Mycorrhiza governs plant-plant interactions through preferential allocation of shared nutritional resources: A triple (13C, 15N and 33P) labeling study

Abstract

Plant-plant interactions and coexistence can be directly mediated by symbiotic arbuscular mycorrhizal (AM) fungi through asymmetric resource exchange between the plant and fungal partners. However, little is known about the effects of AM fungal presence on resource allocation in mixed plant stands. Here, we examined how phosphorus (P), nitrogen (N) and carbon (C) resources were distributed between coexisting con- and heterospecific plant individuals in the presence or absence of AM fungus, using radio- and stable isotopes. Congeneric plant species, Panicum bisulcatum and P. maximum, inoculated or not with Rhizophagus irregularis, were grown in two different culture systems, mono- and mixed-species stands. Pots were subjected to different shading regimes to manipulate C sink-source strengths. In monocultures, P. maximum gained more mycorrhizal phosphorus uptake benefits than P.bisulcatum. However, in the mixed culture, the AM fungus appeared to preferentially transfer nutrients (33P and 15N) to P.bisulcatum compared to P. maximum. Further, we observed higher 13C allocation to mycorrhiza by P.bisulcatum in mixed- compared to the mono-systems, which likely contributed to improved competitiveness in the mixed cultures of P.bisulcatum vs. P. maximum regardless of the shading regime. Our results suggest that the presence of mycorrhiza influenced competitiveness of the two Panicum species in mixed stands in favor of those with high quality partner, P. bisulcatum, which provided more C to the mycorrhizal networks. However, in mono-species systems where the AM fungus had no partner choice, even the lower quality partner (i.e., P.maximum) could also have benefitted from the symbiosis. Future research should separate the various contributors (roots vs. common mycorrhizal network) and mechanisms of resource exchange in such a multifaceted interaction.

Carbon and phosphorus exchange rates in arbuscular mycorrhizas depend on environmental context and differ among co‐occurring plants

“…Resource exchange also varies greatly among plant and fungal species. For example, co‐occurring plants differ in the amount of C they allocate to AMF (Walder et al ., 2012; Grman & Robinson, 2013; Faghihinia & Jansa, 2022), which in turn may affect how much P they obtain from AMF (Lekberg et al ., 2010; Kiers et al ., 2011; Fellbaum et al ., 2014). This could help explain some of the documented differences in AM dependency, that is the growth and fitness responses by plants to AMF, which sometimes differ broadly among functional groups (Wilson & Hartnett, 1998).…”

The Invasive Plant Impatiens glandulifera Manipulates Microbial Associates of Competing Native Species

“…The formation of a CMN is thought to be an important aspect of plant invasion and the resulting loss of native plant diversity [ 20 ]. Nutrient transfer can occur through the network to the invader [ 39 ], though the fungi do show preferential effects; for example, nitrogen (N) is most likely to be transferred to hosts that offer the most carbon in return [ 40 , 41 ]. This likely explains why the outcome of an invasive plant entering a CMN can be positive or negative, determined by the diversity of soil resources and the relative nutrient demands and carbon provision of the fungi and the plants involved [ 42 ].…”

Nutrient-dependent cross-kingdom interactions in the hyphosphere of an arbuscular mycorrhizal fungus

“…In return, AM fungi provide a wide range of benefits to the plant, including enhanced uptake of mineral nutrients such as phosphorus (P), nitrogen (N) and micronutrients (e.g., Zn and Cu) from soil to plant, by capitalizing on extensive extraradical (external) hyphal networks to explore a larger volume of soil than would be accessible to the roots ( van der Heijden et al, 2008 ; Gao et al, 2021 ; Hui et al, 2022 ), facilitating water flow between soil and plant ( Kikuchi et al, 2016 ; Delavaux et al, 2017 ; Püschel et al, 2021 ), and increasing resistance to various biotic (e.g., pathogens, grazing) and abiotic (e.g., salinity, drought, heavy metals) stresses ( Smith and Smith, 2011 ; Faghihinia et al, 2020 ; Gao et al, 2020 ; Zai et al, 2021 ). AM fungi can also make connections with neighboring plants, redistributing the resources, benefits and costs, and thus stabilizing plant communities ( Selosse et al, 2006 ; Jakobsen and Hammer, 2015 ; Faghihinia and Jansa, 2023 ), which may eventually increase plant community yield ( Li et al, 2022 ).…”