Divergent functioning of Proteaceae species: the South AmericanEmbothrium coccineumdisplays a combination of adaptive traits to survive in high‐phosphorus soils

Abstract

Summary1. Proteaceae species in south-western Australia thrive on phosphorus-impoverished soils, employing a phosphorus-mining strategy involving carboxylate-releasing cluster roots. Some develop symptoms of phosphorus toxicity at slightly elevated soil phosphorus concentrations, due to their low capacity to down-regulate phosphorus uptake. In contrast, Proteaceae species in Chile, e.g. Embothrium coccineum J.R. Forst. & G. Forst., occur on volcanic soils, which contain high levels of total phosphorus, but phosphorus availability is low. 2. We hypothesised that the functioning of cluster roots of E. coccineum differs from that of south-western Australian Proteaceae species, in accordance with the difference in soil phosphorus status. With more phosphorus to be gained from the soil with high levels of total phosphorus, we expect less investment in biomass and more release of carboxylates. Furthermore, we hypothesised that E. coccineum regulates its phosphorus-uptake capacity, avoiding phosphorus toxicity when grown at elevated phosphorus levels. To test these hypotheses, E. coccineum seedlings were grown at a range of phosphorus supplies in nutrient solution. 3. We show that E. coccineum allocated at least five times less biomass to cluster roots that released at least nine times more carboxylates per unit cluster root weight compared with south-western Australian species (e.g. Banksia, Hakea). The highest phosphorus supply caused a growth inhibition and high leaf phosphorus concentration, without symptoms of phosphorus toxicity. We accept our hypotheses on the functioning of cluster roots and the high capacity to reduce the net phosphorus uptake in plants grown at a high-phosphorus supply. 4. This novel combination of traits indicates divergent functioning of Proteaceae species from southern South America, exposed to frequent phosphorus input due to volcanic activity, in contrast with the functioning of south-western Australian Proteaceae species that thrive on severely phosphorus-impoverished soils. These traits could explain the functioning of E. coccineum on soils that are rich in total phosphorus, but with a low concentration of available phosphorus.

Plant adaptations to severely phosphorus-impoverished soils

“…Furthermore, reducing exudation rate has relatively little effect on P uptake over time in low-P soils, but in high-P soils reducing exudation rate has a much greater effect. This supports the assertion [13] that in high-P soils the most efficient strategy is to construct a relatively small number of cluster roots, maintain them for a relatively long time, and release exudates at relatively rapid rates, while in in low-P soils the most efficient strategy is to construct a relatively large number of cluster roots, maintain them for a relatively short time, and produce exudates at relatively slow rates.…”

“…With so many structures and species showing P-mobilising carboxylate releasing strategies, are there some that function better than others as dependent on soil conditions [13]? To address this question, we developed a simple theoretical model to predict how P uptake over time might vary with different rates of exudate release and in soils with varying levels of bound P. The model represents P uptake by the root, based on Michaelis-Menten kinetics; a constant rate of exudate production; diffusion of P and exudates through the soil volume; and displacement of bound P by exudates.…”

“…Sandy soils in south-western Australia, for example, contain little total P and plant-available P; a range of carboxylate-releasing P-mining strategies have evolved in different plant families in different parts of the world, including species that are used as crop plants for food or fibre production [64]. The specialised cluster-root structures in south-western Australia are short-lived and release relatively large amounts of carboxylates when compared with mycorrhizal species, but not as much as those in Proteaceae from southern South America which occur on young volcanic soils [13]. Such young volcanic soils contain much larger total amounts of P, but due to their low pH and strong P-sorption, the availability of soil P here is barely greater than that of the sandy soils in south-western Australia.…”

“…2) [10]; Hakea prostrata (Proteaceae) releases carboxylates (organic anions) in an exudative burst [11]. In southern South America, Proteaceae occur on young acidic soils with very high total P concentrations, but with a low P availability, due to strong sorption of P to oxides and hydroxides of iron and aluminium [12]; Embothrium coccineum releases predominantly citrate [13]. In tropical rainforests in north-eastern Australia, a mycorrhizal species without cluster roots, Placospermum coriaceum, occurs, together with non-mycorrhizal species with cluster roots [14].…”

Cluster roots of Embothrium coccineum (Proteaceae) affect enzyme activities and phosphorus lability in rhizosphere soil

“…Forst., 13 to 25 days after emergence (Delgado et al 2014)). In contrast, in juvenile or senescent cluster roots, the release of carboxylates is very slow.…”