Arbuscular mycorrhizal fungi enhance plant phosphorus uptake through stimulating hyphosphere soil microbiome functional profiles for phosphorus turnover.

The extraradical hyphae of arbuscular mycorrhizal (AM) fungi are colonized by different bacteria in natural and agricultural systems, but the mechanisms by which AM fungi interact with the hyphosphere soil microbiome and influence soil organic phosphorus (P) mobilization remain unclear. We grew Medicago in two-compartment microcosms, inoculated with Rhizophagus irregularis, or not, in the root compartment and set up P treatments (without P, with P addition as KH2 PO4 or nonsoluble phytate) in the hyphal compartment. We studied the processes of soil P turnover and characterized the microbiome functional profiles for P turnover in the hyphosphere soil by metagenomic sequencing. Compared with the bulk soil, the hyphosphere soil of R. irregularis was inhabited by a specific bacterial community and their functional profiles for P turnover was stimulated. At the species level, the shift in hyphosphere soil microbiome was characterized by the recruitment of the genome bin2.39 harbouring both gcd and phoD genes and genome bin2.97 harbouring the phoD gene, which synergistically drove nonsoluble phytate mobilization in the hyphosphere soil. Our results suggest that AM fungi recruits a specific hyphosphere soil microbiome and stimulated their functional profiles for P turnover to enhance utilization of phytate.

A core microbiome in the hyphosphere of arbuscular mycorrhizal fungi has functional significance in organic phosphorus mineralization.

The mycorrhizal pathway is an important phosphorus (P) uptake pathway for more than two-thirds of land plants. The arbuscular mycorrhizal (AM) fungi-associated hyphosphere microbiome has been considered as the second genome of mycorrhizal P uptake pathway and functionality in mobilizing soil organic P (Po). However, whether there is a core microbiome in the hyphosphere and how this is implicated in mining soil Po are less understood. We established on-site field trials located in humid, semiarid, and arid zones and a microcosm experiment in a glasshouse with specific AM fungi and varying soil types to answer the above questions. The hyphosphere microbiome of AM fungi enhanced soil phosphatase activity and promoted Po mineralization in all sites. Although the assemblage of hyphosphere microbiomes identified in three climate zones was mediated by environmental factors, we detected a core set in three sites and the subsequent microcosm experiment. The core members were co-enriched in the hyphosphere and dominated by Alphaproteobacteria, Actinobacteria, and Gammaproteobacteria. Moreover, these core bacterial members aggregate into stable guilds that contributed to phosphatase activity. The core hyphosphere microbiome is taxonomically conserved and provides functions, with respect to the mineralization of Po, that AM fungi lack.

Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae.

Arbuscular mycorrhizal (AM) fungi gain access to nutrient patches outside the rhizosphere by producing an extensive network of fine hyphae. Here, we focused on establishing the mechanism by which AM fungal hyphae reach discrete organic patches with a cohort of functional bacteria transported in a biofilm on their surface. We investigated the mechanisms and impact of the translocation of phosphate solubilising bacteria (PSB) along AM fungal hyphae in bespoke microcosms. An in vitro culture experiment was also conducted to determine the direct impact of hyphal exudates of AM fungi upon the growth of PSB. The extraradical hyphae of AM fungi can transport PSB to organic phosphorus (P) patches and enhance organic P mineralisation both under in vitro culture and soil conditions. Bacteria move in a thick water film formed around fungal hyphae. However, the bacteria cannot be transferred to the organic P patch without an energy source in the form of hyphal exudates. Our results could be harnessed to better manage plant-microbe interactions and improve the ability of biological inocula involving AM fungi and bacteria to enhance the sustainability of agricultural crops in P limited conditions.

Phosphorus leaching from riparian soils with differing management histories under three grass species.

Plants release carbon-based exudates from their roots into the rhizosphere to increase phosphorus (P) supply to the soil solution. However, if more P than required is brought into solution, additional P could be available for leaching from riparian soils. To investigate this further, soil columns containing a riparian arable and buffer strip soil, which differed in organic matter contents, were sown with three common agricultural and riparian grass species. The P loads in leachate were measured and compared with those from unplanted columns, which were 0.17 ± 0.01 and 0.89 ± 0.04 mg kg-1 for the arable and buffer strip soil, respectively. A mixture of ryegrass and red fescue significantly (p ≤ .05) increased dissolved inorganic P loads in leachate from the arable (0.23 ± 0.01 mg kg-1 ) and buffer strip soil (1.06 ± 0.05 mg kg-1 ), whereas barley significantly reduced P leaching from the buffer strip soil (0.53 ± 0.08 mg kg-1 ). This was dependent on the dissolved organic C released under different plant species and on interactions with soil management history and biogeochemical conditions, rather than on plant uptake of P and accumulation into biomass. This suggested that the amount and forms of P present in the soil and the ability of the plants to mobilize them could be key factors in determining how plants affect leaching of soil P. Selecting grass species for different stages of buffer strip development, basing species selection on root physiological traits, and correcting soil nutrient stoichiometry in riparian soils through vegetative mining could help to lower this contribution.

Simultaneous Quantification of Soil Phosphorus Labile Pool and Desorption Kinetics Using DGTs and 3D-DIFS.

The buffering of phosphorus concentrations in soil solution by the soil-solid phase is an important process for providing plant root access to nutrients. Accordingly, the size of labile solid phase-bound phosphorus pool and the rate at which it can resupply phosphorous into the dissolved phase can be important variables in determining when the plant availability of the nutrient may be limited. The phosphorus labile pool (Plabile) and its desorption kinetics were simultaneously evaluated in 10 agricultural UK soils using the diffusive gradients in thin-films (DGT) technique. The DGT-induced fluxes in the soil and sediments model (DIFS) was fitted to the time series of DGT deployments (1-240 h), which allowed the estimation of Plabile, and the system response time ( Tc). The Plabile concentration was then compared to that obtained by several soil P extracts including Olsen P, FeO-P, and water extractable P, in order to assess if the data from these analytical procedures can be used to represent the labile P across different soils. The Olsen P concentration, commonly used as a representation of the soil labile P pool, overestimated the desorbable P concentration by 6-fold. The use of this approach for the quantification of soil P desorption kinetic parameters found a wide range of equally valid solutions for Tc. Additionally, the performance of different DIFS model versions working in different dimensions (1D, 2D, and 3D) was compared. Although all models could provide a good fit to the experimental DGT time series data, the fitted parameters showed a poor agreement between different model versions. The limitations of the DIFS model family are associated with the assumptions taken in the modeling approach and the three-dimensional (3D) version is here considered to be the most precise among them.

Is Green Manure from Riparian Buffer Strip Species an Effective Nutrient Source for Crops?

Agriculture needs to reduce inputs of inorganic fertilizers and close the loop on nutrients that can otherwise become environmental pollutants. This can be achieved by promoting recycling of nutrients within the agricultural landscape. We investigated the extent to which plants found in riparian buffer zones have the potential to provide nutrients to crops as a green manure, through plant growth and decomposition studies. Under controlled conditions, species typical of Scottish riparian buffer strips were tested for their ability to accumulate biomass and nutrients in tissue under N- and P-replete conditions and whether this ability enhanced the utility of the resulting green manure in promoting crop growth. In this proof-of-concept study, we found that green manure derived from riparian buffer strips did not effectively replace inorganic fertilizer and only had a significant positive effect on growth, yield, and nutrient accumulation in barley ( L.) when it was integrated with the addition of inorganic fertilizers. The individual species tested varied in the amount of P they accumulated in their tissue (1.38-52.73 mg P plant), but individual species did not differ in their ability to promote yield when used as a green manure. Our results indicate that selecting certain species in the buffer strip on the basis of their nutrient accumulating abilities is not an effective way to increase the utility of buffer strip green manure as a nutrient source for crops.

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.

Organic Acids Regulation of Chemical-Microbial Phosphorus Transformations in Soils.

We have used an integrated approach to study the mobility of inorganic phosphorus (P) from soil solid phase as well as the microbial biomass P and respiration at increasing doses of citric and oxalic acid in two different soils with contrasting agronomic P status. Citric or oxalic acids significantly increased soil solution P concentrations for doses over 2 mmol kg-1. However, low organic acid doses (<2 mmol kg-1) were associated with a steep increase in microbial biomass P, which was not seen for higher doses. In both soils, treatment with the tribasic citric acid led to a greater increase in soil solution P than the dibasic oxalic acid, likely due to the rapid degrading of oxalic acids in soils. After equilibration of soils with citric or oxalic acids, the adsorbed-to-solution distribution coefficient (Kd) and desorption rate constants (k-1) decreased whereas an increase in the response time of solution P equilibration (Tc) was observed. The extent of this effect was shown to be both soil and organic acid specific. Our results illustrate the critical thresholds of organic acid concentration necessary to mobilize sorbed and precipitated P, bringing new insight on how the exudation of organic acids regulate chemical-microbial soil phosphorus transformations.

A Holistic Approach to Understanding the Desorption of Phosphorus in Soils.

The mobility and resupply of inorganic phosphorus (P) from the solid phase were studied in 32 soils from the UK. The combined use of diffusive gradients in thin films (DGT), diffusive equilibration in thin films (DET) and the "DGT-induced fluxes in sediments" model (DIFS) were adapted to explore the basic principles of solid-to-solution P desorption kinetics in previously unattainable detail. On average across soil types, the response time (Tc) was 3.6 h, the desorption rate constant (k-1) was 0.0046 h(-1), and the desorption rate was 4.71 nmol l(-1) s(-1). While the relative DGT-induced inorganic P flux responses in the first hour is mainly a function of soil water retention and % Corg, at longer times it is a function of the P resupply from the soil solid phase. Desorption rates and resupply from solid phase were fundamentally influenced by P status as reflected by their high correlation with P concentration in FeO strips, Olsen, NaOH-EDTA and water extracts. Soil pH and particle size distribution showed no significant correlation with the evaluated mobility and resupply parameters. The DGT and DET techniques, along with the DIFS model, were considered accurate and practical tools for studying parameters related to soil P desorption kinetics.

Understanding the genetic control and physiological traits associated with rhizosheath production by barley (Hordeum vulgare).

There is an urgent need for simple rapid screens of root traits that improve the acquisition of nutrients and water. Temperate cereals produce rhizosheaths of variable weight, a trait first noted on desert species sampled by Tansley over 100 yr ago. This trait is almost certainly important in tolerance to abiotic stress. Here, we screened association genetics populations of barley for rhizosheath weight and derived quantitative trait loci (QTLs) and candidate genes. We assessed whether rhizosheath weight was correlated with plant performance and phosphate uptake under combined drought and phosphorus deficiency. Rhizosheath weight was investigated in relation to root hair length, and under both laboratory and field conditions. Our data demonstrated that rhizosheath weight was correlated with phosphate uptake under dry conditions and that the differences in rhizosheath weight between genotypes were maintained in the field. Rhizosheath weight also varied significantly within barley populations, was correlated with root hair length and was associated with a genetic locus (QTL) on chromosome 2H. Putative candidate genes were identified. Rhizosheath weight is easy and rapid to measure, and is associated with relatively high heritability. The breeding of cereal genotypes for beneficial rhizosheath characteristics is achievable and could contribute to agricultural sustainability in nutrient- and water-stressed environments.

Root hairs improve root penetration, root-soil contact, and phosphorus acquisition in soils of different strength.

Root hairs are a key trait for improving the acquisition of phosphorus (P) by plants. However, it is not known whether root hairs provide significant advantage for plant growth under combined soil stresses, particularly under conditions that are known to restrict root hair initiation or elongation (e.g. compacted or high-strength soils). To investigate this, the root growth and P uptake of root hair genotypes of barley, Hordeum vulgare L. (i.e. genotypes with and without root hairs), were assessed under combinations of P deficiency and high soil strength. Genotypes with root hairs were found to have an advantage for root penetration into high-strength layers relative to root hairless genotypes. In P-deficient soils, despite a 20% reduction in root hair length under high-strength conditions, genotypes with root hairs were also found to have an advantage for P uptake. However, in fertilized soils, root hairs conferred an advantage for P uptake in low-strength soil but not in high-strength soil. Improved root-soil contact, coupled with an increased supply of P to the root, may decrease the value of root hairs for P acquisition in high-strength, high-P soils. Nevertheless, this work demonstrates that root hairs are a valuable trait for plant growth and nutrient acquisition under combined soil stresses. Selecting plants with superior root hair traits is important for improving P uptake efficiency and hence the sustainability of agricultural systems.

Matching roots to their environment.

BACKGROUND: Plants form the base of the terrestrial food chain and provide medicines, fuel, fibre and industrial materials to humans. Vascular land plants rely on their roots to acquire the water and mineral elements necessary for their survival in nature or their yield and nutritional quality in agriculture. Major biogeochemical fluxes of all elements occur through plant roots, and the roots of agricultural crops have a significant role to play in soil sustainability, carbon sequestration, reducing emissions of greenhouse gasses, and in preventing the eutrophication of water bodies associated with the application of mineral fertilizers. SCOPE: This article provides the context for a Special Issue of Annals of Botany on 'Matching Roots to Their Environment'. It first examines how land plants and their roots evolved, describes how the ecology of roots and their rhizospheres contributes to the acquisition of soil resources, and discusses the influence of plant roots on biogeochemical cycles. It then describes the role of roots in overcoming the constraints to crop production imposed by hostile or infertile soils, illustrates root phenotypes that improve the acquisition of mineral elements and water, and discusses high-throughput methods to screen for these traits in the laboratory, glasshouse and field. Finally, it considers whether knowledge of adaptations improving the acquisition of resources in natural environments can be used to develop root systems for sustainable agriculture in the future.

Extracellular release of a heterologous phytase from roots of transgenic plants: does manipulation of rhizosphere biochemistry impact microbial community structure?

To maintain the sustainability of agriculture, it is imperative that the reliance of crops on inorganic phosphorus (P) fertilizers is reduced. One approach is to improve the ability of crop plants to acquire P from organic sources. Transgenic plants that produce microbial phytases have been suggested as a possible means to achieve this goal. However, neither the impact of heterologous expression of phytase on the ecology of microorganisms in the rhizosphere nor the impact of rhizosphere microorganisms on the efficacy of phytases in the rhizosphere of transgenic plants has been tested. In this paper, we demonstrate that the presence of rhizosphere microorganisms reduced the dependence of plants on extracellular secretion of phytase from roots when grown in a P-deficient soil. Despite this, the expression of phytase in transgenic plants had little or no impact on the microbial community structure as compared with control plant lines, whereas soil treatments, such as the addition of inorganic P, had large effects. The results demonstrate that soil microorganisms are explicitly involved in the availability of P to plants and that the microbial community in the rhizosphere appears to be resistant to the impacts of single-gene changes in plants designed to alter rhizosphere biochemistry and nutrient cycling.