Root exudates as mediators of mineral acquisition in low-nutrient environments

Plant developmental processes are controlled by internal signals that depend on the adequate supply of mineral nutrients by soil to roots. Thus, the availability of nutrient elements can be a major constraint to plant growth in many environments of the world, especially the tropics where soils are extremely low in nutrients. Plants take up most mineral nutrients through the rhizosphere where micro-organisms interact with plant products in root exudates. Plant root exudates consist of a complex mixture of organic acid anions, phytosiderophores, sugars, vitamins, amino acids, purines, nucleosides, inorganic ions (e.g. HCO₃ ^–, OH^–, H⁺), gaseous molecules (CO₂, H₂), enzymes and root border cells which have major direct or indirect effects on the acquisition of mineral nutrients required for plant growth. Phenolics and aldonic acids exuded directly by roots of N₂-fixing legumes serve as major signals to Rhizobiaceae bacteria which form root nodules where N₂ is reduced to ammonia. Some of the same compounds affect development of mycorrhizal fungi that are crucial for phosphate uptake. Plants growing in low-nutrient environments also employ root exudates in ways other than as symbiotic signals to soil microbes involved in nutrient procurement. Extracellular enzymes release P from organic compounds, and several types of molecules increase iron availability through chelation. Organic acids from root exudates can solubilize unavailable soil Ca, Fe and Al phosphates. Plants growing on nitrate generally maintain electronic neutrality by releasing an excess of anions, including hydroxyl ions. Legumes, which can grow well without nitrate through the benefits of N₂ reduction in the root nodules, must release a net excess of protons. These protons can markedly lower rhizosphere pH and decrease the availability of some mineral nutrients as well as the effective functioning of some soil bacteria, such as the rhizobial bacteria themselves. Thus, environments which are naturally very acidic can pose a challenge to nutrient acquisition by plant roots, and threaten the survival of many beneficial microbes including the roots themselves. A few plants such as Rooibos tea (Aspalathus linearis L.) actively modify their rhizosphere pH by extruding OH^– and HCO₃ ^– to facilitate growth in low pH soils (pH 3 – 5). Our current understanding of how plants use root exudates to modify rhizosphere pH and the potential benefits associated with such processes are assessed in this review.     

Tolerance and avoidance of Al toxicity by Mucuna pruriens var. utilis at different levels of P supply

Previous laboratory experiments showed that velvet bean Mucuna pruriens is moderately tolerant to the presence of Al (up to 185 µM) in the root environment, but that it only develops a shallow root system in acid soils. Field experiments showed that Mucuna can tolerate acid subsoil conditions in a homogeneous root environment, but avoids subsoil if topsoil is present. Subsequent split-root experiments with a recirculating nutrient solution showed that this subsoil avoidance may be based on an Al avoidance mechanism in the root system. This Al avoidance mechanism, however, was not evident when phosphorus (P) supply to the whole plant was adequate. We thus hypothesized that surface application of P may help to overcome Al avoidance in the subsoil.In a field experiment on an ultisol in Lampung (Indonesia), only a moderate increase in aboveground biomass production was found for a wide range of P application rates, although the soil was low in available P, and the P adsorption isotherm was very steep. An increased P status of the topsoil and an increased P concentration in the aboveground biomass (from 50 to 75 mmol kg^-1) had no effect on root development in the subsoil.     

Al avoidance and Al tolerance ofMucuna pruriens var.utilis: Effects of a heterogeneous root environment and the nitrogen form in the root environment

InMucuna pruriens var.utilis, grown with nitrate-N in a hydroponic split-root system, an Al avoidance reaction of root growth was observed, which was ascribed to local P stress in the Al containing compartment. The Al avoidance reaction was similar to the avoidance ofMucuna roots of acid subsoil in the field where roots grew preferentially in the topsoil. In the present paper the effect of different N forms (NO₃ ^– and NH₄ ⁺) on the reactions ofMucuna to Al were studied, since in acid soils N is present as a mixture of NO₃ ^– and NH₄ ⁺. No interaction between the N form and Al toxicity was found. A hydroponic split-root experiment with NH₄NO₃ nutrition, which is comparable to the situation in the field, showed that under these conditions Al avoidance did not occur. It is concluded that a relation between the Al avoidance reaction ofMucuna and P stress is still likely.Abbreviations D_r root diameter - L_pr total root length per plant - L_rw specific root length - NRA nitrate reductase activity - S/R shoot: root ratio     

Plant induced alteration in the rhizosphere and the utilisation of soil heterogeneity

Plant-soil interactions result in a special rhizosphere soil chemistry, differing from that of the bulk soil found only a few mm from the root. The aim of this study was to investigate adaptation mechanisms of herbs growing in acid soils through studying their rhizosphere chemistry in a greenhouse experiment and in a field study. Ten herbs were grown in acid soil (pH 4.2 in the soil solution) in the greenhouse. The concentrations of NO₃ ^-, SO₄ ^2-, phosphates, Ca²⁺, Mg²⁺, Mn²⁺, K⁺, Na⁺, NH₄ ⁺ and pH were analysed in soil solutions obtained by centrifugation. The general pattern found was a depletion of nutrients in the rhizosphere compared with their concentrations in the bulk soil. The pH increase (up to 0.7 units) in the rhizosphere soil appeared to be caused by plant uptake of NO₃ ^- (r²=0.88). The ion concentrations in the soil solution of the rhizosphere were dependent on plant species and biomass increase. Although species with a larger biomass and higher growth rates showed a higher degree of ion depletion (except for Na⁺, SO₄ ^2-) in the rhizosphere, there were also species specific responses. A field study of five herbs at five oak forest sites in Southern Sweden (Scania) was also carried out. In addition to the soil solution concentrations, the loss on ignition (LOI) and the concentrations of 0.1 M BaCl₂ extractable K⁺, Mg²⁺, Mn²⁺, Ca²⁺, and Al ions were measured. The amount of soil solution Al was determined as free ionic (quickly reacting) Al. For all species and sites, the LOI and the concentrations of exchangeable cations were higher in the rhizosphere than in the bulk soil, apparently due to the roots preferably growing at organic-rich microsites. The concentrations of the ions as measured in the centrifuged soil solution, were either higher in the rhizosphere than in the bulk soil or were the same in both, except for NO₃ ^- and quickly reacting Al. The lower concentrations of quickly reacting Al in the rhizosphere, compared with the bulk soil could indicate the uptake of Al by the plant or the exudation of complexing substances. The pH differences were only small and mostly non-significant. Plant-soil interactions and the ability of plants to utilise heterogeneity of the soil appear to be more important for plant growth in acid soils than recognised heretofore. Rhizosphere studies provide an important means of understanding plant strategies in acid soils. This revised version was published online in June 2006 with corrections to the Cover Date.     

Root-induced increases in soil pH and nutrient availability to field-grown cereals and legumes on acid sandy soils of Sudano-Sahelian West Africa

A field experiment with millet (Pennisetum glaucum L.), sorghum [Sorghum bicolor (L.) Moench], cowpea (Vigna unguiculata L.) and groundnut (Arachnis hypogeae L.) was conducted on severely P-deficient acid sandy soils of Niger, Mali and Burkina Faso to measure changes in pH and nutrient availability as affected by distance from the root surface and by mineral fertiliser application. Treatments included three rates of phosphorus (P) and four levels of nitrogen (N) application. Bulk, rhizosphere and rhizoplane soils were sampled at 35, 45 and 75 DAS in 1997 and at 55 and 65 DAS in 1998. Regardless of the cropping system and level of mineral fertiliser applied, soil pH consistently increased between 0.7 and two units from the bulk soil to the rhizoplane of millet. Similar pH gradients were observed in cowpea, but pH changes were much smaller in sorghum with a difference of only 0.3 units. Shifts in pH led to large increases in nutrient availability close to the roots. Compared with the bulk soil, available P in the rhizoplane was between 190 and 270% higher for P-Bray and between 360 and 600% higher for P-water. Exchangeable calcium (Ca) and magnesium (Mg) levels were also higher in the millet rhizoplane than in the bulk soil, whereas exchangeable aluminium (Al) levels decreased with increasing pH close to the root surface. The results suggest an important role of root-induced pH increases for crops to cope with acidity-induced nutrient deficiency and Al stress of soils in the Sudano-Sahelian zone of West Africa. This revised version was published online in June 2006 with corrections to the Cover Date.     

Effect of nitrogen form and phosphorus source on the growth,nutrient uptake and rhizosphere soil property of Camellia sinensis L.

The effects of nitrogen form and phosphorus source on the growth, nutrient uptake and rhizosphere soil property of tea (Camellia sinensis L.) were investigated in a pot experiment. The experiment was performed with a compartmental cropping device, which enables the collection of rhizosphere soil at defined distances from the root of tea plant. Nitrogen was supplied as nitrate or ammonium in combination with soluble phosphorus as Ca(H₂PO₄)₂ or insoluble P as rock phosphate. The leaf dry matter production of tea was significantly greater in the treatments with NH₄ ⁺ than NO₃ ^-, whereas dry matter production of root and stem was not significantly affected. Addition of phosphorus as either source did not influence the dry matter production. The concentrations of K in root, Mg and Ca in both the shoot and root supplied with NO₃ ^- were significantly higher than in NH₄ ⁺ and influence of P sources was minor. On the contrary, Al and Mn concentrations were significantly larger in NH₄ ^--fed plants which could be attributed to remarkably increased availability of Al and Mn caused by acidification of the rhizosphere soil (the first 1-mm soil section from the root surface) with NH₄–N nutrition. The concentration of N in shoot was also significantly higher in NH₄- than in NO₃-fed plants, indicating higher use efficiency of NH₄–N. Whatever the phosphate source, rhizosphere pH declined in ammonium compared to in nitrate treatment. The pH decrease was much larger when no P or soluble P were applied and reached 0.85–1.30 units which extended to 3–5 mm away from the root surface. Exchangeable acidity, content of exchangeable Al and Mn were also considerably higher in the rhizosphere soils of NH₄ ⁺ fed tea plants. Significant amounts of P dissolved from rock phosphate accumulated in rhizosphere of NH₄ ⁺, not NO₃ ^-, suggesting that the dissolution of rock phosphate was induced by the proton excreted by tea root fed with ammonium. With soluble P addition, shoot and root P concentrations were greater in NH₄ ⁺ than in NO₃ ^- treatment and it appeared that this difference could not be sufficiently explained by the available P content in soil which was only slightly higher in NH₄ ⁺ treatment. With rock phosphate addition, the shoot and root P concentrations were hardly affected by nitrogen form, although the available P content was much higher and accumulated in the rhizosphere soil supplied with ammonium. The reason for this was discussed with regard to the inter-relationship of Al with P uptake. This revised version was published online in June 2006 with corrections to the Cover Date.     

Aluminium is essential for root growth and development of tea plants (Camellia sinensis)

On acid soils, the trivalent aluminium ion (Al³⁺) predominates and is very rhizotoxic to most plant species. For some native plant species adapted to acid soils including tea (Camellia sinensis), Al³⁺ has been regarded as a beneficial mineral element. In this study, we discovered that Al³⁺ is actually essential for tea root growth and development in all the tested varieties. Aluminum ion promoted new root growth in five representative tea varieties with dose‐dependent responses to Al³⁺ availability. In the absence of Al³⁺, the tea plants failed to generate new roots, and the root tips were damaged within 1 d of Al deprivation. Structural analysis of root tips demonstrated that Al was required for root meristem development and activity. In situ morin staining of Al³⁺ in roots revealed that Al mainly localized to nuclei in root meristem cells, but then gradually moved to the cytosol when Al³⁺ was subsequently withdrawn. This movement of Al³⁺ from nuclei to cytosols was accompanied by exacerbated DNA damage, which suggests that the nuclear‐targeted Al primarily acts to maintain DNA integrity. Taken together, these results provide novel evidence that Al³⁺ is essential for root growth in tea plants through maintenance of DNA integrity in meristematic cells.     

The Carbon Cost of Protecting the Root Apex from Soil Acidity: A Theoretical Framework

There is an assumption in much recent literature that secreted organic anions (OAs) protect the root meristem from Al toxicity by complexation of Al ions. In fact, several possible mechanisms exist by which common OA might afford some degree of protection. Plants can excrete OA which undergo chemical association with protons (hereafter referred to as protonation) in the soil and increase rhizosphere pH. The cost in reduced carbon relative to protons consumed, C:H⁺, ranges from 2–6. The efficiency of this mechanism can be enhanced in the presence of soil organisms which can oxidise the OA that remain dissociated at soil pH to CO₂ and H₂O, thereby consuming protons which associate with lower pK functional groups (pK 1.2 to ~ 4). For fully dissociated organic acids the C:H⁺ ratio decreases to the range 1–3. The C cost to plants is further minimised if MnO₂ is the terminal electron acceptor rather than O₂, resulting in C:H⁺<1. OA might also complex or chelate Al. Complexes of Al³⁺ with oxalate appear to be effective, with some C:H⁺≤1. However, citrate complexation appears to be more stable in pure solutions and might offer the additional benefit of enhanced P acquisition. Our assessment is that the most efficient strategy for a plant to employ to protect itself from Al toxicity is to increase pH near the root apex by secreting OA into soil where the microbial oxidation of reduced C could be coupled with the reduction of MnO₂. This would consume 0.2–0.67 mole of C per H⁺, which is the order of magnitude better than the C:H⁺ ratio of 2–6 that would occur if only protonation of OA was to be relied upon. These mechanisms have implications for the effectiveness of programs aimed at selecting cultivars for resistance to acidic soils.