Abstract
Deciphering the mechanisms involved in the biocontrol of mycotoxinogenic fungi of cereals.Cereals are the first factor of consumer exposure to mycotoxins, toxic secondary metabolites synthesized by particular moulds and which present a risk for human and animal health. The species Fusarium graminearum and Fusarium verticillioides are thus responsible for the production of trichothecenes and fumonisin-like mycotoxins, respectively, with a high impact especially in pre-harvest. With the decrease of pesticide use due to their toxicity, an alternative strategy to control these fungal diseases in the field may be the use of antagonistic microorganisms. Non-pathogenic, these biocontrol agents (BCAs) are able to limit the progression of Fusaria and their synthesis of mycotoxins through various biological mechanisms, however still poorly understood. In this context, the objectives of this study are to evaluate by which mechanisms three selected BCAs (Streptomyces griseoviridis, Trichoderma asperellum, Pythium oligandrum) can modulate the growth and mycotoxin production of Fusarium pathogens, in vitro and in situ. Antagonistic activities and varying levels of inhibition of growth (up to 80%) and mycotoxinogenesis (up to 90%) have been observed in vitro depending on BCAs, pathogens or culture conditions. The hypotheses are then verified and completed thanks to the development of a toolbox of tests specific to certain modes of action. Their chronology is evaluated throughout the interaction, from pathogenic spore germination to the formation of perithecia, by testing a wide variety of BCA mechanisms: synthesis of anti-germinative compounds, mycophagy, chitinolytic enzyme synthesis, emission of volatile antifungal compounds, inhibition of mycotoxin biosynthesis pathways, mycotoxin bio-transformation, spatial and nutritional competition or impact on pathogen conservation. S. griseoviridis presents nutritional competition capacities, but its main strategy is based on antibiosis, through the synthesis of numerous antifungal compounds that offsets a significant deficit in spatial colonization capacity. However, it can stimulate the mycotoxin production. T. asperellum is capable of activating a very wide range of defenses and attacks combining the synthesis of various antifungal compounds (metabolite, enzymes, VOCs), with different targets (spores, mycelium, mycotoxins), and a direct action by mycoparasitism. The efficacy of P. oligandrum is mainly due to its strong capacity to colonize the environment, with a direct action via microbial predation and reduction of perithecia formation. These in vitro performances could also be analyzed in F. graminearum in situ throughout its life cycle (from colonization of ears to survival in culture residues), and put into perspective with the different modes of action identified in each of the BCAs. The whole project has led to important advances in deciphering the mechanisms of action of BCAs and proposes ways of improvement to optimize the use and efficacy of these antagonists. Thus limit the use of chemical plant protection products, while maintaining a healthy production with low levels of mycotoxins.