Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms

The rhizosphere is a complex environment where roots interact with physical, chemical and biological properties of soil. Structural and functional characteristics of roots contribute to rhizosphere processes and both have significant influence on the capacity of roots to acquire nutrients. Roots also interact extensively with soil microorganisms which further impact on plant nutrition either directly, by influencing nutrient availability and uptake, or indirectly through plant (root) growth promotion. In this paper, features of the rhizosphere that are important for nutrient acquisition from soil are reviewed, with specific emphasis on the characteristics of roots that influence the availability and uptake of phosphorus and nitrogen. The interaction of roots with soil microorganisms, in particular with mycorrhizal fungi and non-symbiotic plant growth promoting rhizobacteria, is also considered in relation to nutrient availability and through the mechanisms that are associated with plant growth promotion.     

硝态氮（NO3^—）对水稻侧根生长及其氮吸收的影响

侧根是植物吸收利用土壤养分的重要器官 ,其生长发育受内部遗传因子和外部环境矿质养分的影响。通过琼脂分层培养发现 :局部供应NO-3 可以诱导水稻 (OryzasativaL .)主根或不定根上侧根的生长。为研究旱种条件下NO-3 对水稻侧根发育及其N吸收的影响 ,设置了 3个蛭石培养实验 :分根处理、全株缺N、全株供N处理。分根处理 (一半根系供应 3mmol/LKNO3,另一半根系供应 3mmol/LKCl)结果表明 :局部供应NO-3 能够促进水稻侧根生长。而在全株处理下 ,N饥饿诱导了侧根的伸长。水稻根系对NO-3 的这两种反应都存在着显著的基因型差异。同时对地上部N浓度、可溶性总糖含量及N含量分析表明 ,这些生理指标在分根处理与全株加N处理中的差异均不显著 ,表明分根处理也能基本满足植株正常生长对N的需求。在分根处理中 ,水稻的N含量与分根处理中供N一侧的平均侧根长度存在显著正相关 ,这表明在养分不均一的介质中 ,侧根长度对水稻N素吸收具有十分重要的作用。而在N素充足的条件下 ,两者之间的相关性并不显著 ,这暗示在养分充足的环境下 ,侧根长度可能并不是决定根系吸收N素的主要因素     

硝态氮(NO-3)对水稻侧根生长及其氮吸收的影响

侧根是植物吸收利用土壤养分的重要器官,其生长发育受内部遗传因子和外部环境矿质养分的影响.通过琼脂分层培养发现:局部供应NO-3可以诱导水稻( Oryza sativa L.)主根或不定根上侧根的生长.为研究旱种条件下NO-3对水稻侧根发育及其N吸收的影响,设置了3个蛭石培养实验:分根处理、全株缺N、全株供N处理.分根处理(一半根系供应3 mmol/L KNO3,另一半根系供应3 mmol/L KCl)结果表明:局部供应NO-3 能够促进水稻侧根生长.而在全株处理下,N饥饿诱导了侧根的伸长.水稻根系对NO-3的这两种反应都存在着显著的基因型差异.同时对地上部N浓度、可溶性总糖含量及N含量分析表明,这些生理指标在分根处理与全株加N处理中的差异均不显著,表明分根处理也能基本满足植株正常生长对N的需求.在分根处理中,水稻的N含量与分根处理中供N一侧的平均侧根长度存在显著正相关,这表明在养分不均一的介质中,侧根长度对水稻N素吸收具有十分重要的作用.而在N素充足的条件下,两者之间的相关性并不显著,这暗示在养分充足的环境下,侧根长度可能并不是决定根系吸收N素的主要因素.     

An overview of rhizosphere processes related with plant nutrition in major cropping systems in China

Rhizosphere processes of individual plants have been widely investigated since 1904 when the term “rhizosphere” was first put forward. However, little attention has been paid to rhizosphere effects at an agro-ecosystem level. This paper presents recent research on the rhizosphere processes in relation to plant nutrition in main cropping systems in China. In the peanut (Arachis hypogaea L.)/maize (Zea mays L.) intercropping system, maize was found to improve the Fe nutrition of peanut through influencing its rhizosphere processes, suggesting an important role of phytosiderophores released from Fe-deficient maize. Intercropping between maize and faba bean (Vicia faba L.) was found to improve nitrogen and phosphorus uptake in the two crops compared with corresponding sole crop. There was a higher land equivalent ratio (LER) in the intercropping system of maize and faba bean than the treatment of no root interactions between the two crops. The increased yield of maize intercropped with faba bean resulted from an interspecific facilitation in nutrient uptake, depending on interspecific root interactions of the two crops. In the rotation system of rice (Oryza sativa L.)-wheat (Triticum aestivum L.) crops, Mn deficiency in wheat was caused by excessive Mn uptake by rice and Mn leaching from topsoil to subsoil due to periodic cycles of flooding and drying. However, wheat genotypes tolerant to Mn deficiency tended to distribute more roots to deeper soil layer and thus expand their rhizosphere zones in the Mn-deficient soils and utilize Mn from the subsoil. Deep ploughing also helped root penetration into subsoil and was propitious to correcting Mn deficiency in wheat rotated with rice. In comparison, oilseed rape (Brassica napus L.) took up more Mn than wheat through mobilizing sparingly soluble soil Mn due to acidification and reduction processes in the rhizosphere. Thus, oilseed rape was tolerant to the Mn-deficient conditions in the rice-oilseed rape rotation. Oxidation reactions on root surface of rice also resulted in the formation of Fe plaque in the rice rhizosphere. Large amounts of Zn were accumulated on the Fe plaque. Zinc uptake by rice plants increased as Fe plaque formed, but decreased at high amounts of Fe plaque. It is suggested that to fine-tune cropping patterns and optimize nutrient management based on a better understanding of rhizosphere processes at an agro-ecosystem level is crucial for increasing nutrient use efficiency and developing sustainable agriculture in China.     

Herbivorous insect decreases plant nutrient uptake: the role of soil nutrient availability and association of below‐ground symbionts

1. Plants take nutrients from the rhizosphere via two pathways: (i) by absorbing soil nutrients directly via their roots and (ii) indirectly via symbiotic associations with nutrient‐providing microbes. Herbivorous insects can alter these pathways by herbivory, adding their excrement to the soil, and affecting plant–microbe associations. 2. Little is known, however, about the effects of herbivorous insects on plant nutrient uptake. Greenhouse experiments with soybean, aphids, and rhizobia were carried out to examine the effects of aphids on plant nutrient uptake. 3. First, the inorganic soil nitrogen and the sugar in aphid honeydew between aphid‐infected and ‐free plants were compared. It was found that aphid honeydew added 41 g m^?2 of sugar to the soil, and that aphids decreased the inorganic soil nitrogen by 86%. This decrease may have been caused by microbial immobilisation of soil nitrogen followed by increased microbial abundance as a result of aphid honeydew. 4. Second, nitrogen forms in xylem sap between aphid‐infected and ‐free plants were compared to examine nitrogen uptake. Aphids decreased the nitrogen uptake via both pathways, and strength of the impact on direct uptake via plant roots was greater than indirect uptake via rhizobia. The reduced nitrogen uptake by the direct pathway was as a result of microbial immobilisation, and that by the indirect pathway was probably because of the interaction of microbial immobilisation and carbon stress, which was caused by aphid infection. 5. The present results demonstrate that herbivorous insects can negatively influence the two pathways of plant nutrient uptake and alter their relative importance.     

Proteins as nitrogen source for plants: A short story about exudation of proteases by plant roots

Interest in the problem of plant nitrogen nutrition is increasing. Certain plants can use not only inorganic nitrogen but also intact amino acids and short peptides. According to our studies, the roots of several agricultural and wild-living plants are able to exude proteases and use them to create a pool of accessible N. This mini-review offers an overview of the problem of protease exudation by plant roots and its potential role in plant nitrogen nutrition.Key words: amino acids, organic nitrogen, nutrient uptake, plant nitrogen nutrition, protease exudation     

丛枝菌根真菌与氮添加对不同根形态基因型水稻氮吸收的影响

植物主要依赖自身根系从土壤中获取矿质养分; 具有不同根形态的植物对于养分的吸收能力存在差异。丛枝菌根真菌(AMF)能与陆地植物根系形成共生关系, 帮助植物吸收矿质养分。但是, AMF对于植物根系养分吸收的促进效应是否会受根形态的影响还鲜有研究。该研究选取4种不同根形态基因型水稻(根毛缺陷突变体rhl1、侧根缺陷突变体iaa11、不定根缺失突变体arl1和野生型Kas)为研究对象, 设置2种施氮水平处理(低氮: 20 mg·kg^-1氨氮; 高氮: 100 mg·kg^-1氨氮), 利用稳定同位素¹⁵N示踪标记技术, 探究AMF和氮添加对不同根形态植物氮吸收的影响。研究结果发现, 相比低氮处理, 高氮处理下, rhl1、Kas、iaa11与arl1的茎叶¹⁵N浓度分别提高了60%、72%、128%与118%, 说明氮添加显著促进了水稻氮吸收, 且iaa11与arl1对氮添加的响应更强烈。在低氮水平下, AMF对rhl1、Kas、iaa11与arl1氮吸收的平均效应值分别为17%、31%、42%、51%, 表明AMF对于植物氮吸收的促进效应受根形态影响, iaa11与arl1对AMF的响应明显高于Kas与rhl1; 相较于低氮水平, 高氮水平下AMF对于不同根形态水稻氮吸收的促进效应都会显著降低, 表明氮添加削弱了AMF对植物氮吸收的促进效应。该研究阐明了4种不同根形态基因型水稻氮养分吸收存在显著差异, 其中氮吸收能力较弱的基因型水稻对AMF的响应更强, 该结果补充了植物与AMF在养分吸收上存在功能互补的控制实验证据。     

不同氮效率水稻全生育期内对增硝营养的响应及其生理机制

通过添加硝化抑制剂（二氰胺,DCD）来控制硝化作用的水培试验方法,研究了氮高效水稻品种南光和氮低效水稻品种ELIO的籽粒产量对增硝营养（NH4＋∶NO3-比例为100∶0和75∶25）的响应,同时从产量构成、不同生育时期水稻生长、氮素吸收和同化4个方面研究了造成其产量差异的生理机制。结果表明：增NO3-营养可以显著促进氮高效水稻品种南光的生长,从而使其籽粒产量水平提高21%,而对氮低效水稻品种ELIO的籽粒产量没有显著影响。进一步分析表明：在增NO3-营养条件下,南光的穗粒数增加了25%,结实率增加了16%,而氮低效水稻品种ELIO的结实率和穗粒数在两种营养条件下没有显著变化;增NO3-营养可以促进南光对氮素的吸收,使其在苗期、分蘖盛期、齐穗期和成熟期对氮素的吸收量平均增加了36%,进而促进了其生长,干物质积累量在四个生育时期平均增加了30%;南光叶片硝酸还原酶和根系谷氨酰胺合成酶的活力在增硝营养条件下分别增加了100%和95%,说明增硝营养促进了南光对NH4＋和NO3-的同化利用。与氮低效水稻品种（ELIO）相比,氮高效水稻品种（南光）对增硝营养表现出较强的生理响应。     

Carbon flow in the rhizosphere: carbon trading at the soil–root interface

The loss of organic and inorganic carbon from roots into soil underpins nearly all the major changes that occur in the rhizosphere. In this review we explore the mechanistic basis of organic carbon and nitrogen flow in the rhizosphere. It is clear that C and N flow in the rhizosphere is extremely complex, being highly plant and environment dependent and varying both spatially and temporally along the root. Consequently, the amount and type of rhizodeposits (e.g. exudates, border cells, mucilage) remains highly context specific. This has severely limited our capacity to quantify and model the amount of rhizodeposition in ecosystem processes such as C sequestration and nutrient acquisition. It is now evident that C and N flow at the soil–root interface is bidirectional with C and N being lost from roots and taken up from the soil simultaneously. Here we present four alternative hypotheses to explain why high and low molecular weight organic compounds are actively cycled in the rhizosphere. These include: (1) indirect, fortuitous root exudate recapture as part of the root’s C and N distribution network, (2) direct re-uptake to enhance the plant’s C efficiency and to reduce rhizosphere microbial growth and pathogen attack, (3) direct uptake to recapture organic nutrients released from soil organic matter, and (4) for inter-root and root–microbial signal exchange. Due to severe flaws in the interpretation of commonly used isotopic labelling techniques, there is still great uncertainty surrounding the importance of these individual fluxes in the rhizosphere. Due to the importance of rhizodeposition in regulating ecosystem functioning, it is critical that future research focuses on resolving the quantitative importance of the different C and N fluxes operating in the rhizosphere and the ways in which these vary spatially and temporally.     

Mineral nutrition and reduction processes in the rhizosphere of rice

Summary The influence of nitrogen, phosphorus, and potassium on the reduction processes in the rhizosphere of rice grown in solution culture and of rice under lowland conditions was studied. In solution culture the redox potential in the complete nutrient solution was highest, indicating that fully nourished roots have the highest oxidizing power. When the supply of only one element was interrupted, the lack of potassium in the nutrient solution caused the greatest decline in redox potential. Redox potential was further decreased when, besides nitrogen, either phosphorus or potassium was discontinued. Simultaneous deficiencies of nitrogen and potassium lowered redox potential even more severely than did deficiency of all three elements. A long-term nitrogen fertilizer trial under lowland conditions, however, revealed that an abundant supply of nitrogen can decrease redox potential. Redox potential was higher in the soil near plants than in the soil away from plants. In solution culture, at low Eh levels, the increase in iron reducing power of the solution was correlated with the decrease in redox potential. The total number of bacteria and iron reducing bacteria increased almost parallel to the decrease in redox potential and increase in iron reducing power. These relationships show that the nutritional status of the rice plant essentially influences bacterial activity and, thus, oxidation-reduction conditions around the roots. Since sufficient potassium nutrition seems important in maintaining the oxidising power of rice roots, root growth in a potassium deficient soil with K application was compared with root growth without K application. Without potassium the fine lateral roots far from the root base showed black coloration due to ferrous sulfide, indicating a loss of oxidising power. With increasing potassium supply, this phenomenon disappeared and the iron content of the rice plants decreased. re]19751208     

Functional aspects of root architecture and mycorrhizal inoculation with respect to nutrient uptake capacity

The aim of this research was to investigate the effect of arbuscular mycorrhizal (AM) colonisation on root morphology and nitrogen uptake capacity of carob ( Ceratonia siliqua L.) under high and low nutrient conditions. The experimental design was a factorial arrangement of presence/absence of mycorrhizal fungus inoculation ( Glomus intraradices) and high/low nutrient status. Percent AM colonisation, nitrate and ammonium uptake capacity, and nitrogen and phosphorus contents were determined in 3-month-old seedlings. Grayscale and colour images were used to study root morphology and topology, and to assess the relation between root pigmentation and physiological activities. AM colonisation lead to a higher allocation of biomass to white and yellow parts of the root. Inorganic nitrogen uptake capacity per unit root length and nitrogen content were greatest in AM colonised plants grown under low nutrient conditions. A better match was found between plant nitrogen content and biomass accumulation, than between plant phosphorus content and biomass accumulation. It is suggested that the increase in nutrient uptake capacity of AM colonised roots is dependent both on changes in root morphology and physiological uptake potential. This study contributes to an understanding of the role of AM fungi and root morphology in plant nutrient uptake and shows that AM colonisation improves the nitrogen nutrition of plants, mainly when growing at low levels of nutrients.     

Phosphate solubilization by organic anion excretion from rice (Oryza sativa L.) growing in aerobic soil

A mathematical model of P solubilization by organic anion excretion from roots is described and used to account for P solubilization by rice (Oryza sativa L.) plants growing in aerobic soil. In previous experiments with rice in an aerobic, highly-weathered, P-deficient soil, we found that the plants were able to solubilize P from an alkali-soluble pool and thereby increase their P uptake. The solubilization could not be explained by pH changes nor by the release of phosphatases. In subsequent experiments we found excretion of citrate from rice roots into nutrient solutions, and the synthesis and excretion of citrate tended to increase under P starvation. The model allows for the diffusion of the organic anion away from a root, its decomposition by soil microbes, its reaction with the soil in solubilizing P, and diffusion of the solubilized P back towards the root as well as away from it. We calculated the rate of citrate excretion from rice roots growing in soil based on measured steady-state citrate concentrations in the rhizosphere and calculated rates of decomposition. Calculations using these and other model parameters obtained independently showed that the observed solubilization and increased P uptake by rice growing in soil could be accounted for. A sensitivity analysis of the model is given. This revised version was published online in June 2006 with corrections to the Cover Date.     

Influence of ammonium on fine root development and rhizosphere pH of Douglas-fir seedlings in sand

Ammonium sulphate is a major component of the air pollutants deposited on forests in the Netherlands. Different amounts of NH₄ ⁺ were added to Douglas-fir seedlings grown in tall containers of sand, to study the influence of high concentrations of NH₄ ⁺ in the soil on the development of fine roots and the effects of nitrogen uptake on rhizosphere pH. At the end of this eight-month experiment part of the ammonium appeared to have nitrified into nitrate. High doses of ammonium negatively affected root length and root length per unit of dry matter (specific root length). Although Douglas fir shows a preferential ammonium uptake in nutrient solutions the increases in the pH of the rhizosphere in this experiment indicate that nitrogen was mostly taken up as nitrate. When the ammonium concentration in the soil is low, it cannot be taken up readily because of its low mobility in soil. Shoot growth was stimulated by high availability of nitrogen. The possible effects of high doses of ammonium on long-term forest vitality are discussed.     

The influence of signals from chilled roots on the proteome of shoot tissues in rice seedlings

Low root temperature causes a decrease in water uptake, which leads to mineral and nutrient deficiencies with potentially decreased root and shoot growth. Differential temperature effects in plants have been studied extensively, however, the effect of root chilling on the global protein expression in shoots has not been explored. In this study, we imposed chilling temperatures on roots of rice plants while maintaining shoots at optimum atmospheric temperature. Shoot materials (growing zones and leaves) were harvested at five points over a time course of four days, including a two‐day recovery period. Proteins were quantified by tandem mass tags and triple stage MS, using a method developed to overcome ratio compression in isobaric‐labelled quantitation. Over 3000 proteins in each of the tissues were quantified by multiple peptides. Proteins significantly differentially expressed as compared with the control included abscisic acid‐responsive and drought‐associated proteins. The data also contained evidence of a possible induction of a sugar signalling pathway.     

丛枝菌根真菌参与下植物-土壤系统的养分交流及调控

近几年随着有机农业的发展,丛枝菌根的作用受到特别关注。丛枝菌根是由植物根系与丛枝菌根真菌(AMF)形成的一种共生体。在植物-AMF-土壤系统中,AMF为植物提供N、P等营养的同时从根系得到所需的C。概述了植物-AMF-土壤系统中C、N、P等营养物质的交流以及AMF与土壤微生物的互作关系。丛枝菌根的形成可显著提高植物对P的吸收,且在高P条件下多余的P可储存于AMF中。AMF对土壤N循环的影响相当复杂,可能参与调控N循环的多个过程,如硝化作用、反硝化作用和氨氧化作用等。在有机质丰富的土壤中AMF菌丝可快速扩增并吸收其中的N,主要供菌丝自身所需,只有一小部分传递给植物。AMF对土壤C库的影响尚存争议,可能存在时间尺度的差异。短期内可活化土壤C,而在长期尺度上可能有利于土壤C的储存。AMF能够通过改变土壤微生物群落结构而影响植物-土壤体系的物质交流。AMF与解磷菌、根瘤菌和放线菌的协同增效作用可促进土壤有机质的降解或增强其固氮能力;AMF对氨氧化菌的抑制作用可降低氨的氧化减少N2O的释放。AMF与外生共生真菌EMF共存时,表现出协同增效作用,但EMF的优先定殖会限制AMF的侵染。AMF不同类群之间则主要表现为竞争和拮抗关系。AMF与土壤微生物之间的互作关系受土壤无机环境的影响,在养分亏缺条件下微生物之间往往表现为竞争关系。因植物、AMF与土壤微生物之间存在复杂的互作关系,为此AMF并不总是表现出其对植物营养的促进作用。目前关于AMF的作用机理仍以假说为主,需要进一步的实验验证。在植物-AMF-土壤系统中N与C的交流和P与C的交流并未表现出一致性,对N、P循环相互关系的进一步探讨有助于深入理解植物-土壤体系中的养分循环。植物、AMF和土壤微生物的养分来源及其对养分的相对需求强度和吸收效率尚未可知,因此无法深入理解AMF在植物-土壤体系中养分交流和转化的作用。在方法上,传统的土壤学方法在养分动态研究中存在局限性,现代分子生物学手段和化学计量学的结合值得尝试。     

Regulation and function of root exudates

Root-secreted chemicals mediate multi-partite interactions in the rhizosphere, where plant roots continually respond to and alter their immediate environment. Increasing evidence suggests that root exudates initiate and modulate dialogue between roots and soil microbes. For example, root exudates serve as signals that initiate symbiosis with rhizobia and mycorrhizal fungi. In addition, root exudates maintain and support a highly specific diversity of microbes in the rhizosphere of a given particular plant species, thus suggesting a close evolutionary link. In this review, we focus mainly on compiling the information available on the regulation and mechanisms of root exudation processes, and provide some ideas related to the evolutionary role of root exudates in shaping soil microbial communities.     

Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles

While there is an emerging view that roots and their associated microbes actively alter resource availability and soil organic matter (SOM) decomposition, the ecosystem consequences of such rhizosphere effects have rarely been quantified. Using a meta‐analysis, we show that multiple indices of microbially mediated C and nitrogen (N) cycling, including SOM decomposition, are significantly enhanced in the rhizospheres of diverse vegetation types. Then, using a numerical model that combines rhizosphere effect sizes with fine root morphology and depth distributions, we show that root‐accelerated mineralization and priming can account for up to one‐third of the total C and N mineralized in temperate forest soils. Finally, using a stoichiometrically constrained microbial decomposition model, we show that these effects can be induced by relatively modest fluxes of root‐derived C, on the order of 4% and 6% of gross and net primary production, respectively. Collectively, our results indicate that rhizosphere processes are a widespread, quantitatively important driver of SOM decomposition and nutrient release at the ecosystem scale, with potential consequences for global C stocks and vegetation feedbacks to climate.     

Beneficial microbes going underground of root immunity

Plant roots interact with an enormous diversity of commensal, mutualistic, and pathogenic microbes, which poses a big challenge to roots to distinguish beneficial microbes from harmful ones. Plants can effectively ward off pathogens following immune recognition of conserved microbe‐associated molecular patterns (MAMPs). However, such immune elicitors are essentially not different from those of neutral and beneficial microbes that are abundantly present in the root microbiome. Recent studies indicate that the plant immune system plays an active role in influencing rhizosphere microbiome composition. Moreover, it has become increasingly clear that root‐invading beneficial microbes, including rhizobia and arbuscular mycorrhiza, evade or suppress host immunity to establish a mutualistic relationship with their host. Evidence is accumulating that many free‐living rhizosphere microbiota members can suppress root immune responses, highlighting root immune suppression as an important function of the root microbiome. Thus, the gate keeping functions of the plant immune system are not restricted to warding off root‐invading pathogens but also extend to rhizosphere microbiota, likely to promote colonization by beneficial microbes and prevent growth‐defense tradeoffs triggered by the MAMP‐rich rhizosphere environment.     

Enhanced zinc uptake by rice through phytosiderophore secretion: a modelling study

Rice (Oryza sativa L.) secretes far smaller amounts of metal-complexing phytosiderophores (PS) than other grasses. But there is increasing evidence that it relies on PS secretion for its zinc (Zn) uptake. After nitrogen, Zn deficiency is the most common nutrient disorder in rice, affecting up to 50% of lowland rice soils globally. We developed a mathematical model of PS secretion from roots and resulting solubilization and uptake of Zn, allowing for root growth, diurnal variation in secretion, decomposition of the PS in the soil, and the transport and interaction of the PS and Zn in the soil. A sensitivity analysis showed that with realistic parameter values for rice in submerged soil, the typically observed rates of PS secretion from rice are sufficient and necessary to explain observed rates of Zn uptake. There is little effect of diurnal variation in secretion on cumulative Zn uptake, irrespective of other model parameter values, indicating that the observed diurnal variation is not causally related to Zn uptake efficiency. Rooting density has a large effect on uptake per unit PS secretion as a result of overlap of the zones of influence of neighbouring roots. The effects of other complications in the rice rhizosphere are discussed.