We found that G. irregulare blocked the accumulation of DAS in roots and tubers, while it did not affect DAS concentration in shoots of plants mycorrhized and infected with F. sambucinum. This could be explained by the requirement of physical proximity of G. irregulare and F. sambucinum. The habitat of AMF is limited in soil and the cortex of plant roots, and their mycelium never reaches the plant shoots. Although, G. irregulare induces PR homologues genes in potato shoots in response to infection by F. sambucinum (Ismail & Hijri, 2012), this defense gene induction is not sufficient to affect the production of DAS by the pathogen in the shoots.
In a previous study, using confrontation cultures in vitro, we demonstrated that G. irregulare inhibited F. sambucinum growth and modulated the expression of trichothecene biosynthetic genes (Ismail et al., 2011). Expression of TRI5, which controls the terpene cyclase that converts farnesyl diphosphate to trichodiene, was up-regulated, and expression of TRI4, which controls conversion of trichodiene to oxygenated trichothecene precursors, was down-regulated (Ismail et al., 2011). Although those results suggested that trichodiene or related compounds might accumulate in F. sambucinum / G. irregulare confrontation cultures, no DAS precursors were detected in this study.
We found that the G. irregulare caused a remarkable reduction in F. sambucinum DAS production, in vitro with confrontation cultures. In addition, G. irregulare stopped DAS production in plant roots, while there was only a partial inhibition of DAS production observed in tubers and no change in plant shoots. It has been documented in many reports that AMF can reduce the incidence and severity of root diseases and protect plants against soil-borne pathogens (Azcón-Aguilar & Barea, 1997; Bødker et al., 2002; Filion et al., 2003; Harrier & Watson, 2004; St-Arnaud & Vujanovic, 2007; Lioussanne et al., 2009; Ismail et al., 2011). Possible mechanisms by which AMF act as biological control agents are as follows: impact on soil microbial communities, antagonisms, and stimulation of plant defenses (Azcón-Aguilar & Barea, 1997; Bødker et al., 2002; Filion et al., 2003; Harrier & Watson, 2004; St-Arnaud & Vujanovic, 2007; Lioussanne et al., 2009; Ismail et al., 2011; Ismail & Hijri, 2012). For example, soil bacteria interact with AMF by forming a biofilm on the surface on the hyphae (Lecomte et al., 2011). In a recent study, Cruz & Ishii (2012) isolated three strains of endobacteria from spores of the AMF Gigaspora margarita using a hypodermic needle. These bacteria, identified as Bacillus sp., Bacillus thuringiensis, and Paenibacillus rhizosphaerae, were evaluated for their antagonistic effect on the soil-borne plant pathogens F. oxysporum f. sp. lactucae, Rosellinia necatrix, Rhizoctonia solani, and Pythium ultimum. Interestingly, all of the bacterial strains showed antagonism activities when confronted in vitro with the pathogens. The same authors have also shown that the isolated endobacteria can form aggregates, which resemble biofilm structures, on the surface of AMF hyphae (Cruz & Ishii, 2012). These observations along with those reported by Lecomte et al. (2011) support the hypothesis that the AMF impact the soil microbial communities, which could be a plausible mechanism for G. irregulare suppression of F. sambucinum growth and DAS production in potato. AMF have been shown to reduce the abundance of pathogenic fungi in plant roots by direct competition via interference competition and chemical interactions (Azcón-Aguilar & Barea, 1997; St-Arnaud & Vujanovic, 2007). In another example, AMF extract reduced the germination of Fusarium oxysporum f. sp. chrysanthemi conidia (Filion et al., 1999). Mycorrhization with G. irregulare strongly reduced disease severity on potato plants, which suggested that the biocontrol effect was due to stimulation of plant defense by inducing the expression of defense-related genes ChtA3, gluB, CEVI16, OSM-8e, and PR-1 (Ismail & Hijri, 2012). In the present study, we have documented a novel and important effect that AMF have on production of mycotoxins by the soil-borne pathogen F. sambucinum in roots and tubers of potato plants.