The phytomicrobiome plays a crucial role in soil and ecosystem health, encompassing both beneficial members providing critical ecosystem goods and services and pathogens threatening food safety and security. The potential benefits of harnessing the power of the phytomicrobiome for plant disease suppression and management are indisputable and of interest in agriculture but also in forestry and landscaping. Indeed, plant diseases can be mitigated by in situ manipulations of resident microorganisms through agronomic practices (such as minimum tillage, crop rotation, cover cropping, organic mulching, etc.) as well as by applying microbial inoculants. However, numerous challenges, such as the lack of standardized methods for microbiome analysis and the difficulty in translating research findings into practical applications are at stake. Moreover, climate change is affecting the distribution, abundance, and virulence of many plant pathogens, while also altering the phytomicrobiome functioning, further compounding disease management strategies. Here, we will first review literature demonstrating how agricultural practices have been found effective in promoting soil health and enhancing disease suppressiveness and mitigation through a shift of the phytomicrobiome. Challenges and barriers to the identification and use of the phytomicrobiome for plant disease management will then be discussed before focusing on the potential impacts of climate change on the phytomicrobiome functioning and disease outcome.

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 interest.

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.

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.