Plasticity in root symbioses following shifts in soil nutrient availability during long‐term ecosystem development

Abstract

The vast majority of terrestrial plants form root symbioses with arbuscular mycorrhizal (AM) fungi to enhance nutrient (particularly phosphorus, P) acquisition. However, some plant species also form dual symbioses involving ectomycorrhizal (ECM) fungi, with a subset of those also forming triple symbioses also involving dinitrogen (N2)‐fixing bacteria. It has been suggested that these plants show plasticity in root symbioses to optimise nutrient acquisition depending on the type and strength of soil nutrient limitation (e.g., N vs. P), yet empirical evidence remains limited. Alternatively, the degree of investment or “preference” in particular root symbioses might simply reflect differences in inoculum potential among soils of contrasting nutrient availability, reflecting adaptations of root symbionts to different edaphic conditions. Here, we grew two co‐occurring plant species forming triple (AM/ECM/N2‐fixing; Acacia rostellifera) or dual (AM/ECM; Melaleuca systena) symbioses in soils of increasing age and contrasting nutrient availability from an Australian long‐term soil chronosequence to disentangle the relative importance of abiotic factors (e.g., soil nutrient availability and stoichiometry) and biotic factors (e.g., soil inoculum potential) in determining root colonisation patterns and functional outcomes of these multiple root symbioses. For both plant species, we found clear hump‐shaped plant growth patterns along the pedogenesis‐driven gradient in soil nutrient availability, with peak growth in intermediate‐aged soils, while high levels of mycorrhizal colonisation by the “preferred” root symbionts were maintained across all soils. We found large increases (540%) in foliar manganese concentrations with increasing soil age and declining P availability, suggesting that plants may be relying on the release of carboxylates to help acquire P in the most P‐impoverished soils. Finally, we found that soil abiotic properties, such as strong differences in soil nutrient availability, are generally more important than soil inoculum potential in explaining these shifts in our plant and root responses. Synthesis. Our study suggests that plants capable of forming multiple root symbioses show plasticity in their nutrient‐acquisition strategies following shifts in soil nutrients during long‐term ecosystem development, yet maintain a preference for certain root symbionts despite changes in soil microbial inoculum.

Dual‐mycorrhizal plants: their ecology and relevance

“…). The study of Teste & Laliberté (), which used the full range of soil ages, including the oldest most impoverished sands, did not find such strong evidence for mycorrhizal switching. Indeed, M. systena simply remained mostly EM along the strong nutrient‐availability gradient, whereas A. rostillefera showed higher variation but a tendency to form mostly arbuscular mycorrhizas when natural levels of AM and EM inoculum were used.…”

“…(), Salomón et al . (), and Teste & Laliberté (). ^ Eucalyptus camaldulensis , Eucalyptus citriodora , Eucalyptus cloeziana , Eucalyptus grandis , Eucalyptus urophylla .…”

“…^ Eucalyptus camaldulensis , Eucalyptus citriodora , Eucalyptus cloeziana , Eucalyptus grandis , Eucalyptus urophylla . Soil inoculum origin from Teste & Laliberté () refers to treatments where plants were grown directly in unaltered field soil, or an average mix of all soil‐age‐specific inoculum, or a soil‐age ‐specific soil inoculum (see section VI.5 and Teste & Laliberté () for more detail). Colonization values in most studies presented here were based on a per root length basis.…”

“…c . 1000‐yr‐old soil), along this soil chronosequence (Teste & Laliberté, ). The switch to EM dominance in Acacia when grown in soil age‐specific inoculum demonstrates how other factors are at play; in this case, EM propagule density and locally adapted mycorrhizal fungi can interact and influence whether arbuscular mycorrhizas or ectomycorrhizas are formed.…”

Ecological succession in a changing world

“…Furthermore, some of these plant species associate with nitrogen‐fixing bacteria, forming a triple symbiosis. In this issue, Teste and Laliberté () examined the symbiotic associations of two dual‐infected species, one of which also associates with nitrogen‐fixing bacteria, across a long‐term chronosequence of coastal dunes in Western Australia. They found plasticity in symbiotic associations during long‐term ecosystem development, although the “favoured” symbiont predominated on both young and old soils despite marked variation in soil fertility.…”