Summary Fusarium oxysporum is well represented among the rhizosphere microflora. While all strains exist saprophytically, some are well‐known for inducing wilt or root rots on plants whereas others are considered as nonpathogenic. Several methods based on phenotypic and genetic traits have been developed to characterize F. oxysporum strains. Results showed the great diversity affecting the soil‐borne populations of F. oxysporum. In suppressive soils, interactions between pathogenic and nonpathogenic strains result in the control of the disease. Therefore nonpathogenic strains are developed as biocontrol agents. The nonpathogenic F. oxysporum strains show several modes of action contributing to their biocontrol capacity. They are able to compete for nutrients in the soil, affecting the rate of chlamydospore germination of the pathogen. They can also compete for infection sites on the root, and can trigger plant defence reactions, inducing systemic resistance. These mechanisms are more or less important depending on the strain. The nonpathogenic F. oxysporum are easy to mass produce and formulate, but application conditions for biocontrol efficacy under field conditions have still to be determined.
Dimorphism or morphogenic conversion is exploited by several pathogenic fungi and is required for tissue invasion and/or survival in the host. We have identified a homolog of a master regulator of this morphological switch in the plant pathogenic fungus Fusarium oxysporum f. sp. lycopersici. This non-dimorphic fungus causes vascular wilt disease in tomato by penetrating the plant roots and colonizing the vascular tissue. Gene knock-out and complementation studies established that the gene for this putative regulator, SGE1 (SIX Gene Expression 1), is essential for pathogenicity. In addition, microscopic analysis using fluorescent proteins revealed that Sge1 is localized in the nucleus, is not required for root colonization and penetration, but is required for parasitic growth. Furthermore, Sge1 is required for expression of genes encoding effectors that are secreted during infection. We propose that Sge1 is required in F. oxysporum and other non-dimorphic (plant) pathogenic fungi for parasitic growth.
Contents Summary 529I.Biological control of plant diseases: state of the art 530II.Main modes of action of biological control agents 530III.The protective strains of F. oxysporum: an unexplored model 532IV.Future directions for the study of the protective capacity of strains of F. oxysporum 539V.How to make biological control successful in the field? 540References 541 Summary Plant diseases induced by soil‐borne plant pathogens are among the most difficult to control. In the absence of effective chemical control methods, there is renewed interest in biological control based on application of populations of antagonistic micro‐organisms. In addition to Pseudomonas spp. and Trichoderma spp., which are the two most widely studied groups of biological control agents, the protective strains of Fusarium oxysporum represent an original model. These protective strains of F. oxysporum can be used to control wilt induced by pathogenic strains of the same species. Exploring the mechanisms involved in the protective capability of these strains is not only necessary for their development as commercial biocontrol agents but raises many basic questions related to the determinism of pathogenicity versus biocontrol capacity in the F. oxysporum species complex. In this paper, current knowledge regarding the interaction between the plant and the protective strains is reviewed in comparison with interactions between the plant and pathogenic strains. The success of biological control depends not only on plant–microbial interactions but also on the ecological fitness of the biological control agents.
The most common approach to biological control consists of selecting antagonistic microorganisms, studying their modes of action and developing a biological control product. Despite progress made in the knowledge of the modes of action of these biological control agents (BCAs), practical application often fails to control disease in the fields. One of the reasons explaining this failure is that the bio-control product is used the same way as a chemical product. Being biological these products have to be applied in accordance with their ecological requirements. Another approach consists of induction of plant defence reactions. This can be done by application of natural substances produced by or extracted from microorganisms, plants, or algae. Since they do not aim at killing the pathogens, these methods of disease control are totally different from chemical control. Although promising, these methods have not been sufficiently implemented under field conditions. A third approach consists of choosing cultural practices that might decrease the incidence or severity of diseases. These methods include the choice of an appropriate crop rotation with management of the crop residues, application of organic amendments and the use of new technology such as the biological disinfestation of soils. Biological control practices need an integrative approach, and more knowledge than chemical control.
The protective Fusarium oxysporum strain Fo47 is effective in controlling Fusarium wilt in tomato. Previous studies have demonstrated the role of direct antagonism and involvement of induced resistance. The aim of the present study was to investigate whether priming of plant defense responses is a mechanism by which Fo47 controls Fusarium wilt. An in vitro design enabled inoculation of the tap root with Fo47 and the pathogenic strain (Fol8) at different locations and different times. The expression levels of six genes known to be involved in tomato defense responses were quantified using reverse-transcription quantitative polymerase chain reaction (qPCR). Three genes-CHI3, GLUA, and PR-1a-were overexpressed in the root preinoculated with Fo47, and then challenged with Fol8. The genes GLUA and PR-1a were upregulated in cotyledons after inoculation of Fo47. Fungal growth in the root was assessed by qPCR, using specific markers for Fo47 and Fol8. Results showed a reduction of the pathogen growth in the root of the tomato plant preinoculated with Fo47. This study demonstrated that priming of tomato defense responses is one of the mechanisms of action of Fo47, which induces a reduced colonization of the root by the pathogen.
In soil, fungal colonization of plant roots has been traditionally studied by indirect methods such as microbial isolation that do not enable direct observation of infection sites or of interactions between fungal pathogens and their antagonists. Confocal laser scanning microscopy was used to visualize the colonization of tomato roots in heat-treated soil and to observe the interactions between a nonpathogenic strain, Fo47, and a pathogenic strain, Fol8, inoculated onto tomato roots in soil. When inoculated separately, both fungi colonized the entire root surface, with the exception of the apical zone. When both strains were introduced together, they both colonized the root surface and were observed at the same locations. When Fo47 was introduced at a higher concentration than Fol8, it colonized much of the root surface, but hyphae of Fol8 could still be observed at the same location on the root. There was no exclusion of the pathogenic strain by the presence of the nonpathogenic strain. These results are not consistent with the hypothesis that specific infection sites exist on the root for Fusarium oxysporum and instead support the hypothesis that competition occurs for nutrients rather than for infection sites.
A pathogenic strain of Fusarium oxysporum f. sp. lycopersici transformed with the glucuronidase (GUS) reporter gene was used to study the colonization process of tomato (Lycopersicon esculentum) roots in hydroponic culture. The plants were treated exactly as those used in a different study with a non‐pathogenic strain of F. oxysporum in order to compare the two types of colonization process. The pathogenic strain rapidly colonized the root surface, forming a dense network of hyphae – shown by the GUS staining assay – as early as 48 h after inoculation. The first images of the pathogen penetrating into the epidermis of the root were observed 24 h after inoculation. The plant showed defence reactions mainly in the hypodermis, but also in the cortex. Generally these barriers failed to prevent the centripetal growth of the pathogen towards the stele. The GUS activity moved with the actively growing hyphae into the tissues; the stele appeared intensely stained 7 d after inoculation, whereas by this time the hyphae at the root surface did not show any more staining. The hyphae formed a dense network at the apex of the root, but direct contact between hyphae and living cells was prevented by several layers of sloughed cap cells. Although rarely observed, penetration of the pathogen into the apex was possible and led to a rapid destruction of apical cells. The only differences between this pattern of root colonization and that observed for a non‐pathogenic strain of F. oxysporum appear to concern the frequency of dead apices and the intensity of fungal colonization in the cortex. When the pathogen passed around the barrier formed in the hypodermis it always reached the xylem, although this barrier and other defence reactions induced at different levels in the cortex always prevented the non‐pathogenic strain from reaching the stele. These observations suggest that the main differences between the two types of interaction – between the plant and either the pathogenic or the non‐pathogenic strain – are quantitative rather than qualitative.
SUMMARYA strain of non-pathogenic Fusarium oxysporum Schlecht. emend, Snyd. & Hans, has been selected for its capacity to reduce the incidence of Fusarium wilt of tomato. Among the possible modes of action of this strain, competition with the pathogen for the colonization of the root surface and tissues has been proposed, in order to study the pattern of root colonization, young Lycopersicon esculentum Miller (tomato) plants grown in a nutrient solution were inoculated by a suspension of F. oxysporum microconidia and processed at time-intervals for microscopic observations. The fungal strain was transformed with the Gus reporter gene to facilitate the observations. Within 24 h of inoculation the root surface was colonized by a dense network of hyphae, with the exception of the apex, which was colonized only after 48 h. A few hyphae were observed penetrating into the epidermis, leading to the internal colonization of the root cortex. This colonization was always discontinuous, since defence reactions of the plant limited the extension of the fungus. The barrier formed by thickenings and coilings of the cell walls and hypertrophied cells was most frequently observed in the external cortex and, sometimes, deeper in the internal cortex, close to the vessels which were never colonized. Typical defence reactions such as wall appositions, intercellular plugging and intracellular osmiophilic deposits, were frequently observed. This is the first report, based on microscopic observations, of the capacity of a non-pathogenic strain of F. oxysporum to colonize roots of tomato.
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