Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource

Background

Nitrogen (N) is one of the key mineral nutrients for plants and its availability has a major impact on their growth and development. Most often N resources are limiting and plants have evolved various strategies to modulate their root uptake capacity to compensate for both spatial and temporal changes in N availability in soil. The main N sources for terrestrial plants in soils of temperate regions are in decreasing order of abundance, nitrate, ammonium and amino acids. N uptake systems combine, for these different N forms, high- and low-affinity transporters belonging to multige families. Expression and activity of most uptake systems are regulated locally by the concentration of their substrate, and by a systemic feedback control exerted by whole-plant signals of N status, giving rise to a complex combinatory network. Besides modulation of the capacity of transport systems, plants are also able to modulate their growth and development to maintain N homeostasis. In particular, root system architecture is highly plastic and its changes can greatly impact N acquisition from soil.

Scope

In this review, we aim at detailing recent advances in the identification of molecular mechanisms responsible for physiological and developmental responses of root N acquisition to changes in N availability. These mechanisms are now unravelled at an increasing rate, especially in the model plant Arabidopsis thaliana L.. Within the past decade, most root membrane transport proteins that determine N acquisition have been identified. More recently, molecular regulators in nitrate or ammonium sensing and signalling have been isolated, revealing common regulatory genes for transport system and root development, as well as a strong connection between N and hormone signalling pathways.

Conclusion

Deciphering the complexity of the regulatory networks that control N uptake, metabolism and plant development will help understanding adaptation of plants to sub-optimal N availability and fluctuating environments. It will also provide solutions for addressing the major issues of pollution and economical costs related to N fertilizer use that threaten agricultural and ecological sustainability.     

Plant–microbial competition for nitrogen increases microbial activities and carbon loss in invaded soils

Many invasive plant species show high rates of nutrient acquisition relative to their competitors. Yet the mechanisms underlying this phenomenon, and its implications for ecosystem functioning, are poorly understood, particularly in nutrient-limited systems. Here, we test the hypothesis that an invasive plant species (Microstegium vimineum) enhances its rate of nitrogen (N) acquisition by outcompeting soil organic matter-degrading microbes for N, which in turn accelerates soil N and carbon (C) cycling. We estimated plant cover as an indicator of plant N acquisition rate and quantified plant tissue N, soil C and N content and transformations, and extracellular enzyme activities in invaded and uninvaded plots. Under low ambient N availability, invaded plots had 77% higher plant cover and lower tissue C:N ratios, suggesting that invasion increased rates of plant N acquisition. Concurrent with this pattern, we observed significantly higher mass-specific enzyme activities in invaded plots as well as 71% higher long-term N availability, 21% lower short-term N availability, and 16% lower particulate organic matter N. A structural equation model showed that these changes were interrelated and associated with 27% lower particulate organic matter C in invaded areas. Our findings suggest that acquisition of N by this plant species enhances microbial N demand, leading to an increased flux of N from organic to inorganic forms and a loss of soil C. We conclude that high N acquisition rates by invasive plants can drive changes in soil N cycling that are linked to effects on soil C.     

The below-ground perspective of forest plants: soil provides mainly organic nitrogen for plants and mycorrhizal fungi

? Nitrogen (N) availability has a major impact on a wide range of biogeochemical processes in terrestrial ecosystems. Changes in N availability modify the capacity of plants to sequester carbon (C), but despite the crucial importance for our understanding of terrestrial ecosystems, the relative contribution of different N forms to plant N nutrition in the field is not known. Until now, reliably assessing the highly dynamic pool of plant-available N in soil microsites was virtually impossible, because of the lack of adequate sampling techniques. ? For the first time we have applied a novel microdialysis technique for disturbance-free monitoring of diffusive fluxes of inorganic and organic N in 15 contrasting boreal forest soils in situ. ? We found that amino acids accounted for 80% of the soil N supply, while ammonium and nitrate contributed only 10% each. In contrast to common soil extractions, microdialysis revealed that the majority of amino acids are available for plant and mycorrhizal uptake. ? Our results suggest that the N supply of boreal forest soils is dominated by organic N as a major component of plant-available N and thus as a regulator of growth and C sequestration.     

根系氮吸收过程及其主要调节因子

氮（N）是植物根系吸收最多的矿质元素之一．全球变化将使土壤中N的有效性发生改变,影响陆地生态系统碳分配格局与过程．研究根系N吸收及其调控对预测生态系统结构和功能具有重要理论意义．由于土壤中存在多种形态的N源,长期的生物进化和环境适应导致植物根系对不同形态N的吸收部位、机理及调控有较大差别．因此,植物长期生长在以某一形态N源为主的土壤上就形成了不同的N吸收机制和策略．本文简述了近年来在植物根系N吸收和调控方面的最新研究进展,重点评述了不同形态N在土壤中的生物有效性,根系N吸收部位,N在木质部中的装载和运输,不同形态N（NO3^-、NH4^＋和有机氮）的吸收机制,以及根系N吸收的自身信号调控和环境因子对根系N吸收的影响．在此基础上,提出了目前根系N吸收研究中存在的几个问题．     

植物氮形态利用策略及对外来植物入侵性的影响

氮是影响外来植物入侵性的重要因素之一, 但相关研究多关注土壤氮水平的效应, 较少考虑氮形态的作用。为从土壤氮形态利用的角度阐释外来植物的入侵机制, 本文在植物氮形态利用策略分析的基础上, 综述了外来植物氮形态利用的偏好性及其对入侵性的影响。植物的氮形态利用策略有偏好性和可塑性两种, 这可能与植物对土壤氮形态特性的长期适应有关; 植物不仅可以对土壤氮形态做出响应, 而且还能改造土壤氮形态, 并对改变后的土壤氮形态做出反馈响应。很多外来植物入侵硝态氮占优势的干扰生境, 偏好硝态氮的外来植物与本地植物竞争硝态氮; 而偏好铵态氮的外来植物通过抑制土壤硝化作用, 营造铵态氮环境, 促进自身生长, 同时抑制偏好硝态氮的本地植物生长。然而, 植物氮形态利用策略不是一成不变的, 而是受多种生物和非生物因素共同作用影响的复杂过程, 今后应加强多因素交互作用对外来入侵植物氮形态利用策略的影响及机制研究, 更好地揭示氮形态利用策略, 尤其是氮形态利用的可塑性与外来植物入侵性的关系。     

Progressive N limitation of plant response to elevated CO2: a microbiological perspective

A major uncertainty in predicting long-term ecosystem C balance is whether stimulation of net primary production will be sustained in future atmospheric CO₂ scenarios. Immobilization of nutrients (N in particular) in plant biomass and soil organic matter (SOM) provides negative feedbacks to plant growth and may lead to progressive N limitation (PNL) of plant response to CO₂ enrichment. Soil microbes mediate N availability to plants by controlling litter decomposition and N transformations as well as dominating biological N fixation. CO₂-induced changes in C inputs, plant nutrient demand and water use efficiency often have interactive and contrasting effects on microbes and microbially mediated N processes. One critical question is whether CO₂-induced N accumulation in plant biomass and SOM will result in N limitation of microbes and subsequently cause them to obtain N from alternative sources or to alter the ecosystem N balance. We reviewed the experimental results that examined elevated CO₂ effects on microbial parameters, focusing on those published since 2000. These results in general show that increased C inputs dominate the CO₂ impact on microbes, microbial activities and their subsequent controls over ecosystem N dynamics, potentially enhancing microbial N acquisition and ecosystem N retention. We reason that microbial mediation of N availability for plants under future CO₂ scenarios will strongly depend on the initial ecosystem N status, and the nature and magnitude of external N inputs. Consequently, microbial processes that exert critical controls over long-term N availability for plants would be ecosystem-specific. The challenge remains to quantify CO₂-induced changes in these processes, and to extrapolate the results from short-term studies with step-up CO₂ increases to native ecosystems that are already experiencing gradual changes in the CO₂ concentration.     

Effect of plant nitrogen status on the contribution of arbuscular mycorrhizal hyphae to plant nitrogen uptake

The contribution of hyphae of Glomus mosseae (Nicol. and Gerd.) Gerd. and Trappe (BEG 107) to the acquisition of mineral nitrogen by Triticum aestivum L. cv. Hano (wheat) was tested under conditions of low P and high N (+N−P) or low N (−N−P). Mycorrhizal colonisation increased the shoot dry weight and plant tissue concentrations of P and cations. However, N tissue concentrations of mycorrhizal plants were not increased, although nitrate reductase activities were significantly higher (in vivo activity) in +N−P mycorrhizal compared to non-mycorrhizal roots. Severe plant N deficiency reduced the percentage root length colonised (but not the percentage viable colonisation), hyphal length, total 15 N uptake by hyphae and dry weight of mycorrhizal plants. Although mycorrhizal colonisation did not affect the overall plant N status, hyphae transported 1% (−N−P) and 7% (+N−P) of the 15 N-labelled NH₄NO₃ to mycorrhizal plants over 48 h. The higher rate of hyphal N uptake was apparently related to the more extensive hyphal growth at the higher level of plant N supply. However, the hyphal N supply was not sufficiently high to sustain adequate N nutrition of the plants supplied with very low amounts of N to the roots. Conversely, a sufficient N supply to the roots was important for the development of an extensive mycelium.     

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.     

地下鼠生物学特征及其在生态系统中的作用

地下鼠生活型、行为、种群结构的特殊性,决定了此类动物对植被、土壤及生态系统作用的多样性。地下挖能改变土壤的物理环境,导致土壤类型、发育速率、营养可利用性、微地形等的变化。地下啃食直接影响植物的形态、丰富度、种间竞争、植被类型和物种多样性、生物是及群落组成构成等,植物对植食性动物的防御策略具有更明显的化学防卫特性。地下鼠与其他植食性动物种间竞争、空间利用等关系密切,是食肉动物重要的食物资源。地下鼠对生态系统生产力、空间异质性、营养结构和循环、碳素储存以及微量气体释放等生物地球化学过程均能产生影响,显示出有别于地面植食性动物的重要性和不可替代性。     

Growth and nitrogen acquisition strategies of Acacia senegal seedlings under exponential phosphorus additions

There remains conflicting evidence on the relationship between P supply and biological N₂-fixation rates, particularly N₂-fixing plant adaptive strategies under P limitation. This is important, as edaphic conditions inherent to many economically and ecologically important semi-arid leguminous tree species, such as Acacia senegal, are P deficient. Our research objective was to verify N acquisition strategies under phosphorus limitations using isotopic techniques. Acacia senegal var. senegal was cultivated in sand culture with three levels of exponentially supplied phosphorus [low (200 μmol of P seedling⁻¹ over 12 weeks), mid (400 μmol) and high (600 μmol)] to achieve steady-state nutrition over the growth period. Uniform additions of N were also supplied. Plant growth and nutrition were evaluated. Seedlings exhibited significantly greater total biomass under high P supply compared to low P supply. Both P and N content significantly increased with increasing P supply. Similarly, N derived from solution increased with elevated P availability. However, both the number of nodules and the N derived from atmosphere, determined by the ¹⁵N natural abundance method, did not increase along the P gradient. Phosphorus stimulated growth and increased mineral N uptake from solution without affecting the amount of N derived from the atmosphere. We conclude that, under non-limiting N conditions, A. senegal N acquisition strategies change with P supply, with less reliance on N₂-fixation when the rhizosphere achieves a sufficient N uptake zone.     

Phenotypic plasticity of the maize root system in response to heterogeneous nitrogen availability

Mineral nutrients are distributed in a non-uniform manner in the soil. Plasticity in root responses to the availability of mineral nutrients is believed to be important for optimizing nutrient acquisition. The response of root architecture to heterogeneous nutrient availability has been documented in various plant species, and the molecular mechanisms coordinating these responses have been investigated particularly in Arabidopsis, a model dicotyledonous plant. Recently, progress has been made in describing the phenotypic plasticity of root architecture in maize, a monocotyledonous crop. This article reviews aspects of phenotypic plasticity of maize root system architecture, with special emphasis on describing (1) the development of its complex root system; (2) phenotypic responses in root system architecture to heterogeneous N availability; (3) the importance of phenotypic plasticity for N acquisition; (4) different regulation of root growth and nutrients uptake by shoot; and (5) root traits in maize breeding. This knowledge will inform breeding strategies for root traits enabling more efficient acquisition of soil resources and synchronizing crop growth demand, root resource acquisition and fertilizer application during crop growing season, thereby maximizing crop yields and nutrient-use efficiency and minimizing environmental pollution.     

Ectomycorrhizal impacts on plant nitrogen nutrition: emerging isotopic patterns,latitudinal variation and hidden mechanisms

Ectomycorrhizal (EcM)‐mediated nitrogen (N) acquisition is one main strategy used by terrestrial plants to facilitate growth. Measurements of natural abundance nitrogen isotope ratios (denoted as δ¹⁵N relative to a standard) increasingly serve as integrative proxies for mycorrhiza‐mediated N acquisition due to biological fractionation processes that alter ¹⁵N:¹⁴N ratios. Current understanding of these processes is based on studies from high‐latitude ecosystems where plant productivity is largely limited by N availability. Much less is known about the cause and utility of ecosystem δ¹⁵N patterns in the tropics. Using structural equation models, model selection and isotope mass balance we assessed relationships among co‐occurring soil, mycorrhizal plants and fungal N pools measured from 40 high‐ and 9 low‐latitude ecosystems. At low latitudes ¹⁵N‐enrichment caused ecosystem components to significantly deviate from those in higher latitudes. Collectively, δ¹⁵N patterns suggested reduced N‐dependency and unique sources of EcM ¹⁵N‐enrichment under conditions of high N availability typical of the tropics. Understanding the role of mycorrhizae in global N cycles will require reevaluation of high‐latitude perspectives on fractionation sources that structure ecosystem δ¹⁵N patterns, as well as better integration of EcM function with biogeochemical theories pertaining to climate‐nutrient cycling relationships.     

Responses of plant growth rate to nitrogen supply: a comparison of relative addition and N interruption treatments

This paper investigates the effects of uptake of nitrate and the availability of internal N reserves on growth rate in times of restricted supply, and examines the extent to which the response is mediated by the different pools of N (nitrate N, organic N and total N) in the plant. Hydroponic experiments were carried out with young lettuce plants (Lactuca sativa L.) to compare responses to either an interruption in external N supply or the imposition of different relative N addition rate (RAR) treatments. The resulting relationships between whole plant relative growth rate (RGR) and N concentration varied between linear and curvilinear (or possibly bi-linear) forms depending on the treatment conditions. The relationship was curvilinear when the external N supply was interrupted, but linear when N was supplied by either RAR methods or as a supra-optimal external N supply. These differences resulted from the ability of the plant to use external sources of N more readily than their internal N reserves. These results show that when sub-optimal sources of external N were available, RGR was maintained at a rate which was dependent on the rate of nitrate uptake by the roots. Newly acquired N was channelled directly to the sites of highest demand, where it was assimilated rapidly. As a result, nitrate only tended to accumulate in plant tissues when its supply was essentially adequate. By comparison, plants forced to rely solely on their internal reserves were never able to mobilize and redistribute N between tissues quickly enough to prevent reductions in growth rate as their tissue N reserves declined. Evidence is presented to show that the rate of remobilization of N depends on the size and type of the N pools within the plant, and that changes in their rates of remobilization and/or transfer between pools are the main factors influencing the form of the relationship between RGR and N concentration.     

Plants actively control nitrogen cycling: uncorking the microbial bottleneck

Ecologists have tried to link plant species composition and ecosystem properties since the inception of the ecosystem concept in ecology. Many have observed that biological communities could feed back to, and not simply result from, soil properties. But which group of organisms, plants or microorganisms, drive those feedback systems? Recent research asserts that soil microorganisms preclude plant species feedback to soil nitrogen (N) transformations due to strong microbial control of soil N cycling. It has been well documented that litter properties influence soil N cycling. In this review, we stress that under many circumstances plant species exert a major influence over soil N cycling rates via unique N attainment strategies, thus influencing soil N availability and their own fitness. We offer two testable mechanisms by which plants impart active control on the N cycle and thereby allow for plant-litter-soil-plant feedback. Finally, we describe the characteristics of plants and ecosystems that are most likely to exhibit feedback.     

Molecular and physiological interactions of urea and nitrate uptake in plants

While nitrate acquisition has been extensively studied, less information is available on transport systems of urea. Furthermore, the reciprocal influence of the two sources has not been clarified, so far. In this review, we will discuss recent developments on plant response to urea and nitrate nutrition. Experimental evidence suggests that, when urea and nitrate are available in the external solution, the induction of the uptake systems of each nitrogen (N) source is limited, while plant growth and N utilization is promoted. This physiological behavior might reflect cooperation among acquisition processes, where the activation of different N assimilatory pathways (cytosolic and plastidic pathways), allow a better control on the nutrient uptake. Based on physiological and molecular evidence, plants might increase (N) metabolism promoting a more efficient assimilation of taken-up nitrogen. The beneficial effect of urea and nitrate nutrition might contribute to develop new agronomical approaches to increase the (N) use efficiency in crops.     

The impacts of increased nitrate supply on Catharanthus roseus growth and alkaloid accumulations under ultraviolet-B stress

It has been reported that nitrate availability was able to modify the detrimental effects induced by excess ultraviolet-B (UV-B) radiation on plants. In this study, the medical plant Catharanthus roseus was subjected to UV-B stress and altered levels of nitrate nutrition to investigate their influence in a sole or combined way on growth and alkaloid productions. Our results showed that the UV-B stress obviously inhibited growth and led to damages of oxidative stress and lipid peroxidation. The simultaneous supply of higher nitrate nutrition could largely alleviate the inhibitory effects and damage symptom under the UV-B stress in C. roseus. Meanwhile, the UV-B-absorbing compounds as well as three alkaloids, vinblastine, vindoline, and catharanthine, were observed to have a remarkable elevation. These compounds were considered to serve as protectants of UV-B radiation. It was concluded that an increased nitrogen (N) supply could not only alleviate the inhibitory effect of UV-B stress on plant growth, but also enhance the accumulation of pharmaceutically used alkaloid in these plants. We proposed that the enrichment of N nutrition might provide more N source for alkaloid synthesis induced by UV-B radiation, eventually resulting in an increase of alkaloids accumulation.     

植物养分捕获策略随成土年龄的变化及生态学意义

自然成土过程中土壤养分的变化与植被原生演替常同时发生。随成土年龄变化的植物养分捕获策略(NASs)对植物竞争能力和演替过程具有重要影响。该文将植物NASs划分为细根、微生物、特殊根系、食虫和寄生策略等5个类型; 发现植物NASs的多样性随成土年龄的增加呈哑铃型变化模式; 特殊根系策略对植物捕获养分的作用在成土中期最小、后期最大, 细根和微生物策略的作用随成土年龄的增加逐渐降低; 分析了成土过程中NASs对植物种间关系影响的变化, 发现NASs对成土早期植物的促进作用和中期的竞争关系具有重要影响, 而成土后期多样和互补的NASs对植被群落的稳定共存及多样性的形成具有影响; 提出应进一步探究成土过程中土壤养分与植物NASs变化之间的定量关系, 开展更多研究以阐明NASs对植被原生演替、物种多样性形成和成土过程的贡献与机理。     

Simulating mycorrhiza contribution to forest C- and N cycling-the MYCOFON model

Although mycorrhiza has been identified to be of major importance for plant nutrition and ecosystem stability, existing C- and N- simulation models on the ecosystem scale do not explicitly consider the feedbacks between ectomycorrhizal fungi and plants. We present a simple dynamic feedback model which allows estimating the main C- and N- flows between ectomycorrhizal fungi and tree roots in order to test the sensitivity of the system fungus-tree to environmental parameters and to assess the fungal contribution to plant N nutrition. Sensitivity tests carried out showed that the model responses to variations of model parameters, particularly with regard to N availability, are in agreement with published results from field and laboratory studies. However, there are still some processes and parameters which are not well constrained. Fungal N uptake rates and the ratio between mycelium, hartig net, and mantle biomass are parameters which significantly affect model results but for which published data are scarce or missing. Nevertheless, the model is already providing a platform to test our understanding of the importance of mycorrhiza for forest stand nutrition. Future coupling to a mechanistic ecosystem model will allow simulating the importance of mycorrhization for e.g. stand growth and C and N retention.     

Stability of the Nitrogen Concentration of Inoculated White Lupins during Pod Development

The general pattern of decrease of the 'critical' plant N concentration(i.e. minimum concentration required for maximum growth rate)during growth has been described for several C₃ non grain-legumespecies, and this can be used as a reference curve for diagnosisof N nutrition in these species. The present study was undertakento investigate changes of N concentration during growth of agrain legume, in different conditions of N nutrition. Whitelupin (Lupinus albus L.) was grown for six crop seasons in fieldtrials in which inoculation with Rhizobium lupini, nitrogenfertilizer rate, cultivar and plant density were density weremanipulated. The yield and dry matter production of noninoculatedplants were lower than, or at the best similar to, those ofinoculated plants, whatever the level of N supply. From anthesisto the beginning of seed filling, the N concentration of shootsof inoculated plants was found to be remarkably stable betweenyears, N fertilization regimes, cultivars, and for individualplants within a plot. Nitrogen concentration only varied withplant density. By contrast, the N concentration of noninoculatedplants was highly variable and generally lower than that ofinoculated plants, whatever the level of N supply. The highand stable N concentration of inoculated plants did not appearto be necessary for maximum growth rate but seemed to be requiredfor maximum production of seed dry matter and N. The potentialuse of these results to diagnose, in any white lupin crop, aninefficiency of the lupin-R. lupini interaction is evaluated.Copyright1993, 1999 Academic Press Lupinus albus L., white lupin, N₂ concentration, inoculated plants, non-inoculated plants, N₂ fixation efficiency, diagnosis     

Phosphate sensing in higher plants

Phosphate (Pi) plays a central role as reactant and effector molecule in plant cell metabolism. However, Pi is the least accessible macronutrient in many ecosystems and its low availability often limits plant growth. Plants have evolved an array of molecular and morphological adaptations to cope with Pi limitation, which include dramatic changes in gene expression and root development to facilitate Pi acquisition and recycling. Although physiological responses to Pi starvation have been increasingly studied and understood, the initial molecular events that monitor and transmit information on external and internal Pi status remain to be elucidated in plants. This review summarizes molecular and developmental Pi starvation responses of higher plants and the evidence for coordinated regulation of gene expression, followed by a discussion of the potential involvement of plant hormones in Pi sensing and of molecular genetic approaches to elucidate plant signalling of low Pi availability. Complementary genetic strategies in Arabidopsis thaliana have been developed that are expected to identify components of plant signal transduction pathways involved in Pi sensing. Innovative screening methods utilize reporter gene constructs, conditional growth on organophosphates and the inhibitory properties of the Pi analogue phosphite, which hold the promise for significant advances in our understanding of the complex mechanisms by which plants regulate Pi-starvation responses.