Modelling plant nutrition of horticultural crops: a review

In this review, studies in plant nutrition are classified according to their time scales and micro- or macroscopic level of approach. Short-time scale studies are mostly dealt by plant physiologists with the prospect of building mechanistic models. They describe elementary plant functions implicated in, or dependent on ion uptake, with the goal of explaining the mechanisms underneath the functions. The concept of 'active ion transport' across the root plasma membrane derives from precise analyses of uptake 'isotherms' describing nutrition as a function of ion concentration in the root medium. Attempts to introduce feedback mechanisms, as required to model whole-plant response to the environment, are reviewed. Similarly, the response of plant photosynthetic capacity to leaf nitrogen status is extremely rapid and the role of nitrogen in regulating photosynthesis seems to hold for a large number of species. Therefore, it appears possible to introduce nitrogen regulation on leaf photosynthesis, thus allowing better simulations of plant growth under nitrogen limiting conditions. Long-time scale studies are dealt by agronomists and have long been the basis of fertilization advice. They attempt to predict crops' mineral nutrient requirements over the entire cycle from the empirical knowledge of 'general laws' governing crop growth. Recent advances propose to manage nutrition on the basis of crop structure independently from species and give opportunities to develop mechanistic concepts at this time scale. For nitrogen, this has been formalized extensively in crops such as cereals and grasses. It deserves to be carefully looked at for horticultural crops. These models also provide a sound basis to diagnosis through plant analysis. In horticultural agrosystems, such as those found for hydroponic cultures under commercial glasshouses, the use of on-line sensors is currently an alternative to crop models, since fertilization is induced by the immediate response of the sensors. This practice made

[1]  A. Ulrich.  Physiological Bases for Assessing the Nutritional Requirements of Plants , 1952 .

[2]  G. Laties.  Dual Mechanisms of Salt Uptake in Relation to Compartmentation and Long-Distance Transport , 1969 .

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

[4]  D. J. Greenwood.  Production or productivity: The nitrate problem?* , 1990 .

[5]  G. I. Åoren.  Ideal nutrient productivities and nutrient proportions in plant growth , 1988 .

[6]  T. Hodges.  Ion Absorption by Plant Roots1 , 1974 .

[7]  M. Sébillotte,et al.  Approche à l'échelle du système racinaire de l'absorption hydro-minérale. Conséquences en matière de modélisation , 1991 .

[8]  R. Sage,et al.  The Nitrogen Use Efficiency of C(3) and C(4) Plants: II. Leaf Nitrogen Effects on the Gas Exchange Characteristics of Chenopodium album (L.) and Amaranthus retroflexus (L.). , 1987, Plant physiology.

[9]  A. Ourry,et al.  Kinetic parameters of nitrate uptake by different catch crop species: effects of low temperatures or previous nitrate starvation , 1993 .

[10]  B. Veen.  Energy cost of ion transport. , 1979, Basic life sciences.

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

[12]  M. Stitt,et al.  Effects of nitrogen and phosphorus deficiencies on levels of carbohydrates, respiratory enzymes and metabolites in seedlings of tobacco and their response to exogenous sucrose , 1993 .

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

[14]  A. Ourry,et al.  Diurnal variation in the simultaneous uptake and ‘sink’ allocation of NH4+ and NO3- by Lolium perenne in flowing solution culture , 1996 .

[15]  A. Glass,et al.  Simultaneous consideration of tissue and substrate potassium concentration in k uptake kinetics: a model. , 1982, Plant physiology.

[16]  S. Jarvis,et al.  Plant Growth in Relation to the Supply and Uptake of NO3–: A Comparison Between Relative Addition Rate and External Concentration as Driving Variables , 1993 .

[17]  M. Benlloch,et al.  Two modes of rubidium uptake in sunflower plants. , 1989, Plant physiology.

[18]  J. Macduff,et al.  Influx and Efflux of Nitrate and Ammonium in Italian Ryegrass and White Clover Roots: Comparisons Between Effects of Darkness and Defoliation , 1992 .

[19]  Croissance estivale en matière sèche de peuplements de fétuque élevée (Festuca arundinacea Schreb.) et de dactyle (Dactylis glomerata L.) dans l'Ouest de la France. I. Etude en conditions de nutrition azotée et d'alimentation hydrique non limitantes , 1987 .

[20]  W. Jackson,et al.  Simultaneous Influx and Efflux of Nitrate during Uptake by Perennial Ryegrass. , 1973, Plant physiology.

[21]  M. Caloin,et al.  Analysis of the Time Course of Change in Nitrogen Content in Dactylis glomerata L. Using a Model of Plant Growth , 1984 .

[22]  Croissance estivale en matière sèche de peuplements de fétuque élevée (Festuca arundinacea Schreb.) et de dactyle (Dactylis glomerata L.) dans l'Ouest de la France. II. Interaction entre les niveaux d'alimentation hydrique et de nutrition azotée , 1987 .

[23]  C. Gary,et al.  An experimental set-up to study carbon, water, and nitrate uptake rates by hydroponically grown plants. , 1996, Journal of plant nutrition.

[24]  E. Epstein.  Mineral Nutrition of Plants: Principles and Perspectives , 1972 .

[25]  A. P. Papadopoulos,et al.  The "Harrow Fertigation Manager(R)" - a computerized multifertilizer injector , 1989 .

[26]  E. Epstein,et al.  A KINETIC STUDY OF THE ABSORPTION OF ALKALI CATIONS BY BARLEY ROOTS. , 1952, Plant physiology.

[27]  I. R. Johnson.  Plant respiration in relation to growth, maintenance, ion uptake and nitrogen assimilation , 1990 .

[28]  S. A. Barber,et al.  A Method for Characterizing the Relation between Nutrient Concentration and Flux into Roots of Intact Plants. , 1974, Plant physiology.

[29]  M. Drew,et al.  Nitrogen-13 Studies of Nitrate Fluxes in Barley Roots II. EFFECT OF PLANT N-STATUS ON THE KINETIC PARAMETERS OF NITRATE INFLUX , 1986 .

[30]  M. Pitman.  Uptake and Transport of Ions in Barley Seedlings I. Estimation of Chloride Fluxes in Cells of Excised Roots , 1971 .

[31]  D. Rc,et al.  Diagnostic Criteria for Plants and Soils. , 1966 .

[32]  R. Bieleski.  Phosphate Pools, Phosphate Transport, and Phosphate Availability , 1973 .

[33]  T. Ingestad,et al.  Nutrition and growth of birch seedlings at varied relative phosphorus addition rates , 1988 .

[34]  Tadaki Hirose,et al.  Nitrogen use efficiency in instantaneous and daily photosynthesis of leaves in the canopy of a Solidago altissima stand , 1987 .

[35]  T. Nielsen,et al.  Distribution of dry matter in sweet pepper plants (Capsicum annuum L.) during the juvenile and generative growth phases , 1988 .

[36]  R. Valentine,et al.  Genetic Engineering of Osmoregulation , 1980, Basic Life Sciences.

[37]  P. Nissen,et al.  Effect of exogenous and endogenous nitrate concentration on nitrate utilization by dwarf bean. , 1982, Plant physiology.

[38]  A. Morisot,et al.  Daily variations of xylemic exudation rate in tomato , 1992 .

[39]  A. Fredeen,et al.  Influence of Phosphorus Nutrition on Growth and Carbon Partitioning in Glycine max. , 1989, Plant physiology.

[40]  H. Have,et al.  Zea mays L. , 1989 .

[41]  J. Lynch,et al.  Vegetative Growth of the Common Bean in Response to Phosphorus Nutrition , 1991 .

[42]  H. Kronzucker,et al.  Kinetics of NO3- Influx in Spruce , 1995, Plant physiology.

[43]  M. Siddiqi,et al.  Regulation of K+ Influx in Barley: Evidence for a Direct Control of Influx by K+ Concentration of Root Cells , 1987 .

[44]  H. Lambers,et al.  Fundamental, Ecological and Agricultural Aspects of Nitrogen Metabolism in Higher Plants , 2011, Developments in Plant and Soil Sciences.

[45]  Studies of the Relationship between the Growth Rate of Young Plants and their Total-N Concentration using Nutrient Interruption Techniques: Theory and Experiments , 1994 .

[46]  R. K. Scott,et al.  A physiological analysis of the diminishing responses of winter wheat to applied nitrogen. 2. Evidence. , 1990 .

[47]  Thomas J. Givnish,et al.  On the economy of plant form and function. , 1988 .

[48]  R. Loomis,et al.  Modeling crop photosynthesis - from biochemistry to canopy. , 1991 .

[49]  P. McClure,et al.  Comparison of nitrate uptake kinetic parameters across maize inbred lines , 1986 .

[50]  M. L. van Beusichem,et al.  Plant Nutrition — Physiology and Applications , 1990, Developments in Plant and Soil Sciences.

[51]  V. Sadras,et al.  Effect of Nitrogen Content on the Photosynthetic Characteristics of Sunflower Leaves , 1993 .

[52]  J. Huguet,et al.  Appréciation de l'état hydrique d'une plante à partir des variations micrométriques de la dimension des fruits ou des tiges au cours de la journée , 1985 .

[53]  M. Noordwijk.  Synchronisation of supply and demand is necessary to increase efficiency of nutrient use in soilless horticulture , 1990 .

[54]  D. Charles-Edwards,et al.  An Analysis of Spatial Variation in the Nitrogen Content of Leaves from Different Horizons Within a Canopy , 1987 .

[55]  D. Clarkson.  Regulation of the absorption and release of nitrate by plant cells: A review of current ideas and methodology , 1986 .

[56]  R. Habib,et al.  Root volume effects on nitrogen uptake and partitioning in peach trees , 1994 .

[57]  B. Osmond,et al.  Effects of Nitrogen Nutrition on Nitrogen Partitioning between Chloroplasts and Mitochondria in Pea and Wheat. , 1991, Plant physiology.

[58]  K. R. Mankin,et al.  Modeling individual nutrient uptake by plants: Relating demand to microclimate , 1996 .

[59]  D. Rains,et al.  Evidence for Substrate Induction of a Nitrate Efflux System in Barley Roots , 1996, Plant physiology.

[60]  J. Thornley.  A Balanced Quantitative Model for Root: Shoot Ratios in Vegetative Plants , 1972 .

[61]  J. Thornley,et al.  Shoot: Root Allocation with Respect to C, N and P: an Investigation and Comparison of Resistance and Teleonomic Models , 1995 .

[62]  P. Nissen.  Uptake Mechanisms: Inorganic and Organic , 1974 .

[63]  D. Lawlor.  Relation between carbon and nitrogen assimilation, tissue composition and whole plant function , 1994 .

[64]  D. D. Lefebvre,et al.  Regulation of phosphate influx in barley roots: Effects of phosphate deprivation and reduction of influx with provision of orthophosphate , 1982 .

[65]  John M. Cheeseman,et al.  Plant growth modelling without integrating mechanisms , 1993 .

[66]  D. Rains,et al.  Effect of root perturbation and excision on nitrate influx and efflux in barley (Hordeum vulgare) seedlings. , 1996, Physiologia plantarum.

[67]  F. Maathuis,et al.  Mechanisms of potassium absorption by higher plant roots , 1996 .

[68]  P. Tillard,et al.  Diurnal regulation of NO3− uptake in soybean plants I. Changes in NO3− influx, efflux, and N utilization in the plant during the day/night cycle , 1995 .

[69]  P. Tillard,et al.  Diurnal regulation of NO3−uptake in soybean plants II. Relationship with accumulation of NO and asparagine in the roots , 1995 .

[70]  D. Rains,et al.  Nitrate absorption by barley: I. Kinetics and energetics. , 1976, Plant physiology.

[71]  T. Ingestad,et al.  A comparison between methods used to control nutrient supply , 1996 .

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

[73]  M. Y. Wang,et al.  Ammonium Uptake by Rice Roots (I. Fluxes and Subcellular Distribution of 13NH4+) , 1993, Plant physiology.

[74]  T. Dejong,et al.  Seasonal relationships between leaf nitrogen content (photosynthetic capacity) and leaf canopy light exposure in peach (Prunus persica) , 1985 .

[75]  C. Mackown.  Nitrate Uptake and Assimilation following Nitrate Deprivation , 1987 .

[76]  R. C. Hardwick.  The Nitrogen Content of Plants and the Self-thinning Rule of Plant Ecology: A Test of the Core-skin Hypothesis , 1987 .

[77]  Anne Schlebusch.  Manual or Automatic , 1993 .

[78]  P. Gill,et al.  Comparative resistance to fruit cracking in tomato (Lycopersicon esculentum Mill.). , 1970 .

[79]  F. Sanders,et al.  Responses of chickpea (Cicer arietinum) to iron stress measured using a computer-controlled continuous-flow hydroponic system , 1990 .

[80]  M. Blom-Zandstra,et al.  A computer‐controlled multi‐titration system to study transpiration, OH− efflux and nitrate uptake by intact lettuce plants (Lactuca sativa L.) under different environmental conditions , 1987 .

[81]  W. J. Lucas,et al.  Potassium Transport in Corn Roots : IV. Characterization of the Linear Component. , 1985, Plant physiology.

[82]  A. Glass,et al.  Nitrate Inhibition of Chloride Influx in Barley: Implications for a Proposed Chloride Homeostat , 1985 .

[83]  B. Muller,et al.  Inhibition of NO⊟3 Uptake by Various Phloem-Translocated Amino Acids in Soybean Seedlings , 1992 .

[84]  P. Nissen.  Multiphasic Uptake Mechanisms in Plants , 1991 .

[85]  G. Ågren,et al.  Theories and methods on plant nutrition and growth , 1992 .

[86]  I. R. Cowan,et al.  Leaf Conductance in Relation to Rate of CO(2) Assimilation: I. Influence of Nitrogen Nutrition, Phosphorus Nutrition, Photon Flux Density, and Ambient Partial Pressure of CO(2) during Ontogeny. , 1985, Plant physiology.

[87]  H. Lambers,et al.  Respiratory energy costs for the maintenance of biomass, for growth and for ion uptake in roots of Carex diandra and Carex acutiformis , 1988 .

[88]  D. Robinson.  The responses of plants to non-uniform supplies of nutrients. , 1994, The New phytologist.

[89]  M. Schenk,et al.  Control of nitrogen supply of cucumber (Cucumis sativus) grown in soilless culture , 1990 .

[90]  J. Roy,et al.  A Whole Plant Perspective on Carbon-Nitrogen Interactions , 1994 .

[91]  J. Abadía,et al.  Changes in leaf phosphate status have only small effects on the photochemical apparatus of sugar beet leaves , 1987 .

[92]  W. Jackson,et al.  Exogenous NO(3) Influx and Endogenous NO(3) Efflux by Two Maize (Zea mays L.) Inbreds during Nitrogen Deprivation. , 1988, Plant physiology.

[93]  A. Freijsen,et al.  A culture system for steady state nutrition in optimum and suboptimum treatments , 1990 .

[94]  S. Goyal,et al.  A novel approach and a fully automated microcomputer-based system to study kinetics of NO3-, NO2-, and NH4+ transport simultaneously by intact wheat seedlings. , 1986 .

[95]  S. Huber,et al.  Alterations in leaf carbohydrate metabolism in response to nitrogen stress. , 1988, Plant physiology.

[96]  R. L. Warner,et al.  Feedback Regulation of Nitrate Influx in Barley Roots by Nitrate, Nitrite, and Ammonium , 1993, Plant physiology.

[97]  O. de Villele,et al.  BESOINS EN EAU DES CULTURES SOUS SERRE - ESSAI DE CONDUITE DES ARROSA GES EN FONCTION DE L'ENSOLEILLEMENT , 1974 .

[98]  A. Brooks.  Effects of Phosphorus Nutrition on Ribulose-1,5-Bisphosphate Carboxylase Activation, Photosynthetic Quantum Yield and Amounts of Some Calvin-Cycle Metabolites in Spinach Leaves , 1986 .

[99]  A. Glass,et al.  Short Term Studies of Nitrate Uptake into Barley Plants Using Ion-Specific Electrodes and 36C103- 1 , 1983 .

[100]  E. Epstein,et al.  RESOLUTION OF DUAL MECHANISMS OF POTASSIUM ABSORPTION BY BARLEY ROOTS. , 1963, Proceedings of the National Academy of Sciences of the United States of America.

[101]  Gilles Lemaire,et al.  Decline in Percentage N of C3 and C4 Crops with Increasing Plant Mass , 1990 .

[102]  R. B. Lee.  Control of Net Uptake of Nutrients by Regulation of Influx in Barley Plants Recovering from Nutrient Deficiency , 1993 .

[103]  P. Kriedemann,et al.  Leaf growth and photosynthetic response to nitrogen and phosphorus in seedling trees of Gmelina arborea , 1993 .

[104]  Takeshi Horie,et al.  Leaf Nitrogen, Photosynthesis, and Crop Radiation Use Efficiency: A Review , 1989 .

[105]  E. A. Kirkby,et al.  Diurnal uptake of nitrate and potassium during the vegetative growth of tomato plants , 1992 .

[106]  Susan J. Smith,et al.  Nitrate transport and compartmentation in cereal root cells , 1996 .

[107]  A. Borstlap.  Invalidity of the multiphasic concept of ion absorption in plants , 1981 .

[108]  C. Clement,et al.  The Uptake of Nitrate by Lolium perenne from Flowing Nutrient Solution I. EFFECT OF CONCENTRATION , 1978 .

[109]  C. Deane‐Drummond.  A substrate cycling model for nitrate uptake by Pisum sativum seedlings: A key to sensitivity of response of net flux to substrate and effectors? , 1986 .

[110]  R. Brun,et al.  Water and nitrate absorption kinetics in the nychthemeral cycle of rose grown in the greenhouse using a recirculating solution , 1996 .

[111]  S. Huber,et al.  Changes in Starch Formation and Activities of Sucrose Phosphate Synthase and Cytoplasmic Fructose-1,6-bisphosphatase in Response to Source-Sink Alterations. , 1983, Plant physiology.

[112]  David T. Clarkson,et al.  Factors Affecting Mineral Nutrient Acquisition by Plants , 1985 .

[113]  E. Pressman,et al.  Effects of root pruning and N-NO3 solution concentration on nutrient uptake and transpiration of tomato plants , 1994 .

[114]  W. J. Lucas,et al.  Potassium Transport in Corn Roots : II. The Significance of the Root Periphery. , 1983, Plant physiology.

[115]  G. Ågren,et al.  The relationship between the growth rate of young plants and their total-N concentration is unique and simple: a comment , 1995 .

[116]  A. Glass,et al.  A Model for the Regulation of K Influx, and Tissue Potassium Concentrations by Negative Feedback Effects upon Plasmalemma Influx. , 1986, Plant physiology.

[117]  T. Bouma,et al.  Energy requirements for maintenance of ion concentrations in roots , 1993 .

[118]  A. Beddows.  Dactylis glomerata L. , 1959 .

[119]  F. W. Smith,et al.  Regulation of sulphate transport in a tropical legume, Macroptilium atropurpureum, cv. Siratro , 1983 .

[120]  Bert Bolin,et al.  The carbon cycle. , 1970, Scientific American.

[121]  C. Clement,et al.  A System for Measuring the Uptake of Ions by Plants from Flowing Solutions of Controlled Composition , 1974 .

[122]  R. C. Muchow,et al.  Nitrogen Response of Leaf Photosynthesis and Canopy Radiation Use Efficiency in Field-Grown Maize and Sorghum , 1994 .

[123]  W. Cram.  Compartmentation and exchange of chloride in carrot root tissue. , 1968, Biochimica et biophysica acta.

[124]  H. Lambers,et al.  Respiration for growth, maintenance and ion uptake. An evaluation of concepts, methods, values and their significance , 1983 .

[125]  G. Farquhar,et al.  Transpiration ratio and plant mineral content are related among genotypes of a range of species , 1992 .

[126]  E. Justes,et al.  Determination of a Critical Nitrogen Dilution Curve for Winter Wheat Crops , 1994 .

[127]  L. T. Evans.  Mechanisms of plant growth and improved productivity: A.S. Basra. Marcel Dekker, New York, 1994. 496 pp., Hardback US $165, ISBN 0-8247-9192-4. , 1994 .

[128]  Göran I. Ågren,et al.  Theory for growth of plants derived from the nitrogen productivity concept , 1985 .

[129]  W. Tanner,et al.  Does transpiration have an essential function in long-distance ion transport in plants ? , 1990 .

[130]  A. Bloom,et al.  Effects of Exposure to Ammonium and Transplant Shock upon the Induction of Nitrate Absorption. , 1990, Plant physiology.

[131]  J. Lynch,et al.  Phosphorus responses of C3 and C4 species , 1996 .

[132]  S. Lips,et al.  Nitrate Uptake by Roots as Regulated by Nitrate Reduction Products of the Shoot , 1971 .

[133]  B. Muller,et al.  Effect of Phloem-Translocated Malate on NO(3) Uptake by Roots of Intact Soybean Plants. , 1992, Plant physiology.

[134]  T. Lamaze,et al.  Nitrate transport in intact wheat roots: I. Estimation of cellular fluxes and NO3− distribution using compartmental analysis from data of 15NO3− efflux , 1994 .

[135]  J. H. Macduff,et al.  Uptake of Mineral Nutrients and Crop Growth: The Use of Flowing Nutrient Solutions , 1987 .

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

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

[138]  John R. Evans,et al.  Partitioning of Nitrogen Between and Within Leaves Grown Under Different Irradiances , 1989 .

[139]  D. Layzell,et al.  Regulation of Assimilate Partitioning in Soybean : Initial Effects following Change in Nitrate Supply. , 1987, Plant physiology.

[140]  C. Gary,et al.  La surface spécifique foliaire comme indicateur de l'équilibre source-puits chez la tomate (Lycopersicon esculentum Mill.) , 1992 .

[141]  Pierre Martin-Prével,et al.  L'analyse végétale dans le contrôle de l'alimentation des plantes temperées et tropicales , 1984 .

[142]  W. Cram.  Chloride Accumulation as a Homeostatic System: Set Points and Perturbations THE PHYSIOLOGICAL SIGNIFICANCE OF INFLUX ISOTHERMS, TEMPERATURE EFFECTS AND THE INFLUENCE OF PLANT GROWTH SUBSTANCES , 1983 .

[143]  A. Sim,et al.  Cortical Cell Fluxes of Ammonium and Nitrate in Excised Root Segments ofAllium cepa L; Studies using15N , 1990 .

[144]  G. Lemaire,et al.  N Uptake and Distribution in Plant Canopies , 1997 .

[145]  A. D. Peuke,et al.  Nitrate or Ammonium Uptake and Transport, and Rapid Regulation of Nitrate Reduction in Higher Plants , 1996 .

[146]  W. J. Lucas,et al.  Potassium transport in corn roots : I. Resolution of kinetics into a saturable and linear component. , 1982, Plant physiology.

[147]  M. Peet,et al.  Modeling Nutrient Uptake in Chrysanthemum as a Function of Growth Rate , 1992 .

[148]  J. R. Evans,et al.  Nitrogen and Photosynthesis in the Flag Leaf of Wheat (Triticum aestivum L.). , 1983, Plant physiology.

[149]  T. Lamaze,et al.  Nitrate transport in intact wheat roots:II. Long-term effects of NO3− concentration in the nutrient solution on NO3− unidirectional fluxes and distribution within the tissues5 , 1994 .

[150]  J. Abadía,et al.  Chlorophyll-Proteins and Electron Transport during Iron Nutrition-Mediated Chloroplast Development. , 1985, Plant physiology.

[151]  Christopher B. Field,et al.  photosynthesis--nitrogen relationship in wild plants , 1986 .

[152]  S. A. Barber,et al.  Potassium Influx Characteristics of Corn Roots and Interaction with N, P, Ca, and Mg Influx1 , 1977 .

[153]  H. J. Gold,et al.  A dynamic growth model of vegetative soya bean plants: model structure and behaviour under varying root temperature and nitrogen concentration. , 1990, Journal of experimental botany.

[154]  Gilles Lemaire,et al.  Diagnosis of the Nitrogen Status in Crops , 1997, Springer Berlin Heidelberg.

[155]  R. Sage,et al.  I. LEAF NITROGEN, GROWTH, AND BIOMASS PARTITIONING IN CHENOPODIUM ALBUM (L.) AND , 1987 .

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

[157]  F. E. Egler.  Ecosystems of the World , 1960 .