Mycotoxigenic Fusarium and Deoxynivalenol Production Repress Chitinase Gene Expression in the Biocontrol Agent Trichoderma atroviride P1

Abstract

Mycotoxin contamination associated with head blight of wheat and other grains caused by Fusarium culmorum and F. graminearum is a chronic threat to crop, human, and animal health throughout the world. One of the most important toxins in terms of human exposure is deoxynivalenol (DON) (formerly called vomitoxin), an inhibitor of protein synthesis with a broad spectrum of toxigenicity against animals. Certain Fusarium toxins have additional antimicrobial activity, and the phytotoxin fusaric acid has recently been shown to modulate fungus-bacterium interactions that affect plant health (Duffy and Défago, Phytopathology 87:1250-1257, 1997). The potential impact of DON on Fusarium competition with other microorganisms has not been described previously. Any competitive advantage conferred by DON would complicate efforts to control Fusarium during its saprophytic growth on crop residues that are left after harvest and constitute the primary inoculum reservoir for outbreaks in subsequent plantings. We examined the effect of the DON mycotoxin on ecological interactions between pathogenic Fusarium and Trichoderma atroviride strain P1, a competitor fungus with biocontrol activity against a wide range of plant diseases. Expression of the Trichoderma chitinase genes, ech42 and nag1, which contribute to biocontrol activity, was monitored in vitro and on crop residues of two maize cultivars by using goxA reporter gene fusions. We found that DON-producing F. culmorum and F. graminearum strains repressed expression of nag1-gox. DON-negative wild-type Fusarium strains and a DONnegative mutant with an insertional disruption in the tricothecene biosynthetic gene, tri5, had no effect on antagonist gene expression. The role of DON as the principal repressor above other pathogen factors was confirmed. Exposure of Trichoderma to synthetic DON or to a non-DON-producing Fusarium mutant resulted in the same level of nag1-gox repression as the level observed with DON-producing Fusarium. DON repression was specific for nag1-gox and had no effect, either positive or negative, on expression of another key chitinase gene, ech42. This is the first demonstration that a target pathogen down-regulates genes in a fungal biocontrol agent, and our results provide evidence that mycotoxins have a novel ecological function as factors in Fusarium competitiveness.

In Vivo Study of Trichoderma -Pathogen-Plant Interactions, Using Constitutive and Inducible Green Fluorescent Protein Reporter Systems

“…For instance, it is possible to discern patterns of gene induction and to observe fungal interactions in vivo that occur in the soil and around the plant (36). This methodology may provide a way to monitor biocontrol activity (20) and the plant-Trichoderma interaction, thereby improving the selection of useful strains and the effectiveness of biopesticide and biofertilizer treatments.…”

The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms

“…Their study showed that the mycotoxin deoxynivalenol produced by Fusarium culmorum and Fusarium graminearum acts as a negative signal repressing the expression of the nag1 chitinase gene in Trichoderma atroviridae. Repression appeared to be specific for nag1 since no adverse effect was observed on the expression of ech42, another important chitinase gene in T. atroviridae (Lutz et al 2003).…”

“…Another example of pathogen-antagonist signalling was described for the interaction between mycotoxigenic Fusarium and mycoparasitic Trichoderma (Lutz et al 2003). Their study showed that the mycotoxin deoxynivalenol produced by Fusarium culmorum and Fusarium graminearum acts as a negative signal repressing the expression of the nag1 chitinase gene in Trichoderma atroviridae.…”

Potential Role of Pathogen Signaling in Multitrophic Plant-Microbe Interactions Involved in Disease Protection

“…Mycotoxins produced by Fusarium spp., including fusaric acid, typically have broad-spectrum antibiotic activity affecting bacteria, fungi, nematodes, insects, and mammals (39, 67), and their activity can be synergistic (13). An unexpectedly diverse range of Fusarium species have been found to produce fusaric acid and other mycotoxins in environments that require aggressive saprophytic competition with other organisms (i.e., grain [2] and crop residues [36]). The potential ecological importance of mycotoxins with respect to the saprophytic life cycles of producing fungi is largely unknown, although inhibition of bacteria and other microbial competitors or animal consumers of crop residues may enhance the saprophytic survival of plant-infectious mycotoxigenic Fusarium in crops.…”