Ecophysiological properties of a cluster root-forming plant, Helicia cochinchinensis (Proteaceae) grown on Miyajima Island, Japan

Aims The family Proteaceae is one of the dominant families in nutrient-impoverished habitats in the Southern hemisphere, and less common in the Northern hemisphere. Helicia cochinchinensis Lour. is the only Proteaceae species in Japan. This study aimed to unveil the ecophysiological properties of H. cochinchinensis grown on Miyajima Island, Hiroshima, Japan.Methods Phosphorus (P) status and dynamics of soils in H. cochinchinensis habitats were measured. Plant P and nitrogen (N) concentrations of leaves were measured after digestion. Roots and rhizosheath soil were collected to assess root morphology and root exudates.Results Available P (Olsen-P) in soils in habitats of H. cochinchinensis was 0.46–3.7 mg P kg-1 soil. Citrate was the major carboxylate in root exudates and its concentration increased during cluster-root formation. Acid phosphatase activity was greater at the surface of cluster roots that on the surface of other roots and bulk soil, especially for mature cluster roots. Sparingly soluble organic P concentrations decreased in the rhizosheath soil of mature cluster roots. The P concentrations of H. cochinchinensis leaves were relatively low; 0.34–0.69 mg P g-1 DW and 0.15–0.29 mg P g-1 DW in mature and senesced leaves, respectively. The P demand of H. cochinchinensis was less than that of nearby trees, showing greater P-remobilization efficiency.Conclusions Phosphorus mobilization from unavailable P by cluster roots supported P uptake by H. cochinchinensis, and P remobilization from senescing leaves contributed to sustain growth under P-deficient conditions.

Nodulated White Lupin Plants Growing in Contaminated Soils Accumulate Unusually High Mercury Concentrations in Their Nodules, Roots and Especially Cluster Roots

Two white lupin (Lupinus albus L.) cultivars were tested for their capacity to accumulate mercury when grown in Hg-contaminated soils. Plants inoculated with a Bradyrhizobium canariense Hg-tolerant strain or non-inoculated were grown in two highly Hg-contaminated soils. All plants were nodulated and presented a large number of cluster roots. They accumulated up to 600 μg Hg g−1 DW in nodules, 1400 μg Hg g−1 DW in roots and 2550 μg Hg g−1 DW in cluster roots. Soil, and not cultivar or inoculation, was accountable for statistically significant differences. No Hg translocation to leaves or seeds took place. Inoculated L. albus cv. G1 plants were grown hydroponically under cluster root-promoting conditions in the presence of Hg. They accumulated about 500 μg Hg g−1 DW in nodules and roots and up to 1300 μg Hg g−1 DW in cluster roots. No translocation to the aerial parts occurred. Bioaccumulation factors were also extremely high, especially in soils and particularly in cluster roots. To our knowledge, Hg accumulation in cluster roots has not been reported to date. Our results suggest that inoculated white lupin might represent a powerful phytoremediation tool through rhizosequestration of Hg in contaminated soils. Potential uptake and immobilization mechanisms are discussed.

Dynamic Development of White Lupin Rootlets Along a Cluster Root

White lupin produces cluster roots in response to phosphorus deficiency. Along the cluster root, numerous short rootlets successively appear, creating a spatial and temporal gradient of developmental stages that constitutes a powerful biological model to study the dynamics of the structural and functional evolution of these organs. The present study proposes a fine histochemical, transcriptomic and functional analysis of the rootlet development from its emergence to its final length. Between these two stages, the tissue structures of the rootlets were observed, the course of transcript expressions for the genes differentially expressed was monitored and some physiological events linked to Pi nutrition were followed. A switch between (i) a growing phase, in which a normal apical meristem is present and (ii) a specialized phase for nutrition, in which the rootlet is completely differentiated, was highlighted. In the final stage of its determinate growth, the rootlet is an organ with a very active metabolism, especially for the solubilization and absorption of several nutrients. This work discusses how the transition between a growing to a determinate state in response to nutritional stresses is found in other species and underlines the fundamental dilemma of roots between soil exploration and soil exploitation.

Leaf Phosphorus Concentration Regulates the Development of Cluster Roots and Exudation of Carboxylates in Macadamia integrifolia

Phosphorus (P) deficiency induces cluster-root formation and carboxylate exudation in most Proteaceae. However, how external P supply regulates these root traits in Macadamia integrifolia remains unclear. Macadamia plants were grown hydroponically with seven P levels to characterize biomass allocation, cluster-root development, and exudation of carboxylates and acid phosphatases. Plant biomass increased with increasing P supply, peaking at 5 μM P, was the same at 5–25 μM P, and declined at 50–100 μM P. Leaf P concentration increased with increasing P supply, but shoot biomass was positively correlated with leaf P concentration up to 0.7–0.8 mg P g–1 dry weight (DW), and declined with further increasing leaf P concentration. The number of cluster roots declined with increasing P supply, with a critical value of leaf P concentration at 0.7–0.8 mg P g–1 DW. We found a similar trend for carboxylate release, with a critical value of leaf P concentration at 0.5 mg g–1 DW, but the activity of acid phosphatases showed a gradually-decreasing trend with increasing P supply. Our results suggest that leaf P concentration regulates the development and functioning of cluster roots, with a critical P concentration of 0.5–0.8 mg g–1, above which macadamia growth is inhibited.

Cluster-root bearing Proteaceae species show a competitive advantage over non-cluster root species

Background and aims Cluster roots (CRs) constitute a special root adaptation that enables plants to take up nutrients, especially phosphorus (P), from soils with low nutrient availability, including recent volcanic deposits. It is unclear, however, how CR species interact with non-cluster root (NCR) species, and how substrates’ fertility modulates potential interactions. Methods We experimentally assessed the net interaction between CR and NCR species using two substrates of contrasting fertility: nutrient-rich nursery mix and tephra (low P availability). We planted seedlings of two southern South America (SSA) Proteaceae species and two NCR Nothofagus species in pairs (conspecifics and heterospecifics) and as singles. We analysed the effect of seedling neighbours on survival, growth performance (e.g. total biomass and leaf area), and leaf and substrate nutrient concentrations (including manganese [Mn], a proxy for P-acquisition efficiency through CR activity) using the relative interaction index (RII). Key Results After three growing seasons, we found that 1) Proteaceae species had fewer CRs, lower CR biomass, and grew less in the tephra than in the nursery substrate; 2) Nothofagus species did not improve their survival and growth in the presence of Proteaceae species in any substrate; 3) contrary to Nothofagus, Proteaceae species improved their growth more when planted with any neighbour (including conspecifics) than when planted alone, which was accompanied by a significant accretion of leaf P; and 4) the presence of a neighbour increased the final N and P concentrations in the nursery substrate, regardless of species identity. Conclusions CRs provide Proteaceae a competitive advantage over NCR species at the seedling stage, which may have important consequences for species coexistence and community structuring. The investigated SSA Proteaceae, which have not evolved in nutrient-impoverished soils as their relatives in southwestern Australia and South Africa, improve their growth when cultivated in pairs, especially in nutrient-rich substrates.