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Phosphorus (P) is essential for plant growth and productivity. It is one of the most limiting macronutrients in soil because it is mainly present as unavailable, bound P whereas plants can only use unbound, inorganic phosphate (Pi), which is found in very low concentrations in soil solution. Some ectomycorrhizal fungi are able to release organic compounds (organic anions or phosphatases) to mobilize unavailable P. Recent studies suggest that bacteria play a major role in the mineralization of nutrients such as P through trophic relationships as they can produce specific phosphatases such as phytases to degrade phytate, the main form of soil organic P. Bacteria are also more effective than other microorganisms or plants at immobilizing free Pi. Therefore, bacterial grazing by grazers, such as nematodes, could release Pi locked in bacterial biomass. Free Pi may be taken up by ectomycorrhizal fungus by specific phosphate transporters and transferred to the plant by mechanisms that have not yet been identified. This mini-review aims to follow the phosphate pathway to understand the ecological and molecular mechanisms responsible for transfer of phosphate from the soil to the plant, to improve plant P nutrition.

Nutrient homeostasis is essential for fungal cells and thus tightly adapted to the local demand in a mycelium with hyphal specialization. Based on selected ectomycorrhizal (ECM) fungal models, we outlined current concepts of nitrogen and phosphate nutrition and their limitations, and included knowledge from Baker's yeast when major gaps had to be filled. We covered the entire pathway from nutrient mobilization, import and local storage, distribution within the mycelium and export at the plant–fungus interface. Even when nutrient import and assimilation were broad issues for ECM fungi, we focused mainly on nitrate and organic phosphorus uptake, as other nitrogen/phosphorus (N/P) sources have been covered by recent reviews. Vacuolar N/P storage and mobilization represented another focus point of this review. Vacuoles are integrated into cellular homeostasis and central for an ECM mycelium at two locations: soil‐growing hyphae and hyphae of the plant–fungus interface. Vacuoles are also involved in long‐distance transport. We further discussed potential mechanisms of bidirectional long‐distance nutrient transport (distances from millimetres to metres). A final focus of the review was N/P export at the plant–fungus interface, where we compared potential efflux mechanisms and pathways, and discussed their prerequisites.

Background In the context of increasing global food demand, ecological intensification of agroecosystems is required to increase nutrient use efficiency in plants while decreasing fertilizer inputs. Better exploration and exploitation of soil resources is a major issue for phosphorus, given that rock phosphate ores are finite resources, which are going to be exhausted in decades from now on. Scope We review the processes governing the acquisition by plants of poorly mobile nutrients in soils, with a particular focus on processes at the root–soil interface. Rhizosphere processes are poorly accounted for in most plant nutrition models. This lack largely explains why present-day models fail at predicting the actual uptake of poorly mobile nutrients such as phosphorus under low input conditions. A first section is dedicated to biophysical processes and the spatial/temporal development of the rhizosphere. A second section concentrates on biochemical/biogeochemical processes, while a third section addresses biological/ecological processes operating in the rhizosphere. Conclusions New routes for improving soil nutrient efficiency are addressed, with a particular focus on breeding and ecological engineering options. Better mimicking natural ecosystems and exploiting plant diversity appears as an appealing way forward, on this long and winding road towards ecological intensification of agroecosystems.

Background & Aims Better understanding of belowground interactions in agroforestry systems is crucial for the success of plant co-existence. Beyond root competition, associated arbuscular mycorrhizal (AM) fungi can also be involved in plant to plant interactions. Thus far, the contribution of each agroforestry component (trees, herbaceous vegetation beneath trees -HVbT- and crops) in the establishment and maintenance of AM communities is poorly documented, particularly in temperate areas. This study investigates the spatio-temporal dynamics of both roots and AM fungi in two alley-cropping sites located in southwestern France. Methods Over a one-year period, (i) root length density, production and distribution, (ii) AM activity (root mycorrhization rate and extra-radical hyphal production) and (iii) AM diversity (metabarcoding) were assessed at different distances from tree rows in two agroforestry systems. Results The mycorrhization rate and hyphal production increased at the interface between tree rows and cultivated alleys, showing a positive effect of the presence of a perennial system (tree and HVbT) and of plant diversity. Compared to HVbT, tree roots colonized farther into superficial layers of the cultivated alleys. However, due to higher root densities and well-established AM fungi observed throughout all the year, HVbT appeared to be more relevant in maintaining an active source of AM inoculum for newly developing crop roots in winter. Conclusion The spatial proximity of roots and common AM fungi provides new perspectives in deciphering the significance of arbuscular mycorrhizal communities in crop nutrition and yield in agroforestry systems.

Through a mutualistic relationship with woody plant roots, ectomycorrhizal fungi provide growth-limiting nutrients, including inorganic phosphate (Pi), to their host. Reciprocal trades occur at the Hartig net, which is the symbiotic interface of ectomycorrhizas where the two partners are symplasmically isolated. Fungal Pi must be exported to the symbiotic interface, but the proteins facilitating this transfer are unknown. In the present study, we combined transcriptomic, microscopy, whole plant physiology, Xray fluorescence mapping, 32P labeling and fungal genetic approaches to unravel the role of HcPT2, a fungal Pi transporter, during the Hebeloma cylindrosporum–Pinus pinaster ectomycorrhizal association. We localized HcPT2 in the extra-radical hyphae and the Hartig net and demonstrated its determinant role for both the establishment of ectomycorrhizas and Pi allocation towards P. pinaster. We showed that the host plant induces HcPT2 expression and that the artificial overexpression of HcPT2 is sufficient to significantly enhance Pi export towards the central cylinder. Together, our results reveal that HcPT2 plays an important role in ectomycorrhizal symbiosis, affecting both Pi influx in the mycelium and efflux towards roots under the control of P. pinaster.

Plants grown at limited P supply can increase the activity of phosphatases in roots to hydrolyse organic-P compounds in the soil thus improving plant P acquisition, but little information is available about the role of these enzymes for internal plant metabolism at limited-P conditions. This work intended to measure the activities of acid phosphatases and phytases in nodules of common bean (Phaseolus vulgaris) genotypes at different levels of P supply. The experiment was carried out in a 5 x 5 factorial design with four replicates, comprising five bean genotypes and five P levels (20, 40, 80, 160 and 320 mu mol P plant(-1) week(-1)) in nutrient solution. Root seedlings were inoculated with Rhizobium tropici and plants were grown in 1-l bottles. Nodule samples were detached from 39-day-old plants and enzyme activities were determined in crude extracts. Plants were harvested at the stage of pod setting. Polynomial models fitted to data indicated maximal values at the level of 194 mu mol P for shoot mass, at 206 mu mol P for nodule mass and at 221 mu mol P for shoot N. Whereas shoot mass was 1.7 times lower at 20 than at 160 mu mol P, nodule mass was 7.5 times lower. Concentration of P in nodules increased from 40 to 320 mu mol P but remained stable between 20 and 40 mu mol P, suggesting a minimal threshold concentration of 3 mg P g(-1) for nodule growth. Activities of phosphatases and phytases in nodules decreased strongly as P supply was raised from 20 to 80 mu mol P, remaining almost stable at higher P levels. Phosphatase activity ranged from 1,154 to 406 nmol min(-1) g(-1) (nodule fresh mass) from 20 to 80 mu mol P respectively, while the phytase activity ranged from 55 to 14 nmol min(-1) g(-1) from 20 to 80 mu mol P. Bean genotypes differed in shoot and nodule mass at the levels of 80 and 160 mu mol P, whilst they differed in nodule enzyme activities only at the lowest P level, the relationship between nodule enzyme activities and growth of different bean genotypes was not evident. It is concluded that bean plants at P-deficient conditions increase the activities of phosphatases and phytases in nodules. This may constitute an adaptive mechanism for N-2-fixing legumes to tolerate P deficiency, by increasing the utilisation of the scarce P within the nodules

This review summarizes and discusses methodological approaches for studies on the impact of plant roots on the surrounding rhizosphere and for elucidation of the related mechanisms, covering a range from simple model experiments up to the field scale. A section on rhizosphere sampling describes tools and culture systems employed for analysis of root growth, root morphology, vitality testing and for monitoring of root activity with respect to nutrient uptake, water, ion and carbon flows in the rhizosphere. The second section on rhizosphere probing covers techniques to detect physicochemical changes in the rhizosphere as a consequence of root activity. This comprises compartment systems to obtain rhizosphere samples, visualisation techniques, reporter gene approaches and remote sensing technologies for monitoring the conditions in the rhizosphere. Approaches for the experimental manipulation of the rhizosphere by use of molecular and genetic methods as tools to study rhizosphere processes are discussed in a third section. Finally it is concluded that in spite of a wide array of methodological approaches developed in the recent past for studying processes and interactions in the rhizosphere mainly under simplified conditions in model experiments, there is still an obvious lack of methods to test the relevance of these findings under real field conditions or even on the scale of ecosystems. This also limits reliable data input and validation in current rhizosphere modelling approaches. Possible interactions between different environmental factors or plant-microbial interactions (e.g. mycorrhizae) are frequently not considered in model experiments. Moreover, most of the available knowledge arises from investigations with a very limited number of plant species, mainly crops and studies considering also intraspecific genotypic differences or the variability within wild plant species are just emerging.

Plants evolve complex interactions with diverse soil mutualist organisms to enhance P mobilization from the soil. These strategies are particularly important when P is poorly available. It is still unclear how the soil P source (e.g., mineral P versus recalcitrant organic P) and its mobility in the soil (high or low) affect soil mutualist biological (ectomycorrhizal fungi, bacteria and bacterial-feeding nematodes) richness—plant P acquisition relationships. Using a set of six microcosm experiments conducted in growth chamber across contrasting P situations, we tested the hypothesis that the relationship between the increasing addition of soil mutualist organisms in the rhizosphere of the plant and plant P acquisition depends on P source and mobility. The highest correlation (R2 = 0.70) between plant P acquisition with soil rhizosphere biological richness was found in a high P-sorbing soil amended with an organic P source. In the five other situations, the relationships became significant either in soil conditions, with or without mineral P addition, or when the P source was supplied as organic P in the absence of soil, although with a low correlation coefficient (0.09 < R2 < 0.15). We thus encourage the systematic and careful consideration of the form and mobility of P in the experimental trials that aim to assess the role of biological complexity on plant P nutrition.

Background and aims Phosphorus from phytate, although constituting the main proportion of organic soil P, is unavailable to plants. Despite the well-known effects of rhizosphere trophic relationships on N mineralization, no work has been done yet on P mineralization. We hypothesized that the interactions between phytate-mineralizing bacteria, mycorrhizal fungi and bacterial grazer nematodes are able to improve plant P use from phytate. Methods We tested this hypothesis by growing Pinus pinaster seedlings in agar containing phytate as P source. The plants, whether or not ectomycorrhizal with the basidiomycete Hebeloma cylindrosporum, were grown alone or with a phytase-producing bacteria Bacillus subtilis and two bacterial-feeder nematodes, Rhabditis sp. and Acrobeloides sp. The bacteria and the nematodes were isolated from ectomycorrhizal roots and soil from P. pinaster plantations. Results Only the grazing of bacteria by nematodes enhanced plant P accumulation. Although plants increased the density of phytase-producing bacteria, these bacteria alone did not improve plant P nutrition. The seedlings, whether ectomycorrhizal or not, displayed a low capacity to use P from phytate. Conclusions In this experiment, the bacteria locked up the phosphorus, which was delivered to plant only by bacterial grazers like nematodes. Our results open an alternative route for better utilization of poorly available organic P by plants.