Flooding Causes Dramatic Compositional Shifts and Depletion of Putative Beneficial Bacteria on the Spring Wheat Microbiota

Abstract

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 bacterial microbiota response to flooding is controlled by plant phenology in wheat (Triticum aestivum L.)

“…Decreases of N and P in leaves during flooding have been already reported in previous studies as a consequence of a diminished uptake of these macronutrients from the flooded soil by plant roots 73 – 76 . Such a trend was also observed in our experiment (see Francioli et al 57 ). Furthermore, under oxygen deprivation plant roots may suffer of energy deficits which can compromise ion transport processes, such as the ability to translocate ions from roots to the leaves 77 , 78 , which might explain the lower concentration of Ca and Mg detected in leaves of flooded wheat plants.…”

“…Flooding had a detrimental impact on spring wheat fitness as reflected by a significant (P < 0.05) decrease of above and belowground plant biomass, especially at tillering and booting 57 , confirming the negative effect of flooding and soil waterlogging on wheat growth 107 – 110 .…”

“…This latter result indicated an important interactive effect of PGS with plant and soil attributes, which in turn significantly affected bacterial microbiota assembly in the phyllosphere. Indeed, shifts in soil and plant nutrient concentrations across the different PGS in the control plants were observed 57 and db-RDA analysis revealed that root Na, leaf Na and total soil N were significant factors (P < 0.05) affecting leaf bacterial microbiota structure (Table 3 ). Plant traits, such as root and leaf nutrient concentrations, have been described as key factors in shaping the plant microbiota 102 – 104 , and their variations along plant phenology significantly influence bacterial community assembly 105 , 106 .…”

“…Flooding significantly reduced spring wheat performance as revealed by above- and belowground biomass changes, and it dramatically altered edaphic and root properties (see Francioli et al 57 . Flooding had also a severe effect on leaf traits, as the concentration of all the measured nutrients were strongly affected by this stressor, especially at tillering and booting stage (Fig.…”

“…The soil and root data have been already published in a previous study 57 . They were used here together with the new, i.e.…”