Effect of mycotoxin production on interactions between Fusarium species during maize infection and on the production of volatile metabolites

Maize (Zea mays L.) is an important cereal crop which provides staple food for humans and livestock. Maize cultivation is threatened by numerous microbial diseases under field conditions. Fungal pathogens belonging to genus Fusarium can infect roots, stalks and ears during growing season causing what so-called fusarioses. Fusarium diseases cause a huge reduction in the yield besides plant material contamination with mycotoxins (fungal metabolites which are toxic to vertebrates). In nature, maize plants are commonly infected by more than one pathogenic Fusarium species. F. graminearum Schwabe [teleomorph = Gibberella zea (Schwein) Petch] and F. verticilloides (Saccardo) Nirenberg [synonym = F.moniliforme J. Scheldon, teleomorph = G. moniliformis Wineland] are major causal agents of Gibberella ear rot and Fusarium ear rot on maize, respectively. The interaction between F. graminearum and F. verticilliodes on maize ears has been reported, however the role of mycotoxins in this interaction is questionable. The main goal of this work was to elucidate the pathological and ecological functions of major Fusarium mycotoxins, which might serve as virulence factor during disease development or might be involved in the competitive interactions among fungal species. These hypothetical functions were studied throughout fungal interaction course on live maize ears (in vivo) or on Petri dishes (in vitro) using wildtype fungal strains belong to F. graminearum (produces trichothecenes; nivalenol, deoxynivalenol) and F. verticillioides (produces fumonisins) and their mutant strains impaired in synthesis of nivalenol, deoxynivalenol and fumonisins. Maize ears were either infected with a single Fusarium species or co-infected with two species (concurrently and sequentially) under controlled greenhouse conditions. Disease severity, fungal biomass and mycotoxins accumulation were monitored on infected ears. Among all fungal strains “wildtypes and mutants” that were compared in single inoculation experiment, the strains belong to F. verticillioides and F. graminearum nivalenol chemotype were less aggressive than strains belong to F. graminearum deoxynivalenol chemotype. Moreover, nivalenol non-producing mutant strain of F. graminearum caused fewer symptoms than the nivalenol-producing strain, though the biomass of the strains in infected kernels was unaffected. Regardless of the ability of F. graminearum to produce nivalenol or deoxynivalenol and F. verticillioides to produce fumonisins, the results indicated that growth of F. verticillioides was stimulated by co-infection with F. graminearum. The growth of F. graminearum deoxynivalenol-producing strain and its mutant was suppressed in co-inoculation with F. verticillioides regardless of the ability of the latter to produce fumonisins. Similarly, disease symptoms caused by deoxynivalenol-producing strain of F. graminearum and its mutant were reduced in mixed inoculation with F. verticillioides regardless of the ability of F. verticillioides to produce fumonisins. The results demonstrated that fumonisins and trichothecenes were not involved in fungal competition between F. graminearum and F. verticillioides on maize ears. Dual cultures of F. verticillioides and F. graminearum on synthetic medium did not show inhibition zones between both Fusarium species regardless the ability of fungal strains to produce mycotoxins. However, F. graminearum occupied more space and grew faster in dual cultures than F. verticillioides. Furthermore, to understand how competitive interactions between both fungal species F. graminearum and F. verticillioides influence plant volatile blends of infected maize ears, solid phase microextraction-GC/MS was used for the detection of volatile organic compounds (VOCs) emitted by infected (single or mixed fungal infection) and uninfected maize ears. Multivariate analysis (PCA) was used to compare complex volatile profiles from infected and non-infected maize ears. The results showed that volatile profiles in mixed infections were modulated by the most competitive fungal strain. Moreover, volatile profiles reflected disease severity by either single or mixed fungal infections. The data also reported volatile biomarkers of maize ear rot disease caused by Fusarium species that were mainly composed of sesquiterpenoids and other compounds, highlighting their potential in precision agriculture and disease monitoring.