Exudation Of Organic Acid Anions Research Articles

Dissecting the Roles of Phosphorus Use Efficiency, Organic Acid Anions, and Aluminum-Responsive Genes under Aluminum Toxicity and Phosphorus Deficiency in Ryegrass Plants.

Aluminum (Al) toxicity and phosphorus (P) deficiency are widely recognized as major constraints to agricultural productivity in acidic soils. Under this scenario, the development of ryegrass plants with enhanced P use efficiency and Al resistance is a promising approach by which to maintain pasture production. In this study, we assessed the contribution of growth traits, P efficiency, organic acid anion (OA) exudation, and the expression of Al-responsive genes in improving tolerance to concurrent low-P and Al stress in ryegrass (Lolium perenne L.). Ryegrass plants were hydroponically grown under optimal (0.1 mM) or low-P (0.01 mM) conditions for 21 days, and further supplied with Al (0 and 0.2 mM) for 3 h, 24 h and 7 days. Accordingly, higher Al accumulation in the roots and lower Al translocation to the shoots were found in ryegrass exposed to both stresses. Aluminum toxicity and P limitation did not change the OA exudation pattern exhibited by roots. However, an improvement in the root growth traits and P accumulation was found, suggesting an enhancement in Al tolerance and P efficiency under combined Al and low-P stress. Al-responsive genes were highly upregulated by Al stress and P limitation, and also closely related to P utilization efficiency. Overall, our results provide evidence of the specific strategies used by ryegrass to co-adapt to multiple stresses in acid soils.

Root exudation of organic acid anions and recruitment of beneficial actinobacteria facilitate phosphorus uptake by maize in compacted silt loam soil

Soil compaction restricts root growth and plant nutrient uptake, but the effects on the abundance and diversity of soil microbiome are poorly understood. A field study with maize (Zea mays L.) was conducted with two soil-compaction treatments (NC: non-compacted; C: compacted) to investigate the interactions of root exudates and microorganisms and the effect on P uptake at two growth stages (seedling and flowering). At the seedling stage, shoot P concentration was decreased by 13.7% in the C treatment compared with the NC. Root growth and arbuscular mycorrhizal fungi colonization were reduced probably due to the decreased soil porosity after compaction. However, root organic acid anions (OAAs) levels were increased by 170%. Several genera of actinobacteria were specifically enriched in the rhizosphere and their abundance was significantly correlated with the concentration of OAAs. However, the positive correlations of concentration of OAAs and abundance of microorganisms or plant P uptake were not observed at flowering stage. Our results indicated that besides the well-known function of exuded organic acid anions on soil P mobilization, maize might also select for microorganisms associated with the facilitation of P acquisition, and mitigating P deficiency at the early growth stage of the plant in compacted soil.

From stress to responses: aluminium-induced signalling in the root apex.

Aluminium (Al) toxicity is one of the major constraints for crop growth and productivity in most of the acid soils worldwide. The primary lesion of Al toxicity is the rapid inhibition of root elongation. The root apex, especially the transition zone (TZ), has been identified as the major site of Al accumulation and injury. The signalling, in particular through phytohormones in the root apex TZ in response to Al stress, has been reported to play crucial roles in the regulation of Al-induced root growth inhibition. The binding of Al in the root apoplast is the initial event leading to inhibition of root elongation. Much progress has been made during recent years in understanding the molecular functions of cell wall modification and Al resistance-related genes in Al resistance or toxicity, and several signals including phytohormones, Ca2+, etc. have been reported to be involved in these processes. Here we summarize the recent advances in the understanding of Al-induced signalling and regulatory networks in the root apex involved in the regulation of Al-induced inhibition of root growth and Al toxicity/resistance. This knowledge provides novel insights into how Al-induced signals are recognized by root apical cells, transmitted from the apoplast to symplast, and finally initiate the defence system against Al. We conclude that the apoplast plays a decisive role in sensing and transmitting the Al-induced signals into the symplast, further stimulating a series of cellular responses (e.g. exudation of organic acid anions from roots) to adapt to the stress. We expect to stimulate new research by focusing on the signalling events in the root apex in response to Al stress, particularly taking into consideration the signal transduction between the meristem zone, TZ, and elongation zone and the apoplast and symplast.

Elevated pH-mediated mitigation of aluminum-toxicity in sweet orange (Citrus sinensis) roots involved the regulation of energy-rich compounds and phytohormones

For the first time, we used targeted metabolome to investigate the effects of pH-aluminum (Al) interactions on energy-rich compounds and their metabolites (ECMs) and phytohormones in sweet orange (Citrus sinensis) roots. The concentration of total ECMs (TECMs) was reduced by Al-toxicity in 4.0-treated roots, but unaffected significantly in pH 3.0-treated roots. However, the concentrations of most ECMs and TECMs were not lower in pH 4.0 + 1.0 mM Al-treated roots (P4AR) than in pH 3.0 + 1.0 mM Al-treated roots (P3AR). Increased pH improved the adaptability of ECMs to Al-toxicity in roots. For example, increased pH improved the utilization efficiency of ECMs and the conversion of organic phosphorus (P) from P-containing ECMs into available phosphate in Al-treated roots. We identified upregulated cytokinins (CKs), downregulated jasmonic acid (JA), methyl jasmonate (MEJA) and jasmonates (JAs), and unaltered indole-3-acetic acid (IAA) and salicylic acid (SA) in P3AR vs pH 3.0 + 0 mM Al-treated roots (P3R); upregulated JA, JAs and IAA, downregulated total CKs, and unaltered MEJA and SA in P4AR vs pH 4.0 + 0 mM Al-treated roots (P4R); and upregulated CKs, downregulated JA, MEJA, JAs and SA, and unaltered IAA in P3AR vs P4AR. Generally viewed, raised pH-mediated increments of JA, MEJA, total JAs, SA and IAA concentrations and reduction of CKs concentration in Al-treated roots might help to maintain nutrient homeostasis, increase Al-toxicity-induced exudation of organic acid anions and the compartmentation of Al in vacuole, and reduce oxidative stress and Al uptake, thereby conferring root Al-tolerance. In short, elevated pH-mediated mitigation of root Al-stress involved the regulation of ECMs and phytohormones.

Applying foliar magnesium enhances wheat growth in acidic soil by stimulating exudation of malate and citrate

Aluminium toxicity in acidic soils adversely affects wheat growth. Foliar-applied magnesium (Mg) contributes to mitigating soil acidity stress in wheat, but the mechanisms are unknown. This study explored the mechanism of foliar-Mg mediated enhancement of wheat growth in acidic soil. Two contrasting near-isogenic wheat (Triticum aestivum L.) genotypes differing in Al resistance (Al-sensitive ES8 and Al-resistant ET8) were grown to the vegetative stage (Zadoks 24) in a reconstituted acidic soil (pH0.1 M CaCl2 4.0) profile with three rates of foliar Mg (0, 200 and 500 mg Mg L− 1 using MgSO4.7H2O). Magnesium was applied to the foliage twice [14 and 28 days after sowing (DAS)], and plant growth and root exuded carboxylates were measured up to 42 DAS. Applying 200 mg Mg L− 1 to the foliage increased organic acid anion exudation from wheat roots by ~ 2-fold compared to 0 foliar Mg treated plants. The Al-resistant wheat genotype exuded 1.3-fold more malate and citrate from roots than the Al-sensitive genotype in the absence of foliar Mg. Malate exudation was delayed relative to citrate following foliar Mg application. The foliar-applied Mg increased shoot and root dry weight (by ~ 38 %), total root length (by ~ 33 %) and intrinsic water-use efficiency (by ~ 80 %) compared to plants treated with no Mg. Applying foliar Mg decreased soil acidity stress (as shown by a significant increase in chlorophyll fluorescence Fv/Fm ratio) in wheat compared to 0 foliar Mg. Increased malate and citrate exudation is the underlying mechanism of enhanced wheat growth following foliar Mg application under acidic soil conditions.

Metabolomic analyses of highbush blueberry (Vaccinium corymbosum L.) cultivars revealed mechanisms of resistance to aluminum toxicity

Aluminum (Al) is an important factor that limits plant growth under acidic soil conditions. However, several plant species developed distinct mechanisms that limit the damage caused by high Al concentrations. In highbush blueberry (Vaccinium corymbosum), the Al resistance mechanisms are not fully understood. This study was designed to evaluate the effect of Al toxicity on roots and leaves of highbush blueberry genotypes with contrasting Al resistance [Star (Al-sensitive) and Camellia and Cargo (Al-resistant)] and identify the main molecular and physiological strategies underpinning adaptive Al stress responses in nutrient solution. After 48 h of Al treatment, the reduced form of ascorbate (ASC) was higher in roots, but unchanged in leaves of Cargo and Camellia genotypes compared to the control. We also observed decreased root exudation of oxalate in the Al-treated sensitive cultivar Star throughout the treatment period. However, in the resistant cultivar (Camellia), the exudation of oxalate increased 2.4- and 2.8-fold at 24 and 48 h, respectively. Al treatment differentially affected the enzyme activity and gene expression of the tricarboxylic acid (TCA) cycle enzymes. NAD-dependent malate dehydrogenase (NAD-MDH) expression in roots of cultivar Cargo was reduced at 24 h and increased at 48 h, whereas in leaves the expression was higher at 24 h and decreased at 48 h compared to the control. Citrate synthase (CS) activity in Al-resistant Cargo roots diminished at 24 h, increasing afterwards, without variation in the CS gene expression, compared with the initial time point (t = 0). In Al-resistant Camellia roots, the gene expression and the activity of CS decreased during Al exposure. NADP-dependent malate dehydrogenase (NADP-MDH) activity showed increased activity and gene expression at 24 h, in the leaves of cultivar Cargo, whereas in roots the gene expression decreased, but the activation state of NADP-MDH increased. The expression of genes encoding TCA cycle enzymes did not differ significantly in the Al-sensitive cultivar Star during Al exposure. In conclusion, the exudation of organic acid anions, particularly oxalate, plays an important role in Al resistance of highbush blueberry genotypes whilst elevated levels of ASC in roots, also contribute to the Al-resistance mechanisms exhibited by genotypes Camellia and Cargo.

Feremycorrhizal symbiosis confers growth and nutritional benefits to mycorrhizal and non-mycorrhizal crops

Feremycorrhiza (FM) is a newly discovered plant-fungus symbiosis that improves plant growth and nutrition without development of interface structures (i.e. no root colonization). The host plant range in the FM symbiosis is currently unknown. We report the results of controlled environment investigations characterizing the capability of crops to establish FM symbiosis with Austroboletus occidentalis, along with comprehensive in vitro studies to unravel the functional mechanisms underlying the phosphorus (P) nutritional benefits conferred to host plants. After 16 weeks of growth in a natural low-nutrient field soil (containing indigenous microbes), two mycorrhizal crops [wheat (Triticum aestivum) and barley (Hordeum vulgare)], and the non-mycorrhizal crop canola (Brassica napus) inoculated with A. occidentalis had significantly higher shoot biomass compared to the control (non-inoculated) plants. The FM symbiosis also led to significant grain yield increases in wheat (by 54%) and barley (by 37%) compared to the control plants, while canola was harvested before setting seeds due to slow growth under nutrient deficiency. In all crops, the FM symbiosis significantly improved the shoot nutrient content, including that of P, potassium and magnesium. Total nitrogen accumulation (shoot + grain content) was also significantly higher in all inoculated vs control crops. Inoculated treatments had reduced soil pH compared to the control, which was attributed to fungal activities in soil, leading to greater nutrient (P, in particular) availability to host plants. Presence of A. occidentalis in soil did not affect root colonization by indigenous arbuscular mycorrhizal fungi in wheat and barley, and no root colonization was detected in canola. Our in vitro studies demonstrated the solubilization, by A. occidentalis, of the water-insoluble P forms, including calcium phosphate (CaP, as hydroxyapatite), iron phosphate (FePO4), and aluminium phosphate (AlPO4) via exudation of organic acid anions (mainly oxalate, along with citrate and fumarate). The 31P nuclear magnetic resonance (NMR) spectroscopy revealed the presence of similar P species (dominated by orthophosphate and long-chain inorganic polyphosphates) in the agar-based media supplemented with different P forms (KH2PO4, CaP, FePO4 or AlPO4), indicating that all three water-insoluble P compounds were solubilized and transformed by the FM fungus. Furthermore, our in vitro studies revealed that the FM fungus converted a large proportion of the solubilized P (free orthophosphate) into long-chain inorganic polyphosphates (making up to 51% of total P in the media). The results demonstrated that the three important grain crops, regardless of their capacity to support arbuscular mycorrhizae, could get the growth and nutritional benefits from the FM symbiosis, emphasizing the potential of A. occidentalis as a novel fungal biofertilizer for agricultural crops.

Exudation of organic acid anions by tropical grasses in response to low phosphorus availability

It has been suggested that some tropical grasses can acquire phosphorus (P) from hematite and gypsite by exuding organic acid anions (OAs). However, it remains to be determined exactly which OAs could be involved in each case. The objective of this study was to verify the exudation OAs by ruzigrass (Urochloa ruziziensis), palisade grass (U. brizantha), and Guinea grass (Megathyrsus maximus) as a response to P deficiency. The grasses were grown in leachate columns with adequate and deficient P nutrient solutions. The concentration of OAs in the leacheate and root surface, as well as shoot and root dry matter, and P uptake were determined. Citrate, isocitrate, and malate concentration in leachates and root surfaces increased with P starvation, mainly for the Urochloa grasses. Oxalate exudation was similar for the grasses under adequate P supply, but was lower in Guinea grass under P starvation. Palisade grass showed a higher concentration of total OAs in the root surface than the other species due to a great production of oxalate and isocitrate. Palisade grass showed greater dry matter yields regardless of P deficiency, and Guinea grass always had the higher shoot:root ratio. Urochloa grasses have a higher capacity to cope with low P availability by exuding OAs along with a lower shoot:root ratio than Guinea grass.

Aluminum exclusion from root zone and maintenance of nutrient uptake are principal mechanisms of Al tolerance in Pisum sativum L.

Our study aimed to evaluate intraspecific variability of pea (Pisum sativum L.) in Al tolerance and to reveal mechanisms underlying genotypic differences in this trait. At the first stage, 106 pea genotypes were screened for Al tolerance using root re-elongation assay based on staining with eriochrome cyanine R. The root re-elongation zone varied from 0.5mm to 14mm and relationships between Al tolerance and provenance or phenotypic traits of genotypes were found. Tolerance index (TI), calculated as a biomass ratio of Al-treated and non-treated contrasting genotypes grown in hydroponics for 10days, varied from 30% to 92% for roots and from 38% to 90% for shoots. TI did not correlate with root or shoot Al content, but correlated positively with increasing pH and negatively with residual Al concentration in nutrient solution in the end of experiments. Root exudation of organic acid anions (mostly acetate, citrate, lactate, pyroglutamate, pyruvate and succinate) significantly increased in several Al-treated genotypes, but did not correlate with TI. Al-treatment decreased Ca, Co, Cu, K, Mg, Mn, Mo, Ni, S and Zn contents in roots and/or shoots, whereas contents of several elements (P, B, Fe and Mo in roots and B and Fe in shoots) increased, suggesting that Al toxicity induced substantial disturbances in uptake and translocation of nutrients. Nutritional disturbances were more pronounced in Al sensitive genotypes. In conclusion, pea has a high intraspecific variability in Al tolerance and this trait is associated with provenance and phenotypic properties of plants. Transformation of Al to unavailable (insoluble) forms in the root zone and the ability to maintain nutrient uptake are considered to be important mechanisms of Al tolerance in this plant species.

Aluminum-tolerant bacteria improve the plant growth and phosphorus content in ryegrass grown in a volcanic soil amended with cattle dung manure

In Chilean volcanic soil, crop production often is limited by a combination of the low available P and high concentration of toxic aluminum (Al). In this study we aimed to isolate Al-tolerant plant-growth-promoting bacteria from the rhizosphere and the endosphere of ryegrass grown in acidic Chilean volcanic soil in order to characterize a bacterial consortium capable of contributing to alleviation of Al3+ toxicity and supporting plant growth in Andisol. Five strains, i.e. Klebsiella sp. RC3, Stenotrophomonas sp. RC5, Klebsiella sp. RCJ4, Serratia sp. RCJ6 and Enterobacter sp. RJAL6, were selected based on their capacity to tolerate high Al concentration (10mM) and to exhibit multiple plant-growth-promoting traits (P solubilization, indole acetic acid production, 1-aminocyclopropane-1-carboxylate deaminase activity, and exudation of organic acid anions and siderophores). Based on the results, we can suggest that selected bacteria could alleviate Al stress by forming Al3+-siderophore complexes. The plant-growth-promoting potential of the bacterial consortium was confirmed in an assay with ryegrass plants. In the treatment with cattle dung manure, the consortium promoted plant growth and the phosphatase activity in the rhizosphere soil. Increased phosphatase activity coincided with elevated P concentration in shoots. Our results suggest that a combination of native Al-tolerant bacteria and cattle dung manure is effective in decreasing Al toxicity and promoting plant growth in Andisols of southern Chile.

Melatonin alleviates aluminium toxicity through modulating antioxidative enzymes and enhancing organic acid anion exudation in soybean.

Aluminium (Al) toxicity is a major chemical constraint limiting plant growth and production on acidic soils. Melatonin (N-acetyl-5-methoxytryptamine) is a ubiquitous molecule that plays crucial roles in plant growth and stress tolerance. However, there is no knowledge regarding whether melatonin is involved in plant responses to Al stress. Here, we show that optimal concentrations of melatonin could effectively ameliorate Al-induced phytotoxicity in soybean (Glycine max L.). The concentration of melatonin in roots was significantly increased by the 50μM Al treatment. Such an increase in endogenous melatonin coincided with the upregulation of the gene encoding acetyltransferase NSI-like (nuclear shuttle protein-interacting) in soybean roots. Supplementation with low concentrations of melatonin (0.1 and 1μM) conferred Al resistance as evident in partial alleviation of root growth inhibition and decreased H2O2 production: in contrast, high concentrations of melatonin (100 and 200μM) had an opposite effect and even decreased root growth in Al-exposed seedlings. Mitigation of Al stress by the 1μM melatonin root treatment was associated with enhanced activities of the antioxidant enzymes and increased exudation of malate and citrate. In conclusion, melatonin might play a critical role in soybean resistance to Al toxicity.

Citrate exudation induced by aluminum is independent of plasma membrane H+-ATPase activity and coupled with potassium efflux from cluster roots of phosphorus-deficient white lupin

Exudation of organic acid anions is one of the mechanisms responsible for aluminum (Al) tolerance. The plasma membrane (PM) H+-ATPase is involved in the exudation of organic acid anions. However, the relationship between organic acid exudation and PM H+-ATPase under Al toxicity remains unclear. This study aims to investigate the correlation among Al-induced citrate exudation, PM H+-ATPase activity and counterions for citrate release from cluster roots of phosphorus-deficient (−P) white lupin. Al and various pharmacological agents were applied to incubate the cluster roots of P-deficient white lupin; the citrate exudation rate, PM H+-ATPase activity and ion exudation of cluster roots were examined. Citrate exudation from cluster roots of P-deficient white lupin was induced by 50 μM Al treatment within 1.5 h, but no extra increase was found when the duration of Al treatment increased. The PM H+-ATPase activity of cluster roots was insensitive to Al treatment, irrespective of Al concentration and duration of Al treatment. Al treatment increased K+ efflux but not H+ efflux from cluster roots. After application of pharmacological agents to P-deficient cluster roots under Al treatment or not, vanadate decreased H+ efflux and increased K+ efflux, but had no inhibitory effect on citrate exudation; fusicoccin increased H+ efflux and citrate exudation, but decreased K+ efflux; tetraethylammonium (TEA) chloride, a K+-channel inhibitor, inhibited K+ efflux and increased H+ efflux. These results indicate that citrate exudation induced by combined treatment with P-deficiency and Al is independent of PM H+-ATPase activity, and is coupled with K+ efflux, which may compensate H+ efflux for keeping the charge balance for Al-induced citrate exudation from cluster roots of P-deficient white lupin.

Contrasting reactions of roots of two coniferous tree species to aluminum stress

The formation of cell-wall polysaccharide callose in tree roots has been suggested to detect aluminum (Al) stress at an early stage in forest trees. The objective of this study was to clarify whether the Japanese plantation tree species Cryptomeria japonica, which grows in acid soils, and Pinus thunbergii, distributed in coastal regions, have sensitive or tolerant root reactions against Al stress. We examined the accumulation and distribution of callose and Al, and the exudation of organic acid anion (OA) of the roots of C. japonica seedlings, and compared them with those of P. thunbergii after one day exposure to Al in hydroponic systems. Callose in the root apices of P. thunbergii was significantly induced at 0.5 mM Al or higher. However, no induction of callose was recorded in C. japonica supplied with 1.0 mM Al. Experiments with the callose elicitor digitonin confirmed that both species could have a capacity of callose induction. Aluminum was found to accumulate mainly in the epidermal cell walls of C. japonica. In contrast, in P. thunbergii, Al penetrated into more inner root cells, such as cortical cell walls and lumen, and callose deposition was also evident in these compartments. Exudations of OA, such as oxalate, malate and citrate, were observed in both tree species after the treatment of Al, but the exudation patterns of the species differed. We conclude that roots of C. japonica with lower callose productions are tolerant to Al due to not allowing Al to penetrate readily into its inner cells of the roots, partly via OA exudation, but the detailed mechanism still remains unclear.

Molecular and physiological strategies to increase aluminum resistance in plants

Aluminum (Al) toxicity is a primary limitation to plant growth on acid soils. Root meristems are the first site for toxic Al accumulation, and therefore inhibition of root elongation is the most evident physiological manifestation of Al toxicity. Plants may resist Al toxicity by avoidance (Al exclusion) and/or tolerance mechanisms (detoxification of Al inside the cells). The Al exclusion involves the exudation of organic acid anions from the root apices, whereas tolerance mechanisms comprise internal Al detoxification by organic acid anions and enhanced scavenging of free oxygen radicals. One of the most important advances in understanding the molecular events associated with the Al exclusion mechanism was the identification of the ALMT1 gene (Al-activated malate transporter) in Triticum aestivum root cells, which codes for a plasma membrane anion channel that allows efflux of organic acid anions, such as malate, citrate or oxalate. On the other hand, the scavenging of free radicals is dependent on the expression of genes involved in antioxidant defenses, such as peroxidases (e.g. in Arabidopsis thaliana and Nicotiana tabacum), catalases (e.g. in Capsicum annuum), and the gene WMnSOD1 from T. aestivum. However, other recent findings show that reactive oxygen species (ROS) induced stress may be due to acidic (low pH) conditions rather than to Al stress. In this review, we summarize recent findings regarding molecular and physiological mechanisms of Al toxicity and resistance in higher plants. Advances have been made in understanding some of the underlying strategies that plants use to cope with Al toxicity. Furthermore, we discuss the physiological and molecular responses to Al toxicity, including genes involved in Al resistance that have been identified and characterized in several plant species. The better understanding of these strategies and mechanisms is essential for improving plant performance in acidic, Al-toxic soils.

Role of magnesium in alleviation of aluminium toxicity in plants

Magnesium is pivotal for activating a large number of enzymes; hence, magnesium plays an important role in numerous physiological and biochemical processes affecting plant growth and development. Magnesium can also ameliorate aluminium phytotoxicity, but literature reports on the dynamics of magnesium homeostasis upon exposure to aluminium are rare. Herein existing knowledge on the magnesium transport mechanisms and homeostasis maintenance in plant cells is critically reviewed. Even though overexpression of magnesium transporters can alleviate aluminium toxicity in plants, the mechanisms governing such alleviation remain obscure. Possible magnesium-dependent mechanisms include (i) better carbon partitioning from shoots to roots; (ii) increased synthesis and exudation of organic acid anions; (iii) enhanced acid phosphatase activity; (iv) maintenance of proton-ATPase activity and cytoplasmic pH regulation; (v) protection against an aluminium-induced cytosolic calcium increase; and (vi) protection against reactive oxygen species. Future research should concentrate on assessing aluminium toxicity and tolerance in plants with overexpressed or antisense magnesium transporters to increase understanding of the aluminium-magnesium interaction.

Rhizosphere interactions between microorganisms and plants govern iron and phosphorus acquisition along the root axis – model and research methods

Iron and phosphorus availability is low in many soils; hence, microorganisms and plants have evolved mechanisms to acquire these nutrients by altering the chemical conditions that affect their solubility. In plants, this includes exudation of organic acid anions and acidification of the rhizosphere by release of protons in response to iron and phosphorus deficiency. Grasses (family Poaceae) and microorganisms further respond to Fe deficiency by production and release of specific chelators (phytosiderophores and siderophores, respectively) that complex Fe to enhance its diffusion to the cell surface. In the rhizosphere, the mutual demand for Fe and P results in competition between plants and microorganisms with the latter being more competitive due to their ability to decompose plant-derived chelators and their proximity to the root surface; however microbial competitiveness is strongly affected by carbon availability. On the other hand, plants are able to avoid direct competition with microorganisms due to the spatial and temporal variability in the amount and composition of exudates they release into the rhizosphere. In this review, we present a model of the interactions that occur between microorganisms and roots along the root axis, and discuss advantages and limitations of methods that can be used to study these interactions at nanometre to centimetre scales. Our analysis suggests mechanisms such as increasing turnover of microbial biomass or enhanced nutrient uptake capacity of mature root zones that may enhance plant competitiveness could be used to develop plant genotypes with enhanced efficiency in nutrient acquisition. Our model of interactions between plants and microorganisms in the rhizosphere will be useful for understanding the biogeochemistry of P and Fe and for enhancing the effectiveness of fertilization.

Phosphorus saturation and pH differentially regulate the efficiency of organic acid anion-mediated P solubilization mechanisms in soil

Exudation of organic acid anions by plants as well as root-induced changes in rhizosphere pH can potentially improve phosphate (Pi) availability in the rhizosphere and are frequently found to occur simultaneously. In non-calcareous soils, a major proportion of Pi is strongly sorbed to metal oxi(hydr)oxides of mainly iron (Fe) and aluminium (Al) and organic anions are known to compete with Pi for the same sorption sites (ligand exchange) or solubilize Pi via ligand-promoted mineral dissolution. Root-induced co-acidification may also further promote Pi release from soil. The relative efficiency of these different solubilization mechanisms, however, is poorly understood. The aims of this study were to gain a better mechanistic understanding of the solubilizing mechanisms of four carboxylates (citrate, malate, oxalate, malonate) in five soils with high and low P surface site saturation. Results indicate that at a lower P saturation of solid phase sorption sites, ligand-promoted mineral dissolution was the main Pi solubilization mechanism, while ligand exchange became more important at higher soil P concentrations. Co-acidification generally increased Pi solubility in the presence of carboxylates; however the relative solubilizing effect of carboxylates compared to the background electrolyte (KCl) control decreased by 20–50%. In soils with high amounts of exchangeable calcium (Ca), the proton-induced Ca solubilization reduced soluble Pi, presumably due to ionic-strength-driven changes in the electric surface potential favoring a higher Pi retention. Across a wider soil pH range (pH 3–8), Pi solubility increased with increasing alkalinity, as a result of both, more negatively charged sorption sites, as well as DOC-driven changes in Fe and Al solubility, which were further enhanced by the presence of citrate. Overall, the relative efficiency of carboxylates in solubilizing Pi was greatest in soils with medium to high amounts of anionic binding sites (mainly Fe- and Al-oxy(hydr)oxides) and a medium P sorption site coverage, with citrate being most effective in solubilizing Pi.

Spatial characteristics of aluminum uptake and translocation in roots of buckwheat (Fagopyrum esculentum)

The detoxification of aluminum (Al) in root tips of the Al accumulator buckwheat by exudation of oxalate leading to reduced Al uptake (Al resistance) is difficult to reconcile with the Al accumulation (Al tolerance). The objective of this study was to analyze resistance and tolerance mechanisms at the same time evaluating particularly possible stratification of Al uptake, Al transport and oxalate exudation along the root apex. The use of a minirhizotron made it possible to differentiate between spatial responses to Al along the root apex with regard to Al uptake and organic acid anion exudation, but also to measure at the same time Al and organic acid transport in the xylem. Al accumulates particularly in the 3-mm root apex. The study showed that Al taken up by the 10-mm root apex is rapidly transferred to the xylem which differentiates in the 10 to 15-mm root zone as revealed by a microscopic study. Al induces the release of oxalate from the root apex but particularly from the subapical 6-20 mm root zone even when Al was applied only to the 5-mm root apex suggesting a basipetal signal transduction. Citrate proved to be the most likely ligand for Al in the xylem because Al and citrate transport rates were positively correlated. In conclusion, the data presented show that the Al-induced release of oxalate, and Al uptake as well as Al accumulation are spatially not separated in the root apex.

Metal Solubility and Speciation in the Rhizosphere of Lupinus albus Cluster Roots

The objective of this study was to investigate the influence of root exudation of organic acid anions on the speciation of major and trace metal cations in the rhizosphere of Lupinus albus cluster roots. Plants were grown in rhizoboxes containing repacked weakly acidic loam. Bulk soil solutions and, during the lifetime of cluster roots, rhizosphere solutions were collected using micro suction cups. During organic acid anion exudation bursts, metals in the rhizosphere of cluster roots were strongly mobilized. The concentrations of dissolved organic carbon derived from soil organic matter increased parallel to organic acid anions. Speciation calculations revealed that, during exudation, Al, Ca, Mn, and Zn in the cluster root rhizosphere were mainly bound with citrate, while Cu and Pb were always strongly bound to soil-derived dissolved organic matter. Our results indicate that cluster root exudation led on one hand to direct mobilization and complexation of metals like Al, Fe, and Zn by citrate and on the other hand to the mobilization of soil organic matter which complexes and solubilizes Cu and Pb.

Spatial and temporal variation in organic acid anion exudation and nutrient anion uptake in the rhizosphere of Lupinus albus L.

We investigated in situ the temporal patterns and spatial extent of organic acid anion exudation into the rhizosphere solution of Lupinus albus, and its relation with the nutrient anions phosphate, nitrate and sulfate by means of a rhizobox micro suction cup method under P sufficient conditions. We compared the soil solution in the rhizosphere of cluster roots with that in the vicinity of normal roots, nodules and bulk soil. Compared to the other rhizosphere and soil compartments, concentrations of organic acid anions were higher in the vicinity of cluster roots during the exudative burst (citrate, oxalate) and nodules (acetate, malate), while concentrations of inorganic nutrient anions were highest in the bulk soil. Both active cluster roots and nodules were most efficient in taking up nitrate and phosphate. The intensity of citrate exudation by cluster roots was highly variable. The overall temporal patterns during the lifetime of cluster roots were overlaid by a diurnal pattern, i.e. in most cases, the exudation burst consisted of one or more peaks occurring in the afternoon. Multiple exudation peaks occurred daily or were separated by 1 or 2 days. Although citrate concentrations decreased with distance from the cluster root apex, they were still significantly higher at a distance of 6 to 10 mm than in the bulk soil. Phosphate concentrations were extremely variable in the proximity of cluster roots. While our results indicate that under P sufficient conditions cluster roots take up phosphate during their entire life time, the influence of citrate exudation on phosphate mobilization from soil could not be assessed conclusively because of the complex interactions between P uptake, organic acid anion exudation and P mobilization. However, we observed indications of P mobilization concurrent with the highest measured citrate concentrations. In conclusion, this study provides semiquantitative in situ data on the reactivity of different root segments of L. albus L. in terms of root exudation and nutrient uptake under nutrient sufficient conditions, in particular on the temporal variability during the lifetime of cluster roots.