MycotoxToBac - un projet Bordeaux Plant Sciences (2023)

Fusarium head blight (FHB) is a damaging disease of cereal crops worldwide caused by a complex of pathogenic Fusarium species (Bai and Shaner, 2004). This disease causes reductions not only in grain yield but also in grain quality due to the production of mycotoxins by the pathogen during the infection.

Since the early stages of infection by Fusarium and mostly few days after anthesis, several mycotoxins are inoculated in plant cells of spikelet tissues by the fungal hyphae, helping the spread and establishment of the pathogen within the host plant. These secondary metabolites are a known virulence factor, capable of inducing plant cells death, oxidative and nitrosative bursts and modulating responsive genes (Bai et al., 2002; Lanubile et al., 2022; Paciolla et al., 2004). Conversely, Righetti et al. (2021) suggested that residues of the mycotoxins deoxynivalenol (DON) and zearalenone (ZEN) absorbed by the wheat roots from soil can act as an alarm signal for the plant, which then triggers a “defence-on-demand response”. Although the mechanism is not yet well described, there is certainly a trade-off for the plant, between the beneficial effect of mycotoxins (i.e. defence priming) and a negative effect when these compounds are produced at higher concentrations by hyphae during infection. However, it is not yet known how the plant microbiota might influence this balance.

The plant microbiota (i.e. the whole assemblage of living microorganisms in the rhizosphere, on the leaf surface and in the endosphere) fulfils crucial functions related to host health, fitness, and productivity. These microbes have intimate interactions with the entire life of plants and serve important host functions that are mainly involved in plant nutrient uptake and enhancement of plant defence. Fusarium is in interaction with the bacteria of the wheat roots, rhizosphere, stem bases, leaves and heads during FHB disease cycle (Karlsson et al., 2021). Up to now, most studies looked at the potential use of beneficial microbial strains for biocontrol purposes, either by applying formulated products containing a strain that inhibits Fusarium (biocontrol agents) or by stimulating the indigenous beneficial microbes (conservation biocontrol). Those approaches consider the capacity of different bacterial strains to suppress Fusarium infection, such as those listed in Dutilloy et al. (2022), but the opposite relationship (the potential impact of Fusarium on wheat beneficial bacteria) is not known so far and need further investigations.

More precisely, nothing is known about the impact of mycotoxins on wheat microbiota at the species level and its contribution to the plant defence priming. Does the plant benefit from the presence of mycotoxins to stimulate its defence system or is the plant affected by the fact that its microbiota is altered by mycotoxins? Unfortunately, the studies about mycotoxin toxicity found in the literature mostly focused on animals, foods, humans and plants (Awuchi et al., 2021) despite the widespread distribution of these compounds in different compartments of the agroecosystem (cereals, corn, rice, water, manure, sewage sludge) as well as in freshwater (Juraschek et al., 2022) suggesting an exposure of other organisms such as bacteria. Only a few studies reported the toxicity of mycotoxins to other biological models in aquatic environments (Eagles et al., 2021; Hamill et al., 1969) but, to the best of our knowledge, nothing is known regarding the toxicity of mycotoxins to wheat (and to plants in general) beneficial bacteria. Finally, the fact that biostimulants are known to promote plant growth and can also modulate plant microbiota (Michl et al., 2023) raises a number of questions, and particularly: are plant beneficial bacteria sensitive to mycotoxins? Does mycotoxin toxicity to plant beneficial bacteria reverse the positive effect of biostimulants? In this context, the main objective of the project is to characterise the sensitivity of wheat-associated bacteria to mycotoxins produced by Fusarium. This will help identifying potential consequences for the plant fitness.

We expect, as main outcome, an exhaustive evaluation of the sensitivity of wheat beneficial bacteria to mycotoxins. The toxicity values obtained in our study will help building toxicity models for the plant microbiota and the expected consequences for the host. The results of our study will also help to further characterize the interactions between bacterial candidates (e.g. the most sensitive and tolerant strains to mycotoxins), the plant and Fusarium by using transcriptomics and/or metabolomics. We also see our study as the first step of the construction of a mycotoxin toxicity database that will contain all toxicity data for wheat-associated bacteria and that will be extended in fine to other plants. Finally, we are convinced that disentangling the role of mycotoxins in the interaction between Fusarium and the plant microbiome constitutes a knowledge gap that need particular attention to help defining novel biostimulant strategies.

MycotoxToBac is funded by Universtiy of Bordeaux, GPR Bordeaux Plant Sciences