Wheat mycobiome dynamics driven by interseasonal crop-crop transfer and Fusarium head blight.

Introduction: Fusarium head blight (FHB) is a devastating disease of wheat that causes mycotoxin contamination in grains. Diseases like FHB have traditionally been managed with integrated strategies; but this has led to a proliferation of fungicide-resistant pathogens and soil erosion while full disease control has remained elusive. Leveraging the microbiome for more sustainable management is an alternative, however, translation of promising strategies is hampered by our limited understanding of crop microbiome differences across plant development and tissue types. Methods: We characterized fungal communities using amplicon sequencing across five developmental timepoints in wheat leaves and wheat heads, as well as in maize debris from the previous growing season. Samples were collected from two locations in Illinois, USA. We assessed how tissue type, site, developmental stage, and wheat variety contributed to mycobiome composition. Source-sink relationships among debris, leaves, and heads were evaluated, and taxa associated with high and low FHB conditions were identified. Network analyses were used to determine the roles of key fungal taxa in wheat head and maize debris microbiomes. Results: Mycobiome composition varied strongly by tissue type, though site and developmental timepoint were also important contributors. Host variety conditionally explained mycobiome variation in wheat heads, but not in leaves or debris. We also identified debris as a major fungal source to leaves early in development, but not later-and found that leaves were never a large inoculum source to head mycobiomes at either developmental stage tested. Taxa enriched under high FHB conditions in wheat heads belonged to the Ascomycota ( Discussion: This work shows that fungal movement from crop to crop across seasons, and between plant tissues within a season, shape phyllosphere microbiome dynamics and can indicate potential disease outcomes in the FHB pathosystem. As microbiome-based disease management develops alongside rapid growth in the biologicals industry and increased recognition of microbial roles in agriculture, this work highlights several promising directions. These include identifying basidiomycetous yeasts associated with low FHB, pinpointing taxa correlated with Fusarium in wheat heads and maize debris, and demonstrating that applying biocontrols to wheat leaves is unlikely to affect pathogen spread to heads. Future research should focus on controlled tests of microbe-microbe interactions and their impacts on plant immunity, disease suppression, and yield.