The impoverished nature of the phosphorus-poor soils which dominate the Australian continent has given rise to an abundant array of adaptations in Australian flora which help to overcome the phosphorus (P) limiting conditions. Attempts to domesticate Australian native plants into conventional nursery production systems have been hampered by the sensitivity of a number of species to the essential mineral element P. Enhanced P uptake and high internal P use efficiency of Australian plants is often ironically linked with sensitivity to even slight increases in P availability, producing symptoms of P toxicity. The non-mycorrhizal Australian native sedge Caustis blakei Kük. (Cyperaceae) occurs on nutrient-poor deep sands and soils derived from weathered sandstones on the east coast of Australia. As a species with commercial potential in the cut flower industry, an understanding of the P nutrition of C. blakei is essential to its viable cultivation. The objective of this study was to characterise the high P-use efficiency of C. blakei, and to examine its extreme sensitivity to P fertilisation.
We hypothesised that the feedback mechanism which triggers the downregulation of P uptake in C. blakei is ineffective and leads to increased sensitivity to P toxicity under application of highly soluble P. The influence of external P supply on two low-P adapted Australian native plants, C. blakei and Chamelaucium uncinatum Schauer. (waxflower), and on the fast-growing crop species Lycopersicon esculentum Mill. (tomato) was determined. Increased P-absorption rates in waxflower and tomato were associated with increasing relative growth rates (RGR); however, the RGR for C. blakei peaked at the lowest P-absorption rate, and due to P toxicity at higher P supply, increasing absorption rates lowered its RGR. These results suggest that, unlike tomato and waxflower, C. blakei may not be able to down-regulate its P uptake, and hence solution P concentrations greater than 10 μM become toxic; C. blakei grown at 250 μM P accumulated P to toxic concentrations as high as 12 mg g-1 DM in the shoots. In contrast, at lower solution P concentrations, C. blakei appeared to be highly efficient in its acquisition and internal use of P, where the highest biomass was produced at the low solution [P] of 1.0 μM. Furthermore, low-P adaptations included an increased root mass ratio and the formation of ‘dauciform’ roots when plants were grown at low solution [P] of 1.0 μM and below.
The intriguing discovery of swollen lateral, hairy, dauciform roots has enabled the elucidation of physiological processes central to the P economy of C. blakei. We tested the hypothesis that these hairy, swollen lateral roots play a similar role to cluster roots in the exudation of organic chelators and ectoenzymes known to aid the chemical mobilisation of sparingly available soil nutrients, such as P. Dauciform-root development and exudate composition (carboxylates and acid phosphatase activity) were analysed in C. blakei plants grown in nutrient solution under P-starved conditions. The distribution of dauciform roots in the field was determined in relation to soil profile depth and matrix. The percentage of dauciform roots of the entire root mass was greatest at the lowest [P] in solution, and was suppressed with increasing solution [P], while in the field, dauciform roots were predominately located in the upper soil horizons, and decreased with increasing soil depth. Citrate was the major carboxylate released in an exudative burst from mature dauciform roots, which also produced elevated levels of acid phosphatase activity. Malonate was the dominant internal carboxylate present, with the highest concentration in young dauciform roots.
The root expression of two putative high affinity P transporters CbPT1 and CbPT2 was assessed in relation to the net-P uptake rate from C. blakei plants after pre-treatment at a range of solution P concentrations (0.01-10μM). Net-P uptake rates were unchanged across the whole range of pre-treatment concentrations, even in plants grown at 10 μM P which showed symptoms of P toxicity. Both CbPT1 and CbPT2 were induced by low P concentrations (0.01-0.1μM) and while CbPT2 was suppressed under increased P concentrations, CbPT1 was less responsive and appeared to down-regulate only at extremely high solution [P] between 100 and 250μM. Expression analysis during dauciform-root development revealed that CbPT2 expression gradually increased in alignment with dauciform root age, reaching its highest expression in mature dauciform roots.
The P uptake system of C. blakei is able to respond at a morphological and molecular level to P limiting conditions through the induction of dauciform roots with enhanced expression of P transporters. The high concentration of carboxylates and phosphatases released from dauciform roots, combined with their prolific distribution in the organic surface layer of nutrient-impoverished soils, provides an ecophysiological advantage for enhancing nutrient acquisition. The refined low-P sensing of C. blakei is contrasted by an inability to down-regulate the P uptake system under luxury P supply, which may be a consequence of natural selection in ecosystems devoid of P in excess of plant demand.
The adaptations to low-P environments of Australian plants such as C. blakei produced through many generations of natural selection may indicate potential areas to be harnessed in the breeding and selection of crops growing in the many P depleted soils of the world. In particular, further unravelling of the intricate nature of dauciform root physiology may provide useful insights into the low-P tolerance of plants.