Photosynthesis and Nitrogen-Use Efficiency

  • P. Ananda Kumar
  • Martin A. J. Parry
  • Rowan A. C. Mitchell
  • Altaf Ahmad
  • Yash P. Abrol
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 12)


In C3 crop plants about 60–80% of leaf nitrogen (N) is invested in the photosynthetic apparatus, and N nutrition plays a crucial role in determining photosynthetic capacity. The proportion of leaf N invested in photosynthetic components is fairly constant. By contrast, both N per unit leaf area and the allocation of N between the component photosynthetic processes depend on environmental factors such as N availability, irradiance and CO2 concentration. Light-harvesting and electron transport components often show a co-ordinated and equivalent response to N nutrition. In contrast, most studies have shown disproportionately large changes in ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) in response to N supply, demonstrating the importance of this protein in leaf N economy. At low light, for a given N availability, more protein is allocated towards light harvesting components in order to maximize light capture and, expressed per unit Chl, electron transport and carboxylation capacities are relatively small. High irradiance tends to alter the partitioning of N away from thylakoid protein to soluble proteins, particularly Rubisco. Growth at elevated CO2 often leads to decreases in the amounts of Rubisco and other photosynthetic components on a leaf area basis. This is explicable in terms of greater N sinks elsewhere in the plant as a result of increased carbohydrate availability and acclimatory changes. Models predict that in order to arrive at optimal N use efficiency (NUE) at likely future ambient CO2 concentrations, leaves will need to achieve a redistribution of N so that the ratio between the capacities for regeneration of ribulose-1,5-bisphosphate and carboxylation increases by 30–40%. Human intervention to improve the NUE of crops would have economic and environmental benefits, reducing pollution of water supply by nitrates. The NUE of photosynthesis could be increased either through manipulation of Rubisco amounts or properties, or by decreasing photorespiration. While decreasing Rubisco content could enhance NUE by only about 5%, eliminating photorespiration could produce a change of more than 50%.


CA1P — 2′carboxy-D-arabinitol 1-phosphate CFo-CF1 — coupling factor Chl — chlorophyll FNR — ferredoxin-NADF+ reductase LHC — light harvesting chlorophyll-protein complexes NUE — nitrogen use efficiency PEP — phosphoenolpyruvate PNUE—photosynthetic nitrogen use efficiency PRK — phosphoribulokinase PS I — Photosystem I (reaction center and antennae) PS II — Photosystem II (reaction center and antennae) RPP — reductive pentose phosphate (RPP pathway=Calvin cycle) Rubisco — ribulose-1,5-bisphosphate carboxylase/oxygenase SBPase — sedoheptulose-1,7-bisphosphatase 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abrol YP (ed) (1993) Nitrogen-Soils, Physiology, Biochemistry, Microbiology, Genetics, Indian National Science Academy, New DelhiGoogle Scholar
  2. Abrol YP, Chatterjee SR, Kumar PA and Jain V (1999) Improvement in nitrogen use efficiency: Physiological and molecular approaches. Curr Sci 76: 1357–1364Google Scholar
  3. Ahmad A and Abdin MZ (2000) Photosynthesis and its related physiological variables in the leaves of Brassica genotypes as influenced by sulphur fertilization. Physiol Plant 110: 144–149CrossRefGoogle Scholar
  4. Badger MR and Price GD (1994) The role of carbonic anhydrase in photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 45: 369–392CrossRefGoogle Scholar
  5. Bainbridge G, Madgwick P, Parmar S, Mitchell R, Paul M, Pitts J, Keys AJ and Parry MAJ (1995) Engineering Rubisco to change its catalytic properties. J Exp Bot 46: 1269–1296Google Scholar
  6. Banks FM, Driscoll SP, Parry MAJ, Lawlor DW, Knight JS, Gray JC and Paul MJ (1999) Decrease in phosphoribulokinase activity by antisense RNA in transgenic tobacco. Relationship between photosynthesis, growth, and allocation at different nitrogen levels. Plant Physiol 119: 1125–1136CrossRefPubMedGoogle Scholar
  7. Berzborn RJ, Muller D, Roos P and Anderson B (1981) Significance of different quantitative determinations of photosynthetic ATP synthetase, CF1, for heterogenous CF2 distribution and grana formation. In: Akoyunoglou G (ed) Proceedings of Vth International Photosynthetic Congress, Vol 3, pp 107–120. Balaban International Science Services, Philadelphia.Google Scholar
  8. Björkman O (1981) Responses to different quantum flux densities. In: Lange OL, Nobel PS, Osmond CB and Ziegler H (eds) Physiological Plant Ecology. 1. Responses to the Physical Environment, pp 57–107. Springer-Verlag, BerlinGoogle Scholar
  9. Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Annu Rev Plant Physiol 13: 221–237Google Scholar
  10. Bowes G (1993) Facing the inevitable: Plants and increasing atmospheric carbon dioxide. Annu Rev Plant Physiol Plant Mol Biol 44: 309–332CrossRefGoogle Scholar
  11. Brisson LF, Zelitch I and Havir EA (1998) Manipulation of catalase levels produces altered photosynthesis in transgenic tobacco plants. Plant Physiol 116: 259–269CrossRefPubMedGoogle Scholar
  12. Brown KR, Thompson WA, Camm EL, Hawkins BJ and Guy RD (1996) Effects of N addition rates on the productivity of Picea sitchensis, Thuja plicarta and Tsuga heterophylla seedlings. II Photosynthesis, 13C discrimination and N partitioning in foliage. Trees 10: 198–205Google Scholar
  13. Caemmerer S von and Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153: 376–387CrossRefGoogle Scholar
  14. Charles-Edwards DA, Sturzel H, Ferraris R and Beech DF (1987) An analysis of spatial variation in the nitrogen content of leaves from different horizon with a canopy. Ann Bot 60: 421–126Google Scholar
  15. Chow WS and Hope AB (1987) The stoichiometries of supermolecular complexes in thylakoid membranes from spinach chloroplasts. Aust J Plant Physiol 14: 21–28Google Scholar
  16. Davies EC, Jordan BR, Partis MD and Chow WS (1987) Immunochemical investigation of thylakoid coupling factor protein during photosynthetic acclimation to irradiance. J Exp Bot 38: 1517–1527Google Scholar
  17. DeJong TM and Doyle JF (1985) Second relationship between leaf nitrogen content (photosynthesis capacity) and leaf canopy light exposure in peach (Prunus persia). Plant Cell Environ 8: 701–706.Google Scholar
  18. Demmig-Adams B and Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43: 599–626CrossRefGoogle Scholar
  19. Drake BG, Gonzalez-Meler MA and Long SP (1997) More efficient plants: A consequence of rising atmospheric CO2 Annu Rev Plant Physiol Plant Mol Biol 48: 609–639CrossRefPubMedGoogle Scholar
  20. Evans JR (1983) Nitrogen and photosynthesis in the flag leaf of wheat (Triticum aestivum L.). Plant Physiol 72: 297–302Google Scholar
  21. Evans JR (1988) Acclimation by the thylakoid membranes to growth irradiance and the partitioning of nitrogen between soluble and thylakoid proteins. In: Evans JR, von Caemmerer S and Adams WW III (eds) Ecology of photosynthesis in sun and shade, pp 93–106. CSIRO, MelbourneGoogle Scholar
  22. Evans JR (1989) Photosynthesis and nitrogen relationship in leaves of C3 plants. Oecologia 78: 9–19Google Scholar
  23. Evans JR (1993) Photosynthetic acclimation and nitrogen partitioning within a lucerne canopy. 2. Stability through time and comparison with a theoretical optimum. Aust J Plant Physiol 20: 69–82Google Scholar
  24. Evans JR and Seemann JR (1984) Differences between wheat genotypes in specific activity of ribulose-1,5-bisphosphate carboxylase and the relationship to photosynthesis. Plant Physiol 74: 759–765Google Scholar
  25. Evans JR and Seemann JR (1989) The allocation of protein nitrogen in the photosynthetic apparatus: Costs, consequences, and control. In: Briggs WR (ed) Photosynthesis, pp 183–205. Alan R Liss Inc., New YorkGoogle Scholar
  26. Evans JR and Terashima I (1987) Effect of nitrogen nutrition on electron transport components and photosynthesis in spinach. Aust J Plant Physiol 14: 59–68Google Scholar
  27. Evans JR and Terashima I (1988) Photosynthetic characteristics of spinach leaves grown with different nitrogen treatments. Plant Cell Physiol 29: 157–165Google Scholar
  28. Farage PK, McKee IF and Long SP (1998) Does a low nitrogen supply necessarily lead to acclimation of photosynthesis to leaves of CO2? Plant Physiol 118: 573–580CrossRefPubMedGoogle Scholar
  29. Farquhar GD and Sharkey TD (1994) Photosynthesis and carbon assimilation. In: Boote KJ, Bennett JM, Sinclair TR and Paulson GM (eds) Physiology and Determination of Crop Yield, pp 187–210. American Society of Agronomy, MadisonGoogle Scholar
  30. Farquhar GD, von Caemmerer S and Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149: 78–90CrossRefGoogle Scholar
  31. Ferrar PJ and Osmond CB (1986) Nitrogen supply as a factor influencing photoinhibition and photosynthetic acclimation after transfer of shade grown Solanum dulcamara to bright light. Planta 168: 563–570CrossRefGoogle Scholar
  32. Field C (1983) Allocating leaf nitrogen for the maximization of carbon gain: Leaf age as a control on the allocation program. Oecologia 56: 341–347Google Scholar
  33. Field C and Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givnish TJ (ed) On the Economy of Plant Form and Function, pp 25–55. Cambridge University Press, CambridgeGoogle Scholar
  34. Getzoff TP, Zhu GH, Bohnert HJ and Jensen RG (1998) Chimeric Arabidopsis thaliana ribulose-1,5-bisphosphate carboxylase/oxygenase containing a pea small subunit protein is compromised in carbamylation. Plant Physiol 116: 695–702CrossRefPubMedGoogle Scholar
  35. Harrison EP, Willingham NM, Lloyd JC and Raines CA (1998) Reduced sedoheptulose-1,7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation. Planta 204: 27–36Google Scholar
  36. Häusler RE, Kleines M, Uhrig H, Hirsch HJ and Smets H (1999) Overexpression of phosphoenolpyruvate carboxylase from Corynebacterium glutamicum lowers the CO2 compensation point Г* and enhances dark and light respiration in transgenic potato. J Exp Bot 50: 1231–1242Google Scholar
  37. Hirose T and Werger MJA (1987) Maximizing daily canopy photosynthesis with respect to the leaf nitrogen allocation pattern in the canopy. Oecologia 72: 520–526CrossRefGoogle Scholar
  38. Hirose T, Werger MJA, Pons TL and Van Rheenem JWA (1988) Canopy studies and leaf nitrogen distribution in a stand of Lysimachia vulgaris L. as influenced by stand density. Oecologia 77: 145–150.CrossRefGoogle Scholar
  39. Hollinger DY (1989) Canopy organisation and foliage photosynthetic capacity in a broad-leaved evergreen montane forest. Forest Ecol 3: 53–62Google Scholar
  40. Hudson GS, Evans JR, von Caemmerer S, Arvidsson YB and Andreus TJ (1992) Reduction of ribulose-1,5-phosphate carboxylase/oxygenase content by antisense RNA reduces photosynthesis in tobacco plants. Plant Physiol 983: 294–302Google Scholar
  41. Jain V, Pal M, Lakkineni KC and Abrol YP (1999) Photosynthetic characteristics in two wheat genotypes as affected by nitrogen nutrition. Biol Plant 42: 217–222CrossRefGoogle Scholar
  42. Kanevski I, Maliga P, Rhoades D and Gutteridge S (1999) Plastome engineering of ribulose-1,5-bisphosphate carboxylase/oxygenase in tobacco to form a sunflower large subunit and tobacco small subunit hybrid. Plant Physiol 119: 133–141CrossRefPubMedGoogle Scholar
  43. Khamis S, Lamaze T, Lemoine Y and Foyer C (1990) Adaptation of the photosynthetic apparatus in maize leaves as a result of nitrogen limitation. Plant Physiol 94: 1436–1443Google Scholar
  44. Khan S, Andralojc P, Lea P and Parry MAJ (1999) 2′-carboxy-D-arabinitol 1-phosphate (CA1P) protects ribulose-1,5-bisphosphate carboxylase/oxygenase against proteolytic breakdown: A possible role in vivo. Eur J Biochem 266: 840–847CrossRefPubMedGoogle Scholar
  45. Kossmann J, Sonnewald U and Willmitzer 1 (1994) Reduction of the chloroplastic fructose-1,6-bisphosphatase in transgenic potato plants impairs photosynthesis and plant growth. Plant J 6: 637–650CrossRefGoogle Scholar
  46. Krapp A, Hofmann B, Schafir C and Stitt M (1993) Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: A mechanism for the sink-regulation of photosynthesis. Plant J 3: 817–828CrossRefGoogle Scholar
  47. Ku MSB, Agarie S, Nomura M, Fukayama H, Tsuchida H, Ono K, Hirose S, Toki S, Miyao M and Matsuoka M (1999) High-level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants. Nature Biotech 17: 76–80CrossRefGoogle Scholar
  48. Kutik J, Natr L, Demmers-Derks HH and Lawlor DW (1995) Chloroplast structure of sugar beet (Beta vulgaris L.) cultivated in normal and elevated CO2 concentrations with two contrasted nitrogen supplies. J Exp Bot 46: 1797–1802Google Scholar
  49. Laurer M, Saptic D, Quick WP, Labate C, Fichtner K, Schulze ED, Rodermal SP, Bogorad L and Stitt M (1993) Decreased ribulose-1,5-bisphosphate carboxylase/oxygenase in transgenic tobacco transformed with ‘antisense’ rbcS. VI. Effect on photosynthesis in plants grown at different irradiance. Planta 190: 332–345Google Scholar
  50. Lawlor DW and Mitchell RAC (1991) The effects of increasing CO2 on crop production and productivity: A review of field studies. Plant Cell Environ 14: 807–818Google Scholar
  51. Lawlor DW, Boyle FA, Young AT, Keys AJ and Kendall AC (1987) Nitrate nutrition and temperature effects on wheat: photosynthesis and photorespiration of leaves. J Exp Bot 38: 393–408Google Scholar
  52. Lawlor DW, Kontturi M and Young AT (1989) Photosynthesis by flag leaves of wheat in relation to protein, ribulose-1,5-bisphosphate carboxylase activity and nitrogen supply. J Exp Bot 40: 43–52Google Scholar
  53. Leegood RC (1990) Enzymes of the Calvin cycle. In: Lea P J (ed) Enzymes of primary metabolism, pp 15–37. Academic Press, LondonGoogle Scholar
  54. Leong TY and Anderson JM (1984a) Adaptation of the thylakoid membranes of pea chloroplast to light intensities. I. Study on the distribution of chlorophyll-protein complexes. Photosynth Res 5: 105–115Google Scholar
  55. Leong TY and Anderson JM (1984b) Adaptation of the thylakoid membranes of pea chloroplast to light intensities. II. Regulation of electron transport capacities, electron carriers, coupling factor (CF1) activity and rates of photosynthesis. Photosynth Res 5: 117–128Google Scholar
  56. Lipka V, Häusler RE, Rademacher T, Li J, Hirsch HJ and Kreuzaler F (1999) Solanum tuberosum double transgenic expressing phosphoenolpyruvate carboxylase and NADP-malic enzyme display reduced electron requirement for CO2 fixation. Plant Sci 144: 93–105CrossRefGoogle Scholar
  57. Lutze JL and Gifford RM (1998) Acquisition and allocation of carbon and nitrogen by Danthonia richardsonii in response to restricted nitrogen supply and CO2 enrichment. Plant Cell Environ 21: 1133–1141Google Scholar
  58. Machler F, Oberson A, Grub A and Noseberger J (1988) Regulation of photosynthesis in nitrogen deficient wheat seedlings. Plant Physiol. 87: 46–49Google Scholar
  59. Makino A and Osmond B (1991) Solubilization of ribulose-1,5-bisphosphate carboxylase from the membrane fraction of pea leaves. Photosynth Res 29: 79–85CrossRefGoogle Scholar
  60. Makino A, Mae T and Ohira K (1985) Photosynthesis and ribulose-1,5-bisphosphate carboxylase oxygenase in rice leaves from emergence through senescence-quantitative-analysis by carboxylation oxygenation and regeneration of ribulose 1,5-bisphosphate. Planta 166: 414–420CrossRefGoogle Scholar
  61. Makino A, Mae T and Ohira K (1988) Differences between wheat and rice in the enzymic properties of ribulose-1,5-bisphosphate carboxylase oxygenase and the relationship to photosynthetic gas-exchange. Planta 174: 30–38CrossRefGoogle Scholar
  62. Makino A, Sakashita H, Hidema J, Mac T, Ojima K and Osmond B (1992) Distinctive responses of riblulose-1,5-bisphosphate decarboxylase and carbonic anhydrase in wheat leaves to nitrogen nutrition and their possible relationships to CO2 transfer resistance. Plant Physiol 100: 1737–1743Google Scholar
  63. Makino A, Nakama H and Mae T (1994) Responses of ribulose-1,5-bisphosphate decarboxylase, cytochrome f and sucrose synthesis in rice leaves to leaf nitrogen and their relationship to photosynthesis. Plant Physiol 105: 173–179PubMedGoogle Scholar
  64. Makino A, Sato T, Nakano H and Mae T (1997a) Leaf photosynthesis, plant growth and nitrogen allocation in rice under different irradiances. Planta 203: 390–398CrossRefGoogle Scholar
  65. Makino A, Shimada T, Takumi S, Kaneko K, Matsuoka M, Shimamoto K, Nakano H, Miyao-Tokutomi M, Mae T and Yamamoto N (1997b) Does decrease in ribulose-1,5-bisphosphate carboxylase by ‘antisense’ RbcS lead to a higher nitrogen-use efficiency of photosynthesis under conditions of saturating CO2 and light in rice plants? Plant Physiol 114: 483–491PubMedGoogle Scholar
  66. Mann CC (1999) Genetic engineers aim to soupup crop photosynthesis. Science 283: 314–316PubMedGoogle Scholar
  67. McMorrow EM and Bradbeer JW (1990) Separation, purification, and comparative properties of chloroplast and cytoplasmic phosphoglycerate kinase from barley leaves. Plant Physiology 93: 374–383Google Scholar
  68. Medina E (1971) Effects of nitrogen supply and light intensity during growth on the photosynthetic capacity and carboxylase activity of leaves of Atriplex patula sp. Hastate. Carnegie Inst Wash Year Book 70: 551–559Google Scholar
  69. Medlyn BE (1996) The optimal allocation of nitrogen within photosynthetic system at elevated CO2. Aust J Plant Physiol 23: 593–603Google Scholar
  70. Millard P and Catt JW (1988) The influence of nitrogen supply on the use of nitrate and ribulose-1,5-bisphosphate carboxylase oxygenase as leaf nitrogen stores for growth of potato-tubers (Solanum tuberosum L). J Exp Bot 39: 1–11Google Scholar
  71. Mitchell RAC, Theobald JC, Parry MAJ and Lawlor DW (2000) Is there scope for improving balance between RuBP-regeneration and carboxylation capacities in wheat at elevated CO2? J Exp Bot 5: 391–397Google Scholar
  72. Nakano H, Makino A and Mae T (1997) The effects of elevated partial pressures of CO2 on the relationship between photosynthetic capacity and N content in rice leaves. Plant Physiol 115: 191–198PubMedGoogle Scholar
  73. Nie GY, Long SP, Garcia RL, Kimball BA, Lamorte RL, Pinter PJ, Wall GW and Webber AN (1995) Effects of free air CO2 enrichment on the development of the photosynthetic apparatus in wheat, as indicated by changes in leaf proteins. Plant Cell Environ 18: 855–864Google Scholar
  74. Novoa R and Loomis RS (1981) Nitrogen and plant production. Plant Soil 58: 177–204CrossRefGoogle Scholar
  75. Osaki M, Shinano T and Tadono T (1993) Effect of nitrogen application on the accumulation of ribulose-1,5-bisphosphate carboxylase oxygenase and chlorophyll in several field crops. Soil Sci Nut 39: 427–436Google Scholar
  76. Paul MJ, Knight JS, Habash D, Parry MAJ, Lawlor DW, Barnes SA, Loynes A and Gray JC (1995) Reduction in phosphoribulokinase activity by antisense RNA in transgenic tobacco— effect on CO2 assimilation and growth in low irradiance. Plant J 7: 535–542CrossRefGoogle Scholar
  77. Poorter H and Evans JR (1998) Photosynthetic nitrogen use efficiency of species that differ inherently in specific leaf area. Oecologia 116: 26–37CrossRefGoogle Scholar
  78. Price GD, Evans JR, Caemmerer S von, Yu JW and Badger MR (1995) Specific reduction of chloroplast glyceraldehyde-3-phosphate dehydrogenase activity by antisense RNA reduces CO2 assimilation via a reduction in ribulose bisphosphate regeneration in transgenic tobacco plants. Planta 195: 369–378CrossRefPubMedGoogle Scholar
  79. Quick WP, Schurr U, Scheibe R, Schulze ED, Rodermel SR, Bogorad L and Stitt M (1991) The impact of decreased Rubisco on photosynthesis, growth, allocation and storage in tobacco plants which have been transformed with antisense rbcS. Plant J 1:51–58CrossRefGoogle Scholar
  80. Quick WP, Fichtner K, Schulze ED, Wendler R, Leegood RC, Mooney H, Rodermel SR, Bogorad L and Stitt M (1992) Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with ‘antisense’ rbcS. IV. Impact on photosynthesis in ambient growth conditions of altered nitrogen supply. Planta 188: 522–531CrossRefGoogle Scholar
  81. Robinson SP and Walker DA (1981) Photosynthetic carbon reduction cycle (Calvin cycle) (including fluxes and regulation). In: Stumpf PK and Conn EE (eds) The Biochemistry of Plants. A Comprehensive Treatise, Vol 8, pp 193–226. Academic Press, LondonGoogle Scholar
  82. Robinson SP, Streusand VJ, Chatfield JM and Portis AR Jr. (1988) Purification and assay of Rubisco activase in leaves. Plant Physiol 88: 1008–1014Google Scholar
  83. Rogers GS, Milham PJ, Gillings M and Conroy JP (1996) Sink strength may be the key to growth and nitrogen responses in N-deficient wheat at elevated CO2. Aust J Plant Physiol 23: 253–264Google Scholar
  84. Roumet C, Bel MP, Sonie L, Jardon F and Roy J (1996) Growth response of grasses to elevated CO2 A physiological plurispecific analysis. New Phytol 133: 595–603Google Scholar
  85. Sage RF (1994) Acclimation to photosynthesis to increasing atmospheric CO2 The gas exchange perspective. Photosynth Res 39: 351–368CrossRefGoogle Scholar
  86. Sage RF (1999) Why C4 photosynthesis? In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 3–16. Academic Press, LondonGoogle Scholar
  87. Sage RF, Pearcy RW and Seemann JR (1987) The nitrogen use efficiency of C3 and C4 plants. I. Leaf nitrogen effects on the gas exchange characteristics of Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiol 84: 959–963Google Scholar
  88. Sage RF, Sharkey TD and Seemann JR (1989) Acclimation of photosynthesis to elevated CO2 in five C3 species. Plant Physiol 89: 590–596Google Scholar
  89. Sage RF, Sharkey TD and Seemann JR (1990) Regulation of ribulose-1,5-bisphosphate carboxylase activity in response to light-intensity and in the C-3 annuals Chenopodium album L and Phaseolus vulgaris L. Plant Physiol 94: 1735–1742Google Scholar
  90. Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: Physics, physiology and rate limitations. Bot Rev 51: 53–105Google Scholar
  91. Sims DA, Luo Y and Seemann JR (1998) Comparison of photosynthetic acclimation to elevated CO2 and limited nitrogen supply in soybean. Plant Cell Environ 21: 945–952Google Scholar
  92. Sinclair TR and Horie T (1989) Leaf nitrogen, photosynthesis and crop radiation use efficiency: A review. Crop Sci 42: 90–98Google Scholar
  93. Sinclair TR and Sheehy JE (1999) Erect leaves and photosynthesis in rice. Science 283: 1456–1457CrossRefGoogle Scholar
  94. Sivasankar A, Bansal KC and Abrol YP (1993) Nitrogen in relation to leaf area development. In: YP Abrol (ed) Nitrogen, pp 75–84. Proc Ind Nat Sci Acad, New DelhiGoogle Scholar
  95. Sivasankar A, Lakkineni KC, Jain V and Abrol YP (1998a) Differential response of two wheat genotypes to nitrogen supply. I. Ontogenic changes in laminae growth and photosynthesis. J Agron Crop Sci 181: 21–27Google Scholar
  96. Sivasankar A, Lakkineni KC, Jain V, Kumar P and Abrol YP (1998b) Differential response of two wheat genotypes to nitrogen supply. II. Mesophyll cell characteristics and photosynthesis of lamina at full expansion. J Agron Crop Sci 181: 65–70Google Scholar
  97. Stitt M and Schulze ED (1994) Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology. Plant Cell Environ 17: 518–552Google Scholar
  98. Stulen I and Den Hertog J (1993) Root growth and functioning under atmospheric CO2 enrichment. Vegetation 104/105: 99–115CrossRefGoogle Scholar
  99. Terashima I and Evans JR (1988) Effects of light and nitrogen nutrition on the organization of the photosynthetic apparatus in spinach. Plant Cell Physiol 29: 143–155Google Scholar
  100. Theobald JC, Mitchell RAC, Parry MAJ and Lawlor DW (1998) Estimation of excess investment in ribulose-1,5-bisphosphate carboxylase/oxygenase in leaves of spring wheat grown under elevated CO2. Plant Physiol 118: 945–955CrossRefPubMedGoogle Scholar
  101. Trost P, Scagliarini S, Valentini V and Pupillo P (1993) Activation of spinach chloroplast glyceraldehyde-3-phosphate dehydrogenase —effect of glycerate 1,3-bisphosphate. Planta 190: 320–326CrossRefGoogle Scholar
  102. Uemura K, Suzuki Y, Shikanai T, Wadano A, Jensen RG, Chmara W and Yokota A (1996) A rapid and sensitive method for determination of relative specificity of Rubisco from various species by anion exchange chromatography. Plant Cell Physiol 37: 325–331Google Scholar
  103. Verhoeven AS, Demmig-Adams B and Adams WW (1997) Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach exposed to high light and N stress. Plant Physiol 113: 817–824PubMedGoogle Scholar
  104. Wong SC (1979) Elevated atmospheric pressure of CO2 and plant growth. I. Interactions of nitrogen nutrition and photosynthetic capacity in C3 and C4. Oecologia 44: 68–74CrossRefGoogle Scholar
  105. Woodrow IE (1994) Control of steady state photosynthesis in sunflowers growing in enhanced CO2. Plant Cell Environ 17: 277–286Google Scholar
  106. Woodrow IE and Berry JA (1988) Enzymatic regulation of photosynthetic CO2 fixation in C3 plants. Annu Rev Plant Physiol Plant Mol Biol 39: 533–594Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • P. Ananda Kumar
    • 1
  • Martin A. J. Parry
    • 2
  • Rowan A. C. Mitchell
    • 2
  • Altaf Ahmad
    • 3
  • Yash P. Abrol
    • 3
  1. 1.National Research Centre for Plant BiotechnologyIndian Agricultural Research InstituteNew DelhiIndia
  2. 2.Biochemistry and Physiology DepartmentlACR-RothamstedHarpendenUK
  3. 3.Division of Plant PhysiologyIndian Agricultural Research InstituteNew DelhiIndia

Personalised recommendations