Evolved Strategies in Nitrogen Acquisition by Plants

Eleven features of nitrogen metabolism in the plant and in the ecosystem are delineated, each appearing to have negative survival value, especially negative effects on yield. These include apparent failures in controls over N2 fixation and over nitrate uptake; preventable energy losses in soil microbial metabolism and in root reduction in nitrate; preventable mass losses of nitrogen via denitrification and ammonia volatilization, and insufficient partitioning of photosynthetic energy to support N2 fixation in N-limited ecosystems. A quantitative examination of the energetics of metabolizing N2, NH3, and NO3 - reveals behind often high costs some energy inefficiencies required for sufficiently fast kinetics and some compromises with other metabolisms. Cost: benefit ratios can be defined for assimilation of the three forms of N, and each ratio may vary significantly according to other physiological demands, such as pH control at the rhizosphere or stomatal closure for efficient use of water. For the individual plant, I then proposed a number of metabolic principles based on the energetics inside the plant, suitably constrained, and also compromised with the metabolic strategy of soil bacteria. These principles rank-order the preferences for N sources. They also outline complementary roles for normal fast or feedback controls based on immediate environmental variations, integrative controls over relative growth rates of tissues, and nonnutritional controls that schedule maturation. The overall view is that plants in their N-nutrition follow a set of quantifiable strategies, or simple patterns in metabolic adaptations to varied conditions. The goal is to maximize yield over a range of conditions, but at times to sacrifice yield potential for clear requirements such as early competitiveness in canopy expansion. The strategies are heavily conditioned by energetics. Indeed, many are principally patterns of optimally allocating photosynthetic (energy) resources between alternatives such as N2 versus NO3 - assimilation. I note that agricultural breeding to alter adaptation ranges and to increase yield readily incurs conflicts of desired traits, such as that between ability to use high levels of fertilizer N and ability to mature. I propose that conflicts are easier to foresee between strategies (controlled blocks of biochemical activities, in genetically fixed patterns) than between individual biochemical activities. A second general use of the strategic view may be simpler prediction of overall plant responses to environmental changes (in atmospheric CO2 levels, soil aeration and acidity, etc.). When one considers competitive uptake of nitrogen by all the plants in an ecosystem, additional plant responses are seen as necessary. Also, a few inherent instabilities of strategies are seen in N2 fixation and in denitrification.

[1]  J. Pate,et al.  Efficiency and regulation of root respiration in a legume: Effects of the N source , 1980 .

[2]  D. Phillips Efficiency of Symbiotic Nitrogen Fixation in Legumes , 1980 .

[3]  D. T. Canvin,et al.  Reduction of Nitrate via a Dicarboxylate Shuttle in a Reconstituted System of Supernatant and Mitochondria from Spinach Leaves. , 1980, Plant physiology.

[4]  J. Pate,et al.  Economy of Carbon and Nitrogen in a Nodulated and Nonnodulated (NO(3)-grown) Legume. , 1979, Plant physiology.

[5]  J. Pate,et al.  Economy of Photosynthate Use in Nitrogen-fixing Legume Nodules: Observations on Two Contrasting Symbioses. , 1979, Plant physiology.

[6]  D. Rains,et al.  Influence of light and ambient carbon dioxide concentration on nitrate assimilation by intact barley seedlings. , 1979, Plant physiology.

[7]  M. Johnson,et al.  Managing the Heavy Metals on the Land. , 1979 .

[8]  J. O. Klemmedson Ecological Importance of Actinomycete-Nodulated Plants in the Western United States , 1979, Botanical Gazette.

[9]  C. E. Powell,et al.  The Respiratory Costs of Nitrogen Fixation in Soyabean, Cowpea, and White Clover II. COMPARISONS OF THE COST OF NITROGEN FIXATION AND THE UTILIZATION OF COMBINED NITROGEN , 1979 .

[10]  M. Caldwell Root Structure: The Considerable Cost of Belowground Function , 1979 .

[11]  G. Farquhar Carbon Assimilation in Relation to Transpiration and Fluxes of Ammonia , 1979 .

[12]  R. L. Steiner,et al.  Substrate inhibition of nitrification , 1979 .

[13]  Dennis R. Drewes,et al.  Solubility of ammonia in water at low concentrations , 1979 .

[14]  G. Schrauzer,et al.  Nitrogen reducing solar cells , 1979 .

[15]  T. Ingestad,et al.  Nitrogen stress in birch seedlings. II. N, K, P, Ca, and Mg nutrition , 1979 .

[16]  W. G. Sanford Cycling of mineral nutrients in agricultural ecosystems , 1979 .

[17]  C. Givan Metabolic detoxification of ammonia in tissues of higher plants , 1979 .

[18]  N. Karimian,et al.  Molybdenum Availability as Predicted from Selected Soil Chemical Properties 1 , 1979 .

[19]  J. Lee,et al.  Ecological Aspects of Nitrogen Assimilation , 1979 .

[20]  Howard M. Taylor,et al.  The Role of Rooting Characteristics in the Supply of Water to Plants , 1979 .

[21]  C. Osmond Integration of photosynthetic carbon metabolism during stress. , 1979, Basic life sciences.

[22]  W. Cleland Substrate inhibition. , 1979, Methods in enzymology.

[23]  D. Button On the theory of control of microbial growth kinetics by limiting nutrient concentrations , 1978 .

[24]  E. Ochiai Principles in the selection of inorganic elements by organisms--application to molybdenum enzymes. , 1978, Bio Systems.

[25]  J. L. Harley Review lecture: Ectomycorrhizas as nutrient absorbing organs , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[26]  M. Lodhi,et al.  COMPARATIVE INHIBITION OF NITRIFIERS AND NITRIFICATION IN A FOREST COMMUNITY AS A RESULT OF THE ALLELOPATHIC NATURE OF VARIOUS TREE SPECIES , 1978 .

[27]  C. Neyra,et al.  Pathway for Nitrate Assimilation in Corn (Zea mays L.) Leaves: Cellular Distribution of Enzymes and Energy Sources for Nitrate Reduction. , 1978, Plant physiology.

[28]  V. Gutschick Energy and nitrogen fixation , 1978 .

[29]  J. A. Hellen Food Production and Consumption: The Efficiency of Human Food Chains and Nutrient Cycles , 1978 .

[30]  R. G. Woodmansee Additions and Losses of Nitrogen in Grassland Ecosystems , 1978 .

[31]  D. Lawlor,et al.  Photosynthesis, Respiration, and Carbon Assimilation in Water-Stressed Maize at Two Oxygen Concentrations , 1978 .

[32]  C. Jordan,et al.  Nutrient Retention by the Root Mat of an Amazonian Rain Forest , 1978 .

[33]  J. Pate,et al.  Partitioning and Utilization of Net Photosynthate in a Nodulated Annual Legume , 1978 .

[34]  S. A. Barber Solute movement in the soil–root system , 1978, Nature.

[35]  R. Morrall,et al.  Energy Flow in the Plant—Microorganism System , 1978 .

[36]  W. Silvester Nitrogen Fixation and Mineralisation in Kauri (Agathis australis) Forest in New Zealand , 1978 .

[37]  D. Rains,et al.  FACTORS INFLUENCING NITRATE ACQUISITION BY PLANTS; ASSIMILATION AND FATE OF REDUCED NITROGEN , 1978 .

[38]  C. Neyra Interactions of Plant Photosynthesis with Dinitrogen Fixation and Nitrate Assimilation , 1978 .

[39]  D. Egli,et al.  Influence of N Stress on Leaf Senescence and N Redistribution in Soybeans1 , 1978 .

[40]  R. Brown,et al.  A Difference in N Use Efficiency in C3 and C4 Plants and its Implications in Adaptation and Evolution1 , 1978 .

[41]  J. Streeter Effect of N Starvation of Soybean Plants at Various Stages of Growth on Seed Yield and N Concentration of Plant Parts at Maturity1 , 1978 .

[42]  D. Tempest,et al.  Eco-Physiological Aspects of Microbial Growth in Aerobic Nutrient-Limited Environments , 1978 .

[43]  P. Roger,et al.  Ndn2-fixing algal biomass in Senegal rice fields. , 1978 .

[44]  J. L. Harley Ectomycorrhizas as nutrient absorbing organs. , 1978, Proceedings of the Royal Society of London. Series B, Biological sciences.

[45]  P. Board Redox regulation of atmospheric oxygen and its consequences , 1977, Nature.

[46]  J. Pate,et al.  Utilization of net photosynthate for nitrogen fixation and protein production in an annual legume. , 1977, Plant physiology.

[47]  J. .. Bassham Increasing crop production through more controlled photosynthesis. , 1977, Science.

[48]  D. W. Nelson,et al.  Nitrification Inhibitors—New Tools for Food Production , 1977 .

[49]  G. A. Dawson Atmospheric ammonia from undisturbed land , 1977 .

[50]  J. Silsbury Energy requirement for symbiotic nitrogen fixation , 1977, Nature.

[51]  D. Lawlor,et al.  Water Stress Induced Changes in the Amounts of Some Photosynthetic Assimilation Products and Respiratory Metabolites of Sunflower Leaves , 1977 .

[52]  J. M. Day,et al.  Nitrogen Nutrition of Cowpea (Vigna unguiculata). I. Effects of Applied Nitrogen and Symbiotic Nitrogen Fixation on Growth and Seed Yield , 1977, Experimental Agriculture.

[53]  M. Lodhi,et al.  THE INFLUENCE AND COMPARISON OF INDIVIDUAL FOREST TREES ON SOIL PROPERTIES AND POSSIBLE INHIBITION OF NITRIFICATION DUE TO INTACT VEGETATION , 1977 .

[54]  J. O. Reuss,et al.  A Grassland Nitrogen Flow Simulation Model , 1977 .

[55]  C. Neyra,et al.  Nitrate reduction nitrogenase activity in Spirillum lipoferum1. , 1977, Canadian journal of microbiology.

[56]  R. Hardy,et al.  POSSIBLE ROUTES TO INCREASE THE CONVERSION OF SOLAR ENERGY TO FOOD AND FEED BY GRAIN LEGUMES AND CEREAL GRAINS (CROP PRODUCTION): CO2 AND N2 FIXATION, FOLIAR FERTILIZATION, AND ASSIMILATE PARTITIONING , 1977 .

[57]  C. W. Jones,et al.  Bacterial respiration. , 1977, Bacteriological reviews.

[58]  I. R. Cowan,et al.  Stomatal function in relation to leaf metabolism and environment. , 1977, Symposia of the Society for Experimental Biology.

[59]  J. Raven,et al.  NITROGEN ASSIMILATION AND TRANSPORT IN VASCULAR LAND PLANTS IN RELATION TO INTRACELLULAR pH REGULATION , 1976 .

[60]  T. Sinclair,et al.  Analysis of the carbon and nitrogen limitations to soybean yield , 1976 .

[61]  W. Cram Negative Feedback Regulation of Transport in Cells. The Maintenance of Turgor, Volume and Nutrient Supply , 1976 .

[62]  D. G. Bishop,et al.  The C4 Pathway of Photosynthesis: Ein Kranz-Typ Wirtschaftswunder? , 1976 .

[63]  J. Passioura Physiology of Grain Yield in Wheat Growing on Stored Water , 1976 .

[64]  P. S. Nutman Symbiotic nitrogen fixation in plants , 1976 .

[65]  F. D. Vries,et al.  The cost of maintenance processes in plant cells , 1975 .

[66]  R. Hardy,et al.  Nitrogen fixation in bacteria and higher plants. , 1975, Molecular biology, biochemistry, and biophysics.

[67]  L. Saker,et al.  Nutrient Supply and the Growth of the Seminal Root System in Barley II. LOCALIZED, COMPENSATORY INCREASES IN LATERAL ROOT GROWTH AND RATES OP NITRATE UPTAKE WHEN NITRATE SUPPLY IS RESTRICTED TO ONLY PART OF THE ROOT SYSTEM , 1975 .

[68]  R. D,et al.  Nitrogen Fixation in Bacteria and Higher Plants , 1975, Molecular Biology, Biochemistry and Biophysics.

[69]  E. L. Rice,et al.  INHIBITION OF NITRIFICATION BY CLIMAX ECOSYSTEMS. III. INHIBITORS OTHER THAN TANNINS , 1974 .

[70]  H. H. Laar,et al.  Products, requirements and efficiency of biosynthesis: a quantitative approach. , 1974, Journal of theoretical biology.

[71]  K. O. Rachie,et al.  Grain legumes of the lowland tropics , 1974 .

[72]  A. Quispel The biology of nitrogen fixation , 1974 .

[73]  L. Saker,et al.  Nutrient Supply and the Growth of the Seminal Root System in Barley III. COMPENSATORY INCREASES IN GROWTH OF LATERAL ROOTS, AND IN RATES OF PHOSPHATE UPTAKE, IN RESPONSE TO A LOCALIZED SUPPLY OF PHOSPHATE , 1978 .

[74]  L. Saker,et al.  Nutrient Supply and the Growth of the Seminal Root System in Barley I. THE EFFECT OF NITRATE CONCENTRATION ON THE GROWTH OF AXES AND LATERALS , 1973 .

[75]  E. L. Rice,et al.  INHIBITION OF NITRIFICATION BY CLIMAX ECOSYSTEMS. II. ADDITIONAL EVIDENCE AND POSSIBLE ROLE OF TANNINS , 1973 .

[76]  R. Daniel,et al.  Nitrate Dependent Anaerobic Acetylene-reduction and Nitrogen-fixation by Soybean Bacteroids , 1973 .

[77]  J. Pate,et al.  The Carbon Balance of a Legume and the Functional Economy of its Root Nodules , 1973 .

[78]  B. Milborrow,et al.  Biosynthesis and its Control in Plants , 1973 .

[79]  Davies Dd Control of and by pH. , 1973 .

[80]  J. Pate Uptake, assimilation and transport of nitrogen compounds by plants , 1973 .

[81]  R. Hardy,et al.  Applications of the acetylene-ethylene assay for measurement of nitrogen fixation , 1973 .

[82]  D. Davies Control of and by pH. , 1973, Symposia of the Society for Experimental Biology.

[83]  J. Hunt Distribution of Carbon in Crust of Earth: GEOLOGICAL NOTES , 1972 .

[84]  Harold A. Mooney,et al.  The Carbon Balance of Plants , 1972 .

[85]  E. L. Rice,et al.  Inhibition of nitrification by climax ecosystems , 1972 .

[86]  J. Passioura The effect of root geometry on the yield of wheat growing on stored water , 1972 .

[87]  R. Hageman,et al.  Generation of reduced nicotinamide adenine dinucleotide for nitrate reduction in green leaves. , 1971, Plant physiology.

[88]  C. R. Weber,et al.  Accumulation of N, P, and K by Soybean (Glycine max (L.) Merrill) Plants1 , 1971 .

[89]  I. Zelitch Photosynthesis, photorespiration, and plant productivity , 1971 .

[90]  S. Lips,et al.  Correlations between nitrate reduction, protein synthesis and malate accumulation. , 1970 .

[91]  R. C. Robbins,et al.  Gaseous nitrogen compound pollutants from urban and natural sources , 1970 .

[92]  D. Huber,et al.  Inhibition of Nitrification as a Deterrent to Nitrogen Loss1 , 1969 .

[93]  A. Beevers,et al.  Nitrate Reduction in Higher Plants , 1969 .

[94]  J. Sutcliffe Plants and water , 1969 .

[95]  R. Victor,et al.  Carbon dioxide fixation. , 1968, Enzymologia.

[96]  R. Brouwer,et al.  A simulation model of plant growth with special attention to root growth and its consequences , 1968 .

[97]  F. Clark Chapter 2 – Bacteria in Soil , 1967 .

[98]  P. Echlin The blue-green algae. , 1966, Scientific American.

[99]  C. R. Weber Nodulating and Nonnodulating Soybean Isolines: II. Response to Applied Nitrogen and Modified Soil Conditions1 , 1966 .

[100]  C. E. Hartt,et al.  Carbon Dioxide Fixation in Sugarcane Leaves. , 1965, Plant physiology.

[101]  E. Kessler Nitrate Assimilation by Plants , 1964 .

[102]  C. T. Wit,et al.  Ionic balance and growth of plants , 1963 .

[103]  E. Adams Amino acid metabolism. , 1962, Annual review of biochemistry.

[104]  D. Hathway The Condensed Tannins , 1962 .

[105]  A. Adams,et al.  STUDIES ON SOIL ORGANIC MATTER: I. INFLUENCE OF PHOSPHORUS CONTENT OF PARENT MATERIALS ON ACCUMULATIONS OF CARBON, NITROGEN, SULFUR, AND ORGANIC PHOSPHORUS IN GRASSLAND SOILS , 1958 .

[106]  C. Junge The distribution of ammonia and nitrate in rain water over the United States , 1958 .

[107]  D. Greenland Nitrate fluctuations in tropical soils , 1958, The Journal of Agricultural Science.

[108]  D. Spencer The reduction and accumulation of nitrate , 1958 .

[109]  E. A. Davis Nitrate Reduction by Chlorella. , 1953, Plant physiology.

[110]  J. G. Wood Nitrogen Metabolism of Higher Plants , 1953 .

[111]  E. Eriksson Composition of Atmospheric Precipitation , 1952 .

[112]  E. Eriksson Composition of Atmospheric Precipitation: I. Nitrogen compounds , 1952 .

[113]  Carl Oppenheimer,et al.  The Enzyme System , 1939 .

[114]  Cost of Maintenance , 1909, Teachers College Record: The Voice of Scholarship in Education.