Abstract
The rhizosphere microbial community of crop plants in intensively managed arable soils is strongly dominated by bacteria, especially in the initial stages of plant development. In order to establish more diverse and balanced rhizosphere microbiomes, as seen for wild plants, crop variety selection could be based on their ability to promote growth of saprotrophic fungi in the rhizosphere. We hypothesized that this can be achieved by increasing the exudation of phenolic acids, as generally higher fungal abundance is observed in environments with phenolic-rich inputs, such as exudates of older plants and litter leachates. To test this, a rhizosphere simulation microcosm was designed to establish gradual diffusion of root exudate metabolites from sterile sand into arable soil. With this system, we tested the fungus-stimulating effect of eight phenolic acids alone or in combination with primary root metabolites. Ergosterol-based fungal biomass measurements revealed that most phenolic acids did not increase fungal abundance in the arable soil layer. These results were supported by comparison of fungal biomass in the rhizosphere of wild type Arabidopsis thaliana plants and mutants with altered phenolic acid metabolism. Salicylic acid was the only phenolic acid that stimulated a higher fungal biomass in the arable soil layer of microcosms, but only when combined with a background of primary root metabolites. However, such effect on rhizosphere fungi was not confirmed for a salicylic acid-impaired A. thaliana mutant. For three phenolic acid treatments (chlorogenic acid, salicylic acid, vanillic acid) fungal and bacterial community compositions were analyzed using amplicon sequencing. Despite having little effect on fungal biomass, phenolic acids combined with primary metabolites promoted a higher relative abundance of soil-borne fungi with the ability to invade plant roots (Fusarium, Trichoderma and Fusicolla spp.) in the simulated rhizosphere. Bacterial community composition was also affected by these phenolic acids. Although this study indicates that phenolic acids do not increase fungal biomass in the rhizosphere, we highlight a potential role of phenolic acids as attractants for root-colonizing fungi.
Highlights
The rhizosphere, the soil volume surrounding plant roots, is a hotspot for microbial activity (Pausch and Kuzyakov, 2018), harboring saprotrophic fungi, alongside bacteria and mycorrhizal fungi (Buée et al, 2009; van der Putten et al, 2016; Hugoni et al, 2018)
The effect of phenolic acids was dependent on the presence of primary root exudate metabolites (PM)
Diffusion of primary root exudate metabolites had a strong positive effect of fungal biomass in the arable soil layer, but combination of primary metabolites with phenolic acids did not result in an additional increase, with exception of one phenolic acid, namely salicylic acid
Summary
The rhizosphere, the soil volume surrounding plant roots, is a hotspot for microbial activity (Pausch and Kuzyakov, 2018), harboring saprotrophic fungi, alongside bacteria and mycorrhizal fungi (Buée et al, 2009; van der Putten et al, 2016; Hugoni et al, 2018). Rhizosphere saprotrophic fungi can provide multiple services to the plant, such as promotion of plant growth and immunity (Koike et al, 2001; Kohler et al, 2007; Yadav et al, 2011; Naznin et al, 2014; Xia et al, 2019), as well as suppression of infection by soil-borne fungal pathogens. Managed arable soils usually harbor low saprotrophic fungal biomass (Djajakirana et al, 1996; de Vries and Bardgett, 2012), which is reflected in low activity of saprotrophic fungi in the rhizosphere of crop plant seedlings (Hünninghaus et al, 2019). Strategies that promote high saprotrophic fungal biomass and activity in the rhizosphere of crops could be important to enhance the sustainability of agricultural cultivation
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