Abstract
Arbuscular mycorrhizal fungi (AMF) are important symbionts for plant nutrient uptake, but their exact role in plant nitrogen (N) nutrition is unclear. Protists on the other hand play an acknowledged role in plant N acquisition, and there is increasing evidence for a close interaction with AMF. In a split root set up, we investigated the distinct roles of mycorrhiza (Rhizophagus irregularis), protists (Acanthamoeba castellanii), and their interaction on plant N uptake, within-root system allocation patterns, and shoot-to-root ratio of winter wheat. In addition, we applied a quantitative metabolomics approach to characterize associated changes in soil microbial communities by microbial phospholipid fatty acid (PLFA) analysis from rhizosphere soil. AMF markedly altered plant shoot-to-root allometry by reducing root biomass of wheat, and mycorrhiza partly took over root system functioning. Protists promoted shoot and root growth, and improved plant N uptake by the release of N from consumed bacterial biomass, a mechanism known as microbial loop. The shoot system however responded little to these alterations of the root system and of the rhizosphere community composition, indicating that the plants optimized shoot growth despite varying investment into roots. Mycorrhiza reduced root biomass and plant N, especially in the combined treatments with protists by changing within root system allocation of N and root biomass. These systemic effects on root allocation pattern suggest that mycorrhiza also gained control over N provided by protist grazers. Protists and mycorrhiza altered rhizosphere bacterial communities in contrasting but consistent ways as shown by quantitative shifts in microbial PLFA profiles. Remarkably, the changes in bacterial community composition were systemically conveyed within the root system to the split-root chamber where the symbionts were lacking. Accordingly the synergistic effects of protists and mycorrhiza indicated systemic effects on nutrient- and on root-allocation within root systems as an emergent property that could not be predicted from single treatments with mycorrhiza or protists alone. The tight plant and microbial feed backs uncovered in this study have far reaching implications for understanding the assembly of plant microbiomes, and testify central roles of both protists and mycorrhizas in the assembly process.
Highlights
Frameworks on shoot-to-root allometry of plants are based on models of competition between shoots and roots for plant carbohydrates and nutrients (Bloom et al, 1985; Van Noordwijk and De Willigen, 1987; Ericsson, 1995)
It seems that plants preferently invested in the shoot system even though root biomass and root nutrient levels were strongly reduced by mycorrhiza
Results of the present study provide compelling evidence for a tight functional coupling of the microbial loop and nutrient foraging by Arbuscular mycorrhizal fungi (AMF)
Summary
Frameworks on shoot-to-root allometry of plants are based on models of competition between shoots and roots for plant carbohydrates and nutrients (Bloom et al, 1985; Van Noordwijk and De Willigen, 1987; Ericsson, 1995). On the other hand an abundant literature exists on influence of soil microorganisms affecting the root architecture of plants. Arbuscular mycorrhizal fungi (AMF) are among the most important mutualists improving nutrient acquisition of plants (Smith and Read, 2008; Bonfante and Genre, 2010). This is well confirmed for plant phosphorus uptake AMF lack the enzymatic machinery for N mineralization E. and Smith, 2011) and rely on other microorganisms for the supply of mineral N (Herman et al, 2012; Koller et al, 2013a)
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