun, 1991). Pathogens controlled include Fusarium spp., Phytophthora spp., Plasmodiophora brassicae, Pythium spp., Sclerotinia sclerofiorum and Sclerofium rolfsii. This rather empirical approach to the development of disease suppression could well deserve further study. Addition of composted material to soil, or more especially, potting mixes, has been widely exploited in recent years as an alternative, biological method of disease control (Hoitink and Fahy, 1986; Hoitink et al., 1991). A wide range of materials have been used for this purpose. For example, incorpora-

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tion of composted sewage sludge into soil has been shown to reduce significantly Aphanomyces root rot of peas (Pisum sarivum) caused by Aphanomyces euteiches, Fusarium wilt of cucumber (Cucumis sativus) caused by F. oxysporum f. sp. cucumerinum, Phytophthora crown rot of pepper (Capsicum sp.) caused by Phytophthora capsici, Rhizoctonia root rot of bean (Phaseolus vulgaris), cotton (Gossypium hirsutum) and radish due to Rhizoctonia solani, and Sclerotinia drop of lettuce (Luctuca sativa) caused by Sclerotinia minor (Lumsden et al., 1983a, 1986). Disease suppression was correlated with a general increase in microbial activity. Composted municipal sludge added to a peat and perlite-based container medium also suppressed damping-off of cucumber caused by Pythium ultimum (Chen et al., 1988). Similarly, composted organic household waste incorporated into sand also gave reduction of root rot of beetroot, beans and peas caused by Pythium ultimum and Rhizoctonia solani, and seed-borne Mycosphaerella pinodes on peas (Schuler et al., 1989, 1993). Interestingly, composts made from sugarcane factory wastes were suppressive to Pythium aphanidermatum (Theodore and Toribio, 1995). Here, following infestation of the compost with oospores of the pathogen, damping-off of cucumber was reduced as recovery of pathogen decreased. Again, suppression was due to an active microbial population in the compost. Most work, however, has focused on the use of composted softwood and hardwood tree barks, used either alone, or as amendments, with inert potting mix materials or with peat. Other than a few batches of light-coloured sphagnum peat which are suppressive to several soil-borne diseases (Tahvonen, 1982; Wolffhechel, 1988), most sphagnum peats are conducive to pathogens such as Pythium and Rhizoctonia spp. Much of the horticultural industry is placed at risk if these pathogens establish in such peat-based potting mixes. Further, with the realization that sphagnum peat is a non-renewable resource, greater emphasis has been placed recently on finding alternative components for potting mixes. To some extent, composted softwood and hardwood may both be ideal peat substitutes, as they can provide appropriate physicochemical characteristics for plant growth and have disease-suppressive activity. Thus, in Ohio. USA, composted softwood and hardwood barks have been found to be suppressive to Fusarium spp., Phythophthora spp., Pythium spp. and Rhizoctonia solani on a range of host plants, especially ornamentals and bedding plants (Stephens ef al., 1981; Spencer and Benson, 1982; Chef et al., 1983; Chen et al., 1988; Boehm and Hoitink, 1992). In Australia, composted eucalyptus bark has been shown to suppress Phytophthora on several woody species (Hardy and Sivasithamparam, 1995) and in Japan, composted hemlock bark has been shown to control Fusarium spp. (Kai et al., 1990). In all cases, suppression has been shown to depend upon compost age. The presence of specific antagonists such as Trichoderma harzianum may be important in some composts, or particular combinations of bacteria in

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fungi in others (Chung and Hoitink, 1990; Boehm and Hoitink, 1992; Hardy and Sivasithamparam, 1995; De Brito Alvarez et al., 1995). In general, successful suppression is related largely to development of a metabolically active microbiota (Chen et al., 1988; Inbar et al., 1991; Hardy and Sivasithamparam, 1995) in much the same way as the general suppressiveness found in suppressive soils discussed earlier in section I1 .A. Nevertheless, bark-based composts may contain a variety of chemicals that may inhibit pathogens (Kai et al., 1990; Ueda et al., 1990) and these factors, as well as other physicochemical properties associated with the composted material, may also play a role in disease suppression (Hoitink and Fahy, 1986; Hardy and Sivasithamparam, 1995). Other composted materials have been added to potting mixes to provide biocontrol. Composted solids of separated cattle manure and composted grape residues remaining after wine processing decreased Rhizoctonia solani disease on radish, Sclerotium rolfsii infection on chickpea (Cicer arietinum) and bean, and damping-off of cucumber caused by Pythium aphanidermatum (Mandelbaum et al., 1988; Gorodecki and Hadar, 1990). Similarly, composted liquorice roots suppressed damping-off in cucumber caused by P. aphanidermatum (Hadar and Mandelbaum, 1986) and composted cattle manure worked by earthworms provided suppression of Phythophthora nicotinae var. nicotinae and Fusarium oxysporum f. sp. lycopersici on tomato (Lycopersicon esculentum) and Plasmodiophora brassicae on cabbage (Brassica oleracea) (Szczech et al., 1993). D. PHYSICAL AND CHEMICAL PRACTICES

Numerous cultural practices are used in agriculture and horticulture that lead to disease control. Frequently, these effects are mediated by microbial activity and can be viewed as a form of biocontrol (Cook and Baker, 1983; Cook, 1988, 1994; Rovira et a f . , 1990). For instance, tillage may break up crop residues and expose pathogens to attack by antagonists. This procedure can also lead to a more rapid breakdown of potential foodbases by the soil microbiota which are required by pathogens for survival and infection. Both ploughing, by burying diseased residues and pathogen propagules below the root systems, and crop rotations, prolong the time during which the pathogen must survive without its host. This can result in a reduction in inoculum potential through the action of soil microbes on the pathogen propagules. Importantly, appropriate crop rotations may also help maintain antagonists at levels suitable for biocontrol (Sumner and Bell, 1994). Break crops in a rotation are also known to support populations of specific microbial biocontrol agents. For instance, natural populations of Phialophora graminicola in British grasslands may possibly delay establishment of severe take-all caused by Gaeumannomyces graminis var. tritici in subsequent cereal

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crops (Deacon, 1973; Slope et al., 1978). Here, the antagonist is thought to colonize wheat roots before G. graminis var. tritici and prevent infection, either by competing for infection sites or by inducing resistance in the plant. Mixed cropping, a practice whereby two different crops are grown together at the same time, may also reduce disease in a susceptible crop. For example, in Japan, bottle gourd (Lagenaria siceraria) has traditionally been grown in mixed cropping with Welsh onion (Allium fistulosum). In these fields Fusarium wilt (Fusarium oxysporum f. sp. lagenariae) of bottle gourd has rarely been a problem (Hasegawa et al., 1991b). This control has been attributed to bacteria, possibly Pseudomonas spp., which colonize the roots of Welsh onion and produce antifungal compounds such as pyrrolnitrin which diffuse into the rhizosphere of the bottle gourd, inhibiting the pathogen. Fertilizer application has also been implicated in natural biocontrol by stimulating indigenous fungal antagonists (Cook and Baker, 1983). For example, sulphur added to soil to maintain a low soil pH reduced root rot and heart rot of pineapple (Ananas comosus) in Australia (Pegg, 1977). Here, control was attributed to a decrease in zoosporangium formation by the pathogen, Phytophthora cinnamomi, and to an increase of an acidophilic, native Trichoderma viride. Similarly, addition of ammonium nitrogen fertilizer to soil also lowers soil pH, and this procedure resulted in a concomitant suppression of take-all of wheat caused by Gaeumunnomyces graminis var. tritici and was associated with an increase in Trichoderma spp. and development of a microbiota antagonistic to G. graminis var. tritici (Simon and Sivasithamparam, 1990). A range of other physical and chemical practices has provided biological disease control. For example, flooding soil during warm periods can control pathogens by stimulating activity of bacterial anaerobes that either decay or cause asphyxiation of pathogen propagules. Thus, flooding has been found to weaken sclerotia of the white rot pathogen (Sclerotium cepivorum) of onions (Allium spp.) in soils in the Fraser Valley of British Columbia, enabling microbial degradation of sclerotia to occur (Leggett and Rahe, 1985). Flooding has also been found to reduce populations of the bacterial wilt pathogen Pseudomonas solanacearum (Nesmith and Jenkins, 1985). Flooding can also be successfully combined with crop rotations involving rice and has been used routinely to control Fusarium wilt in China (Nelson et al., 1981), Verticillium dahliae (Butterfield et al., 1978) and Sclerotinia sclerotiorum (Stoner and Moore, 1953). Soil sterilization or fumigation has been practised for many years and, if carried out successfully, can decrease populations of pathogens whilst allowing saprotrophs to proliferate, and so maintain long-term biocontrol. Heat treatment by steaming was routinely carried out in glasshouses, but its use gradually declined as costs increased, although it may now be returning with the gradual withdrawal of soil fumigants such as methyl bromide and

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the advent of small, moveable, more cost-effective steam generators. In countries with high insolation, solarization has proven a particularly successful form of soil heat treatment on a field scale and its use is increasing in tropical and subtropical areas (Katan and DeVay, 1991). The process involves laying transparent plastic on moist soil for 2-4 weeks and is used in field and tree crops. It has been used to reduce populations of Fusarium oxysporum, Macrophomina phaseolina, Pyrenochaeta lycopersici, Phytophthora spp. , Pythium spp., Rosellinia necatrix, Rhizoctonia solani, Sclerotinia spp., Sclerotium spp. and Thielaviopsis basicola (Sztejnberg et al., 1987; Tjamos, 1992; Lodha, 1995). Frequently, antagonistic populations of bacteria and fungi develop after solarization and are able to attack heat-weakened propagules of the pathogens. Of particular note are potential antagonists such as Talaromyces jlavus and some Aspergillus spp. which are thermotolerant (Tjamos, 1992). The solarization effect can often be enhanced by combining with antagonists such as Gliocladium or Trichoderma spp. (Chet et al., 1982; Ristaino et al., 1991), suitable crop rotations (Katan et a / . , 1983), soil amendments (Ramirez-Villapudua and Munnecke, 1987; Lodha, 1995) and sublethal doses of fumigants such as metham-sodium, dazomet and methyl bromide (Frank et al., 1986; Tjamos, 1992). An alternative to heat treatment of soil is chemical fumigation with all its inherent environmental problems discussed earlier. Although primarily aimed at reducing levels of pathogens directly, there is good evidence that part of the action occurs through the stimulation of an antagonistic population of microorganisms after treatment and a weakening of surviving pathogen propagules (Katan et al., 1992). For example, Trichoderma was shown to be responsible for lasting control of Armillaria mellea on citrus (Citrus spp.) as it was more resistant than the pathogen to both methyl bromide and carbon disulphide soil fumigant treatments (Munnecke et al., 1981). Similarly, increased populations of Trichoderma spp. following soil applications of the fumigant furaldehyde were associated with a reduction in Sclerotium rolfsii disease on lentil (Lens culinaris) (Canullo et al., 1991). This approach has now been extended with various integrated biocontrol strategies. For instance, under glasshouse conditions, an application of a reduced dose of methyl bromide and a methyl bromide-tolerant strain of Trichoderma harzianum completely controlled Rhizoctonia solani on bean and had a synergistic effect on the control of R. solani damping-off in carrots (Daucus carota) (Strashnow et al., 1985). Similarly, Trichoderma application following soil application of either methyl bromide or metham-sodium fumigation improved control of Sclerotium rolfsii (Elad et al., 1983d). Combinations of the use of fungicides with biocontrol agents have also been examined. For example, a selection of fungicides applied to soil with incorporation of T. harzianum has resulted in improved control of Rhizoctonia solani and Sclerotium cepivorum (Henis et al., 1978; Abd-El Moity et al., 1982; Lifshitz et al., 1985). Similarly, metalaxyl seed treatment combined

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with soil treatment with a binucleate Rhizoctonia isolate protected cucumber from Rhizoctonia solani and Pythium damping-off as effectively as the recommended fungicide captan (Cubeta and Echandi, 1991). Integrated use of fungicides with Coniothyrium minitans or Sporidesmium sclerotivorum has also been reported (Adams and Wong, 1991; Budge and Whipps, 1995). Interestingly, application of ammonium sulphamate solution to cut stumps of karri (Eucalyptus diversicolor) was required before either of the known biocontrol agents, Hypholoma australe and Phanerochaete filamentosa, were able to reduce stump colonization by the pathogen Armillaria luteobubalinu (Nelson et al., 1995; Pearce et al., 1995). E. ROLE OF FAUNA IN NATURAL BIOLOGICAL DISEASE CONTROL

The involvement of fauna in the biological control of soil-borne plant pathogens is largely unexplored despite a huge literature on the role of soil fauna in nutrient cycling and their role as herbivore pests. Based largely on observational evidence, fauna are thought to be involved in natural suppression of soil-borne diseases either directly, by attacking or consuming hyphae or propagules, or indirectly, by transmitting propagules of the biocontrol agents through the soil. Amoebae, nematodes, mites, collembolans, sciarid larvae, beetles and earthworms have all been demonstrated to attack or consume a variety of pathogens (Table IV), but much of the work concerns feeding preference tests in vitro rather than studies in the field. Nevertheless, there have been a few experimental studies which have demonstrated that addition of fauna to soil can result in decreases in disease. For instance, the nematode Aphelenchoides hamatus reduced damage caused to wheat by Fusarium culmorum (Rossner and Nagel, 1984) and Aphelenchus cibolensis and Aphelenchus composticola reduced mortality of Pinus ponderosa caused by Armillaria mellea (Riffle, 1973). Similarly, earthworms have also been shown to reduce the level of soil-borne diseases on some plants. For example, addition of Aporrectodea trapezoides to soil artificially infested with Rhizoctonia solani reduced the severity of R. solani disease on wheat (Stephens et al., 1993b) and addition of either A . trapezoides or A . rosea to soil artificially infested with Gaeumannornyces graminis var. tritici resulted in reduced levels of take-all in wheat (Stephens et al., 1994a). Here, the earthworms may have reduced inoculum potential of both pathogens by ingesting fungal mycelia or producing unfavourable conditions for the pathogens in casts or tunnel linings. Alternatively, earthworm movement through the soil profile may have caused enough soil disturbance to decrease pathogen activity. In addition, earthworms are known to increase availability of plant nutrients and may thus have stimulated plant growth and resistance to the pathogens (Stephens et al., 1994b). Collembolans have also been used in attempts to control plant pathogens.

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TABLE IV Examples of fungal pathogens attacked or consumed by fauna Fauna Amoebae

Pathogen

Cochliobolus sativw Fusarium oxysporum Fusarium solani Gaeumannomyces graminis

Nematodes

Arthropods

Phytophthora cinammomi Thielaviopsis basicola Verticillium dahliae Fusarium culmorum Fusarium oxysporum Fusarium solani Pythium arrhenomanes Rhizoctonia solani Botrytis cinerea Fusarium oxysporum Gnomonia leptostyla Macrophomina phaseolina Pythium ultimum Rhizoctonia solani Verticillium dahliae Sclerotinia sclerotiorum

Earthworms

Aspergillus spp. Fusarium oxysporum

Reference Anderson and Patrick (1978); Homma and Ishii (1984) Pussard et al. (1979) Pussard et al. (1979) Homma et al. (1979); Chakraborty and Warcup (1985) Chakraborty and Old (1982) Anderson and Patrick (1978) Pussard et al. (1979) Rossner and Nagel (1984) Allen-Morley and Coleman (1989) Barnes et al. (1981) Rhoades and Linford (1959) Barnes et al. (1981) Hanlon (1981) Curl et al. (1985) Kessler (1990) Curl et al. (1985) El-Titi and Ulber (1991) Curl and Harper (1990); Bollen et al. (1991) Curl et al. (1985) Anas et al. (1989); Whipps (1993); Whipps and Budge (1993) Cooke and Luxton (1980) Cooke and Luxton (1980)

For example, when populations of Proisotoma minuta with Onychiurus encarpatus were added to soil artificially infested with Rhizoctonia solani, root disease of cotton was reduced significantly (Curl, 1979). Further, combinations of the collembolans with any of three fungal biocontrol agents, Gliocladium virens, Trichoderma harzianum incorporated into soil and Laetisaria arvalis applied as a seed treatment, provided a more effective disease suppression than the fungal agents used alone (Lartey et af., 1986, 1991). Proisotoma minuta with L. arvalis provided the most consistent disease control (Lartey et al., 1994). Laboratory feeding trials have demonstrated that both collembolans prefer R. solani to L . arvalis, G. virens and T. harzianum; this allows the possibility of an integrated use of collembolans and fungal agents for biological control (Lartey et al., 1989).

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Other interactions between soil fauna and biocontrol agents are known. For example, larvae of the fungus gnat or sciarid, Bradysia coprophifa,have been shown to attack and consume sclerotia of the pathogen Scferotinia sclerotiorum (Anas and Reeleder, 1988a,b; Anas et al., 1989). However, in part, degradation of sclerotia in soil is due to attack by Trichoderma viride. Here, the mycoparasite invades the sclerotia after they have been weakened due to both direct feeding by the larvae and the activity of a chitinase present in the saliva of the animal (Anas et af., 1989). Sclerotia of S. sclerotiorum, possibly made more palatable following infection with the mycoparasite Coniothyriurn minitans, can also be attacked by sciarid larvae, collembolans, slugs and mites and may result in localized dispersal of the biocontrol fungus (Turner and Tribe, 1976; Trutmann et al., 1980; Whipps, 1993; Whipps and Budge, 1993; Williams and Whipps, 1995). In the case of collembolans, mites and sciarid larvae, spread of C. minitans from infected sclerotia to uninfected sclerotia has been demonstrated in soil and may reflect a natural dispersal mechanism (Whipps and Budge, 1993; R. H. Williams and J . M. Whipps, unpublished data). Similarly, Trichoderma spp. are carried through soil by collembolans and earthworms (Wiggins and Curl, 1979; Visser, 1985), arbuscular mycorrhizal fungi may be spread by a range of soil fauna (McIlveen and Cole, 1976; Rabatin and Stinner, 1988), and earthworms may enhance spread of the biocontrol agent Pseudornonas corrugata in soil and on roots (Stephens et al., 1993~). These observations clearly indicate that soil fauna can be involved in the biocontrol of soil-borne plant pathogens in several ways. However, detailed ecological studies must be carried out before widespread release of soil fauna, with or without biocontrol agents, should take place. Once released, there is little control of animal spread and many of those fauna under study at the moment are known, in some circumstances, to act as minor pests or as vectors of pathogens. For example, many mites and collembolans can carry pathogen spores such as Fusarium and Verticiffiumon their exoskeletons (Parkinson et a f . , 1979; Visser, 1985), sciarid larvae and mites may transfer oospores of Pythium spp. via their gut (Shew, 1983; Gardiner et a f . , 1990) and collembolans, mites and nematodes are known to feed on mycorrhizal fungi and interfere with mycorrhizal establishment (Warnock et al., 1982; Kaiser and Lussenhop, 1991; Ingham, 1992). The interactions between animals, plants, pathogens and biocontrol agents in the soil and rhizosphere clearly deserve further study.

111. MODES OF ACTION Several modes of action of microbial biocontrol agents have been identified, none of which are mutually exclusive. These can involve interactions between the antagonist and pathogen directly, either associated with roots and seeds

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or free in the soil. Three direct modes of action are known: competition, where demand exceeds immediate supply of nutrients o r space; antibiosis, where antagonists secrete metabolites harmful to pathogens; and parasitism, where nutrients of the pathogen are utilized by the biocontrol agent. Alternatively, indirect interactions are known where the plant itself responds to the presence of the antagonist, resulting in induced resistance or perhaps plant growth promotion. Often, one antagonist may exhibit several modes of action simultaneously or sequentially. Also, in the case of natural biocontrol in some suppressive soils, several antagonists exhibiting a range of modes of action may act in concert to control disease (Alabouvette er al., 1993). Great impetus has been given to the study of modes of action in recent years as, with an understanding of the mode of action of a successful biocontrol agent, selection and screening systems can be focused to obtain more antagonists operating in the same way. Further, through molecular biology, the study of modes of action also offers the possibility of improving biocontrol activity directly, perhaps by increasing expression of key genes or deleting undesirable traits (see later in section 111). Significantly, it is through the use of modern molecular techniques that many of the modes of action have been clearly defined. A.

DIRECT MODES OF ACTION

1. Competition Competition for space or specific infection sites on roots and seeds has been suggested as a mode of action for control of numerous soil-borne pathogens, but relatively few studies have provided unequivocal evidence of this hypothesis. Indirect observations on several plant species have shown that in the presence of non-pathogenic strains of Fusarium oxysporum, intensity of root colonization by pathogenic strains of F. oxysporum was decreased (Schneider, 1984; Mandeel and Baker, 1991; Eparvier and Alabouvette, 1994). Competition between non-pathogenic and pathogenic strains of F. oxysporum was also shown to occur within roots and stems (Postma and Rattink, 1991). However, the level of competition differed between non-pathogenic strains of Fusarium, suggesting that a range of mechanisms may be involved in natural biocontrol by non-pathogenic strains of Fusarium (Eparvier and Alabouvette, 1994). Nevertheless, as levels of control of Fusarium wilt by non-pathogenic strains of Fusarium are known to be dependent on the relative inoculurn potentials (Paulitz et al., 1987; Postma and Rattink, 1991), the case for competition between non-pathogenic and pathogenic strains of Fusarium for either space or nutrients is strengthened. Competition for infection sites involving binucleate Rhizoctonia spp. and

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hypovirulent R. solani isolates has also been shown to occur with pathogenic isolates of R. solani (Herr, 1995). For example, a hypovirulent isolate of Rhizoctonia solani densely colonized the outer surface of roots and hypocotyls of cotton and radish with concomitant decrease in disease caused by pathogenic R. soluni (Sneh et al., 1989a,b; Ichielevich-Auster et al., 1985). Significantly, as the hypovirulent isolates did not provide seedlings with protection from attack by Pythium spp., Fusarium spp. and Sclerotium rolfsii, it was suggested that the hypovirulent isolate was only able to provide a barrier to root contact or compete for recognition and infection sites with the virulent isolate of R. solani, and was not a general resistance phenomenon. Several fungi have also been shown to control take-all of wheat caused by Gaeumannomyces graminis var. tritici through occupation of sites on the root. These include Phialophora spp., G. graminis var. graminis and Idriella bolleyi (Deacon, 1974; Wong and Southwell, 1980; Kirk and Deacon, 1987). Interestingly, I. bolleyi exploits the naturally senescing cortical cells of cereal roots during the early stages of the crop and thus outcompetes the pathogen for infection sites and nutrients. Rapid production of spores, which are then carried down the root by water, continue the root colonization process and this is suggested to be a key feature in the establishment of this biocontrol agent on the root (Lascaris and Deacon, 1991; Allan et al., 1992; Douglas and Deacon, 1994). Ectomycorrhizal fungi, by way of their physical sheathing of the root, are another obvious group which may provide biocontrol from root pathogens through occupation of infection sites. The mechanism was suggested over 20 years ago where some evidence for protection of pine roots from infection by Phytophthora cinnamomi was provided (Marx, 1972). However, significant supporting work for this possible mode of action for ectomycorrhizal fungi has not been forthcoming with biocontrol focusing on antibiotic production and, more recently, induced resistance (Perrin, 1990; Duchesne, 1994). In contrast to the relatively small literature on competition for space, which largely concerns fungi, there have been a great number of studies investigating competition for nutrients, which involve both bacteria and fungi. Competition for carbon and nitrogen derived from root and seed exudates and from plant residues has been examined but, in recent years, competition for iron has been studied in great detail as analytical and molecular biological techniques have improved. Evidence for competition for carbon and nitrogen between biocontrol agents and pathogens in soil has been obtained by observing germination of pathogen propagules, development of pathogen populations or infection of plants in the presence or absence of the biocontrol agent. Addition of nutrients, either directly or coming from seeds or roots, as well as manipulation of the environment, have been used as tools in these studies.

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Thus, carbon added to soils suppressive to Fusarium wilt was rapidly utilized and was related to a large population of non-pathogenic fusaria (Alabouvette et al., 1984). This metabolically active population of nonpathogenic fusaria was able to deprive chlamydospores of the pathogen of the nutrients needed for germination and thus provide suppressiveness (Mandeel and Baker, 1991; Couteadier, 1992). However, in addition, suppressiveness was also related to iron availability of the soil (Lemanceau et al., 1993). Competition for carbon and possibly nitrogen may also be involved in the biocontrol of Fusarium oxysporum f. sp. melonis and F. oxysporum f. sp. vasinfectum by Trichoderma harzianum (Sivan and Chet, 1989a), and also in suppression of Pythium aphanidermatum damping-off on several crops due to the activity of a range of antagonistic bacteria (Elad and Chet, 1987). Importantly, in both of these studies, other modes of action were shown to be relatively unimportant under the experimental conditions employed, allowing competition for nutrients to be clearly identified. In contrast, competition for thiamine has been suggested as just one possible mode of action in the control of Gaeumannomyces graminis var. tritici by a sterile red fungus in the rhizosphere of wheat (Shankar el al., 1994). Competition for volatile organic materials derived from germinating seeds which may stimulate spore germination may also be involved in biocontrol of Pythium ultimum by Pseudomonas putida NIR (Paulitz, 1991). Hyphal growth from sporangia of P. ultimum was stimulated by volatiles from germinating seeds of pea and soybean (Glycine max), and the stimulation was reduced when seeds were treated with P. putida. It was suggested that P. putida utilized the active moieties, ethanol and acetaldehyde, arising from the germinating seeds, thus providing biocontrol. Here again, other modes of action such as antibiosis and competition for iron were eliminated (Paulitz, 1991; Paulitz and Loper, 1991). The ability to compete for, and utilize materials from, germinating seeds and young roots has also been reported as a mode of action for other pseudomonads controlling Pythium ultimum on sugar beet (Stephens et al., 1993a; Fukui et al., 1994) and P. aphanidermatum on cucumber (Zhou and Paulitz, 1993). Enterobacter cloacae also competed for seed derived nutrients in the spermosphere during the control of P. aphanidermatum on cucumber (Maloney et al., 1994). Competition for plant residues is another area where biocontrol can operate. For example, when Pythium nunn was added to soil concurrently with plant residues, both disease incidence and the increase in population of Pythium ultimum which normally occurred following addition of plant residue alone were suppressed (Paulitz and Baker, 1987a,b). Similarly, under conditions of high soil salinity, Pythium oligandrum was able to outcompete P. ultimum for occupation of cotton residues, resulting in suppression of seed and seedling rot of cotton (Martin and Hancock, 1986). Pythium oligandrum was more tolerant of elevated chloride levels than P. ultimum and addition

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of P. oligandrum and chloride to conducive soil gave greatest suppression of P. ultimum colonization of cotton leaf debris. Nevertheless, success for any one organism in such competitive situations may depend on the relative inoculum levels. For example, although addition of P. nunn at 300 propagules per gram to a peathand mix containing 1% ground rolled oats resulted in a reduction of population densities of Phytophthora cinnamomi, Phytophthora citrophthora and one of two isolates of P. parasitica, root rot of azalea (Rhododendron spp.) caused by P. cinnamomi or P. parasitica was not suppressed (Fang and Tsao, 1995a). However, when P. nunn was incorporated at 1000 propagules per gram peathand mix, suppression of Phytophthora disease in sweet orange (Citrus sinensis) by P. nunn was increased. Competition for iron, mediated by production by antagonistic microorganisms of iron-chelating moieties, termed siderophores, has been conclusively demonstrated as a mode of action for biocontrol in soils where iron is limiting. Characteristically, these soils have a pH at or above 7. Evidence has been obtained either using Tn5 siderophore-minus mutants of biocontrol strains (Kraus and Loper, 1992; Duijff et al., 1994a) or by addition of purified siderophores or synthetic iron chelators to soil (Kloepper et al., 1980a,b; Elad and Baker, 1985; van Peer et al., 1990a), which has resulted in loss of activity or reproduction of biocontrol respectively. Several species of bacteria have been shown to be active biocontrol agents by competing for iron (Leong, 1986), but the most widely recognized are fluorescent pseudomonads. Pseudomonads produce a range of siderophores including pseudobactins and pyoverdines which are fluorescent, as well as non-fluorescent phyochelins and salicylic acid, but it is the fluorescent siderophores, which have a very high affinity for iron, that are generally implicated in biocontrol (Dowling and O’Gara, 1994). These potent iron chelators are thought to sequester the limited supply of iron that is available in the rhizosphere to a form that is unavailable to pathogenic fungi and other deleterious microorganisms, thereby restricting their growth. However, the observation that fluorescent pseudomonads commonly utilize ferric siderophores produced by other microorganisms (Leong et al., 1991; Jurkevitch et al., 1992; Raaijmakers et al., 1995b) and that siderophore-minus mutants in the rhizosphere can establish at population levels equivalent to siderophore-plus strains (Schippers et al., 1987; Loper and Buyer, 1991), suggests that simple production of siderophores is not enough to result in biocontrol activity. Indeed, some highly active biocontrol strains only produce one siderophore but have several different siderophore receptors in their membranes (Marugg et al., 1989; Koster et al., 1993; Morris et al., 1992a). It may be that the ability to utilize several siderophores is of key importance in biocontrol in some cases. Using Tn5 mutagenesis, siderophore production by Pseudomonas spp. has been shown to be important in the control of both Pythium and Fusarium

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spp. For example, pyoverdine production was responsible for control of Pythium uftimum damping-off of cotton and wheat (Loper, 1988; Becker and Cook, 1988) and pyochelin production was involved in control of Pythium damping-off of tomato by Pseudomonas aeruginosa (Buysens et al., 1993a, 1994). However, siderophores were not important in the control of Pythium damping-off in cucumber (Kraus and Loper, 1992; Paulitz and Loper, 1991) as too little pyoverdine was thought to be produced in time to prevent the pathogen invading the germinating seedling (Loper et a f . , 1994). This is in contrast to cotton, where the slow germination process allows inhibitory levels of siderophores to be produced. Production of siderophores by Pseudomonas spp. was also shown to be important in control of Fusarium wilt of carnation (Dianthus caryophylfus) caused by F. oxysporum f. sp. dianthi in rockwool-grown plants (van Peer et a f . , 1990a, Duijff et al., 1993, 1994b, 1995). However, strains differed in the degree by which control was mediated by siderophore production. For example, Pseudomonas sp. WCS358 produced pyoverdine and Tn5-minus mutants gave no control. In contrast, P. putida (renamed P.JEuorescens) WCS417r was demonstrated to have several modes of action, of which siderophore production was just one. The pH and cultivar of carnation also affected the level of control obtained with P. JEuorescens WCS417r. Further, control depended upon the inoculum level of the pathogen and availability of iron. With Pseudomonas sp. WCS358, control of Fusarium wilt of carnation was best if pathogen levels were moderate and ferric iron was at low levels (Duijff et al., 1994a). In contrast, if pathogen levels were high, siderophore production alone was not sufficient to reduce Fusarium wilt disease of carnation significantly (Duijff et a f . ,1991). Control could be achieved under these environmental conditions if Pseudomonas sp. WCS358 was applied in combination with a nonpathogenic Fusarium oxysporum strain which acted through competition for carbon (Lemanceau et a f . , 1992). A very similar series of experiments was also carried out by the same group using radish (Raphanus sativus) as the test plant (Leeman et a f . , 1995b,c, 1996a,b; Raaijmakers et al., 1995a). This time, P. JEuorescens WCS374, used commercially to control Fusarium wilt of radish, and WCS417r were found to act largely through induced resistance (Leeman et al., 1995c; Raaijmakers et al., 1995a). Nevertheless, the efficiency of the siderophore-mediated disease suppression and induced resistance was highly dependent on the level of disease incidence and iron availability (Raaijmakers et a f . ,1995a; Leeman et a f . , 1996b). Interestingly, the pseudobactin and salicylic acid produced by P. fluorescens WCS374 induced systemic resistance to Fusarium wilt of radish but the pseudobactins of strains WCS358 and WCS417 did not, leading to the suggestion that the role of siderophore-mediated competition for iron in suppression of disease by fluorescent Pseudomonas spp. deserves reevaluation (Leeman ef al., 1996b). Biocontrol or plant growth promotion observed following addition of

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25

fluorescent pseudomonads to soil may not always involve production of siderophores or competition for iron, even under conditions of low iron availability. For example, a fluorescent pseudomonad NZ130 which inhibited Pythium ultimum produced a fungistatic metabolite under low iron conditions which was not a siderophore and its production was antagonized by iron (Gill and Warren, 1988). Similarly, P. fluorescens CHAO produced maximum concentrations of the hydrogen cyanide (HCN) required for suppression of black root rot of tobacco caused by Thielaviopsis basicola in iron-replete media (Voisard et al., 1989). A pyoverdine-minus mutant of CHAO produced HCN and suppressed tobacco black root rot but only under iron-replete conditions (Keel et al., 1989). The lack of biocontrol activity of the siderophore-minus mutant in iron-deficient soils was attributed to poor HCN production rather than a siderophore effect. Many of the studies carried out in the 1980s suggested that biocontrol or plant growth promotion observed or associated with the presence or application of fluorescent pseudomonads in the soil was related to the production of siderophores. For instance, siderophores were thought to be involved with control of Erwinia carotovora (Xu and Gross, 1986), Fusarium oxysporum (Scher and Baker, 1982), Gaeumannomyces graminis var. tritici (Weller and Cook, 1983), Pythium ultimum (Loper, 1988), Thielaviopsis basicola (Ah1 et al., 1986) or ill-defined deleterious microorganisms (Kloepper et al., 1980a; Bakker et al., 1986; Yuen and Schroth, 1986; Schippers et al., 1987). Whereas some molecular studies have subsequently demonstrated this suggestion to be true, others have shown the siderophore production to be purely coincidental and not the major mode of action. Several of these studies have already been described above and, certainly, antibiotic rather than siderophore production seems to be the main mode of action of Pseudomonaspuorescens 2-79 in its control of Gaeumannomyces graminis var. tritici (Hamdan et a f . , 1991). Nevertheless, until comprehensive molecular studies such as these have been completed, the role of any metabolite or enzyme in biocontrol or growth promotion cannot be certain . 2. Antibiotic production Antibiotics are generally considered to be metabolites that can inhibit microbial growth. Often these are secondary metabolites produced by antagonists when nutrients become limiting and are frequently of relatively low molecular weight (
26

J . M. WHIPPS

antagonist in vivo based solely on observations made in vitro of inhibition of growth of a plant pathogen. At least the moieties produced by the antagonist must be determined and then the putative active moieties must be isolated from the soil, rhizosphere or spermosphere where control is thought to act. Thus, against this background, the production and release by antagonists of lytic enzymes such as chitinases, /3-1,3-glucanases, proteases and lipases, which are capable of degrading fungal tissue during biocontrol and could be mistaken for antibiotics in in vitro tests, are considered in section III.A.3 on parasitism. It would seem more likely that these enzymes play a key role during the parasitic process, especially during penetration of cell walls of the host by antagonistic fungi, where production may be regulated, rather than in an energetically wasteful constitutive release which can occur in antibiotic production per se. Evidence for a role for antibiotics in biocontrol by both fungi and bacteria has come from a combination of several different lines of study (Weller and Thomashow, 1993). Briefly, these have involved observations showing: (1) that many biocontrol agents produced antibiotics; (2) that for some agents there was a correlation between antibiotic production and biocontrol efficacy; (3) that purified antibiotics, or cell-free filtrates or extracts of filtrates of some agents, could mimic the effect of the whole agents; and (4) that antibioticdeficient mutants were less suppressive than wild-types. The latter studies (4) have been particularly extended with bacterial agents where genetic manipulation is easier. In general, the strategy adopted has involved site-directed mutagenesis (e.g. using transposons) followed by screening for loss of the trait, preparation of a genomic library of wild-type DNA, genetic complementation of the mutant to restore the target trait, and finally, comparison of the biocontrol abilities of the parental strain, mutant and complemented mutant. The mutant should be impaired in disease suppressiveness and complementation should restore activity if the trait is important. Antibiotic production by fungi exhibiting biocontrol activity has been most commonly reported for isolates of Gliocladium (Howell et al., 1993; Wilhite et al., 1994), Talaromyces Pavus (Kim et al., 1990) and Trichoderma (Ghisalberti and Sivasithamparam, 1991; Scarselletti and Faull, 1994; Huang et al., 1995; Wada et al., 1995). Recently antibiotics have also been at least partially characterized from Chaetomium globosum (Di Pietro et al., 1992), Minimedusa polyspora (Beale and Pitt, 1995) and Verticillium biguttatum (Morris et al., 1995a). These fungi may exhibit other modes of action in addition to antibiosis. Of particular interest here are those where biocontrol activity has a definite link with production of specific antibiotics. For example, production of gliotoxin (an epidiothidiketopiperazine) by Gliocladium virens G20 (synonym GL-21) appears to be implicated as the key factor in its biocontrol activity against Pythium ultimum and Rhizoctonia solani (Wilhite et al., 1994). In vitro inhibition of growth and germination

BIOLOGICAL CONTROL OF SOIL-BORNE PLANT PATHOGENS

27

of P. ultimum and cytoplasmic leakage from R. solani caused by the presence of culture filtrates or extracts of G. virens G20 was attributed to this metabolite (Roberts and Lumsden, 1990; Lewis et al., 1991b). Following incorporation of G. virens in soil and soil-less media, gliotoxin was produced and the media became suppressive to P. ultimum with maximum accumulation of the metabolite occurring at the same time as greatest disease suppression (Lumsden and Locke, 1989; Lumsden et al., 1992a,b). Further, gliotoxin-minus mutants displayed only 54% of the Pythium diseasesuppressive activity on zinnia compared with the wild-type isolate and exhibited a near total loss of antagonistic activity in vitro towards P. ultimum (Wilhite et al., 1994). Several specific polypeptides associated with gliotoxin production have been isolated from G. virens G20 and these may facilitate the identification and characterization of genes expressed during gliotoxin production (Ridout et al., 1992; Ridout and Lumsden, 1993). Nevertheless, the quantity and quality of antibiotics produced by different strains of G. virens can vary markedly and thus reflect on the disease control obtained. Host plants may also have an effect. For instance, some strains in the “P’ group produced the antibiotics gliovirin (a diketopiperazine) and heptelidic acid, but not gliotoxin and dimethyl gliotoxin which characterized strains of the “Q” group (Howell et al., 1993). Gliovirin was very inhibitory to P. ultimum but had no activity against R. solani; “P” strains that produced gliovirin were more effective biocontrol seed treatments against P. ultimum damping-off in cotton than those “Q” strains which produced gliotoxin but no gliovirin. Correspondingly, “Q” strains were more effective against R. solani than P. ultimum when used as cotton seed treatments. Nevertheless, gliotoxin-minus mutants exhibited biocontrol efficacy against R. solunimediated seedling disease equivalent to that of wild-type gliotoxin-producing strains, indicating that gliotoxin was not necessary for protection of the infection court of cotton from R. solani (Howell and Stipanovic, 1995). As mycoparasitism did not seem to be important in biocontrol of R. solani on cotton by G. virens (Howell, 1987), it was suggested that competition may need to be re-evaluated as a mode of action for this biocontrol agent with this host-pathogen combination. The ability of nine strains of Chaetomium globosum to produce the antibiotic chaetomin (an epithiodiketopiperazine) in liquid culture was correlated with efficacy to suppress Pythium damping-off of sugar beet in heat-pasteurized soil (Di Pietro et al., 1992). In addition, chaetomin was extracted from pasteurized soil infested with C . globosum strains Cg-13, an effective biocontrol strain, but not from pasteurized soil inoculated with a spontaneous variant of Cg-13 unable to suppress Pythium damping-off. This further supports the suggestion that chaetomin production in soil plays an important role in antagonism of C. globosum against P. ultimum. Production of glucose oxidase by Talaromyces flavus Tf-1 has been shown to be responsible for biocontrol of Verticillium wilt caused by Verticiflium

28

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dahliae (Fravel et al., 1987; Fravel and Roberts, 1991). Glucose oxidase suppressed radial growth of V. dahliae in vitro and killed microsclerotia of V. dahliae in vitro and in soil. Glucose oxidase exhibited antibiotic activity in the presence of glucose due to the formation of the reaction product, hydrogen peroxide (Kim et al., 1988, 1990). A single-spored variant, Tf-1-np, which produced 2% of the level of glucose oxidase activity of the wild-type, did not control Verticilliurn wilt of eggplant (Solanum melongena) in non-sterile field soil in a greenhouse experiment, whilst the wild-type significantly reduced the incidence of wilt (Fravel and Roberts, 1991). Importantly, purified glucose oxidase of Tf-1 significantly reduced the growth rate of V. dahliae in the preseng, but not in the absence, of eggplant roots, suggesting that a supply of glucose from the roots was of major importance. There are a large number of bacterial biocontrol agents which produce antibiotics (Table V) and different antibiotics appear to be important for the control of different fungal pathogens. Indeed, many individual strains can produce a spectrum of antibiotics and secondary metabolites which have been characterized to various degrees (e.g. Rosales et al., 1995) but not all are important in biocontrol. For example, Pseudomonas fluorescens CHAO produced 2, 4-diacetylphloroglucinol (Phl), pyoluteorin (Plt), pyrrolnitrin (Pln) and HCN as well as a pyoverdine siderophore and indole-3-acetic acid (IAA) (Haas et al., 1991; Maurhofer et al., 1994a; Voisard et al., 1994), but only the antibiotics and HCN were important in disease biocontrol. Similarly, P. jluorescens 2-79 produced phenazine-carboxylic acid (PCA) , pyoverdine and anthranilic acid, with biocontrol activity due mainly to phenazine production (Hamdan et al., 1991; Ownley e/ al., 1992), and P. JEuorescens Pf-5 produced Phl, Pln, Plt, HCN and pyoverdine, with Plt most active against Pythium ultimum (Loper et al. , 1994). Bacterial isolates with similar biocontrol activity may also have a similar spectrum of antibiotic production. For instance, four strains of P. fluorescens from the rhizosphere of wheat in a take-all-suppressive soil produced Phl and HCN (Harrison et al., 1993). Significantly, it is clear from Table V that even for a single strain of bacterium such as P. fluorescens CHAO, different individual antibiotics may be relatively more important in the suppression of some diseases than others. importantly, antibiosis generally only contributes to, rather than accounts for, all the biocontrol activity of a single strain. Other modes of action such as competition or induced host resistance may also play a part. An alternative feature of this mode of action is that specific strains of pathogen may exhibit resistance to individual antibiotics. For example, isolates of Caeumannomyces graminis var. tritici varied in sensitivity to PCA and Phl produced by P. fluorescens 2-79 and P. chlororaphis (formerly P. aureofaciens) 30-84 (Mazzola el al., 1995). This led to the suggestion that mixtures of Pseudomonas spp. or isolates that exhibit different modes of action should be employed to control this disease in the field.

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29

Another approach to improve biocontrol activity could involve increasing the production of antibiotics by specific strains of bacteria. For instance, phenazine production by P. jluore.scen.7 2-79 and P. aureofaciens 30-84 was increased by introducing extra copies of biosynthetic or activator genes (Thomashow and Pierson 111, 1991; Pierson 111 and Keppenne, 1992). This procedure could perhaps be useful with P. Puorescens Pf-5, which produced enough Plt to inhibit Pythium ultimum in vitro and on seeds of cress (Lepidium sativum), but amounts may have been insufficient to suppress P. ultimum on cucumber (Loper et al., 1994). On cucumber, the suppression of P. ultimum by P. fluorescens Pf-5 depended on mechanisms other than Plt production (Kraus and Loper, 1992). Through use of the molecular strategies described earlier, good evidence for the involvement of antibiotics in biocontrol by bacteria has been obtained for most of the examples cited in Table V. Pseudomonas spp. have been by far the most intensively studied and this area has recently been thoroughly reviewed (Weller and Thomashow, 1993; Loper et al., 1994; Keel and Defago, 1997). Additional evidence for a role of antibiotics in biocontrol by Pseudomonas spp. has been obtained by heterologous expression of complementary genes in strains that naturally do not produce the antibiotic, thus increasing their biocontrol activity (Voisard et a l . , 1989; Fenton et al., 1992; Hara et al., 1994; Hill et al., 1994) or by use of Tn5 mutagenesis to inactivate specific genes and affect pathways of antibiotic production (Schnider et al., 1995b). Also, in situ detection of antibiotics in the rhizosphere of plants treated with producing strains has been demonstrated for PCA (Thomashow et al., 1990), Phl (Keel et al., 1992; Maurhofer et al., 1995), Plt (Maurhofer et al., 1995) and Pln (Kempf et al., 1994). Further, by fusing reporter genes such as those encoding P-galactosidase or ice-nucleating activity to promoters of genes encoding for antibiotics, in situ expression of the genes required for the synthesis of OomycinA, phenazines, Plt and pyoverdine on roots or seeds by biocontrol agents has been obtained (Howie and Suslow, 1991; Georgakopoulos et af., 1994; Loper and Lindow, 1994; Kraus and Loper, 1995). Recently, there has been considerable interest in the observation of a two-component regulatory system for antibiotic production in Pseudornonas spp. (Loper et al., 1994; Keel and Defdgo, 1997). The system is based on two protein components, an environmental sensor (possibly a transmembrane protein) and a cytoplasmic response regulator or global activator (GacA) that mediates changes in response to sensor signals. The environmental sensor was first detected in the plant pathogen, Pseudomonas syringae, and was coded by the lemA gene (Hrabak and Willis, 1992) and then another was isolated from Pseudomonas virid@ava coded by the repA gene (Liao et al., 1994). Subsequently, a lemA-like apd gene was found in the biocontrol strain P. fluorescens Pf-5. Strains with a mutation with this region failed to produce Plt, Pln, HCN, tryptophan sidechain oxidase and an extracellular protease

TABLE V Examples of antibiotics or antifungal metabolites (excluding metal chelators and enzymes) produced by bacteria which may be involved in disease biocontrol Antibiotic

Bacterium

Pathogenhost

Agrocin 84

Agrobacteriurn radiobacter K84

Agrocin 434 ALS 84 Ammonia

A. radiobacter K434 A . radiobacter K84 and K1026 Bacillus cereus UW85 Enterobacter cloacae

2,4-diacetyl phoroglucinol

Pseudornonas sp. F113

A. turnefaciens on several woody species A. turnefaciens (biovar 2) A. turnefaciens Phytophthora cactorurn Pythiurn ultirnurn on several plant species Pythiurn ultimurn on sugar beet Gaeurnannomyces grarninis var. tritici on wheat G. grarninis var. tritici on wheat Thielaviopsis basicola on tobacco Thielaviopsis basicola on tobacco Sclerotinia sclerotiorurn on sunflower

Pseudomonas aureofaciens Q2-87 Pseudornonas fiuorescens CHAO

HCN Monochloroaminopyrrolnitrin

Pseudornonas fiuorescens CHAO Pseudornonas cepacia 582

Reference Jones and Kerr (1989) Donner et al. (1993) Pefialver ef al. (1994) Gilbert et al. (1990) Howell et al. (1988) Fenton et al. (1992); Shanahan et al. (1992) Vincent et al. (1991) Keel et al. (1992) Keel et al. (1990, 1992) Voisard et al. (1989) McLoughlin et al. (1992)

Oomycin A Phenazine- 1-carboxylic acid

Pyoluteorin

Pseudomonas fluorescens HV37a Pseudomonas fluorescens 2-79

Pythium ultimum on cotton

Pseudomonas fluorescens 30-84

G. graminis var. tritici on wheat

Pseudomonas fluorescens Pseudomonas fluorescens CHAO Pseudomonas fluorescens Pf-5 Pseudomonas cepacia B37W

Pythium ultimum on cotton Pythium ultimum on cress

G. graminis var. tritici on wheat

Pseudomonas cepacia RB425

Pythium ultimum on cress Fusarium sambucinum dry rot of potato Sclerotinia sclerotiorum on sunflower Rhizoctonia solani on radish

Pseudomonas puorescens

Rhizoctonia solani on cotton

Zwittermycin A

Bacillus cereus UW85

Unknown antibiotic B

Bacillus cereus UW85

Unknown antibiotic

Pseudomonas aureofaciens PA147-2

Phythophthora medicaginis seedling disease of alfalfa P. medicaginis seedling disease of alfalfa Phytophthora megasperma root rot of asparagus

Pyrrolnitrin

Pseudomonas cepacia 582

Gutterson (1990); Howie and Suslow (1991) Thomashow and Weller (1988); Thomashow et al. (1990) Thomashow et al. (1990); Pierson I11 and Thomashow (1992) Howell and Stipanovic (1980) Maurhofer et al. (1994a) Kraus and Loper (1995) Burkhead et al. (1994) McLoughlin et al. (1992) Homma and Suzui (1989); Homma et al. (1989) Howell and Stipanovic (1979); Hill et al. (1994) Silo-Suh et al. (1994) Silo-Suh et al. (1994) Carruthers et al. (1995)

32

J. M. WHIPPS

and lost ability to inhibit Rhizoctonia solani in culture (Kraus and Loper, 1992; Loper et a f . , 1994; Corbel1 and Loper, 1995). A response regulator gene, gacA, was first identified in the biocontrol strain P. fluorescens CHAO and strains with a mutation in this gene lost the ability to produce Phl, Plt and HCN (Laville et al., 1992) and two exoenzymes, protease and phospholipase C (Sacherer ef al., 1994). In addition, antibiotic production in Pseudomonas spp. may be further controlled by the action of housekeeping sigma factors encoded by the rpoS or rpoD genes (Sarniguet and Loper, 1994; Schnider ef a f . , 1995a), indicating the complexity of these regulatory systems. Similar gacA-like genes have also been found in P. fluorescens BL915 (Gaffney et al., 1994) and P. syringae (Rich et al., 1994). The physiological and environmental triggers that affect the expression of the lemAlgacA system are not known, but autoinducing compounds, possibly N-acylhomoserine lactones, which are signals for secondary metabolism and virulence factors in many bacterial species (Bainton et al., 1992; Williams et al., 1992; Pearson et af., 1995), may be involved in phenazine production in P. aureofaciens 30-84 (Pierson I11 ef al., 1994). Significantly, genes encoding synthesis of pyoverdine siderophores are not under the lemAlgacA regulatory system, as gacA-, lemA- and apd- mutants all produce these siderophores (Kraus and Loper, 1992; Laville et al., 1992; Willis ef al., 1994). This indicates the independence of Competition for iron mediated via siderophores and antibiosis in Pseudomonas spp. A final point worth considering before leaving this section concerns the overall ecological significance of antibiotic production. From studies with Pseudomonas strains suppressive to Gneumannomyces graminis var. tritici, there is some evidence that antibiotic production may have effects on the microbial community at large. Thus mutants of P. fluorescens 2-79 and P. aureofaciens 30-84 that were deficient in PCA production exhibited reduced survival in soil compared with parental, wild-types (Mazzola et al., 1992). It was suggested that the mutants were less able to compete with the resident microbiota. Consequently, it may well be that an observed biocontrol effect that is mediated through antibiotic production is actually the result of a survival or competitive mechanism which evolved within the soil microbial population as a whole. 3. Parasitism There are numerous reports of parasitism of plant pathogens by both bacteria and, especially, fungi. Many of these antagonists have been shown to act as biocontrol agents when applied to soil, seeds or roots in separate trials or experiments. However, by necessity, most of the studies of the processes involved in parasitism are based on in vifro work and certainly some care should be exercised when extrapolating observations made in the laboratory to the field. Indeed, due to the relatively ephemeral nature of the mycelium

BIOLOGICAL CONTROL OF SOIL-BORNE PLANT PATHOGENS

33

TABLE VI Exumples of buctericr exhibiting purasitisni qf' .soil-borneplant putkogetu Bacterium - _ _ _ ~ _ .

Pathogen ~~

~

Actinoplunes spp.

Phytophtharu megusperma

Arthrobucter spp.

Pyfhium spp. Pythiiini deburyunurn

Bacillus spp.

Sclerothtn cepivorum

Coryneforms

Sclerotiiirn cepivoruni

Enterohucter ngglomeruns Pseudornonud cepaciii

Rhizoctoniu solani Pythium ultirnum Rhizoctoniu soluni Sclerotiunr rolfsii Rhizoctoniu solani Sclerotiirni roljiii Alternuria bmssicolo Botrytis cinereu Phomopsis sclerotioides Mycocentrosporn ucerinu Sclerotinia sclerotioricm

Serrutia niurcescens Streptomyces griseoviridis

__

Reference ~~

._

Filtnow and Lockwood ( 1985) Khan ei al. (1993) Mitchell and Hurwit? ( 1965) Wong and Hughes (1986); Backhouse and Stewart (1989) Wong and Hughes ( 1986)

Chernin et ul. (1995) Fridlender et ul. (1993) Ordentlich et al. (1987. 1988) Tapio and PohtoLahdenpera (1991)

of most plant pathogens in soil or the rhizosphere, the demonstration of parasitism in nature is frequently limited to the observation of an antagonist within pathogen propagules. Bacteria are rarely described as parasitcs of plant pathogens, but several produce enzymes thought to be involved in parasitic processes or have been consistently recorded in association with plant pathogens (Table VI). Assuming that nutrients pass from the plant pathogen to the antagonist under these circumstances, and that the growth of the pathogen is inhibited by the presence of the antagonist, then parasitism could be represented at one extreme by the apparently simple attachment of cells of Enterohacter cloacae to hyphae of Pythium ultimum (Nelson et al., 1986) to complete lysis, and degradation of hyphae of P. debaryanum by an Arthrobacter sp. (Mitchell and Hurwitz, 1965) and hyphae of Phomopsis sclerotioides, Mycocentrospora acerina and Sclerotinia sclerotiorum by Streptomyces griseoviridis (Tapio and Pohto-Lahdenpera, 1991). The production of antibiotics within close associations between bacteria and plant pathogens may also occur at the same time as production of lytic enzymes, for example during invasion of sclerotia of Sclerotium cepivorum by Bacillus subtilis (Wong and Hughes, 1986;

34

J. M. WHIPPS

Backhouse and Stewart, 1989), but without molecular studies it is difficult to be sure which is more important. Considerable interest has focused on the role and production of cell-wall degrading or lytic enzymes by putative parasitic bacteria. Using molecular techniques, chitinolytic enzymes have been shown to be important in biocontrol of Sclerotium rolfsii by Serratia marcescens (Shapira et al., 1989), Rhizoctonia solani by S. marcescens and Enterobacter agglomerans (Shapira et al., 1989; Chernin et al., 1995), and Fusarium oxysporum f. sp. redolens by recombinant Pseudomonas spp. (Sundheim et al., 1988). Other enzymes may also be involved in bacterial parasitism. For example, p-1,3-glucanase production was suggested to be important in the control of R . solani, S . rolfsii and P. ultimum by a non-chitinolytic strain of Pseudomonas cepacia (Fridlender et al., 1993), and both p-173-glucanaseand protease in the control of Pythium debaryanum by Arthrobacter sp. (Mitchell and Hurwitz, 1965). Cellulases may also be important in the control of Oomycota which have cellulose in their cell walls (Fridlender et al., 1993), and proteases may be involved generally by inhibiting the activity of plant cell-wall degrading enzymes of pathogenic fungi (Borowicz and Pietr, 1994). However, by far the greatest effort has gone into the study of mycoparasitism where a fungal pathogen is parasitized by another fungus. This area has been reviewed extensively in recent years (e.g. Whipps et al., 1988; Adams, 1990; Whipps 1991; Lumsden, 1992; Jeffries and Young, 1994; Goldman et al., 1994a) and only a brief outline of some of the general principles and more recent findings is presented here. Most evidence for a role of mycoparasitism in the control of plant disease comes from field observations of infected fungal propagules such as spores or sclerotia. Oospores of Aphanomyces, Phytophthora, Pythium and Sclerospora species have been found to be infected by a wide range of fungi including Dactylella spp., Fusarium mesmoides, Hyphochytrium catenoides, Olpidiopsis gracilis and Trinacrium subtile (Drechsler, 1938; Rao and Pavgi, 1976; Sneh et al., 1977; Hoch and Abawi, 1979; Wynn and Epton, 1979; Humble and Lockwood, 1981; Daft and Tsao, 1984; Pemberton et al., 1990; Sutherland and Papavizas, 1991). Similarly, facultative mycoparasites such as Trichoderma and Gliocladium species have frequently been reported to occur in sclerotia of many different pathogens including Phymatotrichum omnivorum, Rhizoctonia spp., Sclerotinia spp., Sclerotium spp. and Verticillium dahliae (Gladden and Coley-Smith 1980; Artigues and Davet, 1984; Zazzerini and Tosi, 1985; Howell, 1987; Kenerley and Stack, 1987; Keinath et al., 1991; van den Boogert and Saat, 1991) and Talaromyces flavus has also been repeatedly isolated from sclerotia of Rhizoctonia spp., Sclerotinia spp. and V. dahliae (Marois et al., 1984; McLaren et al., 1986). In contrast, some ecologically obligate sclerotial mycoparasites are only found in association with a suitable host sclerotium, surviving otherwise in soil as inactive spores or growing on plant material colonized by the host. Examples

BIOLOGICAL CONTROL OF SOIL-BORNE PLANT PATHOGENS

35

of these mycoparasites include Coniothyrium minitans and Sporidesmium sclerotivorum, which are restricted to Sclerotinia species and some ascomycetous Sclerotium species (Adams and Ayers, 1979; Whipps and Gerlagh, 1992), and Verticillium biguttatum, which is associated with Rhizoctonia solani (van den Boogert and Saat, 1991; Morris et al., 1992b). Details of mycoparasitic processes have largely been obtained through standard light and electron microscopical studies, but the recent development of video microscopy (Laing and Deacon, 1991; Berry et al., 1993; van den Boogert and Deacon, 1994; Jones and Deacon, 1995) has aided quantitation of the occurrence of many stages of interactions and their timing. Frequently, interactions have been observed on cellophane-covered agar or on thin layers of agar and, despite the lack of ecological realism of such systems, considerable insight into the mechanics of mycoparasitism has often been obtained in this way. Importantly, many of the processes observed in vitro have also been found during studies of mycoparasitism of sclerotia, adding credence to some in vitro work. Interactions between mycoparasites and their hosts may involve an overlapping sequence of events encompassing location, contact, recognition, localized lysis, penetration, intracellular growth and exit. The timing and relative importance of each event can vary depending on the fungi involved, the structure under attack, the habitat and environmental conditions. The key feature is that during this intimate association, the mycoparasite derives some or all of its nutrients from the host while conferring no benefit in return. Initially, during hyphal interactions, directed growth of the mycoparasite towards a host hypha may occur, sometimes accompanied by enhanced branching by the mycoparasite and abnormal growth of the target hypha as with Pythium oligandrum, Trichoderma spp. and Gliocladium spp. (Huang, 1978; Chet el al., 1981; Hubbard et a f . , 1983; Lewis et al., 1989; Benyagoub et al., 1994). This location of target hyphae may involve chemical signals coming from the host. Indeed, spores of Sporidesmium sclerotivorum, which can only germinate in soil in the presence of host sclerotia (Ayers and Adams, 1979), appear to respond specifically to a heat-labile, hydrophobic molecule arising from the melanized layer of Sclerotinia minor sclerotia (Mischke et a f . , 1995). Subsequently, contact is made and the mycoparasite may continue to grow over or along host hyphae, with varying degrees of coiling or hook formation (Elad et al., 1983b,c; Chambers and Scott, 1995). This may bear no relationship to susceptibility to mycoparasitism (Lifshitz et al., 1984b) and has been interpreted as indicating resistance in some cases (Deacon, 1976). Recognition, possibly mediated through lectin binding, has been shown to occur in interactions between Trichoderma harzianum and Rhizoctonia solani (Elad et al., 1983a; Barak et al., 1985). A lectin from Sclerotium rolfsii has

36

J. M. WHIPPS

also been isolated (Barak and Chet, 1990) and, when coated onto nylon fibres, resulted in T. harzianum producing hooks in a similar manner to that observed when T. harzianum encountered host hyphae (Inbar and Chet, 1992, 1994). Significantly, lectin-mediated recognition has been suggested as a first step in a cascade of antagonistic events including induction of chitinolytic enzymes in the T. harzianum-S. rolfsii interaction (Inbar and Chet, 1995). However, it is not clear how common this lectin-mediated phenomenon is in other interactions. At this stage, penetration may occur, effected by fine invasive hyphae or from appressoria (Elad et al., 1983c; McLaren et al., 1986; Huang and Kokko, 1988; Lewis et al., 1989; van den Boogert et al., 1989; Laing and Deacon, 1991; Berry et al., 1993; Jones and Deacon, 1995; Morris et al., 1995b). Alternatively, particularly with some mycoparasitic pythia, hyphal lysis, cytoplasmic collapse and disintegration may occur (Lewis et al., 1989; Chet et al., 1981; Laing and Deacon 1991; Jones and Deacon, 1995). Following this, varying degrees of intracellular growth may occur. This can range, at least initially, from production of haustoria-like branches which are formed without killing of host cells, as with Sporidesmium sclerotivorum infecting sclerotial cells of Sclerotinia minor (Bullock et al., 1986) and Verticilfium biguttatum on hyphae of Rhizoctonia solani (van den Boogert and Deacon, 1994), to massive intracellular invasion followed by frequent exits and renewed attacks o n adjacent host hyphae. This has been recorded with several mycoparasitic pythia and Trichoderma spp. (Elad et al., 1983b,e; Lifshitz el al., 1986; Lewis et al., 1989). Within sclerotia, Coniothyrium minitans, Gliocladium and Trichoderma spp., Stachybotrys elegans, Talaromyces flavus and Verticillium biguttatum have all been observed to grow both intra- and intercellularly (Elad et al., 1982; Artigues and Davet, 1984; Huang and Kokko, 1987; van den Boogert et al., 1989; Fahima et al., 1992). A role for the production of cell-wall degrading enzymes such as /3-1,3-glucanases, chitinases, proteinases and lipases by mycoparasites during interactions with other fungi has frequently been suggested (e.g. Jones et al., 1974; Tu, 1980; Chet and Baker, 1981; Elad etaf., 1982, 1983c, 1985; Ridout et al., 1988; Lewis et al., 1989; Sivan and Chet, 1989b; Benhamou and Chet, 1993; Benyagoub et al., 1994,1996; Tweddell et al., 1994). For instance, there is good microscopical evidence for the involvement of enzymes during penetration (Elad et al., 1982; Benhamou and Chet, 1993; Benyagoub et a f . , 1994) and the presence of cell-wall degrading enzymes in culture filtrates has also been taken to indicate their role in mycoparasitism (Ridout et al., 1988; Sivan and Chet, 1989b). For some strains of mycoparasite there may also be a relationship between production of cell-wall degrading enzymes and mycoparasitic activity (Elad et al., 1982), although this is not always the case (Ordentlich et al., 1991). Interestingly, transgenic tobacco plants constitutively expressing either the bean or Serratia marcescens chitinase genes

BIOLOGICAL CONTROL OF SOIL-BORNE PLANT PATHOGENS

37

exhibited increased resistance to infection by Rhizoctonia solani (Broglie et a f . , 1991; Jach et a f . , 1992). By analogy, this enzyme activity may similarly be involved in mycoparasitism. However, the speed of lysis observed in some interactions may be too fast to be accounted for by induction of such cellwall degrading enzymes. For instance, lysis of hyphae from several different hosts occurred just 55s after contact by Pythium oligandrum (Laing and Deacon, 1991). It was suggested that the release of preformed lytic enzymes from inactive zymogenic forms constitutively present within host cell walls may be involved (Laing and Deacon, 1991) and this merits further examination. In this regard, utilization of host p-1,3-glucanase has similarly been suggested as a process involved in the degradation of sclerotia of Sclerotinia minor by Sporidesmium scferotivorum (Adams and Ayers, 1983). Thus, most of the evidence for a role of cell-wall degrading enzymes in mycoparasitism is still largely based on indirect observations. Irrefutable molecular studies involving mutants lacking specific gene activity or transformants expressing novel genes for cell-wall degrading enzymes are badly needed. Consequently, working on the premise that cell-wall degrading enzymes are involved in mycoparasitism, a great deal of effort is currently being placed on the purification and characterization of these enzymes and their genes, particularly from mycoparasitic strains of Trichoderma and Gliocfadium which exhibit biocontrol activity. The enzymes studied include chitinolytic species, such as p-1,4-N-acetylglucosaminidase(NAGase; E C 3.2.1.30), chitin 1,4-p-chitobiosidase (chitobiosidase), and poly (1,4p-(2-acetamide-2-deoxy-~-glucoside) glucanohydrolase (endochitinase; E C 3.2.1.14) (Ulhoa and Peberdy, 1991a,b, 1992; de la Cruz et al., 1992, 1993, 1995; Di Pietro et a f . ,1993; Harman et al., 1993; Lorito et al., 1993a; Carsolio e t a f . , 1994; Garcia e t a l . , 1994; Hayes et al., 1994; Haran et a f . , 1995), glucan 1,3-p-glucosidase (p-1,3-glucanase; E C 3.2.1.58) (de la Cruz et a f . , 1993; Di Pietro et al., 1993), and proteinases (Geremia et a f . , 1993). In addition, several genes in Trichoderma, which were either induced during growth on Rhizoctonia solani cell walls or constitutively expressed, have been cloned (Goldman et a f . , 1992, 1994b; Vasseur et a f . , 199.5). These provide potential genetic tools for elucidating gene expression in these mycoparasites. Some of the purified enzymes have been examined for inhibitory activity. An endochitinase and chitobiosidase from T. harzianum P1 were inhibitory to cell replication of several fungi as well as to spore germination in Botrytis cinerea (Lorito et al., 1993a), but the endochitinase from G. virens 41 required four-fold greater concentration than the Trichoderma enzymes to obtain 50% inhibition (Di Pietro et a f . , 1993). Synergy was observed when endochitinases, chitobiosidases and p- 1,3-glucanases from the same or different strains of mycoparasite were combined, and also when the cell-wall degrading enzymes were combined with antibiotics or fungicides (Lorito et al., 1994a,b; Schirmbock et al., 1994) or the bacterial biocontrol agent,

38

J. M. WHIPPS

Enterobacter cloacae (Lorito et al., 1993b). Similarly, synergism of effect was also found with a combination of the endochitinase from Gliocladium virens 41 and the antibiotic, gliotoxin (Di Pietro et al., 1993). These studies highlight the probability that a combination of modes of action may function to bring about biocontrol in nature. B. INDIRECT MODES OF ACTION

1. Cross protection and induced resistance Cross protection has been defined as the inhibition of disease symptoms resulting from the prior or simultaneous inoculation of the host with a close relative (generally the same genus) of the pathogen (Cook and Baker, 1983), but there is no widely accepted definition. Certainly for viruses, where much of the terminology and background for this phenomenon was established, this is a fairly specific plant response (van Loon, 1983). When inoculation and pathogen challenge are spatially or temporally separated, it is taken to mean that the plant becomes immunized or exhibits induced resistance. Unfortunately, in some cases, it still allows the possibility that competition, antibiosis and parasitism can also take place at the same time. Thus much work describing the phenomenon of cross protection cannot categorically be attributed solely to induced resistance in the host plant (Table VII). Although induced resistance can be restricted to a localized region close to the initial inoculation, most interest has focused on systemic induced resistance (SIR), where resistance subsequently occurs throughout a plant following the initial triggering inoculation (Kloepper et al., 1992; Dann and Deverall, 1995). Also termed systemic acquired resistance (SAR) by some authors (Ross, 1961; see also Hoffland et al., 1995), the induced resistance concept has been broadened to encompass the non-specific resistance that is induced and transmitted through the plant following infection with necrosis-causing pathogens, or by treatment with abiotic agents such as chitosan, salicylic acid and isonicotinic acid, which are not antimicrobials in themselves (White, 1979; KuC, 1982; Sequeira, 1983; Lyon et al., 1995; Lafontaine and Benhamou, 1996). The spectrum of chemicals and plant extracts found to induce resistance in plants is increasing rapidly (Fought and KuC, 1996). Importantly, development of SAR is generally accompanied by expression of a set of genes within the plant including those which encode for pathogenesis-related proteins such as chitinases, p-1,3-glucanases and thymidine-like proteins with known antifungal activity (Linthorst, 1991; Ward et al., 1991). Synthesis of phytoalexins may also occur (van Peer and Schippers, 1992). To add further to the plethora of terminology, the term induced systemic resistance (ISR) has been used to describe the general resistance which develops following inoculation with non-pathogenic

TABLE VII Examples of microbial inoculations providing cross protection or systemic induced resistance to soil-borne plant pathogens

Microbial inoculant

Plant Carnation

Chickpea Cucumber

Eggplant Mint Pea Radish Sweet potato Tomato

Water melon

Non-or-less-pathogenic Fusarium oxysporum Pseudomonas sp. WCS417r Non-pathogenic Fusarium oxysporum Colletotrichum orbiculare Non-pathogenic Fusarium oxysporum F. oxysporum f . sp. niveum Pseudomonas spp. Pseudomonas putida 89B-27 Serratia marcescens 90- 166 Tobacco necrosis virus Non-pathogenic Fusarium oxysporum MM062 Verticillium nigrescens Non-pathogenic Fusarium oxysporum Pseudomonas sp. WCS374 Pseudomonas sp. WCS417r Non-pathogenic F. oxysporum Avirulent Fusarium spp. Avirulent Verticillium albo-atrum F. oxysporum f . sp. dianthi Non-pathogenic F. oxysporum Mmo62 Avirulent F. oxysporum f. sp. cucumerinum Avirulent F. oxysporum f. sp. niveum Helminthosporium carbonum

-

Pathogen controlled

Induced resistance demonstrated"

Fusarium oxysporum f . sp. dianthi F. oxysporum f . sp. dianthi

E oxysporum f . sp. ciceris F. oxysporum f . sp. cucumerinum F. oxysporum f . sp. cucumerinum F. oxysporum f . sp. cucumerinum Pythium aphanidermatum F. oxysporum f . sp. cucumerinum F. oxysporum f . sp. cucumerinurn F. oxysporum f . sp. cucumerinum Verticillium dahliae V. dahliae Fusarium solani F. oxysporum f . sp. F. oxysporum f . sp. F. oxysporum f . sp. F. oxysporum f . sp. Verticillium dahliae F. oxysporum f . sp. F. oxysporum f . sp. F. oxysporum f . sp.

raphani raphani batatas radicis-lycopersici lycopersici lycopersici niveum

F. oxysporum f . sp. niveum F. oxysporum

"Spatial or temporal separation provides clear evidence of host-mediated response.

Reference Rattink (1987, 1993)

\ \

\ \ \ \

\ \

\ \

\ \

\

\

van Peer et al. (1991) Duijff et al. (1993) Hervas et al. (1995) Gessler and KuC (1982) Mandeel and Baker (1991) Michail et al. (1989) Zhou and Paulitz (1994) Liu et al. (1995b) Liu et al. (1995b) Gessler and KuC (1982) Yamaguchi et al. (1992) Melouk and Homer (1975) Oyarzun et al. (1994) Leeman et al. (1995a) Hoffland et al. (1995) Ogawa and Komada (1985b) Louter and Edgington (1990) Matta and Garibaldi (1977) Kroon el al. (1991) Yamaguchi et al. (1992) Biles and Martyn (1989); Martyn el al. (1991) Shimotsuma et al. (1972)

40

J. M. WHIPPS

Pseudomonas spp. (Tuzun and Kloepper, 1994). Currently the degrees to which SIR, SAR and ISR differ at the molecular and biochemical level is unclear and more work is needed using a range of plant-inoculant systems to clarify this, not least to resolve the confused terminology. The key feature to demonstrate the existence of SAR or ISR is that the subsequent challenge with a pathogen is either spatially separated from the inducing inoculation or, if the challenge is at the same position as the inducing inoculation, that a period elapses where novel genes are switched on and characteristic resistance moieties are produced. Unfortunately, most of the work on induced resistance has concerned foliar pathogens and only relatively recently has the potential of this mechanism been recognized for biocontrol of soil-borne pathogens. Consequently, in contrast to the vast literature covering induced resistance in relation to the control of foliar pathogens, unequivocal examples of SAR or ISR involving soil-borne pathogens are rare. Using split root systems, both bacteria and fungi have been shown to induce resistance in several plants when applied to roots. For example, Pseudomonas putida 89B-27 and Serratia marcescens 90-166 induced systemic resistance to Fusarium oxysporum f. sp cucumerinum in cucumber (Liu et al., 1995a,b); Pseudomonas corrugata and Pseudomonas jluorescens induced systemic resistance to Pythiurn aphanidermatum in cucumber (Zhou and Paulitz, 1994); and P. ffuorescens induced systemic resistance to F. oxysporum f. sp. raphanii in radish (Leeman et al., 1995a,b), with lipopolysaccharides of the bacterial wall strongly implicated as being involved in the induction process. Similarly, non-pathogenic Fusarium oxysporum isolates induced resistance to F. oxysporum f. sp. cucumerinum in cucumber (Mandeel and Baker, 1991), and F. oxysporum f. sp. dianthi induced resistance to F. oxysporum f. sp. lycopersici in tomato (Kroon et al., 1991). In an alternative treatment, inoculation of the first true leaves of cucumber with Colletotrichum orbiculare or tobacco necrosis virus resulted in induced resistance to F. oxysporum f. sp. cucumerinuni on the roots (Gessler and KuC, 1982). The phenomenon of treating seeds, roots or cuttings with inducing bacteria or fungi and achieving induced resistance to subsequent stem or foliage challenge by a range of viral, bacterial and fungal pathogens is also known (Alstrom 1991; Wei et al., 1991; Liu et al., 1992, 1995a,b; Maurhofer et al., 1994b; Meera et al., 1994, 1995), suggesting an important role for induced resistance in biocontrol in general. However, further consideration of this aspect involving biocontrol of foliar pathogens is outside the remit of this review. See Hammerschmidt and KuC (1995) for detailed reviews. There are few data on the molecular and biochemical changes occurring in roots as a result of induced resistance, although phytoalexins and peroxidases are thought to be involved in the response of carnation roots to inoculation with Pseudomonas (van Peer et al., 1991; van Peer and Schippers, 1992) and pathogenesis-related proteins were synthesized in roots

BIOLOGICAL CONTROL OF SOIL-BORNE PLANT PATHOGENS

41

and leaves of cotton plants following inoculation with arbuscular mycorrhizal fungi (Liu erul., 1995d). Based on studies from other SAR systems, responses may involve accumulation of antimicrobial low molecular weight chemicals such as phytoalexins, formation of protective layers via accumulation of polymers such as lignin, callose and hydroxyproline-rich glycoproteins, increases in activators of enzymes leading to the production of such materials, and increases in the amount of chitinases, p-1,3-glucanases, peroxidases and other pathogenesis-related proteins (Tuzun and Kloepper, 1994; Hammerschmidt and Kud, 1995). However, further work is required to substantiate this.

2. Plant growth promotion Over the last 20 years, there have been an increasing number of reports of promotion of plant growth following treatment of seeds, roots, cuttings, soil or artificial growing media with bacteria and fungi, particularly species of Pseudomonas and Trichoderma (Table VIII). Depending on the plant studied, growth promotion has been expressed in a variety of ways but most commonly as increases in germination, emergence, fresh or dry weight of roots or shoots, root length, yield and flowering. Many aspects of this phenomenon have been reviewed in detail several times (Schroth and Hancock, 1981; Burr and Caesar, 1984; Okon, 1985; Schippers et al., 1987; Weller, 1988; Baker, 1989; Kloepper et nl., 1989, 1991; Inbar et al., 1994; Ryder et a f . , 1994) and numerous large screening studies have been carried out specifically to search for such plant growth-promoting microorganisms (Gerhardson et al., 1985; Kloepper et (21.. 1988; Ousley et al., 1994a; Tang, 1994; Glick et al., 1995). Indeed, the term plant growth-promoting rhizobacteria (PGPR) has been coined specifically to describe bacteria which colonize roots and have the ability to stimulate plant growth (Kloepper and Schroth, 1978) and this has led to a new area of work (Ryder et al., 1994). Frequently, growth promotion has involved application of known biocontrol agents, but even so, the modes of action involved in the plant growth promotion observed have not always been clear. In soils containing major pathogens such as Gaeumannomyces graminis var. rritici, Pythium spp. and Rhizoctonia spp, the growth promotion effect may well reflect biocontrol acting through mechanisms such as competition, antibiosis, parasitism and induced resistance, as described earlier. However, growth promotion can still occur in soils or environments lacking such major pathogens. It is then thought to be due either to control of minor pathogens such as deleterious rhizobacteria (Schippers et al., 1987; Baker, 1989) in the same way as major pathogens, or to a direct effect on the plant. Direct effects are commonly thought to be mediated by production of plant hormones such as auxins, cytokinins or gibberellins (Arshad and Frankenberger, 1991). It is difficult to obtain unequivocal evidence for their production in non-sterile soil, although several studies carried out in sterile

TABLE VIII Examples of plant growth promotion following application of bacteria and fungi to seeds, roots or growing media Microorganism

Plant

Growth promotion observed

Reference

Bacteria Arthrobacter citreus

Canola

Leaf area Yield

Kloepper et al. (1988)

Azospirillum sp.

Tomato

Emergence Total dry weight Root and shoot length

Gupta et al. (1995)

Azotobacter chroococcum

Tomato

Emergence Total dry weight Root and shoot length

Gupta et al. (1995)

Bacillus subtilis A-13

Cotton Peanut Cotton Onion

Plant growth Yield Yield Shoot and root dry weight Shoot height

Turner and Backman (1991); Backman et al. (1994) Backman et al. (1994) Reddy and Rahe (1989)

PGPR"

Potato Radish

Root weight

Kloepper and Schroth (1981)

Pseudomonas spp.

Bean

Shoot and root weight Emergence Total dry weight

Elad et al. (1987)

Cucumber

Emergence Shoot and root weight Total dry weight

Elad et al. (1987); van Peer and Schippers (1989)

B. subtilis GB03 B. subtilis

Guayule

Shoot dry weight

Olsen and Misaghi (1984)

Lettuce

Shoot and root dry weight

van Peer and Schippers (1989)

Melon

Emergence Shoot and root weight Total dry weight

Elad et al. (1987)

Pepper

Emergence Shoot and root weight Total dry weight

Elad et al. (1987)

Potato

Shoot and root fresh weight Yield

Kloepper et al. (1980~);van Peer and Schippers (1989)

Radish

Emergence Shoot and root weight Total dry weight

Elad et al. (1987)

Tobacco

Emergence Shoot and root weight Total dry weight

Elad et al. (1987)

Tomato

Emergence Shoot and root weight Total dry weight

Elad et af. (1987); van Peer and Schippers (1989)

Wheat

Shoot and root dry weight

Ryder and Rovira (1993)

Pseudomonas sp. Ps J N

Potato

Emergence Plant development Yield of tubers

Frommel et al. (1993)

Pseudomonas fluorescens

Canola

Leaf area Yield

Kloepper et al. (1988)

Rice

Plant height

Sakthivel et al. (1986)

Tomato

Emergence Total dry weight Shoot and root length

Gupta et al. (1995)

TABLE VIII Contd Microorganism

Plant

Growth promotion observed

Reference

Pseudomonas fluoresceas E6

Carnation Stock Sunflower Vinca Zinnia

Fresh weight of shoots

Yuen and Schroth (1986)

Pseudomonas putida

Canola

Kloepper et al. (1988)

Pseudornonas putida GR12-2

Canola

Serratia liquefaciens

Canola Brassica Lettuce

Leaf area Yield Root length Leaf area Yield Plant development Plant development

Tahvonen (1988) Tahvonen and Lahdenpera (1988)

Pepper

Dry weight of shoots

Hams et al. (1993b)

Fresh and dry weight Fibre weight Fresh and dry weight Shoot weight Fresh and dry weight Grain weight and yield

Sneh et al. (1986)

Shoot dry weight Yield

Shivanna et al. (1994)

Streptomyces griseoviridis

Fungi Rhizoctonia solani (binucleate)

Rhizoctonia solani (non-pathogenic) Carrot Cotton Lettuce Potato Radish Wheat Sterile fungi

Wheat

Lifshitz et al. (1987) Kloepper et al. (1988)

Sterile red fungus

Trichoderma spp.

Trichoderma koningii T8

Barley Chickpea Great brome Medic Oats Peas Rape (Canola) Ryegrass Subterranean clover Wheat Lettuce Marigold Petunia Verbena Tobacco Tomato

Fresh shoot and root weight

Dewan and Sivasithampararn (1989)

Shoot fresh and dry weight Shoot fresh and dry weight Flower number

Ousley et al. (1993, 1994b) Ousley et al. (1994a)

Emergence Dry weight of roots and shoots

Windham et al. (1986)

Trichoderma harzianum BR105

Cucumber Tomato

Emergence Dry weight of roots and shoots Flower set

Besnard and Davet (1993)

Trichoderma harzianum T-12

Radish Tomato

Dry weight Emergence Dry and fresh weight of roots and shoots

Paulitz et af. (1986) Windham et al. (1986)

Trichoderma harzianum T-95

Chrysanthemum Periwinkle Petunia Radish Tomato

Fresh and dry weight Height Fresh and dry weight Dry weight Emergence Dry weight of shoot

Chang et al. (1986) Windham et af. (1986) Windham et al. (1986)

TABLE VIII Contd ~

Microorganism Trichoderma harzianurn T-203

Trichoderrna viride ‘PGPR

Plant

~

~~~

Growth promotion observed

~~

Reference Kleifeld and Chet (1992) Chang et al. (1986); Kleifeld and Chet (1992); Inbar et al. (1994)

Radish Tomato

Germination Germination Height Dry weight Leaf area Germination Germination

Lettuce

Shoot fresh weight

Coley-Smith et al. (1991)

Bean Cucumber Pepper

- Plant growth-promoting rhizobacteria.

Kleifeld and Chet (1992)

BIOLOGICAL CONTROL OF SOIL-BORNE PLANT PATHOGENS

47

conditions have implied their involvement. For example, results from a gnotobiotic growth pouch assay showed that Pseudomonas putida GR12-2 consistently induced a significant elongation of roots of canola (Brassica napus) compared with controls and was associated with enhanced shoot height and phosphorus uptake by roots and subsequent transfer to shoots (Lifshitz et al., 1987). Pseudomonas putida GR12-2 produced indole-1-acetic acid (IAA) and fixed nitrogen (although at rates 20-fold slower than Azotobacter vinelandii based on the acetylene reduction assay, see Hong et al., 1991), which may have influenced plant growth directly. However, in addition it also degraded I-aminocyclopropane-1-carboxylate(ACC), the immediate precursor of ethylene, thereby potentially relieving the normal ethylene-induced inhibition of root development (Glick et al., 1994, 1995). Similarly, work with corn (Zea mays), tomato (Lycopersicon esculentum) and tobacco (Nicotiana tabacum) cultivars suggested that a growth regulator was produced by Trichoderma spp. and that this was directly involved with the increased rate of seed germination and dry weight of shoots and stems following inoculation (Windham et al., 1986). Associative nitrogen fixation may also occur with Azospirillium spp., Azotobacter spp., Bacillus spp. and possibly some Pseudomonas spp. (Okon, 1985; Kloepper et al., 1989; Hong et al., 1991) to increase plant growth directly. Production of vitamins, conversion of non-utilizable material into a form that can be used by the plant, and improved availability and uptake of some minerals may also contribute to the growth promotion phenomenon (Brown, 1974; Baker, 1989; Kleifeld and Chet, 1992). Significantly, especially for microbes that are to be used commercially in the future, it would seem important to understand the mode of action involved in growth promotion to ensure reproducibility of effect. An observation of growth promotion per se may be too limited to allow acceptable development to take place, although the situation with Bacillus subtilis GB03 and GB07 in the USA (Backman et al., 1994) could disprove this theory. It is important to stress at this point that microorganisms forming mutualistic symbioses with plants, such as mycorrhizal fungi and noduleforming nitrogen-fixing bacteria that are known to stimulate plant growth largely through nutritional effects (although other mechanisms may be involved - see section III.A.l),are beyond the scope of this review. Growth promotion by these mutualistic symbionts has been discussed in depth elsewhere (Reid, 1990; Zuberer, 1990; Norris et al., 1994; Linderman, 1994; Pfleger and Linderman, 1994) and these books and reviews should be consulted for further information on this topic. C. RHIZOSPHERE COMPETENCE

One of the key features exhibited by many biocontrol agents of soil-borne plant pathogens is an ability to colonize seeds or roots. By establishing in

48

J . M. WHIPPS

the infection court, the biocontrol agent is able to exhibit a range of direct or indirect biocontrol mechanisms in a key ecological niche and thus prevent or delay infection by pathogens. In some cases, most notably for those antagonists acting through induced resistance, such spermosphere or rhizosphere competence is a prerequisite for biocontrol to occur. Effective root colonization can often be linked directly to successful competition with other microorganisms for colonization sites and nutrients available from root exudates (Paulitz, 1990; O’Sullivan and O’Gara, 1992; Kluepfel, 1993). Not surprisingly, therefore, the need to establish and survive on seeds or roots, and to multiply and become distributed along the whole root system in the presence of the natural microbiota, has been clearly indicated as important for biocontrol in plant-microbe systems involving several bacterial antagonists, particularly pseudomonads (Chao et al., 1986; Bull et al., 1991; Weller, 1988; Parke, 1990; Misaghi et al., 1992; Weller and Thomashow, 1994). Similarly, the ability of fungi including some Trichoderma isolates, strains of non-pathogenic fusaria and Verticillium biguttatum to colonize the rhizosphere has been directly correlated with biocontrol ability (Ahmad and Baker, 1988; Couteaudier et al., 1993; van den Boogert and Velvis, 1992). Several biocontrol agents have been shown to exhibit specificity in colonization of the rhizosphere and spermosphere related to plant or soil conditions. For example, Streptomyces griseoviridis, a biocontrol agent commercialized as Mycostop for the control of several root diseases, colonized 72% of the root length of turnip (Brassica campestris) seedlings but only 1% of the root length of carrot (Kortemaa et al., 1994). Similarly, rhizosphere colonization of cotton by the commercial biocontrol agent Bacillus subtifis GB03 was affected by the seed condition prior to inoculation (Mahaffee and Backman, 1993). Further, inoculum density of the biocontrol agent, plant cultivar, water potential and soil type have all been shown to influence rhizosphere or spermosphere colonization in numerous plantmicrobe systems (Loper et a f . , 1985; Bahme and Schroth, 1987; Davies and Whitbread, 1989; Liddell and Parke, 1989; Beauchamp et al., 1991; Seong et al., 1991; Hebbar et al., 1992; Glandorf et al., 1994). These observations suggest that it could be worthwhile to search for biocontrol agents with a general ability to colonize seeds and roots in a range of environments and thus increase the likelihood of achieving long-term biocontrol (Maplestone and Campbell, 1989; Milus and Rothrock, 1993). The concept of rhizosphere competence has recently been extended with the observation that several biocontrol agents become endophytic within root tissue, which could also provide longer-term biocontrol. For instance Trichoderma harzianum T-203, which provides plant growth promotion, was found to colonize the interior of roots of pepper growing in soil treated with the fungus (Kleifeld and Chet, 1992), and numerous bacteria with biocontrol or plant growth promoting capability were found to grow endophytically

BIOLOGICAL CONTROL OF SOIL-BORNE PLANT PATHOGENS

49

within seeds or roots of several plants including alfalfa (Medicago sativa), cotton and tomato (GagnC et al., 1987; Misaghi and Donndelinger, 1990; van Peer et al., 1990b; Chen et al., 1995; Musson et al., 1995; Pleban et al., 1995). Selection for endophytic behaviour may avoid the problems associated with an inability of some biocontrol agents to occupy the whole root system for the entire growing season (Weller, 1983; Backman et al., 1994). Alternatively, application of mixtures of biocontrol agents with different abilities to colonize root microsites (Deacon, 1994), and possibly exhibiting different complementary modes of action, could be developed. Indeed, combinations of fluorescent pseudomonads and non-pathogenic fusaria or fluorescent pseudomonads with several different fungi have been found to be successful for control of fusarium diseases in experimental systems (Alabouvette et al., 1993; Leeman et al., 1996a). A binary system of Serratia marsecens and Streptomyces anulatus was effective in controlling tomato wilt disease caused by Fusarium oxysporum f. sp. lycopersici (Toyoda et al., 1993); Pythium nunn and Trichoderma harzianum were combined to reduce Pythium damping-off of cucumber (Paulitz et al., 1990); and combinations of different fluorescent pseudomonads, or combinations of fluorescent pseudomonads with Gaeumannomyces graminis var. graminis, or Trichoderma koningii have been used in the field with varying success to control take-all of wheat caused by G . graminis var. tritici (Pierson and Weller, 1994; Duffy and Weller, 1995; Duffy et al., 1996). However, when considering the use of any mixture or consortium of strains for biocontrol, it is important that no member of the mixture is inhibitory to another. Thus, Pseudomonas @orescens 2-79, a known biocontrol agent of take-all of wheat, neither inhibited nor enhanced the biocontrol activity of Trichoderma harzianum ThzID 1 when used in combination against root rot of pea caused by Aphanomyces euteiches (Dandurand and Knudsen, 1993) and P. fluorescens 2-79 did not reduce the ability of T. harzianum ThzIDl to attack sclerotia of Sclerotinia sclerotiorum in the field (Bin et al., 1991). Further, biocontrol agents, whether used in mixtures or not, should not interfere excessively with the existing, normal non-pathogenic microbiota associated with seeds or roots. Significantly, several bacterial and fungal antagonists that have been tested, including Pseudomonas putida, Gliocladium virens and Trichoderma spp., have shown little or no adverse effects on establishment and function of arbuscular mycorrhizas (Meyer and Linderman 1986; Calvet et a)., 1989; Paulitz and Linderman, 1989, 1991; Linderman el a f . ,1991). However, interestingly, two commercial antagonists, Streptomyces griseoviridis (Mycostop) and Trichoderma harzianum (T-35 ; Trichodex) reduce formation of arbuscular mycorrhizas in soybean (Wyss et al., 1992). In another system, Trichoderma koningii adversely affected arbuscular mycorrhiza formation on maize and lettuce (McAllister et al., 1994). Clearly, such complex interactions will have to be carefully considered during development of any individual or mixture of biocontrol agents.

50

J. M. WHIPPS

IV. APPLICATION OF SPECIFIC ANTAGONISTS Since Cook and Baker (1983) compiled their list of antagonistic vitae there has been a continual steady increase in the number of specific antagonists purported to act, or have potential, as biological disease control agents. Several completely novel antagonists have been identified. For example, Cylindrobasidium parasiticum, Phoma nebulosa, Pythium acanthophoron, Pythium mycoparasiticum and Stachbotrys elegans have been shown to be mycoparasites (Woodbridge et al., 1988; Whipps et al., 1993; Benyagoub et al., 1994; Jones and Deacon, 1995); Aeromonas caviae, Cladorhinum foecundissimum and Penicillium simplicissimum have shown biocontrol potential in glasshouse or controlled environment trials (Inbar and Chet, 1991; Dodd and Stewart, 1992; Lewis et al., 1995); and Minimedusa polysporum has provided biocontrol of Fusarium oxysporum f. sp. narcissi in the field (Beale and Pitt, 1990). However, repeated targeted screens for specific groups of antagonists, particularly pseudomonads, Gliocladium spp. and Trichoderma spp., has resulted in numerous reports of biocontrol with new strains of the same genus or species. This trend is clearly illustrated in Tables IX, X and XI, which give examples of specific antagonists applied to soil or growing media, seeds, bulbs and tubers and to cuttings and roots. The tables have been compiled from over 150 references collected over the last five years. It is important to stress that these tables do not include purely in vitro studies and largely consist of bioassays, glasshouse or field trials involving host plants which reflect, at least to some extent, a possible condition of use. Due to the arbitrary cut-off year of 1990, some of the more notable biocontrol agents which have been demonstrated to give reproducible biocontrol in realistic field or glasshouse trials, including some which have gone on to commercialization (Table XII), are poorly represented. Some, such as Agrobacterium radiobacter K84 and K1026 for control of crown gall caused by Agrobacterium tumefaciens, and Phlebia (Peniophora) gigantea for control of stump rot of pine caused by Heterobasidion annosum (Deacon, 1991), are mature products and need little further development. However, others such as Pseudomonas Puorescens CHAO, P. JEuorescens2-79, nonpathogenic Fusarium oxysporum Fo47, Gliocladium virens G20 (GL21) and Streptomyces griseoviridis repeatedly appear as workers continue to examine production, formulation and modes of action, and attempt to extend the host range of control including combining antagonists. Further, there are some antagonists such as Bacillus subtifis GB03 and MBI600 which have gone from initial isolation, through ecological, mode of action and formulation studies to commercialization in this period (Rossall and McKnight, 1991 ; Backman et al., 1994; Fiddaman and Rossall, 1995), illustrating the speed at which development can take place if scientists and industry work together successfully. Several other newly described antagonists mentioned in Tables IX, X and XI may well merit similar collaborative studies.

TABLE IX Recent examples of specific antagonists applied to seeds, bulbs and tubers which show potential to provide biological control of soil-borne plant pathogens Antagonists Bacteria Bacillus cereus UW85

Pathogen or disease

Growing medium

Host

Field

Andrade er a/. (1994)

Field

Backman el al. (1994); Brannen and Backman (1994)

Cells coated onto seeds

CE'

Fiddaman and Rossall

Soil

Cells coated onto seeds

Field

Ehteshamul-Haque and Ghaffar (1993)

Soil

B . subrilis AP183

Rhizocronia solani

Common bean

Soil

B. suhtilis GB03

Fusariwn oxysporum f. sp. vasin,fecrum Rhizocronia soluni

Cotton

Soil

B . subrilis 205

Rhizocronia solani

Oilseed rape

Potting mix

Okra Mungbean Soybean Sunflower

present soil

Reference Handelsman er al. (19%))

Alfalfa

phaseoli Rhiacronio solani

Site Field

Phyrophrhora megaspermu f. sp. medicoginis

Brudyrhizobium laponicrrm

Inoculation technique Cells watered or coated onto seeds Cells coated onto seeds Cells coated onto seeds

(1995)

Enrerobacrer cloacoe

Pvrhium spp.

Cucumber

Soil

Cells coated onto seeds

Glasshouse

Cubeta and Echandi (1991)

Pseudomonos spp. (mixtures)

Gaeumannomvces graminis var. rririci

Wheat

Soil

Cells coated onto seeds

Pierson and Weller (1994)

Pseudomonas spp.

Fusurium oxysporum

Douglas fir

Peat-vermiculite

Seeds coated in cell suspension

CE, glasshouse and field CE

Reddy er 01. (1994a)

Pyrhium ulrimum Rhizoctonia soluni

Cotton

Soil

Cells coated onto seeds in peat

Field

Hagedorn et 01. (1993)

P. ueruginosu S-7

Fusurium oxysporum f. sp. adzukicolu

Adzuki bean

Soil

Cells coated onto seeds

Glasshouse

Hasegawa er a/. (1991a)

P . aeruginosu 7NSK2

Pythium sp.

Tomato

Nutnent film

Cells coated onto Glasshouse seeds + drench with cells

Buysens er a/. (1993b)

Wheat

Soil

Cells coated onto seeds

Thomashow er al. (19%)

P. aureofaciens 30-84 (= Gneumannomyces graminis var. rritici P. chlororaphis 30-84)

Glasshouse

TABLE IX Contd Antagonists P. aureofaciens AB254 (= P. fluorescens AB254) P. cepacia AMMD

Pathogen or disease

Growing medium

Host Maize

Soil

Cells coated onto

Field

Mathre et al. (1994)

Aphanomyces euteiches f. sp. pisi Pythiwn spp.

Pea

Soil

Glasshouselfield

Parke et al. (1991)

Pea

Soil

Cells coated onto seeds Cells coated onto seeds Cells coated onto seeds Cells in peat o n seed Cells on seed Cells drenched onto seeds

Field Glasshouse

Bowers and Parke (1993); King and Parke (1993) Hasegawa et al. (1991a)

Field Field Glasshouse

McLoughlin et al. (1992) Hebbar et al. (1991, 1992) Sanchez et al. (1994)

CE

Mazzola ef al. (1995)

Glasshouse

Dodd and Stewart (1992)

Field

Park and Yeom (1994)

Field

Reddy

Field

Expert and Digat (1995)

Field

Callan et al. (1990)

CE

Kraus and Loper (1992)

Glasshouse/field

Parke et al. (1991)

F. oxysponun f. sp. udzukicoh

Adzuki bean

Soil

P. cepacia J82rif

Sclerotinia sclerotiorum Sclerotium rolfsii Macrophomina phaseolina

Sunflower Sunflower Common bean

Soil Soil Soil

Gaeumannomyces graminis var. trifici Pythiwn debaryunum P. ultimum P. ultimum Rhiroctonia solani R. sohni

Wheat

Soil

Beetroot

Potting mix

Cucumber

Soil

Canola

soil

Sclerotinia sclerotiorum

Sunflower

Soil

P. fluorescens -2.54

P . ultimum

Maize

Soil

P. fluorescens Pf-5

P. ultimum

Cucumber

Soil

P. fluorescens PRA25

Aphanomyces euteiches f. sp pis;

Pea

Soil

P. cepacia UPR5C

(= Burkholderia repacia UPRSC)

P . chlororaphis 30-84 P. fluorescens (+ Penicillium spp.) P . fluorescens

Reference

Site

Pythiwn ultimum

P. cepacia 8-17

P. cepacia N24

Inoculation technique seeds

Cells coated onto

seeds Cells coated onto seeds Cells coated onto seeds Cells coated onto seeds Seeds soaked in cell suspension Cells coated onto seeds and biopriming Cells coated onto seeds Cells coated onto seeds

ef

al. (1994b)

P. puorescens Q2-87

G. graminrs var. trihci

Wheat

Soil

P. fluorescens Q292-80

Pyrhium spp

Chickpea

Soil

P puorescens S-2

F oxysporum f. sp adzukrcola G . graminis var. tritici

Adzuki bean

Soil

Wheat

Soil

P. puorescens 2-79

Cells coated onto seeds Cells coated onto seeds Cells coated onto seeds Cells coated onto seeds

CE

Mazzola ef nl. (1995)

Field

Trapero-Casas er a / . (1990) Hasegawa er a / . (1991a)

Glasshouselfield

CE Glasshouse Field

P. picorescens 13-79

G. graminis var. tritici

Wheat

Soil

P . purida

Sclerotinia scleroriorum

Sunflower

Soil

P. purida NIR

Pyrhium ultimum

Cucumber

Soil

Pea Soybean

Soil

Wheat

Soil

Okra Mungbean Soybean Sunflower

P . prtrida R101

Rhizocronia solani

Rhizobium spp.

Fusariuni spp. Macrophomina phaseolina Rhizoctonia solani

]

Root rot complex present

Cells coated onto seeds Seeds soaked in cell suspension

Field

Ownley er a / . (1992): Mazzola er a / . (1995) Thomashow er a / . (1990) Capper and Higgins (1993)

Field

Capper and Higgins (1993) Expert and Digat (1995)

Cells coated onto seeds

CE

Paulitz and Loper (1991)

Cells coated onto seeds Cells coated onto seeds

CEiglasshouse

Paulin (1991), Paulitz er a/ (1992)

CE

Soil

Cells coated onto seeds

Field

De Freitas and Germida (1991) Ehteshamul-Haque and Ghaffar (1993)

Soil

Cells coated onto seeds

Field

Hussain er a/. (1990)

Soil

Cells coated onto seeds

Glasshouse

El-Abyad er ol. (1993a)

Srrepromyces sp.

soil in Macrophomina phaseolina

Srrepromyces spp.

F. oxysporum f. sp.

Mungbean Sunflower Tomato

F. oxysporum f. sp. phaseoli

French bean

Soil

Cells coated onto seeds

Glasshouse

El-Abyad er a / . (199%)

F. oxysporum f. sp

Adzuki bean

Soil

Cells coated onto seeds

Glasshouse

Hasegawa er a / . (1991a)

Srrepromyces paveits Y-l

lycopersici Verticillium albo-anum

adzukicoh

TABLE IX Contd Antagonists

Pathogen or disease

Growing medium

Host

Alternaria brassicicola

Cauliflower

Damping-off

Pepper

F. oxysponcm f. sp. narcissi

Narcissus

Aspergillus flavus

Peanut

Bipolaris sorokiniana Fusarium culmorum Fusarium monififorme

Barley Wheat Maize

Macrophomina phaseolina Pyrhium ultimum

Mungbean Sunflower Cotton

Soil

Idriella bolleyi

Fusarium culmorum

Wheat

Soil

Laetisaria arvalir

Rhizoctonia solani

Potato

Soil

Minimedusa polyspora

F. oxysporum f. sp. narcissi

Narcissus

Soil

Streptomyces griseoviridis

Unidentified bacteria

FWgi Gliocladium roseum

G. virens

Inoculation technique

Potting compost Cells coated onto seeds Soil Cells coated onto seeds Potting compost Bulbs dipped in spore suspension Soil Seeds soaked in cell suspension +soil drench Soil Soil Soil

Spores applied to seeds Seeds soaked in spore suspension Spores applied to seeds Spores coated onto seeds Spores coated onto seeds Mycelia and sclerotia applied to tuben Bulbs dipped in spore suspension or coated onto bulb

Site

Reference

Glasshouse

Lahdenpera e t a / . (1991)

Glasshouse

Lahdenpera er

Glasshouse

Hiltunen ef al. (1995)

Glasshouselfield

Mickler er al. (1995)

Field

Knudsen er 01. (1995)

Field

Vakili (1992)

Field

Hussain et a / . (1990)

CE

Howell (1991); Howell er d.(1993) Knudsen et al. (1995)

Field Field Field

01.

(1991)

Murdoch and Leach (1993) Beale and Pin (1990)

Mungbean Sunflower Beetroot

Potting mix

Chickpea

Soil

Aphanomyces cochlioides

Sugar beet

Soil

Pyrhium spp.

Chickpea

Soil

Cucumber

Soil

Potato

Soil

Paecilomyces lilacinus

Macrophom’na phoseolina

Penicillium spp. (+ P. fluoiescens) Penicillium oxalicum

Pyrhium debaryanum P. ulthum Pyfhium spp.

Pyrhium oligandrum

Rhirocronia (binrrcleare) Rhizoctonia solani

Trichodema harzianum

Macrophomka phaseolina

T. harzianum 1295-22

Pyrhiwn spp. Pythiwn ulrimwn

T. viride

F. oxysporum f. sp. sesami Rhizoctonia solani

“CE: Controlled Environment Facility.

Soil

Mungbean Sunflower Cucumber Cucumber

Soil Soil

Sesame

Soil

Spores coated onto seeds Spores coated.onto seeds Spores coated onto seeds Oospores commercially coated onto seeds Oospores coated onto seeds Adjacent colonized grain Adjacent colonized grain Spores coated onto seeds Range of systems Spores coated onto seeds Spores coated onto seeds

Field

Hussah el ai. (1990)

Glasshouse

Dodd and Stewan (1992)

Field CE

Trapero-Casas ef al. (1W) McQuilken et 01. (1990b)

Field

Trapero-Casas el a / .

Glasshouse

Cubeta and Echandi

Glasshouse Field

Escande and Echandi (1991) Hussain er al. (1W)

CE Glasshouse

Taylor et a / . (1991) Taylor et a/. (1991)

Glasshouselfield

Chung and Choi (1990)

(1990) (1991)

TABLE X

Recent examples of specijic antagonis& applied to soil or growing media which show potential to provide biological control of soil-borne plant pathogens Antagonist

Growing medium

Pathogen or disease

Host

Phytophthora medicaginis

Alfalfa

Vermiculite

Phytophthora sojae

Soybean

soil

Navy bean

Soil

B. subtih spp

Rhizoctonia solani Phytophthora cllcforum

Apple

Soil

B. subtih E B W 4

Apple replant disease

Apple

Soil

Bradyrhizobium japonicum

Fusariwn spp. Macrophomina phaseolina Rhizoctonia solnni Rhizoctonia solani

Mungbean Okra Soybean Sunflower

Bacteria

Bacillus cereus UW85

B. subtilis

Enterobacter agglomerans Enterobacter aerogenes B8 E. cloacae E. cloacae

Root rot complex present

Phytophthora cactorum

Pythiwn ultimum Sclerotinin homoeocarpa

Inoculation technique

Site

Cells drenched into CE' medium Cells in clay granule Field formulation applied in-furrow Cells incorporated Glasshouse into soil

Reference Silo-Suh et al. (1994) Osburn et al. (1995)

Tu (1991)

Soil and trunk drench Field with cells Soil drench with cells Field

Utkhede and Smith (1991)

Soil

Cell suspension drench in furrow

Ehteshamul-Haque and Ghaffar (1993)

Cotton

Soil

Cell suspension

Apple

Soil

Lettuce

Potting mix

Creeping bentgrasd annual blue

Soil

grass

Field

Glasshouse mixed into soil Soil and trunk drench Field with cells

Cells added to mix Cells in cornmeal sand top dressing

Glasshouse Field

Utkhede and Smith (1%)

Chernin

el

al. (1995)

Utkhede and Smith (1991); Uvesque et al. (1993); Utkhede and Smith (1993a) Lynch et al. (1991) Nelson and Craft (1991)

Pseudomonas spp

Pythium aphanidermatum

Cucumber

Rockwool

Pythium ul~imum

Cotton

Soil

Rhizoctonia solani

Cotton

Soil

Phythophthora megasperma

Asparagus

Peausand mix

Phyrhophrhora cinnamomi

Protea

Potting mix

Pythium ultimum

Cucumber

soil

Rhizoctonia solani

Cotton

Soil

Sclerotium rolfsii

Bean

Soil

P. cepacia 89 G-120

Rhizocronia solani

Cotton

soil

Pseudomonas corrugara

Pythium aphanidermatum

Cucumber

Rockwool

Gaeumannomyces graminis var. tritici Pseudomonas fluorescens Pythium aphanidermatum

Wheat

Soil

Cucumber

Rockwool

P. fluorescens CHAO

Fusarium oxysporum f. sp, cucumerinum G. graminis var. tritici

Cucumber

Artificial soil

Wheat

Artificial soil

Phomopsis sclerotioides

Cucumber

Artificial soil

Pythium ultimum

Cress Cucumber Maize Wheat Maize

Soil

Pseudomonas aureofaciens PA 147-2 Pseudomonas cepacia

P. corrugata 2140

Rhizoctonia solani

Artificial soil

Cell suspension added In-furrow peat inocuIum In-furrow peat inoculum Cells drenched into medium Cells drenched into medium Cells drenched into medium

CE

Zhou and Paulitz (1994)

Field

Hagedorn et al. (1993)

Field

Hagedorn et al. (1993)

Glasshouse

Carruthers er a/. (1995)

CE and glasshouse Glasshouse

Tumbull er al. (1992)

Cells drenched into medium Cells drenched into medium

Glasshouse

Fridlender et al. (1993)

Glasshouse

Fridlender et 01. (1993)

Cells sprayed into furrow Cells drenched into medium

Field

Press and Kloepper (1994)

Glasshouse

Rankin and Paulitz (1994)

into

Glasshouse

Ryder and Rovira (1993)

into

Glasshouse

Rankin and Paulitz (1994)

into

CE

Maurhofer er a/. (1995)

into

CE

Maurhofer er 01. (1995)

Cells drenched into medium Cells drenched into soil

CE

Maurhofer et al. (1995)

CE

Maurhofer er a/. (1992,

Cells drenched into medium

CE

Cells drenched soil Cells drenched medium Cells drenched medium Cells drenched medium

Fridlender er al. (1993)

1994c)

Maurhofer er al. (1995)

TABLE X Contd Antagonist

Pathogen or disease

Host

Growing medium

Inoculation technique

Site

Reference

Thielaviopsis basicola

Tobacco

Artificial soil

Cells drenched into medium

CE

Maurhofer er al. (1995)

P . f7uorescens CH33

Pythium aphonidermarum

Cucumber

Rockwool

Cells drenched into medium

Glasshouse

Moulin et al. (1994)

P . fluorescens M24

Phytophthora cinnamomi

Jacaranda

Peat-sand mix

Glasshouse

Stirling er al. (1992)

P. Puorescens WCS4llr

Fusarium oxysporum f. sp. dianthi Carnation

B r a n s a n d inoculum added to medium Cells drenched into medium

Glasshouse

van Peer et al. (1991)

Rockwool

F. oxysporum f. sp. raphani

Radish

Rockwool

Cells drenched into medium

Glasshouse

Hoffland et al. (1995)

F. oxysporum f. sp. dianthi

Carnation

Rockwool

Glasshouse

Duijff et al. (1994a)

Mungbean Okra Soybean Sunflower

Soil

Cells drenched into medium Cell suspension drenched into furrow

Field

Ehteshamul-Haque and Ghaffar (1993)

Pepper

Soil

Cells sprayed onto soil

Glasshouse

Lahdenpera ef al. (1991)

Sclerotium cepivorum

Onion

Soil

Chaetomium globosum Cg-13

Pythium u h u m

Sugar beet

Soil

Bran-sand inoculum Field added to soil Wheat bran inoculum C E added to soil

Chdorrhinum foecundissimum

Rhizoctonia solani

Eggplant Pepper Sugar beet

Coniothyrium minitans

Sclerotinia sclerotiorum

Carrot

Soil Soil-less mix Soil-less mix Soil

Lettuce

Soil

Pseudomonas p U h h WCS358 Rhizobium spp.

Streptomyces griseoviridis Fungi Chaetomium globosum

Fusarium spp. Macrophomina phaseolina Rhizoctonia solani Damping-off

]

Root rot complex present in soil

Kay and Stewart (1994) Di Pietro et al. (1992)

Bran inoculum incorporated into medium

CE

Lewis et al. (1991a)

Spore spray to plants and soil Maizemeal-perlite and other inocula incorporated into soil

Field

Evenhuis et al. (1995)

Glasshouse/ field

Budge and Whipps (1991); Budge d al. (1995); McQuilken and Whipps (1995)

Oilseed rape

Soil

Coniofhyrium minitans [k Talaromyces

Sclerolinia scleroliorum

Sunflower

Soil

Fusarium hererosporum

Sclerofinia homoeocarpa

Creeping bentgrass

Soil

Fusarium oxysporum (non-pathogenic)

F. oxysponun f. sp. cucwnerinum

Cucumber

Soil

m.4

F. oxysporum f . sp. dianthi

Carnation

Soil

F. oxysporum f. sp. lycopersici

Tomato

Peat-perlite

F. solani

Pea

Soil

(k Pseudomonas SPP.)

F. oxysporum f. sp. lini

Flax

SoUrockwool

(k Pseudomonas C7)

F. oxysporum f. sp. radicis-lycopersici

Tomato

Rockwool

(+ Pseudomonas WCS358)

F. oxysporum f. sp. dianthi

Carnation

Rockwool

F. oxysporum f. sp. lycopersici

Tomato

soil

Verticdliwn dahliae

Eggplant

Soil

F. oxysporum f . sp. dianthi

Carnation

RockwooUsod

F. oxysporum Fo47 (non-pathogenic)

F. oxysporum MT0062 (non-pathogenic)

F. oxysporwn 618-12 (non-pathogenic)

Maizemeal-perlite inoculum incorporated into soil. Spores applied to soil and crop residues. W e a t bran inoculum added to planting furrow Cornmealsand inoculum added as topdressing Chlamydospores incorporated into soil Spores incorporated into soil Spores incorporated into medium Spores incorporated into soil Micrownidia incorporated! drenched into medium Micrownidia drenched into medium Micrownidia drenched into medium Zeolite-spore mixture applied to soil Zeolite-spore mixture applied to soil Spore suspension drenched onto media

Field

McQuilken

Field

McLaren et a/. (1W)

Field

Goodman and Burpee (1991)

Glasshouse

Mandeel and Baker

el

al. (1995)

(1991)

Field Glasshouse

Garibaldi and GuUino (1990) Alabouvette ef al. (1993)

CE

Oyarzun

Glasshouse

Alabouvette

Glasshouse

Lemanceau and Alabouvette (1991)

Glasshouse

Lemanceau

Glasshouse

Yamaguchi et al. (1992)

Glasshouse

Yamaguchi et a / . (1992)

Glasshouse

Rattink (1993); Postma and Rattink (1992)

el

a / . (1994) el a / . (1993)

el

al. (1992)

TABLE X Contd Antagonist

Pathogen or disease

Host

Growing medium

Inoculation technique

Site

Reference

F. solani

Pea

Soil

Spores incorporated into soil

CE

Oyarzun et al. (1994)

F. oxyspomm f. sp.

F. oxysporum f. sp. nivewn

Water melon

Soil

Field

Martyn er al. (1991)

Gaeumannomyces graminis var. graminis

Gaewnannomyces graminis var. tritici

Wheat

Soil

Seedlings and roots drenched in spore suspension Oat grain inoculum incorporated into soil

Field

Wong (1994); Wong e t a [ . (1%)

G . gramink var.

G. gram'nis var. ttitici

Wheat

soil

Field

Duffy and Weller (1995)

Pseudomonas spp.) Gliocladiwn roseum

Oat grain inocdum added to furrow

VenScUium dahliae

Soil

Bran-vermiculite culture incorporated into soil Spores incorporated into soil

CE

Keinath et al. (1991)

Glasshouse

Tu (1991)

Glasshouse

Smith et al. (1990)

Glasshouse

Roiger and Jeffers (1991)

CE

Lewis et al. (1991a)

Field

Ristaino et al. (1994)

niveum (non-pathogenic)

graminis (k

Gliocladiwn virens

G . virens

Rhizoctonia solani Phytophthora cactorum

b

Navy bean

soil

Apple

Potting mix

Apple

Soil Soil

Rhizoctonia solani

Carrot

Soil

Peat-bran inoculum incorporated into medium Peat-bran inoculum incorporated into soil Vermiculite-bran and fermenter biomass added to soil Bran-prill incorporated into soil

G. virem GL-3

G. virens GL-21

Scleronum rolfsii

Rhizoctonia solani

Snapbean

Zinnia

Carrot G. virens G2

Pythium ulfimwn

Cucumber

G . virens G-6

Rhizoctonia solani

Cotton

G . virens G20 (= GL21)

Pyrhium ulfimum

Lettuce Zinnia

Glomus sp.

Phyrophrhora cinnamomi

Pineapple

Pyrax-fermenter biomass incorporated into soil Formulated fermenter biomass incorporated into soil Soil-less potting Alginate pill formulation mix incorporated into medium Soil Bran-pnll incorporated into soil Peat Peat-bran inoculum incorporated into medium Soil Millet-vermiculite inoculum incorporated into medium Fermenter biomass Potting mix incorporated into medium Soil-less potting Wheat bran culture or alginate prill mix formulation incorporated into medium Soil Spores, hyphae, roots and medium from pot culture incorporated into soil

Soil

CE

Papavizas and Collins (1990)

CE

Papavizas er al. (1990)

CE

Lumsden

Field

Ristaino er al. (1994)

CE

Wolffhechel and Funck Jensen (1992)

CE

Howell and Stipanovic (1995)

Glasshouse

Lynch er al. (1991)

CE

Lumsden er al. (1992b); Wilhite et al. (1994)

CE

Guillemin er al. (1994)

el al.

(1992a)

TABLE X C o d ~

Antagonist

Pathogen or disease

Host

Growing medium

Glomus fasciculatum

Fusarium moniliforme

Cardamom

Soil

G . inwaradices

Pythium ubimwn

Marigold

soil

G . mosseae

Pythium ultimum

Marigold

Laccaria bicolor

Fusarium oxysporum

Laetisario arvalis

Rhirocmnia solnni

Soil

Spores, hyphae, roots Glasshouse

Calvet er al. (1993)

Douglas fir

Agar

Agarbhkswith

CE

Strobel and Sinclair (1991)

Cotton

soil

Bran culture incorporated into soil

Glasshouse

Lewis and Papavizas

soil

Milleebran inwrporation or soil spray Bran inoculum placed on soil surface Mycelial preparation incorporated Peat-bran inoculum incorporated into medium Spores drenched into soil

Field

Render er al. (1993)

Glasshouse

Pfender er al. (1996)

CE

Chakravany et al. (1991)

Glasshouse

Fang and Tsao (1995b)

Glasshouse

De Cal el al. (1995)

Pyrenophora tritici-repentir

Penicillium funiculosum

Penicillium oxalicwn

Fusarium moniliforme Fusariwn oxysporum Phytophthora spp. Fusariwn oxysporum f. sp. lycopersici

Reference Thomas er al. (1994)

Soilsand Paxillus involurus

Site

Spores, hyphae, roots Shaded field and medium from pot wlhlre incorporated into soil Spores, hyphae, roots Glasshouse and medium from pot culture incorporated into soil

Lettuce Radish Sugar beet Limonomyces roseipeliv

~~

Inoculation technique

P i w resinosa

Azalea Sweet orange Tomato

Peat-perlitel vermiculite Peat-perlite Soil

and medium from pot culture incorporated into soil mycelium

S t - b a u d et al. (1994)

(1992)

Phialophora sp

Gaeumannomyces graminis var. tritici

Wheat

Phytophthora parasitica var. nicotianae

Phytophthora parasitica

Catharanthus roseus

Pythium aunthicum

Rhizoctonia solani

Carrot

Pythiwn nunn

Phytophthora

Azalea Sweet orange

Pyrhiwn nunn (k Trichoderma harzianum T-95) Pythium oligandrum

Pythiwn u l r i m m

Cucumber

Pythium ultimum

Cress

Soil

Rhizoctonia (binucleate)

Rhizoctonia solani

Capsicum

Potting mix

Cucumber

Soil

SPQ.

Potato Sporidesmiwn sclerotivorum

Sclerotinia minor

Lettuce

Soil

Oat grain inoculum incorporated into soil Peat-vermiculite Colonized around grain incorporated in10 medium Soil Colonized grain inoculum incorporated into soil Peat Oat grain inoculum incorporated into medium Soil Mycelial mats of P. nunn added to soil

Soil Soil

Field

Wong er al. (1996)

Glasshouse

Holmes and Benson (1994)

Glasshouse

Walker (1991)

Glasshouse

Fang and Tsao (199Sa)

Glasshouse

Paulitz er al. (1990)

Oospore preparations CE incorporated into soil Colonized grain and CElglasshouse other organic inocula incorporated into media Colonized grain Field inoculum incorporated into soil Glasshouse Colonized grain inoculum added to furrow Preparation of mycelium and spores added to soil

Field

McQuilken et 01. (1992b) Hams et

01.

(1993b)

Cubeta and Echandi

(1991) Villajuan-Abgona er a/. (1%) Escande and Echandi

(1991) Field

Adams and Fravel (1990); Fravel er al. (1992)

TABLE X Contd Antagonist

Pathogen or disease

Host

Sterile red fungus

G. graminis var. tritici

Wheat

Talaromyces flavus

Verticillium dahliae

Eggplant

Talaromyces flavus ( f Coniothyrium minitans) Talaromyces flavur Tf-1

Sclerotinia sclerotiorum

Sunllower

Verticillium dahlwe

Eggplant

Trichodenna sp. C62

Sclerotium cepivorum

Onion

Trichodenna spp.

G. graminis var. tritici Phytophthora caci?mm

Wheat

Phytophthora cryptogea

Gerbera

Pythiwn ultimum

Cucumber

Apple

Rhizoctonia solani

Lettuce

Growing medium

Inoculation technique

Colonized grain inoculum added to soil Soil Alginate prill formulations with organic carriers added to soil Wheat bran inoculum Soil added to planting furrow Potting mix/soil Spores drenched onto medium Soil Bran-sand inoculum incorporated into soil Soil Spores added to soil Potting mix Peat-bran inoculum incorporated into medium Spores incorporated Peat into medium Peat-bran inoculum Peat incorporated into medium Potting compost Peat-bran inoculum incorporated into medium Maizemeal-perlite Soil

soil

inoculum

incorporated into soil

Site

Reference

CE

de Jong et d.(1993)

Glasshouse

Fravel et al. (1995)

Field

McLaren et af. (1994)

CE

Fravel and Roberts (1991)

Field

Kay and Stewart (1994)

CE Glasshouse

Ghisalberti et al. (1990) Smith ef al. (1990)

Glasshouse

Orlikowski (1995)

CE

Wolffhechel and Funck Jensen (1992)

Glasshouse

Maplestone et al. (1991)

Glasshouse

Coley-Smith er al. (1991)

Soil

Trichoderma hamatum

Rhizoctonia solani

Trichoderma hazianum

Fusariwn graminearwn Glomerella glycines M a c r o p h o m h phaseolina Pyrhium ultimum

Trichodewna harzianwn

Radish

Composted hardwood bark Soil

Lettuce

Potting mix

Tomato

Rockwool

T. harzianum MTR 35

F. oxysporum f. sp. radicis-lycopersici

T. harzianum ThzIDl

Sclerotinia sclerotiorum

T. harzianum T-95 (t Pyrhium nunn)

Pythium ultimum

Cucumber

Soil

Trichoderma koningii

Sclerotium rolfsii

Tomato

Soil

soil

Soil

Sclerorinia sclerotwrum Typhula phacorrhiza

Verticilliwn bigurtatum

Typhda ishikariemis

Creeping bentgrass

soil

Rhizoctonia solani

Potato

Soil

"CE: Controlled environment facility. 'Sclerotia or infected plant material placed in soil in absence of a host plant.

Vermiculite-bran and fermenter biomass incorporated into soil Spores added to growing media

CE

Lewis

CE

Chung and Hoitink (1990)

Conidia sprayed onto soil

Field

Fernandez (1992)

Fermenter biomass inoculum added to medium Spore suspension drenched onto medium Alginate pellet formulation added to soil

Glasshouse

Lynch er al. (1991)

Glasshouse

Rattink (1993)

Field

Knudsen et al. (1991a)

Glasshouse

Paulitz er al. (1990)

Field

Latunde-Dada (1993)

Field

Trutmann and Keane (1990) Lawton and Burpee

Conidia of T. harzianum applied to seed Mycelial powder 01 spore germlings added to soil Spore suspension added to soil Colonized grain applied as a top-dressing Conidia applied to soil

Field

et

al. (1991a)

(1990) Field

van den Boogert and Velvis (1992)

TABLE XI Recent examples of specific antagonists applied to cuttings and roots which show potential to provide biological control of soil-borne plant pathogens Antagonist

Bacteria Agrobacteriwn radiobacter K84; K1026 Bacillus spp.

Pathogen or disease

Host

Growing medium

Agrobacterium nunefaciens

Peach

Soil

Rhizoctonin solani Sclerotium rorfsii

Cotton

soil

Bacillus subtilis EBW4

Replant disease

Apple

Soil

P s e u d o m o m sp. WCS417r Pseudomoms spp.

Furarium oxysporum f. sp. dinnthi Carnation Rhizoctonia solani

Poinsettia

Polyfoam cubes

Tomato

Soil

P. cepacia

Fusarium oxysporum f. sp. lycopersici F. oxysporum f. sp. vasinfectum Sclerotium rolfsii Phytophthora cinnamomi

P. cepacia 5.5B

Rhizoctonia solani

Poinsettia

Soil

Cotton Bean F’rotea

Oasis block/ potting mix Polyfoam cubes

Inoculation technique Wounded roots dipped in peat suspension of cells Trimmed roots dipped in cell suspension Roots dipped in cell suspension Roots dipped in cell suspension Cells onto roots on cubes Roots dipped in cell suspension

Site

Reference

Field

Vicedo et al. (1993)

Glasshouse

Pleban et af. (1995)

Field

Utkhede and Smith (1993b) Duijff et al. (1993)

Glasshouse Glasshouse Glasshouse

Cartwright and Benson (1995b) Gamliel and Katan (1993)

Cell drench

Glasshouse

Turnbull er al. (1992)

Cells onto roots on cubes

Glasshouse

Cartwright and Benson (1995a,b,c)

P. putida WCS 358r

Fusarium oxysporum f. sp. dianthi Carnation

Soil

P. putida 89B - 27

F. oxysporum f. sp. cucumerinum

Cucumber

Potting mix

Serratia marcescens 90- 166 Strepromyces griseoviridis

F. oxysporum f. sp. rucumerinum

Cucumber

Potting mix

F. oxysporum f. sp. dianthi

Carnation

Soil

Fusarium spp

Fusarium oxysporum f. sp. cyclaminis

Cyclamen

Fusarium spp. (non-pathogenic)

F. oxysporum f. sp. radicis-lycopersici

F. oxysporum (non-pathogenic)

Roots dipped in cell suspension Roots dipped in cell suspension Roots dipped in cell suspension Roots dipped in cell suspension + soil spray with cells

Glasshouse

Duijff et a/. (1993)

Glasshouse

Liu er

Glasshouse

Liu et al. (1995b)

Glasshouse

Lahdenpera et a/. (1991)

Potting mix

Roots dipped in spore suspension + cells incorporated into potting mix

Glasshouse

Minuto et

Tomato

PeaUsoil

Glasshouse

Louter and Edgington (1990)

F. oxysporum f. sp. dianthi

Carnation

Soil

Field

F. oxysporum f. sp. dianthi Paecilomyces lilacinus 6.2F

F. oxysporum f. sp. lycopersici

Tomato

Soil

Garibaldi and Gullino (1990) Kroon er al. (1991)

Rhizoctonia solani

Poinsettia

Polyfoam cubes

Homogenized agar culture applied to roots Cuttings dipped in spore suspension Roots dipped in spore suspension Spores placed on cubes

Verticillium chlamydosporium

Phytophthora capsici

Pepper

Soil

Fungi

Roots dipped in spore suspension

Glasshouse Glasshouse Glasshouse

01.

(1995b)

01.

(1995)

Cartwright and Benson (1995a.b) Sutherland and Papavizas (1991)

68

J. M. WHIPPS

Although not a full comprehensive survey of the literature, a range of other features are apparent from Tables IX, X and XI. For example, Pseudomonas spp. were the most frequently reported bacterial antagonists irrespective of the method of application. Isolates of Bacillus spp., Enterobacter spp. and Streptomyces spp. also repeatedly appear in the tables at a lower frequency, although Enterobacter spp. were not reported as being successfully applied directly to roots or cuttings. Numerous other bacterial antagonists were recorded but only sporadically. Overall, seed treatment was generally the application method of choice for bacteria whereas fungi were more commonly applied to soil, growing media, roots or cuttings. Reports of successful use of fungal antagonists were dominated by Gliocladium spp. and Trichoderma spp. and these two antagonists were applied at equal frequency to seeds, soil or growing media. Non-pathogenic fusaria were repeatedly applied to soil and growing media, roots or cuttings but not to seeds. Interestingly, isolates of the arbuscular mycorrhizal genus Glomus were used regularly as antagonists, applied to soil or growing medium. There were also several reports of attempts to combine different isolates of bacteria, different isolates of fungi, or mixtures of bacteria and fungi together, further expressing the trend in research discussed in section 111. In addition, some researchers have examined the possibility of applying antagonists to crop residues to break the pathogen cycle (Fernandez, 1992; Pfender et al., 1993, 1996; Budge et al., 1995). These novel biocontrol systems for soil-borne pathogens could be commercially practical, providing the quantity of inoculum required for control is not excessive. Various aspects of selection, inoculum production, formulation and application related to the use of specific antagonists are discussed in more detail below. A. SELECTION AND SCREENING

The theoretical and practical aspects of selecting potential biological disease control agents and the subsequent screening procedures to ascertain comparative efficiency have been thoroughly reviewed recently (Merriman and Russell, 1990; Campbell, 1994; Whipps, 1997a). Consequently, only the basic principles involved with these procedures will be described here. The first step in any biological disease control programme concerns the initial isolation of potential antagonists. Several approaches have been used with no single system apparently more successful than another. For example, antagonistic microorganisms have been selected from the intended environment of use such as soils, seeds or roots. The pathogen of interest may not even have to be present. This is based on the assumption that any antagonist will be ecologically adapted to this environment and be able to survive and express activity when reapplied as a biocontrol agent. Large collections of

BIOLOGICAL CONTROL OF SOIL-BORNE PLANT PATHOGENS

69

bacteria and fungi have been isolated in this way (Kloepper et al., 1988; Renwick et al., 1991; Swadling and Jeffries, 1996). Another successful approach, already mentioned in section 11, has been to isolate antagonists from soils suppressive to a particular pathogen. Certainly Strepfomycesgriseoviridis and non-pathogenic Fwarium oxysporum Fo47, which are the active moieties in the commercial or near commercial products Mycostop and Fusaclean, respectively (Table XII), were isolated in this way from suppressive peat and soil (Alabouvette et al., 1993; Kortemaa et al., 1994). Alternatively, propagules or mycelia of pathogens have been placed in soil as baits from which antagonists have been isolated. In this case, antagonists would have the potential to attack the pathogen and could also be adapted to the environment where the pathogen is active (Kobayashi ef al., 1995). This procedure has been applied particularly to obtain antagonists from sclerotia of several pathogens including species of Sclerotinia and Sclerotium, Typhula incarnata and Phymatotrichum omnivorum (Adams, 1987; Kenerley and Stack, 1987; Woodbridge et al., 1988; Trutmann and Keane, 1990; Sandys-Winsch et al., 1994) as well as parasites of spores of species of Oomycetes (Sneh et al., 1977; Wynn and Epton, 1979). Further, as an extension of this approach, based on the assumption that biocontrol in the environment can take place through activity of enzymes which can degrade components of fungal cells, antagonists have also been selected from soils enriched with materials such as chitin and laminarin (Mitchell and Alexander, 1962; Ordentlich et al., 1988; Fridlender et al., 1993). Having obtained a collection of antagonists, they then have to be screened for reproducible biocontrol activity. In most cases this involves a bioassay which attempts to mimic, to some extent, the conditions where biocontrol is required to act. Due to the large number of microorganisms which often have to be screened, several thousand in some cases (Weller et al., 1985; Kloepper et al., 1988), this could be a costly, time-consuming exercise. A trade-off between realism of the screening test and cost-effectiveness has to be made. Consequently, for economy, ease and speed, this frequently involves seedling bioassays carried out under controlled conditions to minimize environmental variables which constantly influence reproducibility. This is illustrated in the frequent occurrence of such seedling-based tests in Tables IX, X and XI. Further, seedling diseases caused by pathogens such as Pythium spp. and Rhizoctonia solani are major problems in their own right and, as they can be effectively controlled biologically if protection can be provided in the brief susceptible period or “window of opportunity” for infection (Osburn and Schroth, 1989; Fukui et al., 1994), it further explains the large number of screens for biocontrol agents for these pathogens. Successful isolates from primary screens generally undergo some form of more complex secondary screening. This may involve the use of older plants or different cultivars (Larkin et al., 1993a,b; Mazzola et al., 1995), varying

TABLE XI1 Examples of antagonists available or in the process of registration for use in commercial disease biocontrol preparatiom for soil-borne plant pathogens (revised from Whipps (1992), Lumsden et al. (1955) and following personal communication with R. D. Lumsden and D. R. Fravel) Antagonist

Target pathogen(s)/activity ~~~~~~

Bacteria Agrobacterium radiobacter

Bacillus spp. Bacillus subtilis

Pseudomonas (Burkholderia) cepacia

Diseasehost

Product name and source

Agrobacterium tumefaciens

Crown gall of crucifers, roses and fruit trees

Rhizoctonia cerealis; growth promotion Pythium ultimum; Rhizoctonia solani; Fusarium spp; growth promotion Various fungi

Rice and other crops

Diegall (Fruit Growers Chemical Co., NZ); Galltrol (AgBio Chem, Inc., CA, USA); NoGall (Root Nodule Pty Ltd, Bio-Care Technology Pty Ltd, Australia); Norbac 84-C (New BioProducts Inc., CA, USA) - (Chinese Government)=

Damping-off and root rots of cotton and legumes

Kodiak (A-13) and Epic (MBI600) (Gustafson, Inc., TX, USA)

Vegetables

Seedling pathogens

Field crops

Fusarium spp; Pythium spp; Rhizoctonia solani Fusarium spp; Pythium spp; Rhizoctonia solani

Cotton, maize and vegetables

Bactophyt (NPO Vector, Novosibirsk, Russia) System 3 (GB03) (Helena Chemical Co., TN, USA) Intercept (Soil Technologies, Fairfield, IA, USA) Blue Circle and Deny (CIT Corporation, Carlsbad, CA, USA)

~

Vegetable seeds

Fusarium oxysporum f. sp. raphani Pseudomonas solonacearum

Damping-off or wilt of radish

Streptomyces griseoviridis

Fusarium spp; Pythium spp. and others

Ornamentals and vegetables

Fungi Coniothyrium minitans

Sclerotinia sclerotiorum

Sunflower

Sclerotinia minor; S . sclerotiorum

Vegetable and field crops

Fusarium oxysporum f. sp. batatas

Fusarium wilt of sweet potato

Fusarium oxysporum

Fusarium wilt of carnation and tomato

Pseudomonas fluorescens Pseudomonas solanacearum (non-pathogenic)

Fusarium oxysporum (non-pathogenic)

Gaeumannomyces graminis var. graminis Gliocladium catenulatum

Gaeumannomyces graminis var. tritici Pythium spp.

Gliocladium virens

Pythium ultimum; Rhizoctonh solani

Vegetables

Fusarium wilt of basil, carnation and tomato Take-all of wheat Vegetables Damping-off of bedding plants

BioCoat (S&G Seeds, BV, the Netherlands) PSSOL (Natural Plant Protection, Nogueres, France) Mycostop (K61) and Stirnagrow (Kemira Agro Oy, Helsinki, Finland) Coniothyrin (Russian Government) Contans (Prophyta Biologischer Pfanzenschutz GmbH, Germany) - (Japanese Government) Fusaclean (Fo47) (Natural Plant Protection, Nogueres, France) Biofox-C (S. I.A. P. A., Bologna, Italy) - (Bio-Care Technology, Pty Ltd, Australia)b Primastop (Kemira Agro Oy, Helsinki, Finland) GlioGard and SoilGard (GL-21) (Grace-Sierra Co.,

MD, USA)

TABLE XI1 Contd Antagonist

Target pathogen(s)/activity

Diseasehost

Peniophora (Phlebia) gigantea

Heterobasidion annosum

Stem and root rot of pine

Phialophora sp.

Gaeumannomyces graminis var. tritici Pythium ultimum

Take-all of wheat

Botrytis, Pythium, Sclerotinia and Verticillium spp. Various fungi

Fruit and vegetables

Pythium spp; Rhizoctonia solani

Bedding plants

Pythium spp; Rhizoctonia solani; Sclerotium rorfsii Fusarium spp; Pythium ultimum; Rhizoctonia solani Fusarium spp; Pythium ultimum; Rhizoctonia solani; Sclerotinia homeocarpa

Field crops and vegetables

Pythium oligandrum Trichoderma spp. Trichoderma spp.

Trichoderma harzianum

Damping-off of sugar beet

Fruit and vegetables

Damping-off and root rot of vegetables and row crops Range of crops, ornamentals and turf

Product name and source Pg suspension (Ecological Laboratory Ltd, UK) Rotstop (Kemira Agro Oy, Helsinki, Finland) - (Bio-Care Technology, F’ty Ltd, Australia)b Polygandron (Vyzkummy ustov rastlinnej, Slovak Republic) Trichodermin (Bulgarian and Soviet Governments) Promot (J. H. Biotech, Inc, Ventura, CA, USA) Solsain, Hors-solsain, Plantsain (Prestabiol, Montpellier, France) ANTI-FUNGUS (Grondontsmettingen De Ceuster, Belgium) TY (Mycontrol, Israel) F-Stop (TGT, Inc., NY, USA) T-22G and T-22HB (TGT, Inc., NY, USA)

Various fungi

T. harzianum polysporum

T. harzianum

Fusarium spp; Rhizoctonia solani Armillaria mellea

Field crops and vegetables

Pythium spp; Sclerotinia spp.

Fruit and vegetables

+ T.

Armillaria mellea

Honey fungus of trees

+ T. viride

Heterobasidion annosum Chondrostereum purpureum

Stem and root rot of pine Silverleaf disease in pip and stone fruit trees

Various fungi

Various hosts

Phytophthora spp. Pythium spp?; growth promotion

Ornamentals Cucumber

Trichoderma viride Vesicular-arbuscular mycorrhizas

See Tang (1994). See Wong (1994); Wong et al. (1996). See Orlikowski (1995).

Honey fungus of trees

Supraavit (Bonegaard and Reitzel, Denmark) T-35 (Makhteshim, Israel) Harzian 20 (Natural Plant Protection, Noguerres, France) Harzian 10 (Natural Plant Protection, Noguerres, France) BINAB-T and W (Bio-Innovation AB , Tiireboda, Sweden) Trichodowels, Trichoject and Trichoseal (Agrimm Technologies Ltd, New Zealand) Trichopel (Agrimm Technologies Ltd, New Zealand) Bip T (Po1and)c Vaminoc (AGC Microbio, Cambridge, UK)

74

J. M. WHIPPS

environmental conditions (Budge et al., 1995; Duijff et al., 1995), the use of a range of soils or growing media (Paulitz et al., 1990; Trapero-Casas et al., 1990; Alabouvette et al., 1993), or different inoculum forms of the antagonist and strains of the pathogen (Holmes and Benson, 1994; Fang and Tsao, 1995a). In some cases, the screen may be expanded to test for efficiency against other pathogens and plants, and if still apparently effective, tests extended to consider environmental impact and safety (Mintz and Walter, 1993). Eventually, the screening procedure culminates in large-scale glasshouse or field trials relevant to the host-pathogen combination under consideration. Significantly, in vitro agar plate studies bearing little or no resemblance to environmental or microbiological conditions in the field, and which cannot consider antagonists acting through induced resistance, competition or plant growth promotion, are less frequently used as a primary screen than previously. Nevertheless, in vitro studies can provide useful data on growth parameters of antagonists and these may help with subsequent inoculum production. Information on production of antibiotics, siderophores and lytic enzymes as well as parasitism can also be obtained from in vitro studies and so these tests can have some value. Indeed, if one of these modes of action is viewed as the primary or sole reason for activity against a specific pathogen, targeted in vifro screens, based on obtaining more isolates with the same or greater activity in this mode of action, could be feasible. Therefore, understanding the limitations and advantages of both in vifro bioassays and in vitro studies are of key importance in developing successful biocontrol agents. B. INOCULUM PRODUCTION, FORMULATION AND APPLICATION

Once a biological control agent has shown reproducible activity in a series of screening trials, methods for inoculum production, formulation and application need to be considered in relation to the crop, disease and environment of use. The production of suitable quantities of viable and active cells, spores or biomass is the first step in this procedure. Both liquid and solid substrate fermentation have been used for this purpose. It has been argued that liquid fermentation is the preferred approach for biomass production in countries in Europe and North America, where deep tank fermentation systems are already in place (Churchill, 1982). Certainly all the commercial bacterial antagonists and several of the fungal ones listed in Table XI1 are produced by this method. Inexpensive materials such as molasses, brewer’s yeast, corn steep liquor, sulphite waste liquor, and cotton seed and soy flours are possible suitable substrates (Lisansky, 1985). Certainly, liquid media based on molasses and molasses-yeast have been used widely for the production of antagonists such as Pythium oligandrum,

BIOLOGICAL CONTROL OF SOIL-BORNE PLANT PATHOGENS

75

Gliocladium and Trichoderma spp. (Papavizas et al., 1984; McQuilken et al., 1990a; Jackson et al., 1991a,b). Significantly, for fungal antagonists, spore types required for efficacy and which can withstand the rigours of subsequent formulation and application have been successfully produced in culture. For instance, chlamydospores of Gliocladium and Trichoderma spp. were produced in molasses-yeast media (Papavizas et al., 1984; Jackson et al., 1991a,b) and oospores of Pythium oligandrum were produced in molasses-based medium (McQuilken et al., 1990a). Interestingly, recent studies have suggested that rather than using oospores of P. oligandrum, which germinate slowly and erratically, as propagules for biocontrol, zoospore cysts could be a useful alternative (Madsen et al., 1995). However, it remains to be seen whether a realistic liquid fermentation system for the production of these propagules can be developed. Liquid fermentations have advantages in allowing continual control of nutrients, pH, temperature and other environmental parameters which can help optimize biomass production, spore quantity and quality, and reduce the risk of contamination. For example, changing the C:N ratio of the medium influenced spore quantity and quality in Gliocladium and Trichoderma spp. (Jackson et al., 1991a,b,c,d) and Pythium oligandrum (McQuilken et al., 1992a), addition of complex organic materials such as V8 juice, yeast extract or proteose peptone increased conidial production in Trichoderma harzianum (Tronsmo and Harman, 1992), and addition of osmotica such as polyethylene glycol improved conidial production of T. harzianum and resistance of conidia to desiccation (Harman et al., 1991). Liquid fermentation also allows the kinetics of growth and sporulation to be examined and thus manipulated. For example, unusually, Zdriella bolleyi was found to form spores easily in submerged liquid culture, with sporulation beginning during exponential growth after only 1-2 days (Jadubansa et al., 1993; Lascaris and Deacon, 1994). Such speed of sporulation may suggest a more cost-effective fermentation can be achieved with this fungus than others such as Gliocladium, Talaromyces and Trichoderma spp., which may require 4-7 days for satisfactory quantities of biomass to be obtained (Lumsden and Lewis, 1989). An extension of the liquid fermentation procedure involves the addition of liquid media to inert supports. This can have the advantage of providing a solid inoculum for subsequent use and, for fungi, frequently encourages sporulation in isolates that fail to sporulate or only sporulate poorly in liquid culture. For instance, Rhizobium and Pseudomonas spp. have been grown on nutrient-supplemented vermiculite (Graham-Weiss et al., 1987), Trichoderma harzianum has been produced in diatomaceous earth granules impregnated with 10% molasses (Backman and Rodriguez-Kabana, 1975) and Sporidesmium sclerotivorum has been grown on vermiculite moistened with liquid medium (Adams and Ayres, 1982).

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The alternative method of inoculum production involves the use of solid substrate fermentation. A range of materials including relatively cheap agricultural waste products have been investigated as substrates for production of both bacterial and fungal antagonists. These include lucerne powder, sugar cane bagasse, wheat and rice straw, ground corn cobs, bark, sawdust, compost, various grains, bran and peat, alone or in combination, often mixed with inert fillers as bulking agents such as vermiculite or perlite (Papavizas, 1985; Hoitink and Fahy, 1986; Graham-Weiss et al., 1987; Howell, 1991; Jackson et al., 1991c; Harris et al., 1993a). This system is particularly useful for small-scale laboratory, glasshouse and field tests which require minimal facilities to produce inocula and has the same advantages as the nutrientsupplemented support system described earlier. However, it does have some disadvantages. Solid substrates are bulky, requiring a large space for production, inoculation and storage, and frequently the products need drying and milling, with inherent problems of formation of dusts containing spores. Cost may be high due to packaging, application (if special machinery is required), transport and also due to the amounts which may have to be applied for control to be achieved. In addition, quantity of inoculum may vary as the natural constituents may be inconsistent from batch to batch (Lumsden and Lewis, 1989; Adams, 1990). Nevertheless, commercial mushroom spawn production has been using this type of technology successfully for many years (Flegg et al., 1985) and clearly indicates that cost-effective inoculum can be produced in this way. In many experimental systems, having produced cells, spores or biomass of an antagonist by fermentation, the material is used directly without further treatment. Tables IX,X and XI contain numerous examples where bacterial cells, fungal spores, mycelial biomass or grain-based inocula are applied to seeds, tubers, roots, soil and growing media in this way. However, for most commercial preparations, cells, spores or biomass are generally processed before use. For instance, spores or cells can be concentrated directly from liquid culture media or following washing from solid substrates, by centrifugation, filtration, or occasionally by flocculation (Schmidt-Kastner and Golker, 1987). Biomass may be dried and milled before incorporation into a range of dusts, alginate granules, pellets or prills, wettable powders, emulsifiable liquids or gels. Numerous reports describing the use of a variety of different inoculum forms of antagonists have been published. These range from feasibility studies, demonstrating that antagonists can be formulated and applied in specific ways, to comparative efficacy tests of different types of inocula. Many of the tests carried out in controlled environments or the glasshouse given in Tables IX, X and XI are representative of this type of work, but consideration of a few specific examples demonstrating the different approaches used is of value to illustrate the breadth of this topic. For example, a mixture of chlamydospores, conidia and mycelial fragments of a non-pathogenic isolate of Fusarium oxysporum have been used in a range

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of formulations including dispersal in talc, formulation in alginate pellets or in kaolin-based microgranules. These have then been incorporated into soil or used as an aqueous suspension root dip, for control of F. oxysporum f. sp. cyclaminis, or to determine optimal efficacy (Minuto et al., 1995). Repeated treatments, different treatment intervals and combinations of antagonist were also examined with these formulations. Using a different concept, conidia of Trichoderrna and Gliocladium spp. have been added to a bran-sand mixture and after 1-3 days of incubation, this germling preparation added to soil where colony-forming units of the antagonists continued to increase (Lewis and Papavizas, 1984). This method provides a means of achieving an active population of antagonists in the soil and has been developed further with T. koningii using medium-supplemented ground corn cobs to give control of Sclerotium rolfsii in tomatoes in the field (Latunde-Dada, 1993). Alternatively, fermenter biomass of Gliocladium and Trichoderma spp. has been added to a vermiculite-bran mixture moistened with 0.05 M HCI. After drying, the preparation could be remoistened with 0.05 M HCI and germlings produced as before (Lewis et al., 1991a). This system had the advantage that it did not require sterile conditions during preparation. Considerable research has been carried out on the use of alginate pellet, prill or granule formulations of biocontrol agents. They have been prepared with cells of Pseudomonas spp., spores of Talaromyces flavus, and fermenter biomass of Gliocladium spp., Laetisaria arvalis, Penicillium oxalicum, Pythium oligandrum and Trichoderma spp. (Fravel et al., 1985; Lumsden and Lewis, 1989). These provide materials which are easy to handle and with which the growers are familiar. Frequently, carriers may be added to the prills and these may be inert bulking agents such as pyrophyllite clays, or food bases, such as wheat bran, to enhance proliferation of the biocontrol agent, or a combination of both (Fravel et a [ . , 1995). Since the food base is in the matrix of the granule, it is used preferentially by the biocontrol agent and not by competitors or potential pathogens in the soil. Interestingly, cells of Azospirillum brasilense and Pseudomonas spp. incorporated with alginate pellets with skim milk were found to be released at a slow and constant rate, which could be controlled by the type of hardening treatment given to the pellet during formation (Bashan, 1986). Further, soaking alginate pellets containing biomass of Trichoderma harzianum and wheat bran in polyethylene glycol for 24 h during the drying process resulted in a greater proliferation of hyphae of T. harzianum from the pellets when subsequently placed in soil in comparison with those soaked in water (Knudsen et al., 1991b). This shows the considerable flexibility and adaptability of this process. Various other delivery systems have been explored, particularly concerning applications to seeds. For example, Laetisaria arvalis, Trichoderma harzianum and arbuscular mycorrhizas have been applied in gels to bare roots

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or to seeds, through fluid drilling (Fisher et al., 1983; Conway, 1986; Hung et al., 1991). Commonly, bacterial cells have been incorporated into methylcellulose and coated directly onto seeds (Milus and Rothrock, 1993; Duffy and Weller, 1995; Gupta et al., 1995) and these simple treatments have been extended to xanthum gum-talc or methylcellulose-talc mixtures to improve survival and activity (Kloepper and Schroth, 1981; Suslow and Schroth, 1982; Caesar and Burr, 1991). Similarly, a range of ground solid substrate inocula of Gliocladium virens has been applied to cotton seeds using a latex sticker (Howell, 1991) and cotton seeds pretreated with metalaxyYpentachloronitrobenzenehave been coated with a dust preparation of endospores of Bacillus subtilis GB03 (Mahaffee and Backman, 1993). Although numerous researchers have successfully applied biocontrol agents to seeds using such relatively simple techniques, much effort on formulation and application in the last 5-10 years has focused on specialized seed coating or pelleting procedures (Harman and Lumsden, 1990; Taylor and Harman, 1990; Harman, 1991; Cliquet and Scheffer, 1996). These systems aim to improve the efficacy of the biocontrol agents by optimizing colonization of the seed surface and associated substrate, including seed exudates, as rapidly as possible to prevent germination of propagules and infection by pathogens such as Pythium ultimum. There is also evidence that, for some antagonists such as Pythium oligandrum, application to seeds can provide improved biocontrol in comparison with application of the same propagules to soil or growing media (McQuilken et al., 1990b, 1992b). Many seed coating systems are proprietary or trade secrets (Halmer, 1988) but one successful system, termed a liquid coating, comprised a suspension of aqueous binder (pelgel or polyox-N-lo), finely ground solid particulate matter (Agro-lig or muck soil) and a biocontrol agent, Trichoderma harzianum 1295-22 (Taylor et al., 1991). This was sprayed onto cucumber seeds in a tumbling drum and this process provided control of cucumber damping-off caused by Pythium spp. when treated seeds were planted in pathogen-infested soil. It was suggested that the uniform coating may have, in part, provided a solely physical barrier to the pathogen. In this regard, oospores of Pythium oligandrum applied to cress seeds in a thick pellet generally gave better control of damping-off caused by Pythium ultimum than when oospores were applied as a thin-film coating treatment (McQuilken et al., 1990b) and could be indicative of the approach to be followed for application of biocontrol agents to seeds in general, even though Pseudomonus fluorescens WCS374 in the commercial product “BioCoat” is applied to radish seeds as a thin-film coating (Leeman et al., 1995b). Nevertheless, the concept of applying sequential layers of treatments, such as biological control agents placed on the seeds followed by layers of particulate matter, such as lignaceous shale, as a physical barrier has been suggested (Harman, 1991). This idea relates to the liquid coating system used for Trichoderma harzianurn as the Agro-lig had chemical and physical

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characteristics favourable for the growth of this fungus (Taylor et al., 1988) and this may also have contributed to the biocontrol achieved. The approach of adding compounds to seed coating which specifically enhance growth of the biological control agents has proven successful. For instance, inclusion of specific polysaccharides and polyhydroxy alcohols to pea seed coatings of T. harzianum improved biocontrol activity against damping-off caused by fythium ultimum by 48% (Nelson et al., 1988). The value of adding selective substrates to seeds or soils to enhance survival and performance has also been demonstrated with strains of biocontrol or plant growth-promoting bacteria (Colbert et al., 1993; Devliegher et al.. 1995). Often coating systems have been combined with seed priming systems, where hydration of the seed is controlled to a level that permits pregerminative metabolic activity to take place without emergence of the radicle (Harman, 1991). This combination of seed priming and application of biological control agents should result in seeds which germinate evenly and rapidly, are resistant to various biotic and abiotic stresses, and which are protected from pathogen attack during the susceptible early stages of germination and establishment. Two priming systems are generally available. Osmopriming utilizes aerated aqueous solutions of salts or polyethylene glycol, generating osmotic potential in the primary solution, whereas solid matrix priming (SMP) involves the use of moist, porous solid material, such as powdered coal or peat, generating matric potential. Priming per se, in the presence of applied biocontrol agents, may result in decreased damping-off in sugar beet and several other plants caused by Pyfhium spp. (Taylor et al., 1985; Osburn and Schroth, 1988; Harman ef al., 1989; Rush, 1991). This may be related to a subsequent reduction in exudation of nutrients from seeds, needed for germination of fythium propagules, or a proliferation of indigenous bacteria on the seed. However, of the two processes, SMP has the advantages of being simple and more economical than osmopriming (Harman and Taylor, 1988) and allows for biocontrol agents to be combined with the priming process. For example, cells of Enterobacter cloacae or conidia of Trichoderma harzianum were applied to seeds of cucumber or tomato and placed in Agro-lig for SMP before testing for biocontrol activity in fythium-infested soil. With cucumber, efficacy of T. harzianurn and E. cloacae was enhanced by SMP, increasing initial plant stands from 30 to 90% and from 0 to 70%, respectively. However, post-emergence damping-off was not as effectively controlled, with the plant stand reduced to 60% with T. harzianum and 0% with E. cloacae. With tomato, T. harzianum treatment with SMP again resulted in little daniping-off but efficacy of E . cloacae was virtually lost. The pH of the tomato seeds was 2.8, which inhibited growth of E. cloacae but favoured T. harzianum. Thus. substitution of bituminous coal (pH 6.6) for Agro-lig (pH 4.1) in the SMP process significantly improved biocontrol activity of E. cloacae on tomato but decreased efficacy of T. harzianum,

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demonstrating once again the importance of choice of materials used in any seed treatment system involving biological control agents. Combining SMP with Trichoderma spp. for control of seedling diseases has now been used successfully on a wide range of plants (Harman et a!., 1989) and variations on this theme are now appearing. For example, sweet corn seed has been coated with cells of Pseudomonaspuorescens and primed by incubating treated seed in moist sterile vermiculite for 20-22 h (Callan et al., 1990). Bacterial populations on seeds increased 10- to 10000-fold, and significant increases in plant stand were subsequently obtained in comparison with non-primed, bacterial-treated seeds in cold soils naturally infested with Pythium ultimum. This process, termed biopriming, provided control as good or better than seed treatment with metalaxyl. Combining low rates of imzalil or metalaxyl with Pseudomonas spp. did not affect the efficacy of disease control in this biopriming system (Mathre et al., 1995).

V. CONCLUSIONS AND FUTURE PROSPECTS There has been a gradual increase in the number of commercial biocontrol agents on the market for the control of soil-borne plant pathogens over the last few years (Table XII) and only one product, Dagger-G, a Pseudomonas puorescens marketed by Ecogen, Inc, Lanhorne, PA, USA, for the control of Rhizoctonia and Pythium damping-off of cotton, has been withdrawn from sale because of poor shelf-life of the material (Powell and Jutsum, 1993). This implies that the approaches used for developing commercial biological disease and control agent are becoming more successful. However, chemicals still dominate the disease control market and some consideration should be given to research areas likely to improve further the commercial uptake of biological disease control agents. As discussed in section 11, understanding the ecology and aetiology of any pathogen and the method of cultivation of the crop is of prime importance. Use of cultural methods such as monocropping, rotation, ploughing, solarization and use of compost (sections II.B, C and D) may well be enough to suppress or avoid many diseases. Nevertheless, in most commercial situations, application of a microbial inoculant to achieve biological control is the aim. Consequently, optimizing realistic screening procedures is a first step, which can be refined to target specific types of antagonists (section 1V.A). Recently, for instance, for the first time cyanobacteria (blue-green algae) and other algae have been screened for biocontrol activity against bacterial and fungal pathogens with some success (Kulik, 1995). This opens up the possibility of utilizing a whole group of organisms never previously considered for biological disease control. Once specific antagonists have been identified, they can be developed further by consideration of inoculum production, formulation, storage and

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application, ideally linking the expertise of scientific researchers with industrial partners (Harman and Lumsden, 1990; Lewis and Papavizas, 1991; see section 1V.B). At this stage, if cost-effective, reproducible control has been achieved in small-scale trials, application to regulatory authorities for registration has to be made to obtain permission to market a product. Depending on the country concerned, this can be a major stumbling block for biological disease control agents. For example in the UK, biological control agents fall under the chemical pesticide regulations, and consequently the same type of time-consuming extremely expensive, full efficacy-safety data package must be produced. Currently, the charges made by the MAFF Pesticides Safety Directorate are &4400 for a dossier completeness check, and f60000 and f13400 for evaluation of the dossier for chemicals and biologicals, respectively. This does not include the costs of preparing the dossier in the first place. As many biological disease control agents are targeted at small niche markets, the cost involved in registration becomes prohibitively expensive in view of the likely profit to be made on any product. Hence, at the moment the only biological control agents on sale in the UK for control of soil-borne plant pathogens are BINAB-T and Pg suspension (see Table XII), which were already on the market prior to the new regulations introduced in the late 1980s. Stimagrow and Vaminoc, both of which probably have disease biocontrol activity, are marketed as plant growth promoters and this avoids the pesticide regulations. Similar regulation avoidance loopholes are present in the USA (Cook, 1993). Nevertheless, in general, registration of biological control agents is easier and quicker in the USA because if the “Tier 1” level of toxicological tests (oral, dermal, eye, respiratory and other health hazards using test animals and fish) show no adverse effects, and the microorganism is not a pathogen, usually no further testing is required, although more information may be requested (Cook, 1993; Mintz and Walter, 1993). Even so, based on 1993 data, Tier 1 testing may cost between $100000 and $200000 (US) and may still rule out registration for many biological control agents. However, perhaps the other extreme of registration considerations is seen in China. Between 1985 and 1993, yield-increasing bacteria, mainly species and strains of Bacillus, including several which exhibited disease control activity, were applied to about 40 million hectares on over SO kinds of crop (Tang, 1994). Several factories across China were involved in production of the microorganisms. Nevertheless, regulations associated with their use appear to have been minimal. In global terms, the US approach may seem to be a realistic way forward in this area. This sequential development procedure for biological control agents allows numerous other avenues of research to be followed which may result in improved biocontrol activity in the future. Certainly, the concepts of using combinations of microfauna and antagonists to enhance activity by dissemination of the biocontrol agents (Sutton and Peng, 1993; Whipps and Budge,

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1993; Williams and Whipps, 1995; see section 1I.E) and applying combinations of biocontrol agents to improve the spectrum of activity against one or several diseases (sections 1II.C and IV) deserve further study. The concept of combining systemic acquired resistance (SAR) and treatment with a microbial agent appears novel (Chen et al., 1996) and is also worth examining further. Indeed, the whole area of interactions between antagonists, saprotrophs and soil fauna in the rhizosphere and soil, which is particularly important in terms of establishment, survival and spread of biocontrol agents in general, has been neglected. However, perhaps the most exciting area for further work involves the application of modern molecular methods to biological disease control in all its aspects. Protoplast fusion has been used successfully to enhance efficacy of biocontrol strains of Trichoderma (Harman et al., 1989; Goldman et al., 1991; Pe’er and Chet, 1990; Sivan and Harman, 1991). For example, strain 1295-22, which resulted from a fusion between T. harzianum strains T12 and T45, grew more rapidly than either parental strain, was a more efficient seed protectant on a range of crops including bean, cotton and sweetcorn, and was strongly rhizosphere competent (Harman et al., 1989; Sivan and Harman, 1991). This strain subsequently went on to be registered in the USA as F-stop, for the control of damping-off diseases (Table XII). However, effective biocontrol strains resulting from this process are rare (Migheli et al., 1995). Molecular biology has helped identify the modes of action of many biocontrol agents (section 111). This has enabled targeted screens to be developed, searching for further antagonists acting in the same way. Importantly, in the case of Agrobacteriurn radiobacter, used commercially for the control of crown gall of woody plants caused by Agrobacterium tumefaciens, knowledge of the mode of action obtained through molecular biology has enabled the antagonist to be modified to maintain its use when resistance to the original antagonist strain K84 of A . radiobacrer was observed (Jones er al., 1988; Ryder and Jones, 1990; Stockwell et al., 1996). Strain K84 synthesizes an antibiotic, agrocin 84, which is taken up by the pathogenic bacteria via specific permease systems resulting in death of the pathogen. Strain K84 itself is unaffected by agrocin 84. Transfer of the plasmid coding for agrocin 84 from strain K84 to pathogenic strains results in pathogenic strains becoming resistant to agrocin 84. Consequently, a strain of K84 lacking the ability to transfer the plasmid coding for agrocin 84 production was genetically modified and this strain K1026, the first commercially available genetically modified biological control agent, was marketed in Australia in 1988 as NoGall. This demonstrates that genetically modified microorganisms can be acceptable for commercial use providing the mechanism of action is known and the genetic modifications carried out are clearly understood. Providing the extra level of legislation associated with the use of genetically modified microorganisms does not prove too much of

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a problem for registration in general, this work bodes well for future development of genetically modified disease biocontrol agents. A considerable effort is currently underway to improve biocontrol efficacy of microorganisms through the use of molecular biology. For example, based on mode of action information, a chitinase gene from Serratia marcexens has been introduced into several bacteria including Escherichia coli, Pseudomonas puorescens, P. putida and Rhizobium meliloti, as well as into the fungus Trichoderma harzianum (Sundheim et al., 1988; Shapira et al., 1989; Pe’er et al., 1991; Chet et al., 1993; Haran et al., 1993). Another chitinase gene from Trichoderma harzianum has also been introduced into E. coli (Carsolio et al., 1994). These represent the first steps towards obtaining increased chitinase production in biocontrol strains. With the continued isolation of genes coding for proteins associated with mycoparasitism such as chitinases, ,B-1,3-glucanases and proteases (de la Cruz et al., 1992, 1995; Garcia et al., 1994; Geremia et al., 1093; Goldman et al., 1994b; Hayes et al., 1994), the procedure of introducing extra copies of the same or heterologous genes into biocontrol agents, or obtaining their constitutive expression to achieve enhanced biocontrol activity, will undoubtedly increase. Similarly, since gene sequences coding for the production or regulation of antibiotics and siderophores effective against several soil-borne pathogens are known in bacteria (Gutterson et ul., 1986; Thomashow and Weller, 1988; Gutterson, 1990; Howie and Suslow, 1991; Vincent et al., 1991; Fenton et al., 1992; Dowling and O’Gara, 1994; Gaffney et al., 1994; Hill et al., 1994; Kraus and Loper, 1995; Schnider et al., 1995b; Maurhofer et al., 1995; Keel and Defago, 1997), strains improved by increased production of antibiotics may also be available soon. Nevertheless, all these approaches are dependent on the metabolic load associated with overproduction or expression of novel genes. They should not impair ecological competence. The choice of biological control agent and gene transfer system may be important here (Tang er al., 1995). Significantly, the regulation of some genes involved in biocontrol appears to be cell density dependent, associated with the accumulation of N-(3oxohexanonyl) homoserine lactone and this has been suggested as a possible reason for the apparent necessity for bacterial biocontrol agents which produce this compound, to colonize roots or seeds effectively in order for biocontrol to be achieved (Dowling and O’Gara, 1994). The role of such autoinducing metabolites and the gacAllemA regulatory system (section III.A.2) in biocontrol by bacteria clearly warrants further study. The use of reporter o r marker genes such as lux, lacZ, luc or ice nucleation have also been valuable in studies of biocontrol. For example, when fused to promoters of antibiotic synthesis genes, transcription of these marker genes has enabled antibiotic production to be monitored in situ on the seed coat at levels undetectable by conventional means (Georgakopoulos et al., 1994; Kraus and Loper, 1995; Lindow, 1995). If developed further, this may enable

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biocontrol genes to be expressed by a predetermined environmental trigger such as soil nutrient level, water potential or temperature, or perhaps in response to a specific pathogen in the rhizosphere (Dowling and O’Gara, 1994). In addition, marker genes have been used in the environment tomonitor gene transfer between microbes and to track bacteria and fungi (Couteaudier et al., 1993; de Leij et al., 1995a,b; Green and Jensen, 1995; Keel and DCfago, 1997), providing ecological data which may assist both targeting and application methods of biocontrol agents and which are valuable in risk assessment packages for the registration process. Finally, assuming the broad definition of biological control of Cook and Baker (1983), some brief reference to the use of transgenic plants for the control of soil-borne diseases should be made. Through the use of molecular biology, many of the approaches and concepts parallel those adopted for antagonistic microorganisms. For example, stemming from observations of induced resistance (section 1II.B.l ) , chitinase and, /3-1,3-glucanase genes from a range of sources have been introduced into plants such as canola and tobacco to give enhanced resistance to pathogen attack (Broglie et a f . , 1991, 1993; Jach et al., 1992; Zhu et al., 1994). Similarly, genes conferring resistance to toxins such as tabtoxin produced by pathogenic bacteria (Yoneyama and Anzai, 1993), lytic peptides such as cecropin B and other novel peptides inhibitory to a range of pathogenic bacteria (DestCfano-BeltrBn et al., 1993), and oxalate-degrading enzymes (Thompson et al., 1995) providing tolerance to Sclerotinia sclerotiorum, have all been cloned into plants, and this approach is continuing to develop. Providing expression of the genes is not debilitating to the plant, does not result in production of metabolities toxic to non-target organisms, and resistance does not develop in the pathogen population excessively quickly, the approach has the advantage that no treatments are required once seed is produced. It will be interesting to follow the relative success of the use of genetically modified microbial biocontrol agents and plants genetically modified for disease resistance.

ACKNOWLEDGEMENTS This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) and the Ministry of Agriculture, Fisheries and Food (MAFF) for England and Wales. I would like to thank my colleagues and family for their continued support throughout the production of this review. I dedicate this work to the memory of my mother.

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