Fusarium graminearum is the causal agent of Gibberella ear rot and produces trichothecene mycotoxins. Basic questions remain unanswered regarding the kernel stages associated with trichothecene biosynthesis and the kernel metabolites potentially involved in the regulation of trichothecene production in planta. In a two-year field study, F. graminearum growth, trichothecene accumulation, and phenolic acid composition were monitored in developing maize kernels of a susceptible and a moderately resistant variety using quantitative polymerase chain reaction and liquid chromatography coupled with photodiode array or mass spectrometry detection. Infection started as early as the blister stage and proceeded slowly until the dough stage. Then, a peak of trichothecene accumulation occurred and infection progressed exponentially until the final harvest time. Both F. graminearum growth and trichothecene production were drastically reduced in the moderately resistant variety. We found that chlorogenic acid is more abundant in the moderately resistant variety, with levels spiking in the earliest kernel stages induced by Fusarium infection. This is the first report that precisely describes the kernel stage associated with the initiation of trichothecene production and provides in planta evidence that chlorogenic acid may play a role in maize resistance to Gibberella ear rot and trichothecene accumulation.
The potential involvement of antioxidants (α-tocopherol, lutein, zeaxanthin, β-carotene, and ferulic acid) in the resistance of maize varieties to Fusarium ear rot was the focus of this study. These antioxidants were present in all maize kernel stages, indicating that the fumonisin-producing fungi (mainly Fusarium verticillioides and Fusarium proliferatum ) are likely to face them during ear colonization. The effect of these compounds on fumonisin biosynthesis was studied in F. verticillioides liquid cultures. In carotenoid-treated cultures, no inhibitory effect of fumonisin accumulation was observed while a potent inhibitory activity was obtained for sublethal doses of α-tocopherol (0.1 mM) and ferulic acid (1 mM). Using a set of genotypes with moderate to high susceptibility to Fusarium ear rot, ferulic acid was significantly lower in immature kernels of the very susceptible group. Such a relation was nonexistent for tocopherols and carotenoids. Also, ferulic acid in immature kernels ranged from 3 to 8.5 mg/g, i.e., at levels consistent with the in vitro inhibitory concentration. Overall, our data support the fact that ferulic acid may contribute to resistance to Fusarium ear rot and/or fumonisin accumulation.
Fumonisins are mycotoxins mainly produced by two Fusarium species: F. verticillioides and F. proliferatum. These toxins are of great concern due to their widespread contamination in maize and their adverse effects on animal and human health. In the past decade, progress was made in identifying the genes required for fumonisin biosynthesis. Additionally, molecular mechanisms involved in the regulation of fumonisin production have been very recently elucidated. By covering the latest advances concerning the factors modulating fumonisin production, this review aims at presenting an integrated approach of the overall mechanisms involved in the regulation of fumonisin biosynthesis during maize kernel colonization.
The fungal pathogen Fusarium verticillioides infects maize ears and produces fumonisins, known for their adverse effects on human and animal health. Basic questions remain unanswered regarding the kernel stage(s) associated with fumonisin biosynthesis and the kernel components involved in fumonisin regulation during F. verticillioides-maize interaction under field conditions. In this 2-year field study, the time course of F. verticillioides growth and fumonisin accumulation in developing maize kernels, along with the variations in kernel pH and amylopectin content, were monitored using relevant and accurate analytical tools. In all experiments, the most significant increase in fumonisin accumulation or in fumonisin productivity (i.e., fumonisin production per unit of fungus) was shown to occur within a very short period of time, between 22/32 and 42 days after inoculation and corresponding to the dent stage. This stage was also characterized by acidification in the kernel pH and a maximum level of amylopectin content. Our data clearly support published results based on in vitro experiments suggesting that the physiological stages of the maize kernel play a major role in regulating fumonisin production. Here we have validated this result for in planta and field conditions, and we demonstrate that under such conditions the dent stage is the most conducive for fumonisin accumulation.
Fusarium Head Blight (FHB) is one of the most devastating diseases of cereals worldwide, threatening both crop production by affecting cereal grain development, and human and animal health by contaminating grains with mycotoxins. Despite that maize residues constitute the primary source of inoculum for Fusarium pathogenic species, the structure and diversity of Fusarium spp. and microbial communities in maize residues have received much less attention than in grains. In this study, a metabarcoding approach was used to study the bacterial, fungal and Fusarium communities encountered in maize stalks collected from 8 fields in Brittany, France, after maize harvest during fall 2015. Some predominant genera found in maize residues were cereal or maize pathogens, such as the fungal Fusarium , Acremonium , and Phoma genera, and the bacterial Pseudomonas and Erwinia genera. Furthermore, a high predominance of genera with previously reported biocontrol activity was found, including the bacterial Sphingomonas , Pedobacter , Flavobacterium, Pseudomonas , and Janthinobacterium genera; and the fungal Epicoccum , Articulospora , Exophiala , and Sarocladium genera. Among Fusarium spp., F. graminearum and F. avenaceum were dominant. We also found that the maize cultivar and previous crop could influence the structure of microbial communities. Using SparCC co-occurrence network analysis, significant negative correlations were obtained between Fusarium spp. responsible for FHB (including F. graminearum and F. avenaceum ) and bacterial OTUs classified as Sphingomonas and fungal OTUs classified as Sarocladium and Epicoccum . Considering that isolates belonging to these taxa have already been associated with antagonist effect against different Fusarium spp. and/or other pathogenic microorganisms and due to their predominance and negative associations with Fusarium spp., they may be good candidates as biocontrol agents. Combining the use of Fusarium -specific primers with universal primers for bacteria and fungi allowed us to study the microbial communities, but also to track correlations between Fusarium spp. and other bacterial and fungal genera, using co-occurrence network analysis. Such approach could be a useful tool as part of a screening strategy for novel antagonist candidates against toxigenic Fusarium spp., allowing the selection of taxa of i...
Fungal interactions of Fusarium verticillioides and F. graminearum in maize ears and the impact on fungal development and toxin accumulation were investigated in a 2-year field study at two locations in France. Maize ears were inoculated either with a spore mixture of F. graminearum and F. verticillioides or using a sequential inoculation procedure consisting of a first inoculation with F. graminearum followed by a second with F. verticillioides 1 week later. Toxin and fungal biomass were assessed on mature kernels, using HPLC and quantitative PCR. Correlation between the levels of DNA and toxin was high concerning F. graminearum DNA and deoxynivalenol (R 2 = 0AE73) and moderate for F. verticillioides DNA and fumonisin (R 2 = 0AE44). Fusarium graminearum DNA either decreased in mixed inoculations or was not influenced by subsequent inoculations with F. verticillioides, compared to single inoculations. In contrast, F. verticillioides DNA either significantly increased or was not affected in mixed and sequential inoculations. In two of the replicates, it can be assumed that natural contamination by F. verticillioides was favoured by previous contamination with F. graminearum. Overall, the results suggest that F. verticillioides has competitive advantages over the F. graminearum strains. Additionally, the data provide, for the first time, key evidence that previous contamination by F. graminearum in maize ears can facilitate subsequent infections by F. verticillioides.
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