Flooding affects both above- and below-ground ecosystem processes, and it represents a substantial threat for crop and cereal productivity under climate change. Plant-associated microbiota play a crucial role in plant growth and fitness, but we still have a limited understanding of the response of the crop-microbiota complex under extreme weather events, such as flooding. Soil microbes are highly sensitive to abiotic disturbance, and shifts in microbial community composition, structure and functions are expected when soil conditions are altered due to flooding events (e.g., anoxia, pH alteration, changes in nutrient concentration). Here, we established a pot experiment to determine the effects of flooding stress on the spring wheat-microbiota complex. Since plant phenology could be an important factor in the response to hydrological stress, flooding was induced only once and at different plant growth stages (PGSs), such as tillering, booting and flowering. After each flooding event, we measured in the control and flooded pots several edaphic and plant properties and characterized the bacterial community associated to the rhizosphere and roots of wheat plant using a metabarcoding approach. In our study, flooding caused a significant reduction in plant development and we observed dramatic shifts in bacterial community composition at each PGS in which the hydrological stress was induced. However, a more pronounced disruption in community assembly was always shown in younger plants. Generally, flooding caused a (i) significant increase of bacterial taxa with anaerobic respiratory capabilities, such as members of Firmicutes and Desulfobacterota, (ii) a significant reduction in Actinobacteria and Proteobacteria, (iii) depletion of several putative plant-beneficial taxa, and (iv) increases of the abundance of potential detrimental bacteria. These significant differences in community composition between flooded and control samples were correlated with changes in soil conditions and plant properties caused by the hydrological stress, with pH and total N as the soil, and S, Na, Mn, and Ca concentrations as the root properties most influencing microbial assemblage in the wheat mircobiota under flooding stress. Collectively, our findings demonstrated the role of flooding on restructuring the spring wheat microbiota, and highlighted the detrimental effect of this hydrological stress on plant fitness and performance.

Leaf microbiota mediates foliar functional traits, influences plant fitness, and contributes to various ecosystem functions, including nutrient and water cycling. Plant phenology and harsh environmental conditions have been described as the main determinants of leaf microbiota assembly. How climate change may modulate the leaf microbiota is unresolved and thus, we have a limited understanding on how environmental stresses associated with climate change driven weather events affect composition and functions of the microbes inhabiting the phyllosphere. Thus, we conducted a pot experiment to determine the effects of flooding stress on the wheat leaf microbiota. Since plant phenology might be an important factor in the response to hydrological stress, flooding was induced at different plant growth stages (tillering, booting and flowering). Using a metabarcoding approach, we monitored the response of leaf bacteria to flooding, while key soil and plant traits were measured to correlate physiological plant and edaphic factor changes with shifts in the bacterial leaf microbiota assembly. In our study, plant growth stage represented the main driver in leaf microbiota composition, as early and late plants showed distinct bacterial communities. Overall, flooding had a differential effect on leaf microbiota dynamics depending at which developmental stage it was induced, as a more pronounced disruption in community assembly was observed in younger plants.

Extreme weather conditions lead to significant imbalances in crop productivity, which in turn affect food security. Flooding events cause serious problems to many crop species such as wheat. Although metabolic readjustments under flooding are important for plant regeneration, underlying processes remain poorly understood. Here, we investigated the systemic response of wheat to waterlogging using metabolomics and transcriptomics. A 12-day exposure to excess water triggered nutritional imbalances and disruption of metabolite synthesis and translocation, reflected by reduction of plant biomass and growth performance. Metabolic and transcriptomic profiling in roots, xylem, and leaves indicated anaerobic fermentation processes as a local response occurring in roots. Differentially expressed genes and ontological categories revealed that carbohydrate metabolism plays an important role as a systemic response. Analysis of the translocation rate of specific compounds in the xylem showed how waterlogging alters the composition of xylem exudates and thus the root to shoot communication. Interestingly, among all metabolites determined in our study, alanine was the most abundant transported in the xylem. Our results suggest an important role of this amino acid not only as amino-nitrogen source but also as the major root-to-shoot translocated and systemically acting metabolite crucial for balancing C/N between roots and shoots during waterlogging

Rainfall extremes are intensifying as a result of climate change, leading to increased flood risk. Flooding affects above- and belowground ecosystem processes, representing a substantial threat to crop productivity under climate change. Plant-associated fungi play important roles in plant performance, but their response to abnormal rain events is unresolved. Here, we established a glasshouse experiment to determine the effects of flooding stress on the spring wheat-mycobiota complex. Since plant phenology could be an important factor in the response to hydrological stress, flooding was induced only once and at different plant growth stages, such as tillering, booting and flowering. We assessed the wheat mycobiota response to flooding in three soil-plant compartments (phyllosphere, roots and rhizosphere) using metabarcoding. Key soil and plant traits were measured to correlate physiological plant and edaphic changes with shifts in mycobiota structure and functional guilds. Flooding reduced plant fitness, and caused dramatic shifts in mycobiota assembly across the entire plant. Notably, we observed a functional transition consisting of a decline in mutualist abundance and richness with a concomitant increase in plant pathogens. Indeed, fungal pathogens associated with important cereal diseases, such as Gibberella intricans, Mycosphaerella graminicola, Typhula incarnata and Olpidium brassicae significantly increased their abundance under flooding. Overall, our study demonstrate the detrimental effect of flooding on the wheat mycobiota complex, highlighting the urgent need to understand how climate change-associated abiotic stressors alter plant-microbe interactions in cereal crops.