L. D. B. Suriyagoda

Carbon trading for phosphorus gain: The balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition

Two key plant adaptations for phosphorus (P) acquisition are carboxylate exudation into the rhizosphere and mycorrhizal symbioses. These target different soil P resources, presumably with different plant carbon costs. We examined the effect of inoculation with arbuscular mycorrhizal fungi (AMF) on amount of rhizosphere carboxylates and plant P uptake for 10 species of low-P adapted Kennedia grown for 23 weeks in low-P sand. Inoculation decreased carboxylates in some species (up to 50%), decreased plant dry weight (21%) and increased plant P content (23%). There was a positive logarithmic relationship between plant P content and the amount of rhizosphere citric acid for inoculated and uninoculated plants. Causality was indicated by experiments using sand where little citric acid was lost from the soil solution over 2 h and citric acid at low concentrations desorbed P into the soil solution. Senesced leaf P concentration was often low and P-resorption efficiencies reached >90%. In conclusion, we propose that mycorrhizally mediated resource partitioning occurred because inoculation reduced rhizosphere carboxylates, but increased plant P uptake. Hence, presumably, the proportion of plant P acquired from strongly sorbed sources decreased with inoculation, while the proportion from labile inorganic P increased. Implications for plant fitness under field conditions now require investigation.

Multiple adaptive responses of Australian native perennial legumes with pasture potential to grow in phosphorus- and moisture-limited environments

BACKGROUND AND AIMS Many Australian legumes have evolved in low-phosphorus (P) soils and low-rainfall areas. Therefore a study was made of the interaction of soil [P] and water availability on growth, photosynthesis, water-use efficiency (WUE) and P nutrition of two Australian native legumes with pasture potential, Cullen australasicum and C. pallidum, and the widely grown exotic pasture legume, lucerne (Medicago sativa). METHODS Plants were grown in a glasshouse at 3, 10 and 30 mg P kg(-1) dry soil for 5 months. At week 10, two drought treatments were imposed, total pot dried (all-dry) and only top soil dried (top-dry), while control pots were maintained at field capacity. KEY RESULTS Shoot dry weight produced by lucerne was never higher than that of C. australasicum. For C. pallidum only, shoot dry weight was reduced at 30 mg P kg(-1) dry soil. The small root system of the Cullen species was quite plastic, allowing plants to access P and moisture efficiently. Lucerne always had a higher proportion of its large root system in the top soil layer compared with Cullen species. All species showed decreased photosynthesis, leaf water potential and stomatal conductance when exposed to drought, but the reductions were less for Cullen species, due to tighter stomatal control, and consequently they achieved a higher WUE. All species showed highest rhizosphere carboxylate concentrations in the all-dry treatment. For lucerne only, carboxylates decreased as P supply increased. Citrate was the main carboxylate in the control and top-dry treatments, and malate in the all-dry treatment. CONCLUSIONS Multiple adaptive responses of Cullen species and lucerne favoured exploitation of low-P soils under drought. The performance of undomesticated Cullen species, relative to that of lucerne, shows their promise as pasture species for environments such as in south-western Australia where water and P are limiting, especially in view of a predicted drying and warming climate.

Plant responses to limited moisture and phosphorus availability: A meta-analysis

Abstract Phosphorus (P) is a scarce, nonrenewable resource; its acquisition by plants decreases when soil moisture declines, as anticipated under future climate-change scenarios. It is, therefore, important to understand plant responses and adaptations to dual moisture and P limitations, in order to maintain crop productivity and predict plant performance in natural ecosystems. We review current knowledge of the effect of simultaneous water and P shortage on plant function, and identify key knowledge gaps. Plants have developed a range of adaptations to ensure P uptake is adequate to maintain vital functions within a broad range, at least until a certain level of P and/or drought stress is exceeded. Differences in plant growth and amount of P taken up under dual moisture and P limitations greatly depend on the rate of soil drying and wetting, the severity and duration of drought cycles, plant uptake capacity, root system plasticity, presence and magnitude of hydraulic redistribution, P-resorption ability, and soil properties such as waterholding capacity, P diffusion rate, P mineralization and fixation rates, and the activity of arbuscular mycorrhizal (AM) symbioses. During the process of soil drying, both P fertilization and association with AM fungi may increase performance under drought, until a certain level of water stress is exceeded. A small number of previously reported contradictory results probably reflect differences/limitations in experimental approaches. When breeding crop varieties to increase the efficiency of P and water acquisition, and when examining performance of species in natural ecosystems, multiple and interacting processes, from the scale of cellular to whole plant, must be considered.

Plant Responses to Limited Moisture and Phosphorus Availability

Abstract Phosphorus (P) is a scarce, nonrenewable resource; its acquisition by plants decreases when soil moisture declines, as anticipated under future climate-change scenarios. It is, therefore, important to understand plant responses and adaptations to dual moisture and P limitations, in order to maintain crop productivity and predict plant performance in natural ecosystems. We review current knowledge of the effect of simultaneous water and P shortage on plant function, and identify key knowledge gaps. Plants have developed a range of adaptations to ensure P uptake is adequate to maintain vital functions within a broad range, at least until a certain level of P and/or drought stress is exceeded. Differences in plant growth and amount of P taken up under dual moisture and P limitations greatly depend on the rate of soil drying and wetting, the severity and duration of drought cycles, plant uptake capacity, root system plasticity, presence and magnitude of hydraulic redistribution, P-resorption ability, and soil properties such as waterholding capacity, P diffusion rate, P mineralization and fixation rates, and the activity of arbuscular mycorrhizal (AM) symbioses. During the process of soil drying, both P fertilization and association with AM fungi may increase performance under drought, until a certain level of water stress is exceeded. A small number of previously reported contradictory results probably reflect differences/limitations in experimental approaches. When breeding crop varieties to increase the efficiency of P and water acquisition, and when examining performance of species in natural ecosystems, multiple and interacting processes, from the scale of cellular to whole plant, must be considered.

Divergent functioning of Proteaceae species: the South American Embothrium coccineum displays a combination of adaptive traits to survive in high‐phosphorus soils

Summary 1. 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.

Establishment, survival, and herbage production of novel, summer-active perennial pasture legumes in the low-rainfall cropping zone of Western Australia as affected by plant density and cutting frequency

Abstract. Herbaceous perennial legumes that can provide forage in the summer–autumn dry period are urgently required in Mediterranean climates to complement annual pastures and the perennial legume lucerne (Medicago sativa). This study evaluated the establishment, survival, and herbage production of tedera (Bituminaria bituminosa var. albomarginata) and Cullen spp. native to Australia. Two experiments were replicated at Buntine (warmer site) and Newdegate (cooler site) in the low-rainfall cropping zone (<350 mm average annual rainfall) of Western Australia from June 2008 to September 2010. In the first experiment, established by transplanting seedlings, survival and herbage production of two accessions each of B. bituminosa and C. australasicum were studied under densities of 1, 2, 4, 8, and 16 plants/m2 with 0, 1, 2, or 3 cuts in summer–autumn in addition to a winter–spring cut. In the second experiment, established from seed, emergence and survival of several accessions of B. bituminosa, C. australasicum, and M. sativa were studied, along with C. pallidum and C. cinereum. In the first experiment, B. bituminosa survived better than C. australasicum (70–80% v. 18–45%), especially at Buntine, but there was little impact of density or cutting frequency on survival. Plant death was highest during summer. Shoot dry weight (DW) accumulation varied greatly with site, year, and plant density. When rainfall was close to average, shoot DW was greater at Newdegate (B. bituminosa ≤7.4 t/ha, C. australasicum ≤4.5 t/ha) than at Buntine (≤2.3 t/ha), and both species produced much of their shoot DW in summer–autumn (e.g. 6 t/ha for B. bituminosa and 3 t/ha for C. australasicum at Newdegate). An early-summer cut reduced the DW that could be harvested later in summer–autumn. In the second experiment, emergence of B. bituminosa was either similar to, or higher than, emergence of the other species, being 43% at Buntine and 44% at Newdegate. Survival of B. bituminosa, compared with M. sativa, was similar at Buntine (13%) and slightly lower at Newdegate (14%). Emergence and survival of Cullen spp. varied among species and accessions, with survival of the best performing accession of C. australasicum (SA4966) similar to that of B. bituminosa and M. sativa at both sites. We conclude that B. bituminosa shows promise as a perennial summer forage for low-rainfall zones, with a density of 8–16 plants/m2 and cutting frequency of 3 cuts/year (i.e. cut twice in summer–autumn), while C. australasicum and C. pallidum warrant further study.

Effects of leaf development and phosphorus supply on the photosynthetic characteristics of perennial legume species with pasture potential: modelling photosynthesis with leaf development

Age-dependent changes in leaf photosynthetic characteristics (i.e. parameters of the light response curve (maximum photosynthetic rate (Pmax), quantum yield (Φ) and the convexity parameter (θ)), stomatal conductance (gs) and dark respiration rate (Rd)) of an exotic perennial legume, Medicago sativa L. (lucerne), and two potential pasture legumes native to Australia, Cullen australasicum (Schltdl.) J.W. Grime and Cullen pallidum A. Lee, grown in a glasshouse for 5 months at two phosphorus (P) levels (3 (P3) and 30 (P30) mg P kg–1 dry soil) were tested. Leaf appearance rate and leaf area were lower at P3 than at P30 in all species, with M. sativa being the most sensitive to P3. At any leaf age, photosynthetic characteristics did not differ between P treatments. However, Pmax and gs for all the species and Φ for Cullen species increased until full leaf expansion and then decreased. The convexity parameter, θ, did not change with leaf age, whereas Rd decreased. The estimates of leaf net photosynthetic rate (Pleaf) obtained through simulations at variable Pmax and Φ were lower during early and late leaf developmental stages and at lower light intensities than those obtained when Φ was assumed to be constant (e.g. for a horizontally placed leaf, during the 1500°C days developmental period, 3 and 19% reduction of Pleaf at light intensities of 1500 and 500 µmol m–2 s–1, respectively). Therefore, developmental changes in leaf photosynthetic characteristics should be considered when estimating and simulating Pleaf of these pasture species.

Adaptive shoot and root responses collectively enhance growth at optimum temperature and limited phosphorus supply of three herbaceous legume species

BACKGROUND AND AIMS Studies on the effects of sub- and/or supraoptimal temperatures on growth and phosphorus (P) nutrition of perennial herbaceous species at growth-limiting P availability are few, and the impacts of temperature on rhizosphere carboxylate dynamics are not known for any species. METHODS The effect of three day/night temperature regimes (low, 20/13 °C; medium, 27/20 °C; and high, 32/25 °C) on growth and P nutrition of Cullen cinereum, Kennedia nigricans and Lotus australis was determined. KEY RESULTS The highest temperature was optimal for growth of C. cinereum, while the lowest temperature was optimal for K. nigricans and L. australis. At optimum temperatures, the relative growth rate (RGR), root length, root length per leaf area, total P content, P productivity and water-use efficiency were higher for all species, and rhizosphere carboxylate content was higher for K. nigricans and L. australis. Cullen cinereum, with a slower RGR, had long (higher root length per leaf area) and thin roots to enhance P uptake by exploring a greater volume of soil at its optimum temperature, while K. nigricans and L. australis, with faster RGRs, had only long roots (higher root length per leaf area) as a morphological adaptation, but had a higher content of carboxylates in their rhizospheres at the optimum temperature. Irrespective of the species, the amount of P taken up by a plant was mainly determined by root length, rather than by P uptake rate per unit root surface area. Phosphorus productivity was correlated with RGR and plant biomass. CONCLUSIONS All three species exhibited adaptive shoot and root traits to enhance growth at their optimum temperatures at growth-limiting P supply. The species with a slower RGR (i.e. C. cinereum) showed only morphological root adaptations, while K. nigricans and L. australis, with faster RGRs, had both morphological and physiological (i.e. root carboxylate dynamics) root adaptations.

The future of phosphorus in our hands

AbstractWe live in a global phosphorus (P) system paradox. P access is becoming increasingly limiting, leading to food insecurity but at the same time an over-application or abundance of P in many agricultural and urban settings is causing environmental degradation. This has been recognised in the academic literature and at regulatory levels, but swift action and multi-level cooperation of all stakeholders is required to ensure the economically, environmentally and socially responsible use of P. To provide foundations for future cooperation, a conceptual model describing the elements of P need, P availability and P use in different systems and at different scales was developed during the Young Scientists Workshop in P Week 2014 in Montpellier, France. Here we describe our extended conceptual model and a theoretical P balance calculation tool for describing multi-scale P balances and imbalances to impartially advise all stakeholders on more sustainable P use across the world.

Genotypic Variation in Grain P Loading across Diverse Rice Growing Environments and Implications for Field P Balances

More than 60% of phosphorus (P) taken up by rice (Oryza spp.) is accumulated in the grains at harvest and hence exported from fields, leading to a continuous removal of P. If P removed from fields is not replaced by P inputs then soil P stocks decline, with consequences for subsequent crops. Breeding rice genotypes with a low concentration of P in the grains could be a strategy to reduce maintenance fertilizer needs and slow soil P depletion in low input systems. This study aimed to assess variation in grain P concentrations among rice genotypes across diverse environments and evaluate the implications for field P balances at various grain yield levels. Multi-location screening experiments were conducted at different sites across Africa and Asia and yield components and grain P concentrations were determined at harvest. Genotypic variation in grain P concentration was evaluated while considering differences in P supply and grain yield using cluster analysis to group environments and boundary line analysis to determine minimum grain P concentrations at various yield levels. Average grain P concentrations across genotypes varied almost 3-fold among environments, from 1.4 to 3.9 mg g−1. Minimum grain P concentrations associated with grain yields of 150, 300, and 500 g m−2 varied between 1.2 and 1.7, 1.3 and 1.8, and 1.7 and 2.2 mg g−1 among genotypes respectively. Two genotypes, Santhi Sufaid and DJ123, were identified as potential donors for breeding for low grain P concentration. Improvements in P balances that could be achieved by exploiting this genotypic variation are in the range of less than 0.10 g P m−2 (1 kg P ha−1) in low yielding systems, and 0.15–0.50 g P m−2 (1.5–5.0 kg P ha−1) in higher yielding systems. Improved crop management and alternative breeding approaches may be required to achieve larger reductions in grain P concentrations in rice.