Research in Plant Sciences
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Research in Plant Sciences. 2017, 5(1), 26-42
DOI: 10.12691/plant-5-1-4
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Mechanisms of Phosphorous Uptake Efficiency of Safflower and Sunflower Grown in Different Soils

Jehad Abbadi1, Klaus Dittert2, Bernd Steingrobe2 and Norbert Claassen2

1Biology Department, College of Science and Technology, Al-Quds University, Jerusalem, Palestine

2Department of Plant Nutrition and Yield Physiology, George-August University, Carl-Sprengel Weg 1, Göttingen, Germany

Pub. Date: September 05, 2017

Cite this paper:
Jehad Abbadi, Klaus Dittert, Bernd Steingrobe and Norbert Claassen. Mechanisms of Phosphorous Uptake Efficiency of Safflower and Sunflower Grown in Different Soils. Research in Plant Sciences. 2017; 5(1):26-42. doi: 10.12691/plant-5-1-4


Plant species vary in their phosphorous (P) use efficiency under suboptimal P supplies using different strategies, but the mechanisms are not clearly documented for some alternative plant species. Safflower was considered as low input oil crop, but its P uptake efficiency mechanism was not fully investigated. Therefore P uptake efficiency of safflower was studied as compared to sunflower under semi-controlled conditions in sandy and loamy soils. Both species responded strongly to increasing P supplies in both soils and performed better in loamy soil. Both species had similar agronomic P efficiency in both soils, indicated by similar external P requirement under P-deficient conditions. Under P deficiency, safflower had less relative shoot and root production when they were grown in sandy soils and the opposite was found in terms of loamy soil. Safflower had the disadvantage of less root length and root shoot ratio in both soils under low and high P supplies but had the advantage of higher specific root density, less root radius, and slower shoot growth rate. Under P deficiency in both soil types, both species responded similarly in terms of P influx, depleting P from soil solution and P concentration in shoots. Under high P supply, P influx and P concentration in shoots was less in safflower in both soil types. Safflower was characterized by higher shoot demand on roots for P under low and high P supplies in both soil types. Therefore the cause of high root demand on P in safflower roots at low and high P supplies stems from the low root shoot ratio of safflower at both P supplies, low P concentration and low P influx of safflower at high P supplies not because of higher shoot growth rate of safflower at low and high P supplies. Therefore using different measures of utilization efficiency parameters to differentiate plant species and genotypes to superior and inferior could be in some cases misleading.

P uptake efficiency alternative crops safflower P influx root shoot ratio shoot demand

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[1]  Marschner, H, Mineral Nutrition of Higher Plants, 2nd ed., Academic Press, London, 1995.
[2]  Vance, C.P., Uhde-Stone, C., and Allan, D.L, “Phosphorus acquisition and use: critical adaptations by plants securing a nonrenewable resource”, New Phytologist, 157. 423-457. 2003.
[3]  Winfried, E. and Blum, H, “Soil and Land Resources for Agricultural Production: General Trends and Future Scenarios-A Worldwide Perspective”, International Soil and Water Conservation Research, 1 (3). 1-14. 2013.
[4]  Ashley, K., Cordell, D., Mavinic, D, “A brief history of phosphorus: From the philosopher’s stone to nutrient recovery and reuse”, Chemosphere 84. 737-746. 2011.
[5]  Lambers, H., Shane, M.W, Cramer M.D, Pearse S.J. and Veneklaas E.J, “Root Structure and Functioning for Efficient Acquisition of Phosphorus: Matching Morphological and Physiological Traits”, Annals of Botany, 98. 693-713. 2006.
[6]  Nadira, U.A., Ahmed, I.M., Zhu, B., Zeng, J., Cai, S., Wu, F. and Zhang, G, “Identification of Tibetan wild barley genotypes with high tolerance to low phosphorus stress”, Journal of Food, Agriculture & Environment, 12 (2). 408-214. 2014.
[7]  Richardson, S.J., Peltzer, D.A., Allen, R.B., McGlone, M.S. and Parfitt, R.L, “Rapid development of phosphorus limitation in temperate rainforest along the Franz Josef soil chronosequence”, Oecologia, 139. 267-276. 2004.
[8]  Pachauri, R.K. and Meyer, L.A, (eds.), IPCC, Climate Change: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, IPCC, Geneva, Switzerland, 2014.
[9]  Johnson, A.H., Frizano, J., Vann, D.R., and Johnson, R.A.H, “Biogeochemical implications of labile phosphorus in forest soils determined by the Hedley fractionation procedure”, Oecologia, 135. 487-499. 2003.
[10]  Roy, R.N., Finck, A., Blair, G.J., Tandon, H.L.S, “Plant nutrition for food security, a guide for integrated nutrient management”, FAO, Rom-Italy, 2006.
[11]  Chardon, W., Withers, P, “Introduction to papers from the UE-COST Action 832, Quantifying the agricultural contribution to eutrophication”, Journal of Plant Nutrition and Soil Science, 166. 401. 2003.
[12]  Abbadi, J. and Gerendás, J, “Phosphorous use efficiency of Safflower as compared to Sunflower”, Journal of Plant Nutrition, 38 (7). 1121-1142. 2015.
[13]  Abbadi, J, “Phosphorous use efficiency of safflower and sunflower grown in different soils”, World Journal of Agricultural Research, 5 (4), 212-220. 2017.
[14]  Abbadi, J, “Importance of nutrient supply (N, P, K) for yield formation and nutrient use efficiency of safflower (Carthamus tinctorius L.) compared to sunflower (Helianthus annuus L.) including an assessment to grow safflower under north German conditions”, Grauer Publisher, Beuren Stuttgart, Germany, 2007.
[15]  Abbadi, J. and Gerendás, J, “Effects of phosphorous supply on growth and yield of safflower as compared to sunflower”, Journal of Plant Nutrition, 34 (12). 1769-1787. 2011.
[16]  Abbadi, J. and Gerendás, J, “Phosphorous use efficiency of Safflower and Sunflower studied in nutrient solutions”, Journal of Agricultural Science and Technology A, 2. 1260-1280. 2012.
[17]  Watson, C.A., Atkinson, D., Gosling, P., Jackson, L.R. and Rays, F.W, “Managing soil fertility in organic farming systems”, Soil Use and Management, 18. 239-247. 2002.
[18]  Berry, P., Stockdale, E., Sylvester-Bradley, R., Philipps, L., Smith, K., Lord, E., Watson, C. and Fortune, S, “N, P and K budgets for crop rotations on nine organic farms in the UK”, Soil Use and Management, 19. 112-118. 2003.
[19]  Maranguit, D., Guillaume, T. and Kuzyakov, Y, “Land-use change affects phosphorus fractions in highly weathered tropical soils”, Catena, 149. 385-393. 2017.
[20]  Singh, B. and Ryan, J, “Managing Fertilizers to Enhance Soil Health”, International Fertilizer Industry Association (IFA). Paris. France. 2015.
[21]  Gourley, C.J.P., Allan, D.L. and Russelle, M.P, “Plant nutrient efficiency: A comparison of definitions and suggested improvement”, Plant and Soil, 158. 29-37. 1994.
[22]  Shahid, S.A. and Al-Shankiti, A, “Sustainable food production in marginal lands-Case of GDLA member countries”, International Soil and Water Conservation Research, 1 (1). 24-38. 2013.
[23]  Spiertz, H, “Challenges for Crop Production Research in Improving Land Use, Productivity and Sustainability”, Sustainability, 5. 1632-1644. 2013.
[24]  Wang, Y.P., Law, R.M., and Pak, B, “A global model of carbon, nitrogen and phosphorus cycles for the terrestrial biosphere”, Biogeosciences, 7. 2261-2282. 2010.
[25]  Goll, D.S., Brovkin, V., Parida, B.R., Reick, C.H., Kattge, J., Reich, P.B., Van Bodegom, P.M., and Niinemets, Ü, “Nutrient limitation reduces land carbon uptake in simulations with a model of combined carbon, nitrogen and phosphorus cycling”, Biogeosciences, 9. 3547-3569. 2012.
[26]  Yang, X., Thornton, P.E., Ricciuto, D.M., and Post, W.M, “The role of phosphorus dynamics in tropical forests – A modeling study using CLM-CNP”, Biogeosciences, 11. 1667-1681. 2014.
[27]  Reed, S.C., Yang, X., and Thornton, P.E, “Incorporating phosphorus cycling into global modeling efforts: A worthwhile, tractable endeavor”, New Phytologist, 208. 324-329. 2015.
[28]  Dessougi, H. Claassen, N, and Steingrobe, B. “Potassium efficiency mechanisms of wheat, barley and sugar beet grown on a K fixing soil under controlled conditions”, Journal of Plant Nutrition and Soil Science, 165, 732-737. 2002.
[29]  Dechassa, N., Schenk, M.K., Claassen, N., and Steingrobe, B, “Phosphorus efficiency of cabbage (Brassica oleraceae L. var. capitata), carrot (Daucus carota L.), and potato (Solanum tuberosum L.) “, Plant and Soil, 250. 215-224. 2003.
[30]  Sattelmacher, B., Horst, W.J. Becker, H.C, “Factors that contribute to genetic variation for nutrient efficiency of crops”, Journal of Plant Nutrition and Soil Science, 157. 215-224. 1994.
[31]  Abbadi, J., Gerendás, J. and Sattelmacher, B, “Effects of nitrogen supply on growth, yield and yield components of safflower and sunflower”, Plant and Soil, 360. 167-180. 2008.
[32]  Abbadi, J. and Gerendás, J, “Nitrogen Use Efficiency of Safflower as compared to Sunflower”, Journal of Plant Nutrition, 32(6). 929-945. 2009.
[33]  Nye, PA. and Tinker. P.B, “Solute Movement in the soil-root system”, Studies in Ecology, Blackwell Scientific Publisher, Oxford. 1977.
[34]  Barber, S.A, Soil Nutrient Bioavailability. John Wiley & Sons, New York. 1984.
[35]  Jungk, A, “Root hairs and the acquisition of plant nutrients from soil”, Journal of Plant Nutrition and Soil Science 164. 121-129. 2001.
[36]  Jungk, A. and Claassen, N, “Ion diffusion in the soil-root system”, Advances in Agronomy, 61. 53-110. 1997.
[37]  Syers, J.K., Johnston, A.E. and Curtin. D, “Efficiency of soil and fertilizer phosphorus use”, FAO Fertilizer and Plant Nutrition Bulletin, 18. Rome, Italy. 2008.
[38]  Johnston, A.E, “Principles of crop nutrition for sustainable food production”, Proceedings, 459., International Fertilizer Society., York, UK., 2001.
[39]  Bhadoria, P.S., Singh, S. and Claassen, N, “Phosphorus efficiency of wheat, maize and groundnut grown in low phosphorus supplying soil”, In W.J. Horst et al. eds. Plant Nutrition- Food security and sustainability of Agro-ecosystems. Dordrecht, Kluwer Academic Publishers. 530-531. 2001.
[40]  Schenk, M.K, “Nutrient efficiency of vegetable crops”, Acta Horticulturae, 700. 21-34. 2006.
[41]  Johnston, A.E.J., and Syers, J.K, “A new approach to assessing phosphorus use efficiency in agriculture”, Better Crops Plant Food, 93. 14-16. 2009.
[42]  Rausch, C. and Bucher, M, “Molecular mechanisms of phosphate transport in plants”, Planta, 216. 23-37. 2002
[43]  Fitter, A, “Characteristics and functions of root systems”, in Plant Roots: The Hidden Half. Waisel, Y., Eshel, A., and Kafkafi, U. (eds.), 2nd ed., Dekker, New York. 1-20. 1996.
[44]  Koevoets IT, Venema JH, Elzenga JTM and Testerink, C, “Roots Withstanding their Environment: Exploiting Root System Architecture Responses to Abiotic Stress to Improve Crop Tolerance”, Frontiers in Plant Science, 7. 1335. 2016.
[45]  Trona, S., Bodnerb, G., Laioc, F., Ridolfic, L. and Leitnera, D, “Can diversity in root architecture explain plant water use efficiency? A modeling study”, Ecological Modeling, 312. 200-210. 2015.
[46]  Zaehle, S. and Friend, A.D, “Carbon and nitrogen cycle dynamics in the O-CN land surface model: 1. Model description, site-scale evaluation, and sensitivity to parameter estimates”, Global Biogeochemical Cycles, 24. 1-13. 2010.
[47]  Oliveira, E.M.M., Ruiz, H.A., Hugo, V., Ferreira P.A., Costa F.O. and Ameida I.C.C, “Nutrient supply by mass flow and diffusion to maize plants in response to soil aggregate size and water potential”, Revista Brasileira De Ciência Do Solo, 34. 317-328. 2010.
[48]  Giehl, R.F.H. and von Wirén, N, “Root Nutrient Foraging”, Plant Physiology, 166. 509-517. 2014.
[49]  Tinker, P.B, Nye, P.H, Solute Movement in the Rhizosphere, Blackwell Scientific, Oxford. 2000.
[50]  Rashmi, I., Biswas, A.K., Shinogi, K.C., Kala, S., Karthika, K.S., Prabha, S.P. and Sao, Y, “Phosphorus Movement and Vertical Distribution in Four Soil Orders of India: Column Leaching Experiment”, International Journal of Current Microbiology and Applied Sciences, 6(4). 1919-1930. 2017.
[51]  Ticconi, C.A., Lucero, R.D., Sakhonwasee, S., Adamson, A.W., Creff, A., Nussaume, L., Desnos, T. and Abel, S, “ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability”, Proceedings of the National Academy of Sciences, USA 106: 14174-14179. 2009.
[52]  Gericke, S., Kurmies, B, “Die kolorimetrische Phosphorsäure bestimmung mit Ammonium, Vanadat, Molybdat und ihre Anwendung in der Pflanzenanalyse”, Zeitschrift für Pflanzenernährung, Düngung, Bodenkunde, 59. 235-247. 1952.
[53]  Adams F, “Soil solution”, in Carson EW (ed) The plant root and its environment. University of Virginia, Charlottesville, 441-481. 1974.
[54]  Schüller, H, “Die CAL-Methode, eine neue Methode zur Bestimmung des pflanzenverfügbaren phosphates in Böden” [The CAL method, a new method for the determination of plant-available phosphate in soils]. Journal of Plant Nutrition and Soil Science, 123. 48-63.1969.
[55]  Tennant, D, “A test of a modified line intersect method of estimating root length”, Journal of Ecology, 63. 995-1001. 1975.
[56]  Williams, R.F, “The effect of phosphorus supply on the rates of intake of phosphorus and nitrogen upon certain aspects of phosphorus metabolism in gramineous plants”, Australian Journal of Scientific Research (B) Biological Sciences, 11. 333-361. 1948.
[57]  West, G.B., Brown, J.H., and Enquist, B.J, “A general model for the structure and allometry of plant vascular systems”, Nature 400. 664-667. 1999.
[58]  Niklas, K.J. and Enquist, B.J, “On the vegetative biomass partitioning of seed plant leaves, stems, and roots”, American Naturalist, 159. 482-497. 2002.
[59]  Cornelissen, J.H.C., Lavorel, S., Garnier, E., Dı´az, S., Buchmann, N., Gurvich, D.E., Reich, P.B., ter Steege, H., Morgan, H.D., van der Heijden, M.G.A., Pausas, J.G. and Poorter. H, “A handbook of protocols for standardised and easy measurement of plant functional traits worldwide”, Australian Journal of Botany, 51. 335-380. 2003.
[60]  Gill, M.A., Mansoor, S., Aziz, T., Rahmatullah and Akhtar, M.S, “Differential growth response and phosphorus utilization efficiency of rice genotypes”, Pakistan Journal of Agricultural Sciences, 39.83-87. 2002.
[61]  Gill, M.A., Sabir, M., Ashraf, S., Rahmatullah, and Aziz, T, “Effect of P-stress on growth, phosphorus uptake and utilization efficiency of different cotton cultivars”, Pakistan Journal of Agricultural Sciences, 42. 42-47. 2005.
[62]  Hecht-Bucholz, C, “Über die Dunkelfarbung des Blattgruns bei Phosphormangel”, Zeischrift für Pflanzenernährung und Bodenkunde, 118. 12-22. 1967.
[63]  Rao, I.M. and Terry. N, “Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet. IV. Changes with time following increased supply of phosphate to low-phosphate plants”, Plant Physiology, 107, 1313-1321. 1995.
[64]  Lynch, J., Läuchli, A. and Epstein, E, “Vegetative growth of the common bean in response to phosphorous nutrition”, Crop Science, 31. 380-387. 1991.
[65]  Munns, R., Passioura, J.B., Guo, J., Chazen, O. and Cramer, G.R, “Water relations and leaf expansion: importance of time scale”, Journal of Experimental Botany, 51. 1495-1504. 2000.
[66]  Radin, J.W, “Responses of transpiration and hydraulic conductance to root temperature in nitrogen-and phosphorusde®cient cotton seedlings”, Plant Physiology, 92, 855-857. 1990.
[67]  Clarkson, D.T., Carvajal, M., Henzler, T., Waterhouse, R.N., Smyth, A.J., Cooke, D.T. and Steudle, E, “Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress”, Journal of Experimental Botany 51, 61-70. 2000.
[68]  Rodríguez, D., Zubillaga, M. M. Ploschuk, E.L. Keltjens, W.G. Goudriaan, J. and Lavado, R.S, “Leaf area expression and assimilate production in sunflower (Helianthus annuus L.) growing under low phosphorus conditions”, Plant and Soil, 202. 133-147. 1998.
[69]  Freeden, A.L., Rao, I.M. and Terry, N, “Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max”, Plant Physiology, 89. 225-230. 1989.
[70]  Colomb, B., Debaeke, P. Jouany, C. and Nolot. J.M, “Phosphorus management in low input stockless cropping systems: Crop and soil responses to contrasting P regimes in a 36-year experiment in southern France”, European Journal of Agronomy, 26. 154-165. 2007.
[71]  Persanov, V.M., Andreeva, T.F, “Effect of duration of phosphorus starvation on outflow and utilization of assimilates in connection with plant growth and productivity”, Fiziol Rast, 17. 1175-1181. 1970.
[72]  Steingrobe, B., “Root renewal of sugar beet as a mechanism of P uptake efficiency. Journal of Plant Nutrition and Soil Science”, 164. 533-539. 2001.
[73]  Powell, C.L, “Mycorrhizal status of rushes and sedges in New Zealand”, PhD thesis, University of Otago. Otago, New Zealand. 1974.
[74]  Mollier A. and Pellerin S, “Maize root system growth and development as influenced by phosphorus deficiency”, Journal of Experimental Botany, 50. 487-497. 1999.
[75]  Schroeder, M.S., Janos, D.P, “Plant growth, phosphorus nutrition, and root morphological responses to arbuscular mycorrhizas, phosphorus fertilization, and intraspecific density”, Mycorrhiza, 15. 203-216. 2005.
[76]  Ciereszko, I., Janonis, A., Kociakowska, M, “Growth and metabolism of cucumber in phosphate-deficient conditions. Journal of Plant Nutrition”, 25. 1115-1127. 2002.
[77]  Claassen, N. and Jungk, A, “Bedeutung von Kaliumaufnahmerate, Würzelwachstum und Würzelhaaren für das Kaliumaneignungsvermtigen verschiedener Pflanzenarten”, Zeitschrift für. Pflanzenernaehrung und Bodenkunde, 147,276-289. 1984.
[78]  Pearse, S.J., Veneklaas, E.J., Cawthray, G., Bolland, M.D.A. and Lambers, H, “Triticum aestivum shows a greater biomass response to a supply of aluminium phosphate than Lupinus albus, despite releasing fewer carboxylates into the rhizosphere”, New Phytologist, 169. 515-524. 2006.
[79]  Trehan, S.P, and Sharma, R.C. “Differences in phosphorus use efficiency in potato genotypes”, Advances in Horticultural Science, 19 (1). 13-20. 2005.
[80]  Castañeda Ortiz. N, “Phosphorus efficiency of Arachis pintoi genotypes and possible mechanisms for tolerance to low soil P supply”. Doctoral Dissertation Submitted for the degree of Doctor of Agricultural Science of the Faculty of Agricultural Science Georg-August-University of Göttingen. 2006.
[81]  Marschner, H. “Mechanisms of adaptation of plants to acid soils”, Plant and Soil, 134, 1-20. 1991.
[82]  Trehan, S.P. and Sharma, R.C, “Root-shoot ratio as an indicator of zinc uptake efficiency of different potato cultivars”, Communications in Soil Science and Plant Analysis, 34. 919-32. 2003.
[83]  Rao, I.M. and Terry, N. “Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet. IV. Changes with time following increased supply of phosphate to low-phosphate plants”, Plant Physiology, 107, 1313-1321. 1995.
[84]  Marschner, H., Kirkby, E.A. and Cakmak, I, “Effect of mineral nutritional status on shoot-root partitioning of photoassimilates and cycling of mineral nutrients”, Journal of Experimental Botany, 47. 1255-1263. 1996.
[85]  Akhtar, M.S, Oki. Y. and Adachi, T, “Genetic Diversity in Brassica Cultivars under Deficiently Buffered P-Stress Environment: I. Biomass Accumulation, P-Concentration, P-Uptake, and Related Growth Parameters”, Journal of American Science, 3(2). 55-63. 2007.
[86]  Nielsen, K.L., Eshel, A. and Lynch, J.P, “The effect of phosphorus availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes”, Journal of Experimental Botany, 52. 329-339. 2001.
[87]  Trolove, S.N., Hedley, M.J. Kirk, G.J.D. Bolan, N.S. and Loganathan, P, “Progress in selected areas of rhizosphere research on P acquisition”, Australian Journal of Soil Research, 41 (3). 471-499. 2003.
[88]  Oliver, S. and Barber, S.A, “An evaluation of the mechanisms governing the supply Of Ca, Mg, K and Na to soybeen roots”, Soil Science Society of America, Proceedings, 30. 82-86. 1966.
[89]  Jungk, A. and Claassen, N, “Availability in soil and acquisition by plants as the basis for potassium and phosphorus supply to plants”, Zeitschrift für Pflanzenernährung und Bodenke, 152. 151-158. 1989.
[90]  Kraimat, M. and Bissati, S, Characterization of genotypic variability associated to the phosphorus bioavailability in peanut (Arachis hypogaea L.), Annals of Agricultural Science, 62. 45-49. 2017.
[91]  Steingrobe, B. and Claassen, N. “Potassium dynamics in the rhizosphere and K efficiency of crops”, Journal of Plant Nutrition and Soil Science, 163. 101-106. 2000.
[92]  Nielsen, N.E. “Is the efficiency of nutrient uptake genetically controlled?, in: J.L. Harley, Russel, R.S. (eds.). The Soil-Root Interface. New York: Academic Press, pp 429. 1979.
[93]  Buhse, J, “Wirkung der Wurzelraumtemperatur auf das Phosphataneinungsvermögen von Pflanzen und die Phosphatverfügbarkeit im Boden”, Ph.D. Thesis. University of Göttingen, Germany. 1992.
[94]  Fontes, P.C.R., Barber, S.A. and Wilcox, G.E, “Prediction of phosphorus uptake by 2 tomato cultivars growing under insufficient and sufficient phosphorus soil-conditions using a mechanistic mathematical-model”, Plant and Soil 94, 87-97. 1986.
[95]  Trehan, S.P. and Claassen, N, “External K requirement of young plants of potato, sugar beet and wheat in flowing solution culture resulting from different internal requirements and uptake efficiency”, Potato Research, 41. 229-37. 1998.
[96]  Trehan, S.P. and Sharma, R.C, “Phosphorus and zinc uptake efficiency of potato (Solanum tuberosum) in comparison to wheat (Triticum aestivum), maize (Zea mays) and sunflower (Helianthus annuus). Indian Journal of Agricultural Science, 70. 840-45. 2000.
[97]  Trehan, S.P. and Sharma, R.C, “Potassium uptake efficiency of young plants of three potato cultivars as related to root and shoot parameters”, Communications in Soil Science and Plant Analysis, 33. 1813-24. 2002.
[98]  Horst, W.J., Abdou, M. and Wiesler. F, “Genotypic differences in phosphorus efficiency of wheat”, Plant and Soil, 156, 293-296. 1993.
[99]  Fransen, B., Blijjenberg, J. and de Kroon, H, “Root morphological and physiological plasticity of perennial grass species and the exploitation of spatial and temporal heterogeneous nutrient patches”, Plant and Soil, 211. 179-189. 1999.
[100]  Henriksen, G.H., Raja Raman, D. Walker, L.P. and Spanswick, R.M, “Measurement of net fluxes of ammonium and nitrate at the surface of barley roots using ion-selective microelectrodes. II. Patterns of uptake along the root axis and evaluation of the microelectrode flux estimation technique”, Plant Physiology, 99 (2). 734-747. 1992.
[101]  Engels, C, “Differences between maize and wheat in growth-related nutrient demand and uptake of potassium and phosphorus at suboptimal root-zone temperatures”, Plant and Soil, 150 (1). 129-138. 1993.
[102]  Hart, A.L. and Jessop. D.J, “Phosphorus fractions in trifoliate leaves of white clover and lotus at various levels of phosphorus supply”, New Zealand Journal of Agricultural Research, 26 (3). 357-361. 1983.
[103]  Adu-Gyamfi, J.J., Fujita, K., and Ogata, S, “Phosphorus fractions in relation to growth in pigeon pea at various levels of P supply”, Soil Science and Plant Nutrition, 36. 531-543. 1990.
[104]  Rao, I.M, “The role of phosphorus in photosynthesis”, in Pessarakli, M. (ed,). Handbook of Photosynthesis. New York: Marcel Dekker, pp 173-194. 1996.
[105]  Bélanger, G., Claessens, A., Ziadi, N. “Grain N and P relationships in maize”, Field Crops Research, 126. 1-7. 2012.
[106]  Zhang, H.Y., Wu, H.H., Yu, Q., Wang, Z.W. and Wei, C,Z., et al. “Sampling date, leaf age and root size: implications for the study of plant C:N:P stoichiometry, Plos One, 8. 60360. 2013.
[107]  Mengel, K., and Kirkby, E.A, Principle of Plant Nutrition, Kluver academic pub., London. 2001.
[108]  Graham, R.D, “Breeding for nutritional characteristics in cereals”, Advances in Plant Nutrition, 1. 57-102. 1984.
[109]  Gerloff, G.C., “Intact-plant screening for tolerance to nutrient-deficiency stress”, Plant Soil, 99. 3-16. 1987.
[110]  Bhadoria, P.S., El Dessougi, H., Liebersbach, H., and Claassen, N, “Phosphorus uptake kinetics, size of root system and growth of maize and groundnut in solution culture”, Plant and Soil, 262. 327-336. 2004.
[111]  Trehan, S.P., Singh, B.P, “Nutrient efficiency of different crop species and potato varieties – in retrospect and prospect”, Potato Journal, 40 (1). 1-21. 2013.
[112]  Sanchez, P.A., Palm C.A. and Buol. S.W, “Fertility capability soil classification: a tool to help assess soil quality in the tropics”, Geoderma, 114 (3-4). 157-185. 2003.
[113]  Sanchez, P.A. and Uehara, G, “Management considerations for acid soils with high phosphorus fixation capacity”, in Khasawneh, F.E. Sample, E.C. Kamprath E.J. (eds.), The Role of Phosphorus in Agriculture. Madison, WI: ASA CSSA, SSSA, pp 471-514. 1980.
[114]  Barber, S.A, “Soil-plant interactions in the phosphorus nutrition of plants”, in Khasawneh, E. Sample, E.C. Kamprath E.J. (eds.), The Role of Phosphorus in Agriculture. Madison, WI: American Society of Agronomy, 591-616. 1980.
[115]  Barber, S.A, “A diffusion and mass-flow concept of soil nutrient availability”, Soil Science, 93. 39-49, 1962
[116]  Trehan, S.P, “Mechanism of high nitrogen efficiency in potato cultivars”, Advances in Horticultural Science, 23(3). 179-84. 2009.
[117]  Kamprath, E.J. and Watson, M.E, “Conventional soil and tissue tests for assessing the phosphorus status of soils”, in Khasawneh, F.E. Sample, E.C. Kamprath E.J. (eds.), The Role of Phosphorus in Agriculture, Madison, WI: ASA, CSSA, SSSA, pp 433-469. 1980.
[118]  Wild, A, “Plant nutrients in soil: phosphate”, in Wild A. (ed.), Russell's Soil Conditions and Plant Growth, 11th ed. Essex, England: Longman Scientific and Technical, pp 695-742. 1988.
[119]  Fox, R.L, “External phosphorus requirements of crops”, in Dowdy, R.H. Ryan, J.A. Volk, V.V. Baker D.E. (Eds.), Chemistry in the Soil Environment, Spec. Publ. No. 40, American Society of Agronomy and Soil Society of America, Madison, 1981, pp. 223-239.
[120]  Asher, C.J, in Rechcigl, M. Jr, (ed.), CRC Handbook Series in Nutrition and Food, 3. Boca Rotan, FL: CRC Press, 575. 1978.
[121]  Darrah, P.R, “The rhizosphere and plant nutrition: A quantitative approach”, Plant and Soil, 155/156. 1-20. 1993.
[122]  Gahoonia, T.S., Claassen, N. and Jungk, A, “Mobilization of phosphate in different soils by ryegrass supplied with ammonium or nitrate”, Plant and Soil, 140. 241-48. 1992.
[123]  Gardener, W.K., Parbery, D.G. and Barber, D.A, “The acquisition of phosphorus by Lupinus albus L. II. The effect of varying phosphorus supply and soil type on some characteristics of the soil/ root interface”, Plant and Soil, 68. 33-41. 1982.
[124]  Jones, D.L. and Darrah, P.R, “Role of root derived organic acids in the mobilization of nutrients from the rhizosphere”, Plant and Soil, 166. 247-257. 1994.
[125]  Seeling, B. and Jungk, A, “Utilization of organic phosphorus in calcium chloride Extracts of soil by barley plants and hydrolysis by acid and alkaline phosphatases”, Plant and Soil, 178. 179-84. 1996.