P. R. Darrah

The rhizosphere and plant nutrition: a quantitative approach

The role of the rhizosphere in relation to mineral nutrition is discussed within a quantitative framework using the Barber-Cushman model as a starting point. The uptake or release of nutrients by roots growing in soil leads to concentration gradients forming in the soil: the zone so affected is termed the rhizosphere. The nature of these gradients depends on three factors: the rate of uptake/release; the mobility of the nutrient in soil; and the rate of conversion between available and unavailable forms. The interplay between these factors determines the amount of mineral nutrients acquired by the plant and it is the complexity of the interplay which demands the use of mathematical models in order to understand which factors most limit uptake. Despite extensive experimental evidence of root-mediated changes to the physical, chemical and biological status of rhizosphere soil, the quantitative significance of these changes for mineral nutrition has not been assessed. The problems of making this quantitative transition are reviewed.

Models of the rhizosphere

A mathematical model has been developed which is capable of simulating the population dynamics of microbial biomass surrounding a root which is releasing soluble and insoluble carbon compounds into the soil. The model simulates the interconversions of C between different pools within the soil as well as the diffusion and mass flow of soluble carbon. Two main aspects of carbon release were examined: (i) a strategy where exudate was released uniformly over the root surface was compared to the case where exudation was confined to a small region behind the root tip; (ii) the situation in which all the C released was in soluble form was compared to the case of an approximately equal partition between soluble and insoluble forms. Substantial differences between the different simulations were found. It was shown that the maximum concentration and penetration of soluble exudates differed markedly between different simulations and the implications of this for micronutrient acquisition by phytosiderophores and for colonisation of the rhizosphere by root pathogens were discussed. The different simulations also predicted very different biomass distributions in the rhizosphere in both space and time.

Re-sorption of organic components by roots of Zea mays L. and its consequences in the rhizosphere

The re-sorption of carbon compounds from the rhizosphere was investigated using 14C-labelled glucose, mannose and citric acid. Uptake in roots of 5-day-old, intact Zea mays plants in sterile solution culture was determined over a period of 48 hours. Under optimal growth conditions significant re-absorption of glucose and mannose occurred with the uptake rates being 70.5 and 40.2 μg compound g-1 root DW h-1, respectively. For glucose and mannose approximately 25% of the 14C label taken up by the root was recovered inside the plant as low-MW compounds and 33% polymerized into high MW compounds. 42% was respired as 14C-CO2. Citric acid by comparison showed little accumulation within plant tissues (11.4%) with most being respired and recovered as 14C-CO2 in KOH traps (88%). The uptake rate for citric acid was 34.8 μg g-1 root DW h-1. Over the 48-hour period a net efflux (i.e. exudation) of labelled plus unlabelled C was observed at a rate of 608 μg C g-1 root DW h-1 (equivalent to 1520 μg glucose/mannose). Of the C released as root exudates, a minimum estimate of the amount of C taken back into the plant was therefore 9.5%. The two main C fluxes within the rhizosphere, namely release of C by the root and uptake by the microorganisms, have been well documented in recent years. It is now apparent however that a third flux term, re-sorption of C by roots, can also be identified. This may play an important but previously overlooked role within the rhizosphere, and further work is needed to determine its significance.A comparison between exudate release in static (permitting accumulation of C) and flowing culture (C removed as it is released) was also made with the respective rates being 15.36 and 45.18 mg C g-1 root DW in 2 days. The relative important of re-sorption in natural environments and laboratory experiments is discussed.

Role of proteinaceous amino acids released in root exudates in nutrient acquisition from the rhizosphere

The role of proteinaceous amino acids in rhizosphere nutrient mobilization was assessed both experimentally and theoretically. The degree of adsorption onto the soils solid phase was dependent on both the amino acid species and on soil properties. On addition of amino acids to both soil and freshly precipitated Fe(OH)3, no detectable mobilization of nutrients (K, Na, Ca, Mg, Cu, Mn, Zn, Fe, S, P, Si and Al) was observed, indicating a very low complexation ability of the acidic, neutral and basic amino acids. This was supported by results from a solution equilibria computer model which also predicted low levels of amino acid complexation with solutes present in the soil solution. On comparison with the Fe(OH)3 and equilibria data obtained for the organic acid, citrate, it was concluded that amino acids released into the rhizosphere have a limited role in the direct acquisition of nutrients by plants. The effectiveness of root exudates such as amino acids, phytosiderophores and organic acids in nutrient mobilization from the rhizosphere is discussed with reference to rhizosphere diffusion distances, microbial degradation, rate of complexation and the roots capacity to recapture exudate-metal complexes from the soil.

Biological solutions to transport network design

Transport networks are vital components of multicellular organisms, distributing nutrients and removing waste products. Animal and plant transport systems are branching trees whose architecture is linked to universal scaling laws in these organisms. In contrast, many fungi form reticulated mycelia via the branching and fusion of thread-like hyphae that continuously adapt to the environment. Fungal networks have evolved to explore and exploit a patchy environment, rather than ramify through a three-dimensional organism. However, there has been no explicit analysis of the network structures formed, their dynamic behaviour nor how either impact on their ecological function. Using the woodland saprotroph Phanerochaete velutina, we show that fungal networks can display both high transport capacity and robustness to damage. These properties are enhanced as the network grows, while the relative cost of building the network decreases. Thus, mycelia achieve the seemingly competing goals of efficient transport and robustness, with decreasing relative investment, by selective reinforcement and recycling of transport pathways. Fungal networks demonstrate that indeterminate, decentralized systems can yield highly adaptive networks. Understanding how these relatively simple organisms have found effective transport networks through a process of natural selection may inform the design of man-made networks.

Influx and efflux of Amino acids from Zea mays L. roots and their implications for N nutrition and the rhizosphere

The aim of the study was to investigate the ability of Zea mays L. roots to regulate the amount of free amino acids present in the rhizosphere. The active uptake of amino acids was shown to conform to Michaelis-Menten kinetics. Comparison of amino acid-N and NO3-N kinetic parameters and soil solution concentrations showed that root uptake of free amino acids from soil may contribute significantly to a plant’s N budget. The influx of amino acids also helps to minimize net C/N losses to the soil, and is therefore important in regulating the size of the rhizosphere microbial population. Experimental data and a computer simulation model of amino acid influx/efflux in a sterile solution culture, showed that roots were capable of re-sorping over 90 % of the amino acids previously lost into solution as a result of passive diffusion.

Fungi in Biogeochemical Cycles: The role of wood decay fungi in the carbon and nitrogen dynamics of the forest floor

decomposed amino acid that tracks the mycelial free amino acid pool. Its movement can be imaged by counting photon emissions from a scintillant screen in contact with the mycelial system. This method allows real-time imaging at high temporal and spatial resolution, for periods of weeks and areas up to 1 m 2 , in microcosms that mimic the mineral/organic soil interface of the forest floor. The results reveal a hitherto unsuspected dynamism and responsiveness in amino acid flows through mycelial networks of cord-forming, wood-decomposing basidiomycetes. We interpret these in the light of current understanding of the pivotal role of fungi in boreal and temperate forest floor nutrient cycling, and attempt to formulate key questions to investigate the effects of mycelial nitrogen translocation on forest floor decomposition and nitrogen absorption.

The vacuole system is a significant intracellular pathway for longitudinal solute transport in basidiomycete fungi.

ABSTRACT Mycelial fungi have a growth form which is unique among multicellular organisms. The data presented here suggest that they have developed a unique solution to internal solute translocation involving a complex, extended vacuole. In all filamentous fungi examined, this extended vacuole forms an interconnected network, dynamically linked by tubules, which has been hypothesized to act as an internal distribution system. We have tested this hypothesis directly by quantifying solute movement within the organelle by photobleaching a fluorescent vacuolar marker. Predictive simulation models were then used to determine the transport characteristics over extended length scales. This modeling showed that the vacuolar organelle forms a functionally important, bidirectional diffusive transport pathway over distances of millimeters to centimeters. Flux through the pathway is regulated by the dynamic tubular connections involving homotypic fusion and fission. There is also a strongly predicted interaction among vacuolar organization, predicted diffusion transport distances, and the architecture of the branching colony margin.

The effect of high solute concentrations on nitrification rates in soil

SummaryA short term nitrification assay (<18 h) was used to assess the effect of high concentrations of different solutes on the rate of nitrate production. High solute concentrations were found to inhibit nitrification and the degree of inhibition was related both to the osmotic pressure of the soil solution and the osmoticum used. Ammonium chloride, ammonium sulphate and sorbitol were used as sources of osmotic pressure. The results showed that, with ammonium salts, no inhibition was observed with pressures less than 2 atm. Above these values, the severity of the inhibition followed the order ammonium chloride>ammonium sulphate>sorbitol up to the maximum osmotic pressure studied (25 atm). With ammonium chloride, a pressure of 3.5 atm. was sufficient to cause a 90% inhibition of nitrification rate.The inhibition produced by mixtures of ammonium chloride and sorbitol, each mixture generating an osmotic pressure of 5 atm. in the assay, was also investigated. The results suggest that inhibition by Cl-ion is disproportionate to its contribution to the osmotic pressure of the soil solution.The recovery of the nitrification rate, following exposure to high osmotic pressure solutions, was also investigated. It was found that the recovery of the nitrification rate was only partial, with the extent of the recovery diminishing as the severity of the initial osmotic stress applied increased. These results suggest that both reversible and irreversible mechanisms are involved in the inhibition of nitrification.

Rhizodeposition under ambient and elevated CO2 levels

As global CO2 levels rise, can soils store more carbon and so buffer atmospheric CO2 levels? Answering this question requires a knowledge of the rates of C inputs to soil and of CO2 outputs via decomposition. Below-ground inputs from roots are a major component of the C flow into soils but are still poorly understood. In this article, new techniques for measuring rhizodeposition are reviewed and discussed and the need for cross-comparisons between methods is identified. One component of rhizodeposition, root exudation, is examined in more detail and evidence is presented which suggests that current estimates of exudate flow into soils are incorrect. A mechanistic mathematical model is used to explore how exudate flows might change under elevated CO2.