Caixian Tang

Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review

The aim of the present review is to define the various origins of root-mediated changes of pH in the rhizosphere, i.e., the volume of soil around roots that is influenced by root activities. Root-mediated pH changes are of major relevance in an ecological perspective as soil pH is a critical parameter that influences the bioavailability of many nutrients and toxic elements and the physiology of the roots and rhizosphere microorganisms. A major process that contributes root-induced pH changes in the rhizosphere is the release of charges carried by H+ or OH− to compensate for an unbalanced cation–anion uptake at the soil–root interface. In addition to the ions taken up by the plant, all the ions crossing the plasma membrane of root cells (e.g., organic anions exuded by plant roots) should be taken into account, since they all need to be balanced by an exchange of charges, i.e., by a release of either H+ or OH−. Although poorly documented, root exudation and respiration can contribute some proportion of rhizosphere pH decrease as a result of a build-up of the CO2 concentration. This will form carbonic acid in the rhizosphere that may dissociate in neutral to alkaline soils, and result in some pH decrease. Ultimately, plant roots and associated microorganisms can also alter rhizosphere pH via redox-coupled reactions. These various processes involved in root-mediated pH changes in the rhizosphere also depend on environmental constraints, especially nutritional constraints to which plants can respond. This is briefly addressed, with a special emphasis on the response of plant roots to deficiencies of P and Fe and to Al toxicity. Finally, soil pH itself and pH buffering capacity also have a dramatic influence on root-mediated pH changes.

Responses of root architecture development to low phosphorus availability: a review

Background Phosphorus (P) is an essential element for plant growth and development but it is often a limiting nutrient in soils. Hence, P acquisition from soil by plant roots is a subject of considerable interest in agriculture, ecology and plant root biology. Root architecture, with its shape and structured development, can be considered as an evolutionary response to scarcity of resources. Scope This review discusses the significance of root architecture development in response to low P availability and its beneficial effects on alleviation of P stress. It also focuses on recent progress in unravelling cellular, physiological and molecular mechanisms in root developmental adaptation to P starvation. The progress in a more detailed understanding of these mechanisms might be used for developing strategies that build upon the observed explorative behaviour of plant roots. Conclusions The role of root architecture in alleviation of P stress is well documented. However, this paper describes how plants adjust their root architecture to low-P conditions through inhibition of primary root growth, promotion of lateral root growth, enhancement of root hair development and cluster root formation, which all promote P acquisition by plants. The mechanisms for activating alterations in root architecture in response to P deprivation depend on changes in the localized P concentration, and transport of or sensitivity to growth regulators such as sugars, auxins, ethylene, cytokinins, nitric oxide (NO), reactive oxygen species (ROS) and abscisic acid (ABA). In the process, many genes are activated, which in turn trigger changes in molecular, physiological and cellular processes. As a result, root architecture is modified, allowing plants to adapt effectively to the low-P environment. This review provides a framework for understanding how P deficiency alters root architecture, with a focus on integrated physiological and molecular signalling.

Iron deficiency-induced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover

Phenolic compounds are frequently reported to be the main components of root exudates in response to iron (Fe) deficiency in Strategy I plants, but relatively little is known about their function. Here, we show that removal of secreted phenolics from the root-bathing solution almost completely inhibited the reutilization of apoplastic Fe in roots of red clover (Trifolium pratense). This resulted in much lower levels of shoot Fe and significantly higher root Fe compared with control and also resulted in leaf chlorosis, suggesting this approach stimulated Fe deficiency. This was supported by the observation that phenolic removal significantly enhanced root ferric chelate reductase activity, which is normally induced by plant Fe deficiency. Furthermore, root proton extrusion, which also is normally increased during Fe deficiency, was found to be higher in plants exposed to the phenolic removal treatment too. These results indicate that Fe deficiency-induced phenolics secretion plays an important role in the reutilization of root apoplastic Fe, and this reutilization is not mediated by proton extrusion or the root ferric chelate reductase. In vitro studies with extracted root cell walls further demonstrate that excreted phenolics efficiently desorbed a significant amount of Fe from cell walls, indicating a direct involvement of phenolics in Fe remobilization. All of these results constitute the first direct experimental evidence, to our knowledge, that Fe deficiency-induced secretion of phenolics by the roots of a dicot species improves plant Fe nutrition by enhancing reutilization of apoplastic Fe, thereby improving Fe nutrition in the shoot.

Chickpea facilitates phosphorus uptake by intercropped wheat from an organic phosphorus source

Pot experiments were conducted to investigate interspecific complementation in utilization of phytate and FePO4 by plants in the wheat (Triticum aestivum L.)/chickpea (Cicer arietinum L.) intercropping under sterile and non-sterile conditions. The pots were separated into two compartments by either a solid root barrier to eliminate root contact and solute movement, by a nylon mesh (30 μM) to prevent root contact but permit solute exchange, or not separated between the compartments. Wheat plants were grown in one compartment and chickpea in the other. Two P sources were tested at 60 mg P kg−1 soil (sodium phytate or FePO4). Under non-sterile conditions, the biomass of wheat was significantly greater when the roots were intermingled with chickpea than when the roots were separated from chickpea roots by a solid root barrier or nylon mesh. When phytate–P was applied, P concentrations in wheat (2.9 g kg−1 in shoots and 1.4 g kg−1 in roots) without root barrier between the two species were higher than those in the treatments with nylon mesh or with the solid root barrier separation (1.9 g kg−1 in shoots and 1.0 g kg−1 in roots). In contrast, P concentrations in wheat supplied with FePO4 were similar between the root separation treatments. There was no significant difference in P uptake by chickpea between the P sources or between the root separation treatments, except that P uptake was greater in the phytate treatment with the root barrier. Total P uptake from phytate was increased by 25% without root separation compared to the root separation treatments. Under sterile conditions and supply of phytate–P, the biomass of wheat was doubled when the roots were intermingled with chickpea and increased by a third with the nylon mesh separation compared to that with the solid root barrier. Biomass production in wheat at various treatments correlated with P concentration in shoot. Biomass production and P concentration in chickpea were unaffected by root separation. Total P uptake by plants was 68% greater with root intermingling and 37% greater with nylon mesh separation than that with the solid root barrier. The results suggest that chickpea roots facilitate P utilization from the organic P by wheat.

Interspecific facilitation of nutrient uptake by intercropped maize and faba bean

Interspecific complementary interactions in N, P and K uptake betweenintercropped maize (Zea mays L. cv. Zhongdan No. 2) andfababean (Vicia faba L. cv. Linxia Dacaidou) were investigatedin a field experiment. A root barrier study was also set up in whichbelowgroundpartitions were used to determine the contribution of interspecific rootinteractions to crop nutrient uptake. Nitrogen uptake by intercropped faba beanwas higher than (no P fertilizer) or similar to (33 kg Pha−1 of P fertilizer) that by sole faba bean during theearly growth stages (first to third sampling) of faba bean, and was similar to(no P fertilizer) or higher than (33 kg P ha−1 ofP fertilizer) that by sole faba bean at maturity. Nitrogen uptake byintercropped maize did not differ from that by sole maize at maturity, exceptwhen P fertilizer was applied. Intermingling of maize and faba bean rootsincreased N uptake by both crop species by about 20% compared with complete orpartial separation of the root systems. Intercropping also led to someimprovement in P nutrition of both crop species. Maize shoot P concentrationswere similar to those of sole maize during early growth stages and becameprogressively higher until they were significantly higher than those of solemaize at maturity. Intercropping increased shoot P concentration in faba beanatthe flowering stage and in maize at maturity, and increased P uptake by bothplant species at maturity. Phosphorus uptake by faba bean with rootintermingling (no root partition) was 28 and 11% higher than with complete(plastic sheet) and partial (400 mesh nylon net) root barriers, respectively.Maize showed similar trends, with corresponding P uptake values of 29 and 17%.Unlike N and P, K nutrition was not affected by the presence of root barriers.

Excess cation uptake, and extrusion of protons and organic acid anions by Lupinus albus under phosphorus deficiency

In symbiotically-grown legumes, rhizosphere acidification may be caused by a high cation/anion uptake ratio and the excretion of organic acids, the relative importance of the two processes depending on the phosphorus nutritional status of the plants. The present study examined the effect of P deficiency on extrusions of H(+) and organic acid anions (OA(-)) in relation to uptake of excess cations in N(2)-fixing white lupin (cv. Kiev Mutant). Plants were grown for 49 days in nutrient solutions treated with 1, 5 or 25 mmol P m(-3) Na(2)HPO(4) in a phytotron room. The increased formation of cluster roots occurred prior to a decrease in plant growth in response to P deficiency. The number of cluster roots was negatively correlated with tissue P concentrations below 2.0 g kg(-1) in shoots and 3 g kg(-1) in roots. Cluster roots generally had higher concentrations of Mg, Ca, N, Cu, Fe, and Mn but lower concentrations of K than non-cluster roots. Extrusion of protons and OA(-) (90% citrate and 10% malate) from roots was highly dependent on P supply. The amounts of H(+) extruded per unit root biomass decreased with time during the experiment. On the equimolar basis, H(+) extrusion by P-deficient plants (grown at 1 and 5 mmol P m(-3)) were, on average, 2-3-fold greater than OA(-) exudation. The excess cation content in plants was generally the highest at 1 mmol P m(-3) and decreased with increasing P supply. The ratio of H(+) release to excess cation uptake increased with decreasing P supply. The results suggest that increased exudation of OA(-) due to P deficiency is associated with H(+) extrusion but contributes only a part of total acidification.

Role of phosphorus nutrition in development of cluster roots and release of carboxylates in soil-grown Lupinus albus

The present study examined the effect of phosphorus (P) limitation on cluster root formation and exudation of carboxylates by N2-fixing white lupin (Lupinus albus L. cv. Kiev) grown in a P-deficient sandy soil. Plants received 10 (limited P) or 200 μg P g−1 soil as FePO4 (adequate P) and were grown in a phytotron at 20/12 °C (12/12 h) for 76 days in soil columns. Cluster root formation was assessed and root exudates were collected at 9-day intervals. Shoot and root dry weights were higher in plants grown in the adequate-P compared to the limited-P treatment for 67 days. No clear difference in the total root length was observed between two P treatments before day 58. However, the specific root length increased rapidly from 17 m g−1 DW at day 40 to 28 m g−1 at day 49 in the P-limited plants, but decreased in the P-adequate plants. The effect of P limitation on enhancement of cluster root formation was observed from day 40 and reached the maximum at day 58. The number of cluster roots was negatively correlated with the P concentration in both roots and shoots. Phosphorus limitation increased exudation of citrate from day 40. The exudation of citrate displayed a cyclic pattern throughout the experiment, and appeared related to internal P concentration in plants, particularly P concentration in shoots. The sorption of exogenously added citrate in the soil was also examined. The amount of extractable citrate remained unchanged for 2 h, but decreased thereafter, suggesting that the soil had a low capacity to sorb citrate, and the rate of its decomposition by microorganisms was slow. Collecting solution leached through a soil column is a simple and reliable method to acquire root exudates from white lupin grown in soil. The results suggest that formation of cluster roots and exudation of citrate in white lupin are regulated by P concentration in shoots.

Changes in phosphorus fractions at various soil depths following long-term P fertiliser application on a Black Vertosol from south-eastern Queensland

Long-term removal of grain P and soil test data suggested that the Colwell phosphorus (P) extraction from the surface 0.10 m of a Black Vertosol from south-eastern Queensland was a poor indicator of run-down of soil P pools. We proposed that plants were also accessing P from layers below 0.10 m or from surface soil P pools not extracted by the Colwell extraction. Both topsoil and subsoil samples in 1994 and 2003 were collected from nil and 20 kg P/ha per crop treatments in a long-term N × P field experiment established in 1985 for detailed P fractionation. An uncropped reference soil was also taken in 2003 from an adjacent area. The long-term effect of the field treatments on soil P fractions was evaluated by comparing the reference site, which was assumed to represent the original soil condition, to the 2003 samples. Without addition of P fertiliser, 55%, 35%, and 10% of total P removal were from 0 to 0.10, 0.10 to 0.30, and 0.30 to 0.60 m, respectively, compared with the uncropped reference soil. Labile fractions comprising resin, bicarbonate, and hydroxide pools in the top 0.10 m decreased by approximately 60% and accounted for 15% of the total P decrease from 0 to 0.60 m depth. Acid and residual-P fractions decreased by 50% and 20%, respectively, and accounted for ~20% and 15% of the total P decrease. In contrast, P addition at 20 kg P/ha per crop over 18 crops doubled the resin and bicarbonate inorganic P (NaHCO3-Pi) pools in the surface 0.10 m. Hydroxide (NaOH-Pi) and acid extracted inorganic P increased by 25% and 10%, respectively, while the residual-P pool decreased by about 15%. Below 0.10 m, very little P was removed by the first 3 extractants. Most of the P was present in the acid and residual fractions irrespective of fertiliser application. The acid and residual-P dropped by 30% and 12%, respectively, at 0.10–0.30 m and 12% and 8% at 0.30–0.60 m. When comparing the experimental soil samples in 2003 with those in 1994, similar trends were observed in the changes of each soil P fraction. In the surface 0.10 m, acid and residual-P pools decreased greatly and explained almost all of the total P decrease in the surface soil without P input. With P addition, labile pools acted as the main sink for P. The acid pool increased by 7%, while the residual-P showed a decrease in the topsoil. Total P level was elevated noticeably in this soil layer. However, at 0.10–0.30 m depth, acid and residual pools were the dominant fractions and decreased significantly irrespective of P fertiliser addition. Below 0.30 m, no significant changes were detected for each fraction and total P. The results suggest that crops had accessed significant amounts of P at 0.10–0.30 m depth irrespective of P fertiliser application, and that subsoil sampling (0.10–0.30 m) should be considered in order to improve the monitoring of soil P status. However, choice of appropriate extractants for monitoring subsoil P reserves is yet to be undertaken.

Proton release of two genotypes of bean (Phaseolus vulgaris L.) as affected by N nutrition and P deficiency

The study compared the release of protons by two genotypes (BAT477 and DOR364) of bean (Phaseolus vulgaris L.) relying on various sources of N (urea, nitrate and N2 fixation), at two levels of P supply: 1 μM (or 0 for urea-fed plants) and 25 μM. The plants grown at low P showed reduced growth and P concentration in tissues. The proton release was assessed at two levels: (i) at the whole plant level using pH-stat system in hydroponic culture; (ii) at the level of single roots by the combined use of agarose gel-dye indicator and videodensitometry measurements which provided information on the spatial variation of proton release along root axes. The pH-stat measurements showed that urea resulted in the greatest proton release while nitrate led to net hydroxyl release. Moreover, decreased proton release was observed at night for plants relying on urea and N2 fixation, while no diurnal pattern occurred for plants relying on nitrate. Phophorus deficiency increased proton release in urea-fed plants and decreased hydroxyl release in nitrate-fed plants. Conversely, N2-fixing plants showed an opposite behaviour, i.e. lower proton release at low than high P supply. Less effect of P supply on proton/hydroxyl release was found at the level of single root tips (videodensitometry experiment) in N2-fixing plants. Little genotypic difference in proton release was found although BAT477 showed a greater ability to respond to P deficiency than DOR364 when relying on urea or nitrate. Proton release of N2-fixing plants was greater in BAT477 than in DOR364, both at the whole plant and single root levels.

Differential regulatory role of nitric oxide in mediating nitrate reductase activity in roots of tomato (Solanum lycocarpum)

BACKGROUND AND AIMS Nitric oxide (NO) has been demonstrated to stimulate the activity of nitrate reductase (NR) in plant roots supplied with a low level of nitrate, and to affect proteins differently, depending on the ratio of NO to the level of protein. Nitrate has been suggested to regulate the level of NO in plants. This present study examined interactive effects of NO and nitrate level on NR activity in roots of tomato (Solanum lycocarpum). METHODS NR activity, mRNA level of NR gene and concentration of NR protein in roots fed with 0.5 mM or 5 mM nitrate and treated with the NO donors, sodium nitroprusside (SNP) and diethylamine NONOate sodium (NONOate), and the NO scavenger, 2-(4-carboxyphenyl)-4,4,5,5-tetramethyl-imidazoline-1-oxyl-3-oxide (cPTIO), were measured in 25-d-old seedlings. KEY RESULTS Addition of SNP and NONOate enhanced but cPTIO decreased NR activity in the roots fed with 0.5 mm nitrate. The opposite was true for the roots fed with 5 mM nitrate. However, the mRNA level of the NR gene and the protein concentration of NR enzyme in the roots were not affected by SNP treatment, irrespective of nitrate pre-treatment. Nevertheless, a low rate of NO gas increased while cPTIO decreased the NR activities of the enzyme extracts from the roots at both nitrate levels. Increasing the rate of NO gas further increased NR activity in the enzyme extracts of the roots fed with 0.5 mM nitrate but decreased it when 5 mM nitrate was supplied. Interestingly, the stimulative effect of NO gas on NR activity could be reversed by NO removal through N(2) flushing in the enzyme extracts from the roots fed with 0.5 mM nitrate but not from those with 5 mM nitrate. CONCLUSIONS The effects of NO on NR activity in tomato roots depend on levels of nitrate supply, and probably result from direct interactions between NO and NR protein.