How belowground interactions contribute to the coexistence of mycorrhizal and non-mycorrhizal species in severely phosphorus-impoverished hyperdiverse ecosystems

Abstract

Background Mycorrhizal strategies are very effective in enhancing plant acquisition of poorly-mobile nutrients, particularly phosphorus (P) from infertile soil. However, on very old and severely P-impoverished soils, a carboxylate-releasing and P-mobilising cluster-root strategy is more effective at acquiring this growthlimiting resource. Carboxylates are released during a period of only a few days from ephemeral cluster roots. Despite the cluster-root strategy being superior for P acquisition in such environments, these species coexist with a wide range of mycorrhizal species, raising questions about the mechanisms contributing to their coexistence. Scope We surmise that the coexistence of mycorrhizal and non-mycorrhizal strategies is primarily accounted for by a combination of belowground mechanisms, namely (i) facilitation of P acquisition by mycorrhizal plants from neighbouring cluster-rooted plants, and (ii) interactions between roots, pathogens and mycorrhizal fungi, which enhance the plants' defence against pathogens. Facilitation of nutrient acquisition by clusterrooted plants involves carboxylate exudation, making more P available for both themselves and their mycorrhizal neighbours. Belowground nutrient exchanges between carboxylate-exuding plants and mycorrhizal N 2 -fixing plants appear likely, but require further experimental testing to determine their nutritional and ecological relevance. Anatomical studies of roots of clusterrooted Proteaceae species show that they do not form a complete suberised exodermis. Conclusions The absence of an exodermis may well be important to rapidly release carboxylates, but likely lowers root structural defences against pathogens, Plant Soil (2018) particularly oomycetes. Conversely, roots of mycorrhizal plants may not be as effective at acquiring P when P availability is very low, but they are better defended against pathogens, and this superior defence likely involves mycorrhizal fungi. Taken together, we are beginning to understand how an exceptionally large number of plant species and P-acquisition strategies coexist on the most severely P-impoverished soils.

Biotic and abiotic plant–soil feedback depends on nitrogen‐acquisition strategy and shifts during long‐term ecosystem development

“…The absence of negative biotic PSF in non‐N‐fixing plants from the old, severely P‐impoverished dune system might be due to the strong impact of soil biota on plant growth in these soils (Figures , and ). For example, the negative effect of soil biota on the growth of two (out of three) non‐N‐fixing species examined in the old dune system (Figure ) might be explained by many plant species in these P‐impoverished soils having root traits that enhance P acquisition (e.g., high specific root length, high root hair density) which trade‐off against pathogen defence (Laliberté et al, ; Lambers et al, ; Newsham et al, ). This might increase plant susceptibility to a broad range of non‐host‐specific soil‐borne pathogens which could outweigh the potential negative effects of host‐specific pathogens.…”

“…We hypothesised that: (H1) Abiotic PSF is more important in young, N‐poor soils than in old, severely P‐impoverished soils, because N‐fixing plants increase soil N availability (via N fixation) in young soils, while biotic PSF is predominant in old soils. Biotic PSF is likely important in old soils due to many plants possessing root traits that enhance P acquisition at the expense of defence against soil‐borne pathogens, and root traits enabling mutualistic associations with soil microbes that assist with nutrient acquisition and/or pathogen defence (Laliberté et al, ; Lambers et al, ). (H2) The magnitude and direction of PSF in young soils differ between N‐fixing and non‐N‐fixing plants. Specifically, we expected that non‐N‐fixing plants would grow better in soils conditioned by N‐fixing plants (through having higher N availability) than in soils conditioned by non‐N‐fixing plants, while growth of N‐fixing plants would be less in soils from non‐N‐fixing plants and would be unresponsive to soils from heterospecific N‐fixing plants relative to conspecifics. (H3) Shifts in PSF for both N‐fixing and non‐N‐fixing plants depend on soil age.…”

Phosphorus‐ and nitrogen‐acquisition strategies in two Bossiaea species (Fabaceae) along retrogressive soil chronosequences in south‐western Australia

“…In fact, colonisation was constant along the chronosequences for both species. At the oldest stages, the costs of maintaining a mycorrhizal symbiosis are expected to be greater than the nutritional benefits (Lambers et al , Raven et al ). However, at extremely low soil [P], where B. eriocarpa occurs, mycorrhizal fungi might have a different role.…”

“…However, at extremely low soil [P], where B. eriocarpa occurs, mycorrhizal fungi might have a different role. Rather than increase the uptake of P, the fungi may provide protection against soil pathogens (Laliberté et al , Albornoz et al , Lambers et al ). Because, the total soil [P] at the youngest stages of the Warren chronosequence is much lower than that at the youngest stages at Jurien Bay (Turner et al ), it is likely that the role of mycorrhizal fungi in pathogen defence dominates much earlier during pedogenesis.…”

Trait convergence in photosynthetic nutrient‐use efficiency along a 2‐million year dune chronosequence in a global biodiversity hotspot

“…We focused on both leaf photosynthesis and respiration of a range of species, beyond Proteaceae, across a chronosequence in a biodiversity hotspot (Lambers, ; Myers, Mittermeier, Mittermeier, Fonseca, & Kent, ). Thus, we significantly expanded our work with a component not yet studied along the Jurien Bay chronosequence (Albornoz, Burgess, Lambers, Etchells, & Laliberté, ; Hayes et al, ; Laliberté et al, ; Laliberté, Turner et al, ; Lambers et al, ; Li, Zhang, Han, Lambers, & Finnegan, ; Png et al, ; Teste et al, ; Turner, Laliberté, & Hayes, ; Zemunik et al, , ). We focused on traits that affect leaf carbon uptake and release, and related these to leaf [N] and [P].…”