In-soil trophic interactions between plants, bacteria and nematodes:Potential for increasing plant availability of organic phosphorus

Significant disparities exist between phosphorus (P) fertilizer applications and plant P uptake, in part induced by the in-soil conversion of inorganic P (Pi) to organic P forms (Po), which are not readily plant available. In-soil trophic interactions have been implicated in increased plant access to Po, specifically interactions between bacteria and bacterivorous nematodes. However, the existing data remains inconclusive and lack detail in arable systems, which are of increased economic importance. This work aimed to (1) assess the impact of nematodes as an additional trophic-level on Po use by plants in arable systems and (2) further understand the mechanisms of in-soil trophic interactions in improving plant acquisition of Po. To address these aims, criteria based meta-analysis, glasshouse plant growth trials, in vitro and in soil, and long term experimental (LTE) platforms were used. Results supported the conclusion that nematodes did not improve plant acquisition of Po per se. Time, soil P concentration and soil biological community composition had significant impacts on plant response. Although these factors were identified in two contrasting studies, their impacts on plant responses were stochastic. However, complexity, which describes the average number of trophic links per species, proved to be useful when understanding these data. For example, data from the meta-analysis and the plant growth trials demonstrated it was not simply the additive effect of the number of species or the addition of a specific species which resulted in predictable plant P responses. Both studies employed complexity as a system descriptor, which framed an understanding of these data where they evaded predictability, specifically when considering the temporal nature of these relationships, as complexity inherently includes a temporal element. The LTEs provided empirical data to support such assertions and yielded characteristics indicative of stability in the biotic component of systems previously considered disturbed. This exposed the question of the nature of disturbance (whether natural or anthropogenic). Additionally, it highlighted the importance of which successional time-point was being studied and the impact this has on the data captured. For example, nematode community analysis in the arable site assumed to represent disturbed land, showed characteristics of an undisturbed system, therefore it is not enough to assume an arable system is ‘disturbed’ or that an arable system after 150 years of continuous treatment would replicate results from a site under continuous management of a different temporal scale. Results allowed for the assessment of the experimental approaches used to interrogate complex systems and suggestions are made for a more pragmatic approach for the future. Although simple experimental systems exploring discrete mechanisms should not be abandoned, extrapolation of such data and predictions to more complex systems must involve the abandonment of the linear reductionist model and undergo transformative inclusion into one of complexity

Soils training and research: Who's legacy?

Abstract and Poste

Inter- and intra-species intercropping of barley cultivars and legume species, as affected by soil phosphorus availability

Aims Intercropping can improve plant yields and soil phosphorus (P) use efficiency. This study compares inter- and intra-species intercropping, and determines whether P uptake and shoot biomass accumulation in intercrops are affected by soil P availability. Methods Four barley cultivars (Hordeum vulgare L.) and three legume species (Trifolium subterreneum, Ornithopus sativus and Medicago truncatula) were selected on the basis of their contrasting root exudation and morphological responses to P deficiency. Monocultures and barley-barley and barley-legume intercrops were grown for 6 weeks in a pot trial at very limiting, slightly limiting and excess available soil P. Aboveground biomass and shoot P were measured. Results Barley-legume intercrops had 10–70% greater P accumulation and 0–40% greater biomass than monocultures, with the greatest gains occurring at or below the sub-critical P requirement for barley. No benefit of barley-barley intercropping was observed. The plant combination had no significant effect on biomass and P uptake observed in intercropped treatments. Conclusions Barley-legume intercropping shows promise for sustainable production systems, especially at low soil P. Gains in biomass and P uptake come from inter- rather than intra-species intercropping, indicating that plant diversity resulted in decreased competition between plants for P

On pedagogy of a Soil Science Centre for Doctoral Training

Here we describe and evaluate the success of a multi-institutional Centre for Doctoral Training (CDT), which was established to address a UK skills shortage in Soil Science. The government-funded ‘STARS’ (Soils Training And Research Studentships) CDT was established in 2015 across a range of universities and research institutes in the UK. It recruited 41 PhD students equitably split across the institutions under four core research themes identified as being central to the national need, namely, (1) Understanding the soil–root interface, (2) Soils and the delivery of ecosystem services, (3) Resilience and response of functions in soil systems and (4) Modelling the soil ecosystem at different spatial and temporal scales. In addition, the STARS CDT provided a diverse skills programme, including: Holistic training in soils, the promotion of collegiality and joint working, strategies to promote science and generate impact, internships with end users (e.g., policymakers, industry), personal wellbeing, and ways to generate a lasting soils training legacy. Overall, both supervisors and students have reported a positive experience of the CDT in comparison to the conventional doctoral training programmes, which have less discipline focus and little chance for students to scientifically interact with their cohorts or to undertake joint training activities. The STARS CDT also allowed students to freely access research infrastructure across the partner institutions (e.g., long-term field trials, specialised analytical facilities, high-performance computing), breaking down traditional institutional barriers and thus maximising the students' potential to undertake high-quality research. The success and legacy of the STARS CDT can be evidenced in many ways; however, it is exemplified by the large number and diversity of journal papers produced, the lasting collaborations, final career destinations, and creation of a web-based legacy portal including new and reflective video material.STARS CDT, Grant/Award Numbers: NE/V017667/1, NE/R010218/1, NE/M009106/1; UKR

Linking the depletion of rhizosphere phosphorus to the heterologous expression of a fungal phytase in Nicotiana tabacum as revealed by enzyme-labile P and solution 31P NMR spectroscopy

Root exudation of phytase could improve the ability of plants to access organic forms of soil phosphorus (P), thereby minimizing fertilizer requirements and improving P use efficiency in agroecosystems. After 75 days growth in a high available P soil, shoot biomass and P accumulation, soil pH, and rhizosphere P depletion were investigated in Nicotiana tabacum wild-type and transgenic plant-lines expressing and exuding Aspergillus niger phytase (ex::phyA), or a null-vector control. Solution 31P NMR analysis revealed a 7% to 11% increase in orthophosphate and a comparable depletion of undefined monoester P compounds (-13 to -18%) in the rhizosphere of tobacco plants relative to the unplanted soil control. Wild-type plants had the greatest impact on the composition of rhizosphere P based on the depletion of other monoester P, polyphosphate, and phosphonate species. The depletion of phytase-labile P by ex::phyA plants was associated with decreased proportions of other monoester P, rather than myo-InsP6 as expected. Rhizosphere pH increased from 6.0 to 6.5–6.7 in transgenic plant soils, beyond the pH optimum for A. niger phyA activity (pH=5), and may explain the limited specificity of ex::phyA plants for phytate in this soil. The efficacy of single exudation traits (e.g., phytase) therefore appear to be limited in P-replete soil conditions and may be improved where soil pH matches the functional requirements of the enzyme or trait of interest

Response-based selection of barley cultivars and legume species for complementarity:root morphology and exudation in relation to nutrient source

Phosphorus (P) and nitrogen (N) use efficiency may be improved through increased biodiversity in agroecosystems. Phenotypic variation in plants’ response to nutrient deficiency may influence positive complementarity in intercropping systems. A multicomponent screening approach was used to assess the influence of P supply and N source on the phenotypic plasticity of nutrient foraging traits in barley (H. vulgare L.) and legume species. Root morphology and exudation were determined in six plant nutrient treatments. A clear divergence in the response of barley and legumes to the nutrient treatments was observed. Root morphology varied most among legumes, whereas exudate citrate and phytase activity were most variable in barley. Changes in root morphology were minimized in plants provided with ammonium in comparison to nitrate but increased under P deficiency. Exudate phytase activity and pH varied with legume species, whereas citrate efflux, specific root length, and root diameter lengths were more variable among barley cultivars. Three legume species and four barley cultivars were identified as the most responsive to P deficiency and the most contrasting of the cultivars and species tested. Phenotypic response to nutrient availability may be a promising approach for the selection of plant combinations for minimal input cropping systems

Opportunity to improve global phosphorus governance : Nutrient Cycling

Nutrient recycling is key for the circularity and sustainability of food systems. Understanding the movement of phosphorus through trade enables better geospatial planning and highlights opportunities for more effective global phosphorus governance

A meta-analysis of phosphatase activity in agricultural settings in response to phosphorus deficiency

Phosphorus (P) is a key limiting factor in crop growth and essential for agriculture. As plant uptake of P is inefficient, it is commonly applied to maintain crop yields leading to a range of negative environmental issues when applied in excess. Additionally, P in mineral fertilisers is derived from mined rock phosphate, which is a finite resource that needs to be sustainably managed in order to maintain food security in the long-term. Phosphatase activity is one of several mechanistic responses to P deficiency in the plant-soil system, enabling the mineralization of organic P to increase P availability for both plants and soil organisms. In this study we address the need to further understanding of the role of phosphatase enzyme activity in P acquisition in agricultural settings, using a systematic review of the literature and subsequent meta-analysis. We find that monoesterase activity is inhibited by availability of inorganic P (−23%, −39.8 - -2.2%) yet is enhanced by the availability of organic P (+74%, 8.4–232.1%). This indicates that phosphatase enzyme activity is important in P deficient agricultural systems, yet that the availability of organic P is more important in determining phosphatase activity than the level of P deficiency. We also investigated the role of other factors such as nitrogen addition, pH of growth substrate and changes in plant composition and physiology but, none of these factors explained significant variance in the data. We highlight need for consistent recording and reporting of additional variables in association with phosphatase enzyme assay data, which is required to enable quantification of the potential utilisation of organic P resources in agriculture, and the contribution of phosphatase activity to P acquisition in both agricultural and semi-natural ecosystems

Effect of citrate on Aspergillus niger phytase adsorption and catalytic activity in soil

Phytase enzymes from bacteria, fungus and plant root exudates are known to hydrolyse organic phosphorus (Po) to bioavailable inorganic orthophosphate in soil. Exploiting such biochemical functions in agricultural systems, offers the potential for alternative sustainable phosphorus sources. Phytase adsorption to soil particles and phytate metal complexation has been shown to inhibit phytate (InsP6) dephosphorylation. Organic acid anions such as citrate increase phytase catalytic efficiency towards complexed forms of InsP6, but the mechanisms are poorly understood. The aim of this work was to evaluate Aspergillus niger phytase inactivation and changes in its catalytic properties upon addition to soil, as well as the effect of citrate on phytase adsorption and activity towards free, precipitated and adsorbed InsP6. We performed a series of enzyme hydrolysis activity assays when the enzymes were free, in soil solution and adsorbed to soil under varying chemical conditions, with and without citrate. A. niger phytase showed a relatively low absorption affinity for the Cambisol test soil. Phytase activity reduced by 37.3% due to adsorption. Citrate had no effect on the rate or total amount of phytase adsorption or soil adsorbed phytase activity thereafter. Free phytases and phytases in soil solution showed optimum activity (≥ 80%) at pH 4.5–5.5. Activity decreased slightly for soil adsorbed enzymes compared to enzymes which were free or in soil solution > pH 5 and 0.6 M in adsorbed and free enzymes, while activity from enzymes in soil solution reduced in all tested ionic strengths. Citrate significantly increased phytase activity towards InsP6 adsorbed to soil when the phytases were free (p ≤ 0.003) but not in other treatments (Na, Al and Ca-phytate). These results suggest that the effect of citrate on soil InsP6 dephosphorylation is associated with the availability of the substrate (InsP6) rather than its effect on the enzyme per se. The ionic strength and pH of soil solution has been shown to impact on phytase activity, suggesting that salinity, quality of irrigation water, wetting/drying cycles and fertilisation will have discrete impacts on the activity of phytases once released in soil and thus the ability to make Po available for uptake by plants and microbes. The optimum acidic pH of A. niger also brings into question its suitability for application in many agricultural soils

Corrigendum to “Using a meta-analysis approach to understand complexity in soil biodiversity and phosphorus acquisition in plants” [Soil Biol. Biochem. 142 (2020) 107695] (Soil Biology and Biochemistry (2020) 142, (S0038071719303591), (10.1016/j.soilbio.2019.107695))

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