The influence of mycorrhizal hyphal connections and neighbouring plants on Plantago lanceolata physiology and nutrient uptake

Abstract

Most plants extend their zone of interaction with surrounding soils and plants via mycorrhizal hyphae, which in some cases can form common mycorrhizal networks with hyphal continuity to other neighbouring plants. These interactions can impact plant health and ecosystem function, yet the role of these radial plants in mycorrhizal interactions and subsequent plant performance remains underexplored. Here we investigated the influence of hyphal exploration and interaction with neighbouring mycorrhizal plants, plants that are weakly mycorrhizal, and a lack of neighbouring plants on the performance of Plantago lanceolata, a mycotrophic perennial herb common to many European grasslands, using mesh cores and the manipulation of neighbouring plant communities. Allowing growth of hyphae beyond the mesh core increased carbon capture above-ground and release below-ground as root exudates and resulted in the greater accumulation of elements relevant to plant health in P. lanceolata. However, contrary to expectations, the presence of mycorrhizal, or weakly mycorrhizal neighbours as well as an absence of neighbours did not significantly alter the benefits of hyphal networks to P. lanceolata. Our findings demonstrate that enabling the development of a fungal network beyond the immediate host rhizosphere significantly influences plant leaf elemental stoichiometry, enhances plant carbon capture, and increases the amount of carbon they release via their roots as exudates. Our experimental design also provides a simple set of controls to prevent attributing positive mycorrhizal effects to neighbouring plant connections.

Keywords: Carbon; Common mycorrhizal network; Copper; Grassland; Magnesium; Net ecosystem exchange; Phosphorus; Photosynthesis; Sulphur; Zinc.

Fig. 1

A schematic of the experimental design in this study

Fig. 2

The impact of the experimental treatments on plant biomass. (A) The radial plant community and (B) the rotation of an in-growth core on dry leaf biomass as well as (C) their interaction on the dry root biomass of Plantago lanceolata. Boxplots show the range, median, and interquartile range of each treatment. Dots overlaid show individual data points. Significance between treatments is shown: *** < 0.001, ** < 0.01, and * < 0.05

Fig. 3

The impact of the experimental treatments on phosphorus accumulation. The effect of (A) the rotation of an in-growth core and (B) the radial plant community on phosphorus leaf content in Plantago lanceolata. Boxplots show the range, median, and interquartile range of each treatment. Dots overlaid show individual data points. Significance between main effect of rotation treatment is shown: *** < 0.001, ** < 0.01, and * < 0.05

Fig. 4

The impact of the experimental treatments on carbon exchange. The effect of the rotation of an in-growth core on (A) gross ecosystem exchange and (B) total carbon in root exudates of Plantago lanceolata. (C) The relationship between gross ecosystem exchange and (D) total dissolved carbon in root exudates with leaf biomass. Boxplots show the range, median, and interquartile range of each treatment. Dots overlaid show individual data points. Significance between treatments is shown: *** < 0.001, ** < 0.01, and * < 0.05

Fig. 5

The impact of the experimental treatment on fungal colonisation. The effect of the rotation of the in-growth core on the presence of (A) vesicles and (B) hyphae in the roots of Plantago lanceolata as well as (C) the impact of core rotation on the average hyphal length found in the soil within the core. Boxplots show the range, median, and interquartile range of each treatment. Dots overlaid show individual data points. Significance between treatments is shown: *** < 0.001, ** < 0.01, and * < 0.05