Temporal tracking of quantum-dot apatite across in vitro mycorrhizal networks shows how host demand can influence fungal nutrient transfer strategies

Abstract

Arbuscular mycorrhizal fungi function as conduits for underground nutrient transport. While the fungal partner is dependent on the plant host for its carbon (C) needs, the amount of nutrients that the fungus allocates to hosts can vary with context. Because fungal allocation patterns to hosts can change over time, they have historically been difficult to quantify accurately. We developed a technique to tag rock phosphorus (P) apatite with fluorescent quantum-dot (QD) nanoparticles of three different colors, allowing us to study nutrient transfer in an in vitro fungal network formed between two host roots of different ages and different P demands over a 3-week period. Using confocal microscopy and raster image correlation spectroscopy, we could distinguish between P transfer from the hyphae to the roots and P retention in the hyphae. By tracking QD-apatite from its point of origin, we found that the P demands of the younger root influenced both: (1) how the fungus distributed nutrients among different root hosts and (2) the storage patterns in the fungus itself. Our work highlights that fungal trade strategies are highly dynamic over time to local conditions, and stresses the need for precise measurements of symbiotic nutrient transfer across both space and time.

Mycorrhizal fungi control phosphorus value in trade symbiosis with host roots when exposed to abrupt ‘crashes’ and ‘booms’ of resource availability

“…While the exact apatite uptake mechanism for arbuscular mycorrhizal fungi is still unknown, fungi generally use endocytic pathways to take up large particles, with invaginating cells reaching diameters of 100 nm (Fischer‐Parton et al ., 2000; Read & Kalkman, 2003; Epp et al ., 2013; Lu et al ., 2016). The ability of the fungus to take up apatite was supported with bright‐field imaging videos of nutrient flows that showed vacuoles inside hyphae when the fungus was given access to QD‐tagged apatite and the absence of large vacuoles when QD‐tagged apatite is absent (van’t Padje et al ., 2020). Second, while no studies directly investigated whether R. irregularis can repress the ‘direct uptake’ pathway of P by D. carota roots, the fungus R. irregularis can repress direct P uptake in roots of Medicago truncatula (Watts‐Williams et al ., 2015) and there is evidence that colonisation by arbuscular mycorrhizal fungi can suppress the direct P uptake in several other roots (Smith et al ., 2004; Javot et al ., 2007; Grønlund et al ., 2013; Watts‐Williams et al ., 2015), such that highly colonised mycorrhizal roots are unlikely to rely solely on the direct uptake pathway.…”

“…Because arbuscular mycorrhizal fungi are obligate biotrophs, all C gained by the fungus to form and maintain fungal networks is derived from the host (Jiang et al ., 2017; Luginbuehl et al ., 2017). We used biomass as a proxy for host allocation (Olsson, 2002; Hammer et al ., 2011b; Fortuna et al ., 2012; Engelmoer et al ., 2014; Whiteside et al ., 2019; van’t Padje et al ., 2020). This approach did not take into account potential metabolic differences in the fungi among treatments.…”

“…Apatite is difficult for plant roots to dissolve directly, however arbuscular mycorrhizal fungi can help break down apatite (Reynolds et al ., 2006; Pel et al ., 2018). Past work has shown that arbuscular mycorrhizal fungi can increase the dissolution and uptake of apatite, even under sterile conditions when no other microbes are present (Reynolds et al ., 2006; Pel et al ., 2018; van’t Padje et al ., 2020). We constructed three colours of QD‐apatite (cyan (490 nm), yellow (576 nm) and red (666 nm)) that were equal in size and mass.…”

Common Mycorrhizae Network: A Review of the Theories and Mechanisms Behind Underground Interactions

“…The great majority of mycorrhizae fungi are not host specific, being that a single mycorrhizae fungi specie is able to colonize a wide range of plant species. Once a fungi colonize the host plant, its mycelium is able to grow over large distances in the soil and may reach and colonize the roots of multiple neighboring plants, from the same or different species (Van Der Heijden and Horton, 2009). Therefore, plants sharing the same host fungi are reported to become interconnected by the so-called common mycorrhiza network (CMN) (Heaton et al, 2012;Rhodes, 2017;Wipf et al, 2019).…”

“…In the review made by Van Der Heijden and Horton (2009) it is stated that CMN can be compared either to "socialist" or "capitalist" systems, or even to a "superorganism." For the "socialist" behavior, individuals are able to have equal opportunities and resources are distributed more evenly providing benefits for all connected plants.…”