Photosynthetica 2009, 47(2):163-183 | DOI: 10.1007/s11099-009-0030-7

Pioneering research on C4 leaf anatomical, physiological, and agronomic characteristics of tropical monocot and dicot plant species: Implications for crop water relations and productivity in comparison to C3 cropping systems

M. A. El-Sharkawy1,*
1 Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia

The review is done to summarise the history of the discoveries of the many anatomical, agronomical, and physiological aspects of C4 photosynthesis (where the first chemical products of CO2 fixation in illuminated leaves are four-carbon dicarboxylic acids) and to document correctly the scientists at the University of Arizona and the University of California, Davis, who made these early discoveries. The findings were milestones in plant science that occurred shortly after the biochemical pathway of C3 photosynthesis in green algae (where the first chemical product is a three-carbon compound) was elucidated at the University of California, Berkeley, and earned a Nobel Prize in chemistry. These remarkable achievements were the result of ground-breaking pioneering research efforts carried out by many agronomists, plant physiologists and biochemists in several laboratories, particularly in the USA. Numerous reviews and books written in the past four decades on the history of C4 photosynthesis have focused on the biochemical aspects and give an unbalanced history of the multidisciplinary/multinstitutional nature of the achievements made by agronomists, who published much of their work in Crop Science. Most notable among the characteristics of the C4 species that differentiated them from the C3 ones are: (I) high optimum temperature and high irradiance saturation for maximum leaf photosynthetic rates; (II) apparent lack of CO2 release in a rapid stream of CO2-free air in illuminated leaves in varying temperatures and high irradiances; (III) a very low CO2 compensation point; (IV) lower mesophyll resistances to CO2 diffusion coupled with higher stomatal resistances, and, hence, higher instantaneous leaf water use efficiency; (V) the existence of the so-called "Kranz leaf anatomy" and the higher internal exposed mesophyll surface area per cell volume; and (VI) the ability to recycle respiratory CO2 by illuminated leaves.

Additional key words: agriculture; biochemistry; breeding; carbon assimilation; crops; drought; enzymes; gas exchange; photorespiration; photosynthesis; water use efficiency

Received: September 2, 2008; Accepted: April 29, 2009; Published: June 1, 2009  Show citation

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El-Sharkawy, M.A. (2009). Pioneering research on C4 leaf anatomical, physiological, and agronomic characteristics of tropical monocot and dicot plant species: Implications for crop water relations and productivity in comparison to C3 cropping systems. Photosynthetica47(2), 163-183. doi: 10.1007/s11099-009-0030-7
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References

  1. Albrechtová, J., Janáècek, J., Lhotáková, Z., Radochová, B., Kubinová, L.: Novel efficient methods for measuring mesophyll anatomical characteristics from fresh sections using stereology and confocal microscopy: application on acid rain-treated Norway pruce needles.-J. Exp. Bot. 58: 1451-1461, 2007. Go to original source...
  2. Andre, M.: Oxygenation capacity and Rubisco evolution.-Online (http://www.photorespiration.fr/oxygenation.htm), 2006.
  3. Arnon, I.D.: The discovery of photosynthetic phosphorylation.-TIBS 9: 258-262, 1984. Go to original source...
  4. Bailey, K.J., Battistelli, A., Dever, L.V., Lea, P.J., Leegood, R.C.: Control of C4 photosynthesis: effects of reduced activities of phosphoenolpyruvate carboxylase on CO2 assimilation in Amaranthus edulis L.-J. Exp. Bot. 51: 339-346, 2000. Go to original source...
  5. Baker, D.N., Musgrave, R.B.: Photosynthesis under field conditions. V. Further plant chamber studies of the effects of light on corn (Zea mays L.).-Crop Sci. 2: 127-131, 1964. Go to original source...
  6. Bazzaz, F.A.: The response of natural ecosystems to the rising global CO2 levels.-Annu. Rev. Ecol. Syst. 21: 167-196, 1990. Go to original source...
  7. Begonia, G.B., Begonia, M.T.: Plant photosynthetic production as controlled by leaf growth, phenology, and behavior.-Photosynthetica 45: 321-333,2007. Go to original source...
  8. Bhatt, J.G., Rao, M.R.K.: Heterosis in growth and photosynthetic rate in hybrids of cotton.-Euphytica 30: 129-133, 1981. Go to original source...
  9. Björkman, O.: Further studies of the effect of oxygen concentration on photosynthetic CO2 uptake in higher plants.-Carnegie Inst. Year Book 66: 220-228, 1968.
  10. Björkman, O., Boynton, J., Berry, J.: Comparison of the heat stability of photosynthesis, chloroplast membrane reactions, photosynthetic enzymes, and soluble protein in leaves of heat-adapted and cool-adapted C4 species.-Carnegie Inst. Year Book 75: 400-407, 1976.
  11. Black, C.C., Jr.: Ecological implications of dividing plants into groups with distinct photosynthetic production capacities.-Adv. Ecol. Res. 7: 87-113, 1971. Go to original source...
  12. Black, C.C., Jr.: Photosynthetic carbon fixation in relation to net CO2 uptake.-Annu. Rev. Plant Physiol. 24: 253-286, 1973. Go to original source...
  13. Black, C.C., Jr.: Martin Gibbs (1922-2006): Pioneer of 14C research, sugar metabolism & photosynthesis;vigilant Editor-in-Chief of Plant Physiology; sage Educator; and humanistic Mentor.-Photosynth. Res. 95: 1-10, 2008. (online at doi 10.1007/s11120-007-9232-7). Go to original source...
  14. Black, C.C., Goldstein, L.D., Ray, T.B., Kestler, D.P., Mayne, B.C.: The relationship of plant metabolism to internal leaf and cell morphology and to the efficiency of CO2 assimilation.-In: Burris, R. H., Black, C.C., Jr. (ed.): CO2 Metabolism and Plant Productivity, Pp. 113-139. Univ. Park Press, Baltimore-London-Tokyo 1976.
  15. Bohning, R.H., Burnside, C.A.: The effect of light intensity on rate of apparent photosynthesis in leaves of sun and shade plants.-Am. J. Bot. 43: 557-561, 1956. Go to original source...
  16. Boote, K.J., Loomis, R.S. (ed.).: Modeling Crop Photosynthesis-from Biochemistry to Canopy.-Crop Science Society of America and American Society of Agronomy, Madison1991. Go to original source...
  17. Boote, K.J., Sinclair, T.R.: Significant discoveries and our changing perspective on research.-Crop Sci. 46: 2270-2277, 2006. Go to original source...
  18. Borlaug, N.E.: Contributions of conventional plant breeding to food production.-Science 219: 689-693, 1983. Go to original source...
  19. Bosian, G.: Über die Vollautomatisierung der CO2-Assimilationsbestimming und zur Methodik des Kuvettenklimas.-Planta 45: 470-492, 1955. Go to original source...
  20. Bowes, G., Ogren, W.L., Hageman, R.H.: Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase.-Biochem. Biophys. Res. Commun. 45: 716-722, 1971. Go to original source...
  21. Boyer, J.S.: Advances in drought tolerance in plants.-Adv. Agron. 56: 187-218, 1996. Go to original source...
  22. Briggs, L.J., Shantz, H. L.: Relative water requirement of plants.-J. Agric. Res. 3: 1-63, 1914.
  23. Brown, R. H.: Difference in the N use efficiency in C3 and C4 plants and its implications in adaptation and evolution.-Crop Sci. 18: 93-98, 1978. Go to original source...
  24. Burnside, C.A., Bohning, R.H.: The effect of prolonged shading on the light saturation curves of apparent photosynthesis in sun plants.-Plant Physiol. 32: 61-63, 1957. Go to original source...
  25. Burris, R. H., Black, C.C., Jr. (ed.): CO2 Metabolism and Plant Productivity.-University Park Press, Baltimore-London-Tokyo 1976.
  26. Cadavid, L.F., El-Sharkawy, M.A., Acosta, A., Sánchez, T.: Long-term effects of mulch, fertilization and tillage on cassava grown in sandy soils in northern Colombia.-Field Crops Res. 57: 45-56, 1998. Go to original source...
  27. Calvin, M.: Forty years of photosynthesis and related activities.-Photosynth. Res. 21: 3-16, 1989. Go to original source...
  28. Castrillo, M., Aso, P., Longart, M., Vermehren, A.: In situ immunofluorescent localization of ribulose-1,5-bisphosphate carboxylase/oxygenase in mesophyll of C4 dicotyledonous plants.-Photosynthetica 33: 39-50, 1997. Go to original source...
  29. Chollet, R., Ogren, W.L.: Regulation of photorespiration in C3 and C4 species.-Bot. Rev. 41: 137-179, 1975. Go to original source...
  30. CIAT: Cassava Program Annual Reports for 1986-1996.-Centro Internacional de Agricultural Tropical, Cali 1986-1996.
  31. CIAT: Cassava Program Annual Report for 1992.-Centro Internacional de Agricultura Tropical, Cali 1992.
  32. Cock, J.H., Yoshida, S.: Accumulation of 14C-labelled carbohydrate before flowering and its subsequent redistribution and respiration in the rice plant.-Proc. Crop Sci. Soc. Japan 41: 226-234, 1972. Go to original source...
  33. Cock, J.H., Yoshida, S.: Photosynthesis, crop growth, and respiration of a tall and short rice varieties.-Soil Sci. Plant Nutr. 19: 53-59, 1973. Go to original source...
  34. Crookston, R.K., Moss, D.N.: Interveinal distance for carbohydrate transport in leaves of C3 and C4 grasses.-Crop Sci. 14: 123-125, 1974. Go to original source...
  35. Dai, Z.Y., Ku, M.S.B., Edwards, G.E.: C4 photosynthesis. The CO2-concentrating mechanism and photorespiration.-Plant Physiol. 103: 83-90, 1993. Go to original source...
  36. De Tafur, S. M., El-Sharkawy, M. A., Cadavid, L.F.: Response of cassava (Manihot esculenta Crantz) to water stress and fertilization.-Photosynthetica 34: 233-239, 1997a. Go to original source...
  37. De Tafur, S. M., El-Sharkawy, M. A., Calle, F.: Photosynthesis and yield performance of cassava in seasonally dry and semiarid environments.-Photosynthetica 33: 249-257, 1997b. Go to original source...
  38. de Veau, E.J., Burris, J.E.: Photorespiratory rates in wheat and maize as determined by 18O-labeling.-Plant Physiol. 90: 500-511, 1989. Go to original source...
  39. Devlin, R. M.: Plant Physiology. 3rd Ed.-D. Van Nostrand Company, New York 1975.
  40. Dever, L.V., Bailey, K.J., Leegood, R.C., Lea, P.J.: Control of photosynthesis in Amaranthus edulis mutants with reduced amounts of PEP carboxylase.-Aust. J. Plant Physiol. 24: 469-476, 1997. Go to original source...
  41. Downton, W.J.S., Tregunna, E.B.: Carbon dioxide compensation-its relation to photosynthetic carboxylation reactions, systematics of the Gramineae and leaf anatomy.-Can. J. Bot. 46: 207-215, 1968. Go to original source...
  42. Dunstone, R.L., Evans, L.T.: Role of changes in cell size in the evolution of wheat.-Aust. J. Plant. Physiol. 1: 157-165, 1974. Go to original source...
  43. Duysens, L.N.M.: The discovery of the 2 photosynthetic systems: a personal account.-Photosynth. Res. 21: 61-79, 1989. Go to original source...
  44. Edwards, G.E., Franceschi, V.R., Voznesenskaya, E.V: Single-cell C4 photosynthesis versus the dual-cell (Kranz) paradigm.-Annu. Rev. Plant Biol. 55: 173-196, 2004. Go to original source...
  45. Edwards, G.E., Ku, M.S.B., Monson, R.K.: C4 photosynthesis and its regulation.-In: Barber, J., Baker, N.R. (ed.).: Photosynthetic Mechanisms and Environments. Pp. 287-327. Elsevier, Amsterdam-New York-Oxford 1985.
  46. Edwards, G.E., Walker, D.A.: C3, C4: Mechanisms, and Cellular and Environmental Regulation of Photosynthesis.-Blackwell, Oxford 1983.
  47. Egle, K.: Methoden der Photosynthesessung. Landpflanzen.-In: Ruhland, W. (ed.): Encyclopedia of Plant Physiol. V, Pt.1, Pp. 115-163. Springer-Verlag, Berlin-Göttingen-Hiedelberg 1960. Go to original source...
  48. Ehleringer, J., Björkman, O.: Quantum yields for CO2 uptake in C3 and C4 Plants: dependence on temperature, CO2, and O2 concentration.-Plant Physiol. 59: 86-90, 1977. Go to original source...
  49. Ehleringer, J., Pearcy, R.W.: Variation in quantum yield for CO2 uptake among C3 and C4 plants.-Plant Physiol. 73: 555-559, 1983. Go to original source...
  50. Elmore, C.D.: The paradox of no correlation between leaf photosynthetic rates and crop yields.-In: Hesketh, J.D., Jones, J.W. (ed.): Predicting Photosynthesis for Ecosystem Models. Vol. II, Pp. 155-167. CRC Press, Boca Raton 1980.
  51. Elmore, C.D., Paul, R.N.: Composite list of C4 weeds.-Weed Sci. 31: 686-692, 1983. Go to original source...
  52. El-Sharkawy, M. A.: Factors limiting photosynthetic rates of different plant species.-Ph.D. Dissertation.The University of Arizona, Tucson 1965.
  53. El-Sharkawy, M.A.: Drought-tolerant cassava for Africa, Asia, and Latin America: breeding projects work to stabilize productivity without increasing pressures on limited natural resources.-BioScience 43: 441-451, 1993. Go to original source...
  54. El-Sharkawy, M.A.: Cassava biology and physiology.-Plant Mol. Biol. 56: 481-501, 2004. Go to original source...
  55. El-Sharkawy, M.A.: How can calibrated research-based models be improved for use as a tool in identifying genes controlling crop tolerance to environmental stresses in the era of genomics-from an experimentalist's perspective.-Photosynthetica 43: 161-176, 2005. Go to original source...
  56. El-Sharkawy, M.A.: Utility of basic research in plant/crop physiology in relation to crop improvement: a review and personal account.-Braz. J. Plant Physiol. 18: 419-446, 2006a. Go to original source...
  57. El-Sharkawy, M. A.: International research on cassava photosynthesis, productivity, eco-physiology, and responses to environmental stresses in the tropics.-Photosynthetica 44: 481-512, 2006b. Go to original source...
  58. El-Sharkawy, M. A.: Physiological characteristics of cassava tolerance to prolonged drought in the tropics: Implications for breeding cultivars adapted to seasonally dry and semiarid environments.-Braz. J. Plant Physiol. 19: 257-286, 2007. Go to original source...
  59. El-Sharkawy, M. A., Cadavid, L. F.: Response of cassava to prolonged water stress imposed at different stages of growth.-Exp. Agr. 38: 333-350, 2002. Go to original source...
  60. El-Sharkawy, M. A., Cock, J. H.: C3-C4 intermediate photosynthetic characteristics of cassava (Manihot esculenta Crantz). 1. Gas-exchange.-Photosynth. Res. 12: 219-235, 1987. Go to original source...
  61. El-Sharkawy, M.A., Cock, J.H.: Photosynthesis of cassava (Manihot esculenta Crantz).-Exp. Agr. 26: 325-340, 1990. Go to original source...
  62. El-Sharkawy, M.A., Cock, J.H., De Cadena, G.: Influence of differences of leaf anatomy on net photosynthetic rates of some cultivars of cassava.-Photosynth. Res. 5: 235-242, 1984. Go to original source...
  63. El-Sharkawy, M., Hesketh, J.D.: Plant efficiency measured by photosynthesis.-Prog. Agric. Ariz. Agr. Exp. Sta. May-June, Tucson. P. 15. Tucson 1964a.
  64. El-Sharkawy, M. A., Hesketh, JD.: Effects of temperature and water deficit on leaf photosynthetic rates of different species.-Crop Sci. 4: 514-518, 1964b. Go to original source...
  65. El-Sharkawy, M.A., Hesketh, J.D.: Effect of stomatal differences among species on leaf photosynthesis.-Crop Sci. 4: 619-621, 1964c. Go to original source...
  66. El-Sharkawy, M., Hesketh, J.: Photosynthesis among species in relation to characteristics of leaf anatomy and CO2 diffusion resistances.-Crop Sci. 5: 517-521, 1965. Go to original source...
  67. El-Sharkawy, M.A., Hesketh, J.D., Elmore, D.: Photosynthesis and transpiration among species.-Adv. Front Plant Sci. 18: 33-37, 1967.
  68. El-Sharkawy, M.A., Hesketh, J.D.: Citation Classic-Photosynthesis among species in relation to characteristics of leaf anatomy and CO2 diffusion resistances.-Curr. Cont./Agr. Biol. Environ. 27: 14, 1986. (Online http://www.library.upenn/edu/classics1986/A1986C891300001.pdf).
  69. El-Sharkawy, M.A., Hesketh, J.D., Muramoto, H.: Further studies of limiting factors to photosynthesis.-Agronomy Abstracts, November, 1964, ASA, Madison 1964.
  70. El-Sharkawy, M., Hesketh, J., Muramoto, H.: Leaf photosynthetic rates and other growth characteristics among 26 species of Gossypium.-Crop Sci. 5: 173-175, 1965. Go to original source...
  71. El-Sharkawy, M.A., Loomis, R.S., Williams, W.A.: Apparent reassimilation of respiratory carbon dioxide by different plant species.-Physiol. Plant. 20: 171-186, 1967. Go to original source...
  72. El-Sharkawy, M.A., Loomis, R.S., Williams, W.A.: Photosynthetic and respiratory exchanges of carbon dioxide by leaves of grain amaranth.-J. Appl. Ecol. 5: 243-251, 1968. Go to original source...
  73. El-Sharkawy, M. A., Lopez, Y., Bernal, L.M.: Genotypic variations in activities of phosphoenolpyruvate carboxylase and correlations with leaf photosynthetic characteristics and crop productivity of cassava grown in low-land seasonally-dry tropics.-Photosynthetica 46: 238-247, 2008. Go to original source...
  74. Evans, L.T.: Crop Evolution, Adaptation and Yield.-Cambridge University Press, Cambridge 1993.
  75. Farquhar, G. D.: On the nature of carbon isotope discrimination in C4 species.-Aust. J. Plant Physiol. 10: 205-226, 1983. Go to original source...
  76. Forrester, M.L., Krotkov, G., Nelson. C.D.: Effect of oxygen on photosynthesis, photorespiration and respiration in detached leaves. I. Soybean.-Plant Physiol. 41: 422-427, 1966a. Go to original source...
  77. Forrester, M.L., Krotkov, G., Nelson, C.D.: Effect of oxygen on photosynthesis, photorespiration, and respiration in detached leaves. II. Corn and other monocotyledons.-Plant Physiol. 41: 428-431, 1966b. Go to original source...
  78. Furbank, R.T., Hatch, M.D.: Mechainsm of C4 photosynthesis. The size and composition of the inorganic carbon pool in bundle sheath-cells.-Plant Physiol. 85: 958-964, 1987. Go to original source...
  79. Gallagher, R.: Citation violations.-The Scientist 23: 13, 2009.
  80. Garfield, E.: Bibliographic negligence: A serious transgression.-The Scientist 5:14, 1991.
  81. Garfield, E.: The effectiveness of American Society of Agronomy journals: A citationist's perspective.-In: Mayland, H.F., Sojka, R.E (ed.): Research Ethics, Manuscript Review and Journal Quality. Pp. 1-13. ACS, ASA, Madison 1992. Go to original source...
  82. Gaastra, P.: Photosynthesis of crop plants as influenced by light, carbon dixoide, temperature and stomatal diffusion resistance.-Meded. Landbouwhogeschool (Wageningen) 59: 1-68, 1959.
  83. Giaquinta, R.T.: Phloen loading of sucrose.-Annu. Rev. Plant Physiol. 34: 347-387, 1983. Go to original source...
  84. Gifford, R.M.: A comparison of potential photosynthesis, productivity and yield of plant species with differing photosynthetic metabolism.-Aust. J. Plant Physiol. 1: 107-117, 1974. Go to original source...
  85. Gifford, R.M., Evans, L.T.: Photosynthesis, carbon partitioning, and yield.-Annu. Rev. Plant Physiol. 32: 485-509, 1981. Go to original source...
  86. Gilland, B.: World population and food supply. Can food production keep pace with population growth in the next halfcentury?-Food Policy 27: 47-63, 2002. Go to original source...
  87. Gregory, F.C., Spear, I., Thiman, K.V.: The interrelation between CO2 metabolism and photoperiodism in Kalanchoe.-Plant Physiol. 29: 220-229, 1954. Go to original source...
  88. Haberlandt, G.: Physiologische Pflanzenanatomie.-Engelmann, Leipzig 1904. Go to original source...
  89. Hatch, M.D.: The C4 pathway of photosynthesis: mechanism and function.-In: Burris, R.H., Black, C.C., Jr. (ed.): CO2 metabolism and plant Productivity. Pp. 59-81. Univ. Park Press, Baltimore-London-Tokyo 1976.
  90. Hatch, M.D.: C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure.-Biochim. Biophys. Acta 895: 81-106, 1987. Go to original source...
  91. Hatch, M.D.: I can't believe my luck.-Photosynth. Res. 33: 1-14, 1992a. Go to original source...
  92. Hatch, M.D.: C4 photosynthesis: an unlikely process full of surprises.-Plant Cell Physiol. 33: 333-342, 1992b.
  93. Hatch, M.D.: C4 photosynthesis: a historical overview.-In: Sage, R.F., Monson, R.K. (ed.): C4 Plant Biology. Pp.17-46. Academic Press, San Diego 1999. Go to original source...
  94. Hatch, M.D., Slack, C.R.: Photosynthesis by sugar-cane leaves. A new carboxylation reaction and the pathway of sugar formation.-Biochem. J. 101: 103-111, 1966. Go to original source...
  95. Hatch, M.D., Slack, C.R.: Photosynthetic CO2-fixation pathways.-Annu. Rev. Plant Physiol. 21: 141-162, 1970. Go to original source...
  96. Hattersley, P.W., Browning, A.J.: Occurrence of the suberized lamella in leaves of grasses of different photosynthetic types. I. In parenchymatous bundle sheaths and PCR (Kranz) sheaths.-Protoplasma 109: 371-401, 1981. Go to original source...
  97. Helson, V. H., Minshall, W.H.: Effects of petroleum oils on the carbon dioxide output in respiration of parsnip and mustard.-Plant Physiol. 31: 5-11, 1956. Go to original source...
  98. Hesketh, J.D.: Limitations to photosynthesis responsible for differences among species.-Crop Sci. 3: 493-496, 1963. Go to original source...
  99. Hesketh, J.D., Moss, D.N.: Variation in the response of photosynthesis to light.-Crop Sci. 3: 107-110, 1963. Go to original source...
  100. Hesketh, J. D.: Musgrave R.B. (Photosynthesis under field conditions). IV. Light studies with individual corn leaves.-Crop Sci. 2: 311-315, 1962. Go to original source...
  101. Ho, L. C.: Metabolism and compartmentation of imported sugars in sink organs in relation to sink strength.-Annu. Rev. Plant Physiol. Mol. Biol. 39: 355-378, 1988. Go to original source...
  102. Hong, J., Jiang, D.-A, Weng, X.-Y, Wang, W.-B, Hu, D.-W.: Leaf anatomy,chloroplast ultrastructure, and cellular localization of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPCO) and RuBPCO activase in Amaranthus tricolor L.-Photosynthetica 43: 519-528, 2005. Go to original source...
  103. Howeler, R.H.: Cassava mineral nutrition and fertilization.-In: Hillocks, R.J., Thresh, J.M., Bellotti, A.C. (ed.): Cassava: Biology, Production and Utilization. Pp. 115-147. CABI Publishing, New York 2002. Go to original source...
  104. Howeler, R.H., Cadavid, L.F.: Short-and long-term fertility trials in Colombia to determine the nutrient requirements of cassava.-Fertilizer Res. 26: 61-80, 1990. Go to original source...
  105. Huzisige, H., Ke, B.: Dynamics of the history of photosynthesis research.-Photosynth. Res. 38: 185-209, 1993. Go to original source...
  106. IPCC: Intergovernmental panel on climate change:IPCC special report on the regional impact of climate change. An assessment of vulnerability.-UNEP, WMO, 2006. Online (http://www.grida.no/climate/ipcc/regional/502.htm.)
  107. Irvine, J.E.: Evidence for photorespiration in tropical grasses.-Physiol. Plant. 23: 607-612, 1970. Go to original source...
  108. Jackson, W.A., Volk, R. J.: Oxygen uptake by illuminated maize leaves.-Nature 222: 269-271, 1969. Go to original source...
  109. Jackson, W.A., Volk. R. J.: Photorespiration.-Annu. Rev. Plant Physiol. 21: 385-432, 1970. Go to original source...
  110. Janardhan, K.V., Murty, K.S., Rawlo, S.: Path coefficient analysis and heritability of photosynthetic rate and associated leaf characters in rice varieties.-Indian J. Plant Physiol. 26: 168-176, 1983.
  111. Jenkins, C.L.D.: Effects of the phosohoenolpyruvate carboxylase inhibitor 3,3-dichloro-2-(dihydroxyphosphinoyl-methyl) propenoate on photosynthesis. C4 selectivity and studies on C4 photosynthesis.-Plant Physiol. 89: 1231-1237, 1989. Go to original source...
  112. Jenkins, C.L.D., Furbank, R.T., Hatch, M.D.: Mechanism of C4 photosynthesis-a model describing the inorganic carbon pool in bundle sheath-cells.-Plant Physiol. 91: 1372-1381, 1989. Go to original source...
  113. Johnson, B.L., Henderson, T.L.: Water use patterns of grain amaranth in the northern Great Plains.-Agron. J. 94: 1437-1443, 2002. Go to original source...
  114. Kamukondiwa, W.: Alternative food crops to adapt to potential climate change in southern Africa.-Clim. Res. 6: 153-155, 1996. Go to original source...
  115. Kanai, R., Edwards, G.E.: Biochemistry of C4 photosynthesis.-In: Sage, R. F., Monson, R. K. (ed.): C4 Plant Biology. Pp. 49-87. Academic Press, London-New York-San Diego 1999. Go to original source...
  116. Karpilov, Y. S.: The distribution of radioactivity in carbon-14 among the products of photosynthesis in maize.-Proc. Kazan Agric. Inst. 14: 15-24, 1960.
  117. Kimball, B.A., Kobayashi, K., Bindi, M.: Responses of agricultural crops to free air CO2 enrichment.-Adv. Agron. 77: 293-368, 2002. Go to original source...
  118. Kortschak, H.P., Hart, C.E., Burr, G.O.: Carbon dioxide fixation in sugarcane leaves.-Plant Physiol. 40: 209-213, 1965. Go to original source...
  119. Krenzer, E.G., Jr., Moss, D.N., Crookston, R.K.: Carbon dioxide compensation points of flowering plants.-Plant Physiol. 56: 194-206, 1975. Go to original source...
  120. Ku, M.S.B., Edwards, G.E.: Oxygen inhibition of photosynthesis. III. Temperature dependence of quantum yield and its relation to O2/CO2 solubility ratio.-Planta 140: 1-6, 1978. Go to original source...
  121. Ku, M.S.B., Edwards, G. E.: Oxygen inhibition of photosynthesis in the C4 species Amaranthus graecizans L.-Planta 147: 277-282, 1980. Go to original source...
  122. Kubinová, L.: Recent stereological methods for the measurement of leaf anatomical characteristics: estimation of volume density, volume and surface area.-J. Exp. Bot. 44: 165-173, 1993. Go to original source...
  123. Laetsch, W. M.: C4 syndrome: structural analysis.-Annu. Rev. Plant Physiol. 25: 27-52, 1974. Go to original source...
  124. Laing, W.A., Forde, B.J.: Comparative photorespiration in Amaranthus, soybean and corn.-Planta 98: 221-231, 1971. Go to original source...
  125. Langdale, J.A., Nelson, T.: Spatial regulation of photosynthetic development.-TIG 7: 191-196, 1991. Go to original source...
  126. LeCain, D.R., Morgan, J.A.: Growth, gas exchange, leaf nitrogen and carbohydrate concentrations in NAD-ME and NADP-ME C4 grasses grown in elevated CO2.-Physiol. Plant. 102: 297-306, 1998. Go to original source...
  127. LeCain, D.R., Morgan, J.A., Zerbi, G.: Leaf anatomy and gas-exchange in nearly isogenic semidwarf and tall winter-wheat.-Crop Sci. 29: 1246-1251, 1989. Go to original source...
  128. Leopold, A.C.: Citation classic-plant growth and development.-Curr. Cont./Agr. Biol. Environ. 22: 20, 1988.
  129. Lester, J.N., Goldsworthy, A.: The occurrence of high CO2-compensation points in Amaranthus species.-J. Exp. Bot. 24: 1031-1034, 1973. Go to original source...
  130. Lieckfeldt, E.: Importance of leaf anatomy for characterization of primary leaf photosynthetic efficiency in different genotypes of wheat (Triticum).-Photosynthetica 23: 63-70, 1989.
  131. Lin, Z.F., Ehleringer, J.: Phosoynthetic characteristics of Amaranthus tricolor, a C4 tropical leafy vegetable.-Photosynth. Res. 4: 171-178, 1983. Go to original source...
  132. Lister, G.R., Krotkov, G., Nelson, C.D.: A closed-circuit apparatus with infrared CO2 analyzer and a Geiger tube for continuous measurement of CO2 exchange in photosynthesis and respiration.-Can. J. Bot. 39: 581-591, 1961. Go to original source...
  133. Long, S.P., Ainsworth, E.A., Leakey, A.D.B., Nösberger, J., Ort, D.R.: Food for thought: lower-than-expected crop yield stimulation with rising CO2 concentration.-Science 312: 1918-1921, 2006. Go to original source...
  134. Longstreth, D.J., Hartsock, T.L., Nobel, P.S.: Mesophyll cell properties for some C3 and C4 species with high photosynthetic rates.-Physiol. Plant. 48: 494-498, 1980. Go to original source...
  135. Loomis, R.S., Gerakis, P.A.: Productivity of agricultural ecosystems.-In: Cooper, J.P. (ed.): Photosynthesis and Productivity in Different Environments. Pp. 145-172. Cambridge University Press, Cambridge-London-New York-Melbourne 1975.
  136. Loomis, R.S., Connor, D. J.: Crop Ecology: Productivity and Management in Agricultural Systems. Cambridge Univ. Press, Cambridge 1992. Go to original source...
  137. Loomis, R.S., Williams, W.A., Hall, A.E.: Agricultural productivity.-Annu. Rev. Plant Physiol. 22: 431-468, 1971. Go to original source...
  138. Ludlow, M.M.: Ecophysiology of C4 grasses.-In: Lange, O. L., Kappen, L., Schulze, E.-D. ed.): Water and Plant Life. Pp. 364-386. Springer-Verlag, Berlin-Heidelberg-New York 1976. Go to original source...
  139. Ludlow, M.M.: Photosynthesis and dry matter production in C3 and C4 pasture plants, with special emphasis on tropical C3 legumes and C4 grasses.-Aust. J. Plant Physiol. 12: 557-572, 1985. Go to original source...
  140. Ludlow, M.M., Wilson, G.L.: Photosynthesis of tropical pasture plants. 4. Basis and consequences of differences between grasses and legumes.-Aust. J. Biol. Sci. 25: 1133-1145, 1972. Go to original source...
  141. Mansfield, T.A.: Carbon dioxide compensation points in maize and pelargonium.-Physiol. Plant. 21: 1159-1162, 1968. Go to original source...
  142. Maroco, J.P., Ku, M.S.B., Lea, P.J., Dever, L.V., Leegood, R.C., Furbank, R.T., Edwards, G.E.: Oxygen requirement and inhibition of C4 photosynthesis-An analysis of C4 plants deficient in the C3 and C4 cycles.-Plant Physiol. 116: 823-832, 1998. Go to original source...
  143. Meidner, H.: Minimum intercellular-space CO2 concentration (Gamma) of maize leaves and its influence on stomatal movement.-J. Exp. Bot. 13: 284-293, 1962. Go to original source...
  144. Monteith, J.L.: Reassessment of maximum growth rates for C3 and C4 crops.-Exp. Agric. 14: 1-5, 1978. Go to original source...
  145. Moss, D.N.: The effect of environment on gas exchange of leaves. The Connecticut Agric. Exp. Sta. Bull. (New Haven) Vol. 664, New Haven 1963.
  146. Moss, D.N.: The limiting carbon dioxide concentration for photosynthesis.-Nature 193: 587, 1962. Go to original source...
  147. Moss, D.N., Musgrave, R.B.: Photosynthesis and crop production.-Adv. Agron. 23: 317-336, 1971. Go to original source...
  148. Moss, D.N., Musgrave, R.B., Lemon, E.R.: Photosynthesis under field conditions. III. Some effects of light, carbon dioxide, temperature, and soil moisture on photosynthesis, respiration, and transpiration of corn.-Crop Sci. 1: 83-87, 1961. Go to original source...
  149. Muramoto, H., Hesketh, J., El-Sharkawy, M.: Relationships among rate of leaf area development, photosynthetic rate, and rate of dry matter production among American cultivated cottons and other species.-Crop Sci. 5: 163-166, 1965. Go to original source...
  150. Murata, Y.: Studies on the photosynthesis of rice plants and its culture significance.-Bull. Nat. Inst. Agric. Sci. Japan, Series D, 9: 1-169, 1961.
  151. Murata, Y.: Physiological responses to nitrogen in plants.-In: Eastin, J.D., Haskins, F.A., Sullivan, C.Y., van Bavel, C.H.M. (ed.): Physiological Aspects of Crop Yield. Pp. 235-259. ASA and CSSA, Madison 1969. Go to original source...
  152. Murata, Y., Iyama, J.: Studies on the photosynthesis of forage crops. I. Diurnal changes in the photosynthesis of several grasses and barley seedlings under constant temperature and light intensity.-Proc. Crop Sci. Soc. Japan, 31: 311-314,1963a. Go to original source...
  153. Murata, Y., Iyama, J.: Studies on the photosynthesis of forage crops. II. Influence of air-temperature upon the photosynthesis of some forage and grain crops.-Proc. Crop Sci. Soc. Japan 31: 315-322, 1963b. Go to original source...
  154. Musgrave, R.B., Moss, D.N.: Photosynthesis under field conditions. I. A portable, closed system for determining net assimilation and respiration of corn.-Crop Sci. 1: 37-41, 1961. Go to original source...
  155. Nasyrov, Y.S.: Genetic-control of photosynthesis and improving of crop productivity.-Annu. Rev. Plant Physiol. 29: 215-237, 1978. Go to original source...
  156. Nasyrov, Y. S.: Genetic-modification of the CO2 carboxylation reactions as a factor improving efficiency of photosynthesis.-Indian J. Plant Physiol. 24: 26-36, 1981.
  157. Neales, T.F., Incoll, L.D.: The control of leaf photosynthesis rate by the level of assimilate concentration in leaf: a review of the hypothesis.-Bot. Rev. 34: 107-125, 1968. Go to original source...
  158. Nelson, N.D.: Woody plants are not inherently low in photosynthetic capacity.-Photosynthetica 18: 600-605, 1984.
  159. Nelson, T., Langdale, J.A.: Pattern of leaf development in C4 plants.-Plant Cell 1: 3-13, 1989. Go to original source...
  160. Nelson, T., Langdale, J.A.: Developmental genetics of C4 photosynthesis.-Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 25-47, 1992. Go to original source...
  161. Nobel, P.S.: Leaf anatomy and water use efficiency.-In: Turner, N.C., Kramer, P.J. (ed.): Adaptation of Plants to Water and High Temperature Stress. Pp. 43-55. John Wiley & Sons, New York-Chichester-Brisbane-Toronto 1980.
  162. Nobel, P.S., Zaragoza, L.J., Smith, W.K.: Relation between mesophyll surface-area, photosynthetic rate, and illumination level during development for leaves of Plectranthus parviflorus Henckel.-Plant Physiol. 55: 1067-1070, 1975. Go to original source...
  163. Oaks, A.: Efficiency of nitrogen utilization in C3 and C4 cereals.-Plant Physiol. 106: 407-414, 1994. Go to original source...
  164. Ogren, W.L.: Photorespiration: pathways, regulation, and modification.-Annu. Rev. Plant Physiol. 35: 415-442, 1984. Go to original source...
  165. Ogren, W. L., Bowes, G.: Ribulose diphosphate carboxylase regulates photorespiration.-Nature 230: 159-160, 1971. Go to original source...
  166. Osada, A.: Studies on the photosynthesis of indica rice.-Proc. Crop Sci. Soc. Japan 33: 69-76, 1964. Go to original source...
  167. Osmond, C.B., Winter, K., Ziegler, H.: Functional significance of different pathways of CO2 fixation in photosynthesis.-In: Lange, O.L., Nobel, P.S., Osmond, C.B., Ziegler, H. (ed.): Physiological Plant Ecology II Water Relations and Carbon Assimilation. Pp. 479-547. Springer-Verlag, Berlin-Heidelberg-New York 1982. Go to original source...
  168. Parker, J.: Photosynthesis of Picea excelsa in winter.-Ecology 34: 605-609, 1953. Go to original source...
  169. Parkhurst, D.F.: A three-dimensional model for CO2 uptake by continuously distributed mesophyll in leaves.-J. Theoretical Biol. 67: 471-478, 1977. Go to original source...
  170. Parkhurst, D.F.: Adaptive significance of stomatal occurrence on one or both surfaces of leaves.-J. Ecol. 66: 367-383, 1978. Go to original source...
  171. Patton, L., Jones, M.B.: Some relationships between leaf anatomy and photosynthetic characteristics of willows.-New Phytol. 111: 657-661, 1989. Go to original source...
  172. Pearcy, R.W., Ehleringer, J.: Comparative ecophysiology of C3 and C4 plants.-Plant Cell Environ. 7: 1-13, 1984. Go to original source...
  173. Pellet, D., El-Sharkawy, M.A.: Cassava varietal response to phosphorus fertilization. 1. Yield, biomass and gas exchange.-Field Crops Res. 35: 1-11, 1993a. Go to original source...
  174. Pellet, D., El-Sharkawy, M.A.: Cassava varietal response to phosphorus fertilization. 2. Phosphorus uptake and use efficiency.-Field Crops Res. 35: 13-20, 1993b. Go to original source...
  175. Pellet, D.M., El-Sharkawy, M.A.: Cassava varietal response to fertilization: growth dynamics and implications for cropping sustainability.-Exp. Agric. 33: 353-365, 1997. Go to original source...
  176. Pettigrew, W.T, Gerik, T.J.: Cotton leaf photosynthesis and carbon metabolism.-Adv. Agron 94: 209-236, 2007. Go to original source...
  177. Pettigrew, W.T., Heitholt, J.J., Vaughn, K.C.: Gas exchange and comparative anatomy among cotton leaf-type isolines.-Crop Sci. 33: 1295-1299, 1993. Go to original source...
  178. Rabinowitch, E.: Photosynthesis and related processes. Vol. I,II/1,II/2. Intersci. Publ., New York 1945, 1951, 1955.
  179. Rathnam, C.K.: Evidence for re-assimilation of CO2 released from C4 acids by PEP carboxylase in leaves of C4 plants.-FEBS Lett. 82: 288-292, 1977. Go to original source...
  180. Raven, J.A.: Endogenous inorganic carbon sources in plant photosynthesis. 2. Comparison of total CO2 production in the light with measured CO2 evolution in the light.-New Phytol. 71: 995-1014, 1972. Go to original source...
  181. Ray, T.B., Black, C.C.: The C4 pathways and its regulation.-In: Gibbs, M., Latzko, E. (ed.): Photosynthesis II. (Encycl. Plant Physiol. NS Vol. 6), Pp. 77-101. Springer-Verlag, New York 1979. Go to original source...
  182. Rosenzweig, C., Parry, M.L.: Potential impact of climate-change on world food-supply.-Nature 367: 133-138, 1994. Go to original source...
  183. Ruhland, W. (ed.): Encyclopedia of Plant Physiology.-Vol. V. Springer-Verlag, Berlin 1960.
  184. Sage, R.F.: The evolution of C4 photosynthesis.-New Phytol. 161: 341-370, 2004. Go to original source...
  185. Sage, R.F., Monson, R.K. (ed.): C4 Plant Biology.-Academic Press, London-New York-San Diego 1999.
  186. Sage, R.F., Pearcy, R.W.: The nitrogen use efficiency of C3 and C4 plants. 1. Leaf nitrogen, growth, and biomass partitioning in Chenopodium album (L.) and Amaranthus retroflexus (L.).-Plant Physiol. 84: 954-958, 1987. Go to original source...
  187. Salisbury, F. B., Ross, C. W.: Plant Physiology. 2nd Ed.-Wadsworth Publish. Comp., Belmont 1978.
  188. ©esták, Z., Èatský, J., Jarvis, P.G. (ed.): Plant Photosynthetic Production. Manual of Methods.-Dr. W. Junk Publ., The Hague 1971.
  189. Shantz, H.L., Piemeisel, L.N.: The water requirements of plants at Akron, CO.-J. Agric. Res. (Washington) 34: 1093-1190, 1927.
  190. Sheen, J.: C4 gene expression.-Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 187-217, 1999. Go to original source...
  191. Shomer-Ilan, A., Beer, S., Waisel, Y.: Suaeda monoica, a C4 plant without typical bundle sheath.-Plant Physiol. 56: 676-679, 1975. Go to original source...
  192. Spear, I., Thimann, K.V.: The interrelation between CO2 metabolism and photoperiodism in Kalanchoe. 2. Effect of prolonged darkness and high temperatures.-Plant Physiol. 29: 414-417, 1954. Go to original source...
  193. Stanhill, G.: Water use efficiency.-Adv. Agron. 39: 53-85, 1986. Go to original source...
  194. Steiner, J.L., Hatfield, J.L.: Winds of change: A century of agroclimate research.-Agron. J. 100: S132-S152, 2008. (doi:10.2134/agronj2006.0372c). Go to original source...
  195. Stoy, V.: Interrelationships among photosynthesis, respiration, and movement of carbon in developing crops.-In: Eastin, J.D, Haskins, F.A., Sullivan, C.Y., van Bavel, C.H.M. (ed.): Physiological Aspects of Crop Yield. Pp. 185-206. ASA and CSSA, Madison 1969. Online (http://digitalcommons.unl.edu/agronomyfacpub/199) Go to original source...
  196. Strogonova, L.E.: Photosynthesis in corn under field conditions.-Biol. Abs. 45: 7029, 1964.
  197. Tanaka, A., Kawano, K., Yamaguchi, J.: Photosynthesis, respiration, and plant type of the tropical rice plant.-Int. Rice Res. Inst. (Los Baños), Tech. Bull. 7: 3-46. 1966.
  198. Terashima, I.: Anatomy of non-uniform leaf photosynthesis.-Photosynth. Res. 31: 195-212, 1992. Go to original source...
  199. Todd, G.W.: Effect of ozone and ozonated 1-hexene on respiration and photosynthesis of leaves.-Plant Physiol. 33: 416-420, 1958. Go to original source...
  200. Tolbert, N.E.: Microbodies-peroxisomes and glyoxysomes.-Annu. Rev. Plant Physiol. 22: 45-74, 1971. Go to original source...
  201. Tolbert, N.E., Oeser, A., Yamazaki, R.K., Hageman, R.H., Kisaki, T.: A survey of plants for peroxisomes.-Plant Physiol. 44: 135-147, 1969. Go to original source...
  202. Tregunna, E.B., Downton, J.: Carbon dioxide compensation in members of the Amaranthaceae and some related families.-Can. J. Bot. 45: 2385-2387, 1967. Go to original source...
  203. Tregunna, E. B., Krotkov, G., Nelson, C. D.: Further evidence on the effects of light on respiration during photosynthesis.-Can. J. Bot. 42: 989-997, 1964. Go to original source...
  204. Turrell, F.M.: The area of the internal exposed surface of dicotyledon leaves.-Am. J. Bot. 23: 255-264, 1936. Go to original source...
  205. Verduin, J.: A table of photosynthesis rates under optimal, near natural conditions.-Am. J. Bot. 40: 675-679, 1953. Go to original source...
  206. Verduin, J., Whitwer, E.E., Cowell, B.C.: Maximal photosynthetic rates in nature.-Science 130: 268-269, 1959. Go to original source...
  207. Volk, R.J., Jackson, W.A.: Photorespiratory phenomena in maize. Oxygen-uptake, isotope discrimination, and carbon-dioxide efflux.-Plant Physiol. 49: 218-223, 1972. Go to original source...
  208. von Caemmerer, S., Furbank, R. T. (ed.): C4 photosynthesis: 30 (or 40) years on.-Aust. J. Plant Physiol. 24: 409-555, 1997. Go to original source...
  209. Voznesenskaya, E.V., Franceschi, V.R., Edwards, G.E.: Light-dependent development of single cell C4 photosynthesis in cotyledons of Borszczowia aralocaspica (Chenopodiaceae) during transformation from a storage to a photosynthetic organ.-Ann. Bot. 93: 177-187, 2004. Go to original source...
  210. Waggoner, P.E., Moss, D.N., Hesketh, J.D.: Radiation in the plant environment and photosynthesis.-Agron. J. 55: 36-39, 1963. Go to original source...
  211. Wardlaw, I.F.: Control of carbon partitioning in plants.-New Phytol. 116: 341-381, 1990. Go to original source...
  212. Wells, R., Meredith, W.R., Jr., Williford, J.R.: Canopy photosynthesis and its relationship to plant productivity in near-isogenic cotton lines differing in leaf morphology.-Plant Physiol. 82: 635-640, 1986. Go to original source...
  213. Williamson, D.E.: The double-beam infrared gas analyzer of John Tyndall.-Am. Scientist 39: 672-681, 1951.
  214. Wilson, D., Cooper, J.P.: Effect of light intensity and CO2 on apparent photosynthesis and its relationship with leaf anatomy in genotypes of Lolium perenne L.-New Phytol. 68: 627-644, 1969a. Go to original source...
  215. Wilson, D., Cooper, J.P.: Diallel analysis of photosynthetic rate and related leaf characters among contrasting genotypes of Lolium perenne L.-Heredity 24: 633-649, 1969b. Go to original source...
  216. Wilson, D., Cooper, J.P.: Effect of selection for mesophyll cell size on growth and assimilation in Lolium perenne L.-New Phytol. 69: 233-245, 1970. Go to original source...
  217. Yoshida, S.: Physiological aspects of grain yield.-Annu. Rev. Plant Physiol. 23: 437-464, 1972. Go to original source...
  218. Yoshida, S., Cock, J. H., Parao, F.T.: Physiological aspects of high yields.-In: Rice Breeding. Pp. 455-469. IRRI, Los Baños 1972.
  219. Zelitch, I.: The close relationship between net photosynthesis and crop yield.-BioScience 32: 796-802, 1982. Go to original source...
  220. Zelitch, I.: Photosynthesis, Photorespiration, and Plant Productivity.-Academic Press, New York-London 1971.
  221. Ziska, L.H., Sicher, R.C. Bunce, J.A.: The impact of elevated carbon dioxide on the growth and gas exchange of three C4 species differing in CO2 leak rates.-Physiol. Plant. 105: 74-80, 1999. Go to original source...