Roots, nitrogen transformations, and ecosystem services.

This review considers some of the mechanistic processes that involve roots in the soil nitrogen (N) cycle, and their implications for the ecological functions that retain N within ecosystems: 1) root signaling pathways for N transport systems, and feedback inhibition, especially for NO(3)(-) uptake; 2) dependence on the mycorrhizal and Rhizobium/legume symbioses and their tradeoffs for N acquisition; 3) soil factors that influence the supply of NH(4)(+) and NO(3)(-) to roots and soil microbes; and 4) rhizosphere processes that increase N cycling and retention, such as priming effects and interactions with the soil food web. By integrating information on these plant-microbe-soil N processes across scales and disciplinary boundaries, we propose ideas for better manipulating ecological functions and processes by which the environment provides for human needs, i.e., ecosystem services. Emphasis is placed on agricultural systems, effects of N deposition in natural ecosystems, and ecosystem responses to elevated CO(2) concentrations. This shows the need for multiscale approaches to increase human dependence on a biologically based N supply.

[1]  R. Bol,et al.  Preferences for different nitrogen forms by coexisting plant species and soil microbes. , 2008, Ecology.

[2]  R. Richards,et al.  Physiological traits and cereal germplasm for sustainable agricultural systems , 2007, Euphytica.

[3]  J. Six,et al.  Elevated CO2 increases nitrogen rhizodeposition and microbial immobilization of root-derived nitrogen. , 2007, The New phytologist.

[4]  P. Tillard,et al.  The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches , 2006, Proceedings of the National Academy of Sciences.

[5]  P. Reich,et al.  Carbon-Nitrogen Interactions in Terrestrial Ecosystems in Response to Rising Atmospheric Carbon Dioxide , 2006 .

[6]  Z. Cardon,et al.  Resource Exchange in the Rhizosphere: Molecular Tools and the Microbial Perspective , 2006 .

[7]  Michael Wagner,et al.  Wastewater treatment: a model system for microbial ecology. , 2006, Trends in biotechnology.

[8]  Johan Six,et al.  Interactions between plant growth and soil nutrient cycling under elevated CO2: a meta‐analysis , 2006 .

[9]  Erik J Veneklaas,et al.  Root structure and functioning for efficient acquisition of phosphorus: Matching morphological and physiological traits. , 2006, Annals of botany.

[10]  P. Högberg,et al.  Towards a more plant physiological perspective on soil ecology. , 2006, Trends in ecology & evolution.

[11]  D. Herman,et al.  Root Influence on Nitrogen Mineralization and Nitrification in Avena barbata Rhizosphere Soil , 2006 .

[12]  G. Subbarao,et al.  A bioluminescence assay to detect nitrification inhibitors released from plant roots: a case study with Brachiaria humidicola , 2006, Plant and Soil.

[13]  J. Vivanco,et al.  The role of root exudates in rhizosphere interactions with plants and other organisms. , 2006, Annual review of plant biology.

[14]  P. Hugenholtz,et al.  Numbers and locations of native bacteria on field-grown wheat roots quantified by fluorescence in situ hybridization (FISH). , 2006, Environmental microbiology.

[15]  J. Passioura,et al.  Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere. , 2006, Annals of botany.

[16]  G. Asner,et al.  Nitrogen cycling in tropical and temperate savannas , 2006 .

[17]  P. Reich,et al.  Nitrogen limitation constrains sustainability of ecosystem response to CO2 , 2006, Nature.

[18]  J. Six,et al.  Arbuscular Mycorrhizas, Microbial Communities, Nutrient Availability, and Soil Aggregates in Organic Tomato Production , 2006, Plant and Soil.

[19]  K. Yano,et al.  Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied , 2005 .

[20]  A. Lüscher,et al.  Significance of Legumes for the Distribution of Plant Species in Grassland Ecosystems at Different Altitudes in the Alps , 2005, Plant Ecology.

[21]  Christopher B Field,et al.  Responses of Grassland Production to Single and Multiple Global Environmental Changes , 2005, PLoS biology.

[22]  S. Filleur,et al.  Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana , 2005, Planta.

[23]  Kate M. Scow,et al.  Microbial responses and nitrous oxide emissions during wetting and drying of organically and conventionally managed soil under tomatoes , 2005, Biology and Fertility of Soils.

[24]  A. Miller,et al.  Root Nitrogen Acquisition and Assimilation , 2005, Plant and Soil.

[25]  R. Miller,et al.  Mycorrhizas: Gene to Function , 2005, Plant and Soil.

[26]  M. Peoples,et al.  Can the Synchrony of Nitrogen Supply and Crop Demand be Improved in Legume and Fertilizer-based Agroecosystems? A Review , 2005, Nutrient Cycling in Agroecosystems.

[27]  T. Cavagnaro,et al.  Functional diversity in arbuscular mycorrhizas: exploitation of soil patches with different phosphate enrichment differs among fungal species , 2005 .

[28]  Pamela A. Matson,et al.  Agricultural runoff fuels large phytoplankton blooms in vulnerable areas of the ocean , 2005, Nature.

[29]  Edward B. Rastetter,et al.  CONTROLS ON NITROGEN CYCLING IN TERRESTRIAL ECOSYSTEMS: A SYNTHETIC ANALYSIS OF LITERATURE DATA , 2005 .

[30]  K. Treseder A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. , 2004, The New phytologist.

[31]  A. Hodge,et al.  Plant and mycorrhizal regulation of rhizodeposition. , 2004, The New phytologist.

[32]  G. Asner,et al.  Nitrogen Cycles: Past, Present, and Future , 2004 .

[33]  D. Phillips,et al.  Microbial Products Trigger Amino Acid Exudation from Plant Roots1 , 2004, Plant Physiology.

[34]  Shimon Rachmilevitch,et al.  Nitrate assimilation in plant shoots depends on photorespiration. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Herbert Blum,et al.  Ten years of free‐air CO2 enrichment altered the mobilization of N from soil in Lolium perenne L. swards , 2004 .

[36]  L. Verchot,et al.  Soil emissions of nitric oxide in two forest watersheds subjected to elevated N inputs , 2004 .

[37]  S. Frey,et al.  Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests , 2004 .

[38]  L. Verchot,et al.  Gross nitrogen process rates in temperate forest soils exhibiting symptoms of nitrogen saturation , 2004 .

[39]  W. McDowell,et al.  Ecosystem response to 15 years of chronic nitrogen additions at the Harvard Forest LTER, Massachusetts, USA , 2004 .

[40]  G. Berntson,et al.  Effects of chronic N additions on tissue chemistry, photosynthetic capacity, and carbon sequestration potential of a red pine (Pinus resinosa Ait.) stand in the NE United States , 2004 .

[41]  N. von Wirén,et al.  Regulatory levels for the transport of ammonium in plant roots. , 2004, Journal of experimental botany.

[42]  M. Bonkowski Protozoa and plant growth: the microbial loop in soil revisited. , 2004, The New phytologist.

[43]  Angela Hodge,et al.  The plastic plant: root responses to heterogeneous supplies of nutrients , 2004 .

[44]  J. Schimel,et al.  NITROGEN MINERALIZATION: CHALLENGES OF A CHANGING PARADIGM , 2004 .

[45]  T. Yamaya,et al.  Feedback regulation of the ammonium transporter gene family AMT1 by glutamine in rice. , 2003, Plant & cell physiology.

[46]  Keith A. Smith,et al.  Exchange of greenhouse gases between soil and atmosphere: interactions of soil physical factors and biological processes , 2003 .

[47]  A. Glass Nitrogen Use Efficiency of Crop Plants: Physiological Constraints upon Nitrogen Absorption , 2003 .

[48]  P. Reich,et al.  Contrasting growth response of an N2-fixing and non-fixing forb to elevated CO2: dependence on soil N supply , 2003, Plant and Soil.

[49]  N. von Wirén,et al.  Distinct expression and function of three ammonium transporter genes (OsAMT1;1-1;3) in rice. , 2003, Plant & cell physiology.

[50]  Robert M. Boddey,et al.  The success of BNF in soybean in Brazil , 2003, Plant and Soil.

[51]  I. Jakobsen,et al.  Beyond the rhizosphere: growth and function of arbuscular mycorrhizal external hyphae in sands of varying pore sizes , 2003, Plant and Soil.

[52]  D. Strong,et al.  MOLECULAR CONTROL POINTS IN RHIZOSPHERE FOOD WEBS , 2003 .

[53]  Davey L. Jones,et al.  HOW ROOTS CONTROL THE FLUX OF CARBON TO THE RHIZOSPHERE , 2003 .

[54]  M. Fenn,et al.  Nitrogen Emissions, Deposition, and Monitoring in the Western United States , 2003 .

[55]  S. Okabe,et al.  Ammonia-oxidizing bacteria on root biofilms and their possible contribution to N use efficiency of different rice cultivars , 2003, Plant and Soil.

[56]  M. Bonkowski,et al.  Do soil protozoa enhance plant growth by hormonal effects , 2002 .

[57]  O. Leyser,et al.  Root system architecture determines fitness in an Arabidopsis mutant in competition for immobile phosphate ions but not for nitrate ions , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[58]  T. Sinclair,et al.  Physiological traits for crop yield improvement in low N and P environments , 2002, Plant and Soil.

[59]  B. Forde Local and long-range signaling pathways regulating plant responses to nitrate. , 2002, Annual review of plant biology.

[60]  M. Okamoto,et al.  The regulation of nitrate and ammonium transport systems in plants. , 2002, Journal of experimental botany.

[61]  F. Daniel-Vedele,et al.  Nitrate transport in plants: which gene and which control? , 2002, Journal of experimental botany.

[62]  Xiang Jia Min,et al.  Effects of ammonium and inorganic carbon enrichment on growth and yield of a hydroponic tomato crop , 2002 .

[63]  A. Hodge,et al.  An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material , 2001, Nature.

[64]  D. Frank,et al.  CAN PLANTS STIMULATE SOIL MICROBES AND THEIR OWN NUTRIENT SUPPLY? EVIDENCE FROM A GRAZING TOLERANT GRASS , 2001 .

[65]  P. Brookes,et al.  Soil microbial biomass is triggered into activity by trace amounts of substrate , 2001 .

[66]  Thomas L. Thompson,et al.  Elevated CO2, drought and soil nitrogen effects on wheat grain quality , 2001 .

[67]  P. Tillard,et al.  Differential regulation of the NO3- and NH4+ transporter genes AtNrt2.1 and AtAmt1.1 in Arabidopsis: relation with long-distance and local controls by N status of the plant. , 2001, The Plant journal : for cell and molecular biology.

[68]  D. T. Britto,et al.  Futile transmembrane NH4+ cycling: A cellular hypothesis to explain ammonium toxicity in plants , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[69]  J A Raven,et al.  Roots: evolutionary origins and biogeochemical significance. , 2001, Journal of experimental botany.

[70]  C. Field,et al.  Nitrogen limitation of microbial decomposition in a grassland under elevated CO2 , 2001, Nature.

[71]  R. Conrad,et al.  Influence of soil properties on the turnover of nitric oxide and nitrous oxide by nitrification and denitrification at constant temperature and moisture , 2000, Biology and Fertility of Soils.

[72]  A. Lüscher,et al.  Direct evidence that symbiotic N2 fixation in fertile grassland is an important trait for a strong response of plants to elevated atmospheric CO2 , 2000 .

[73]  T. Becker,et al.  Manipulating the pathway of ammonia assimilation through genetic engineering and breeding: consequences to plant physiology and plant development , 2000, Plant and Soil.

[74]  J. Schjoerring,et al.  Regulation of high-affinity nitrate transporter genes and high-affinity nitrate influx by nitrogen pools in roots of barley. , 2000, Plant physiology.

[75]  P. B. Tinker,et al.  Solute Movement in the Rhizosphere , 2000 .

[76]  D. Phillips,et al.  Identification of lumichrome as a sinorhizobium enhancer of alfalfa root respiration and shoot growth. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[77]  H. Kronzucker,et al.  Atamt1 Gene Expression and Nh 4 + Uptake in Roots of Arabidopsis Thaliana: Evidence for Regulation by Root Glutamine Levels , 2022 .

[78]  R. Guy,et al.  A comparative study of fluxes and compartmentation of nitrate and ammonium in early‐successional tree species , 1999 .

[79]  Alastair Fitter,et al.  Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete , 1999 .

[80]  P W Barlow,et al.  Dual pathways for regulation of root branching by nitrate. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[81]  W. Frommer,et al.  Three Functional Transporters for Constitutive, Diurnally Regulated, and Starvation-Induced Uptake of Ammonium into Arabidopsis Roots , 1999, Plant Cell.

[82]  B. Griffiths,et al.  Plant root proliferation in nitrogen–rich patches confers competitive advantage , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[83]  J. Schjoerring,et al.  Dynamic Interactions between Root NH4+ Influx and Long-Distance N Translocation in Rice: Insights into Feedback Processes , 1998 .

[84]  A. Bloom,et al.  Ammonium, nitrate, and proton fluxes along the maize root , 1998 .

[85]  William H. McDowell,et al.  Nitrogen Saturation in Temperate Forest Ecosystems , 1998 .

[86]  B. Griffiths,et al.  Root proliferation, soil fauna and plant nitrogen capture from nutrient‐rich patches in soil , 1998 .

[87]  H. de Kroon,et al.  Root morphological plasticity and nutrient acquisition of perennial grass species from habitats of different nutrient availability , 1998, Oecologia.

[88]  H. Rennenberg,et al.  Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. , 1998, The New phytologist.

[89]  P. Ineson,et al.  Elevated CO2 reduces the nitrogen concentration of plant tissues , 1998 .

[90]  R. B. Jackson,et al.  A global budget for fine root biomass, surface area, and nutrient contents. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[91]  J. Graham,et al.  Functioning of mycorrhizal associations along the mutualism–parasitism continuum* , 1997 .

[92]  F. Chapin,et al.  Tundra Plant Uptake of Amino Acid and NH4+ Nitrogen in Situ: Plants Complete Well for Amino Acid N , 1996 .

[93]  Dennis P. Swaney,et al.  Regional nitrogen budgets and riverine N & P fluxes for the drainages to the North Atlantic Ocean: Natural and human influences , 1996 .

[94]  T. J. Ruth,et al.  Ammonium Uptake by Rice Roots (II. Kinetics of 13NH4+ Influx across the Plasmalemma) , 1993, Plant physiology.

[95]  A. Smith,et al.  Isolation and Sequencing of Tomato Fruit Sucrose Synthase cDNA , 1993, Plant physiology.

[96]  J. V. Purves,et al.  Nitrogen Assimilation and the Control of Ammonium and Nitrate Absorption by Maize Roots , 1992 .

[97]  R. L. Warner,et al.  Root respiration associated with ammonium and nitrate absorption and assimilation by barley. , 1992, Plant physiology.

[98]  L. Kochian,et al.  Studies of the Uptake of Nitrate in Barley : IV. Electrophysiology. , 1992, Plant physiology.

[99]  M. Gersani,et al.  Development correlations between roots in heterogeneous environments , 1992 .

[100]  T. Ruth,et al.  Studies of the Uptake of Nitrate in Barley III. COMPARTMENTATION OF NO3 , 1991 .

[101]  B. Hetrick,et al.  Mycorrhizas and root architecture , 1991, Experientia.

[102]  T. Rufty,et al.  Studies of the Uptake of Nitrate in Barley: I. Kinetics of NO(3) Influx. , 1990, Plant physiology.

[103]  E. Davidson,et al.  Microbiological basis of NO and N2O production and consumption in soil. , 1989 .

[104]  C. Raper,et al.  Proliferation of maize (Zea mays L.) roots in response to localized supply of nitrate. , 1989, Journal of experimental botany.

[105]  S. A. Barber,et al.  Sensitivity Analysis of Parameters Used in Simulating K Uptake with a Mechanistic Mathematical Model1 , 1983 .

[106]  L. K. Porter,et al.  HYPHAL UPTAKE AND TRANSPORT OF NITROGEN FROM TWO 15N‐LABELLED SOURCES BY GLOMUS MOSSEAE, A VESICULAR‐ARBUSCULAR MYCORRHIZAL FUNGUS * , 1983 .

[107]  M. Drew,et al.  COMPARISON OF THE EFFECTS OF A LOCALISED SUPPLY OF PHOSPHATE, NITRATE, AMMONIUM AND POTASSIUM ON THE GROWTH OF THE SEMINAL ROOT SYSTEM, AND THE SHOOT, IN BARLEY , 1975 .

[108]  Laurie E. Drinkwater,et al.  Nutrients in agroecosystems: Rethinking the management paradigm , 2007 .

[109]  Meghan L. Avolio,et al.  Nitrogen transport in the ectomycorrhiza association: the Hebeloma cylindrosporum-Pinus pinaster model. , 2007, Phytochemistry.

[110]  Laurie E. Drinkwater,et al.  Understanding and managing the rhizosphere in agroecosystems , 2007 .

[111]  M. Burger,et al.  Plant and microbial nitrogen use and turnover: Rapid conversion of nitrate to ammonium in soil with roots , 2005, Plant and Soil.

[112]  H. Wu,et al.  The rhizosphere: the key functional unit in plant/soil/microbial interactions in the field. implications for the understanding of allelopathic effects. , 2005 .

[113]  J. Six,et al.  Efficiency of Fertilizer Nitrogen in Cereal Production: Retrospects and Prospects , 2005 .

[114]  Naeem,et al.  Ecosystems and Human Well-Being: Biodiversity Synthesis , 2005 .

[115]  B. Griffiths,et al.  Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in soil , 2004, Plant and Soil.

[116]  A. Mosier,et al.  Nitrogen fertilizer: an essential component of increased food, feed, and fiber production. , 2004 .

[117]  J. Olesen,et al.  Societal responses for addressing nitrogen fertilizer needs: Balancing food production and environmental concerns , 2004 .

[118]  M. Tibbett Roots, foraging and the exploitation of soil nutrient patches: the role of mycorrhizal symbiosis , 2000 .

[119]  W. McDowell,et al.  The globalization of N deposition: ecosystem consequences in tropical environments , 1999 .

[120]  Harvey Alexander Nature's services: Societal dependence on natural ecosystems: Edited by Gretchen C. Daily Island Press, 1997, $24.95, 392 pages , 1999 .

[121]  U. Hartwig,et al.  The regulation of symbiotic N2 fixation: a conceptual model of N feedback from the ecosystem to the gene expression level , 1998 .

[122]  A. Fitter 11 – Architecture and Biomass Allocation as Components of the Plastic Response of Root Systems to Soil Heterogeneity , 1994 .

[123]  Miaoying Wang Ammonium uptake by rice roots , 1994 .

[124]  D. Arora Soil and plants , 1991 .

[125]  M. Firestone,et al.  Short-term partitioning of ammonium and nitrate between plants and microbes in an annual grassland , 1989 .

[126]  M. Clarholm Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen , 1985 .