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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

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  • Published:
Photosynthetica

Abstract

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.

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Abbreviations

C i :

intercellular CO2 concentration

DM:

dry mass

NAD-ME:

NAD-dependent malic enzyme

NADP-ME:

NADP-dependent malic enzyme

PAR:

photosynthetically active radiation

PCK:

phosphoenolpyruvate carboxykinase

PCRC:

photosynthetic carbon reduction cycle

PEPC:

phosphoenolpyruvate carboxylase

PGA:

3-phosphoglycerate

PNUE:

photosynthetic nitrogen use efficiency

PPDK:

pyruvate orthophosphate dikinase

P N :

leaf net photosynthetic rate

rm :

mesophyll resistances to CO2 diffusion

rk :

intracellular resistances to CO2 diffusion

Rubisco:

ribulose-1,5-bisphosphate carboxylase/oxygenase

S:

internal exposed surface area per external leaf area

S/V:

internal exposed surface area per volume of cell

WUE:

water use efficiency

References

  • Albrechtová, J., Janáčcek, 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.

    Article  PubMed  CAS  Google Scholar 

  • Andre, M.: Oxygenation capacity and Rubisco evolution.-Online (http://www.photorespiration.fr/oxygenation.htm), 2006.

  • Arnon, I.D.: The discovery of photosynthetic phosphorylation.-TIBS 9: 258–262, 1984.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Bazzaz, F.A.: The response of natural ecosystems to the rising global CO2 levels.-Annu. Rev. Ecol. Syst. 21: 167–196, 1990.

    Article  Google Scholar 

  • Begonia, G.B., Begonia, M.T.: Plant photosynthetic production as controlled by leaf growth, phenology, and behavior.-Photosynthetica 45: 321–333,2007.

    Article  Google Scholar 

  • Bhatt, J.G., Rao, M.R.K.: Heterosis in growth and photosynthetic rate in hybrids of cotton.-Euphytica 30: 129–133, 1981.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Black, C.C., Jr.: Ecological implications of dividing plants into groups with distinct photosynthetic production capacities.-Adv. Ecol. Res. 7: 87–113, 1971.

    Article  Google Scholar 

  • Black, C.C., Jr.: Photosynthetic carbon fixation in relation to net CO2 uptake.-Annu. Rev. Plant Physiol. 24: 253–286, 1973.

    Article  CAS  Google Scholar 

  • 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).

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Boote, K.J., Sinclair, T.R.: Significant discoveries and our changing perspective on research.-Crop Sci. 46: 2270–2277, 2006.

    Article  Google Scholar 

  • Borlaug, N.E.: Contributions of conventional plant breeding to food production.-Science 219: 689–693, 1983.

    Article  PubMed  CAS  Google Scholar 

  • Bosian, G.: Über die Vollautomatisierung der CO2-Assimilationsbestimming und zur Methodik des Kuvettenklimas.-Planta 45: 470–492, 1955.

    Article  CAS  Google Scholar 

  • Bowes, G., Ogren, W.L., Hageman, R.H.: Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase.-Biochem. Biophys. Res. Commun. 45: 716–722, 1971.

    Article  PubMed  CAS  Google Scholar 

  • Boyer, J.S.: Advances in drought tolerance in plants.-Adv. Agron. 56: 187–218, 1996.

    Article  Google Scholar 

  • Briggs, L.J., Shantz, H. L.: Relative water requirement of plants.-J. Agric. Res. 3: 1–63, 1914.

    CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Burris, R. H., Black, C.C., Jr. (ed.): CO2 Metabolism and Plant Productivity.-University Park Press, Baltimore-London-Tokyo 1976.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Calvin, M.: Forty years of photosynthesis and related activities.-Photosynth. Res. 21: 3–16, 1989.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Chollet, R., Ogren, W.L.: Regulation of photorespiration in C3 and C4 species.-Bot. Rev. 41: 137–179, 1975.

    Article  CAS  Google Scholar 

  • CIAT: Cassava Program Annual Reports for 1986–1996.-Centro Internacional de Agricultural Tropical, Cali 1986–1996.

    Google Scholar 

  • CIAT: Cassava Program Annual Report for 1992.-Centro Internacional de Agricultura Tropical, Cali 1992.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Crookston, R.K., Moss, D.N.: Interveinal distance for carbohydrate transport in leaves of C3 and C4 grasses.-Crop Sci. 14: 123–125, 1974.

    Article  Google Scholar 

  • Dai, Z.Y., Ku, M.S.B., Edwards, G.E.: C4 photosynthesis. The CO2-concentrating mechanism and photorespiration.-Plant Physiol. 103: 83–90, 1993.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • de Veau, E.J., Burris, J.E.: Photorespiratory rates in wheat and maize as determined by 18O-labeling.-Plant Physiol. 90: 500–511, 1989.

    Article  PubMed  Google Scholar 

  • Devlin, R. M.: Plant Physiology. 3rd Ed.-D. Van Nostrand Company, New York 1975.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Duysens, L.N.M.: The discovery of the 2 photosynthetic systems: a personal account.-Photosynth. Res. 21: 61–79, 1989.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Edwards, G.E., Walker, D.A.: C3, C4: Mechanisms, and Cellular and Environmental Regulation of Photosynthesis.-Blackwell, Oxford 1983.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ehleringer, J., Pearcy, R.W.: Variation in quantum yield for CO2 uptake among C3 and C4 plants.-Plant Physiol. 73: 555–559, 1983.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Elmore, C.D., Paul, R.N.: Composite list of C4 weeds.-Weed Sci. 31: 686–692, 1983.

    Google Scholar 

  • El-Sharkawy, M. A.: Factors limiting photosynthetic rates of different plant species.-Ph.D. Dissertation.The University of Arizona, Tucson 1965.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • El-Sharkawy, M.A.: Cassava biology and physiology.-Plant Mol. Biol. 56: 481–501, 2004.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • El-Sharkawy, M.A., Cock, J.H.: Photosynthesis of cassava (Manihot esculenta Crantz).-Exp. Agr. 26: 325–340, 1990.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • El-Sharkawy, M., Hesketh, J.D.: Plant efficiency measured by photosynthesis.-Prog. Agric. Ariz. Agr. Exp. Sta. May-June, Tucson. P. 15. Tucson 1964a.

  • 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.

    Article  Google Scholar 

  • El-Sharkawy, M.A., Hesketh, J.D.: Effect of stomatal differences among species on leaf photosynthesis.-Crop Sci. 4: 619–621, 1964c.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • El-Sharkawy, M.A., Hesketh, J.D., Elmore, D.: Photosynthesis and transpiration among species.-Adv. Front Plant Sci. 18: 33–37, 1967.

    Google Scholar 

  • 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).

    Google Scholar 

  • El-Sharkawy, M.A., Hesketh, J.D., Muramoto, H.: Further studies of limiting factors to photosynthesis.-Agronomy Abstracts, November, 1964, ASA, Madison 1964.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Evans, L.T.: Crop Evolution, Adaptation and Yield.-Cambridge University Press, Cambridge 1993.

    Google Scholar 

  • Farquhar, G. D.: On the nature of carbon isotope discrimination in C4 species.-Aust. J. Plant Physiol. 10: 205–226, 1983.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Gallagher, R.: Citation violations.-The Scientist 23: 13, 2009.

    Google Scholar 

  • Garfield, E.: Bibliographic negligence: A serious transgression.-The Scientist 5:14, 1991.

    Google Scholar 

  • 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.

    Google Scholar 

  • Gaastra, P.: Photosynthesis of crop plants as influenced by light, carbon dixoide, temperature and stomatal diffusion resistance.-Meded. Landbouwhogeschool (Wageningen) 59: 1–68, 1959.

    Google Scholar 

  • Giaquinta, R.T.: Phloen loading of sucrose.-Annu. Rev. Plant Physiol. 34: 347–387, 1983.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Gifford, R.M., Evans, L.T.: Photosynthesis, carbon partitioning, and yield.-Annu. Rev. Plant Physiol. 32: 485–509, 1981.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Gregory, F.C., Spear, I., Thiman, K.V.: The interrelation between CO2 metabolism and photoperiodism in Kalanchoe.-Plant Physiol. 29: 220–229, 1954.

    Article  PubMed  CAS  Google Scholar 

  • Haberlandt, G.: Physiologische Pflanzenanatomie.-Engelmann, Leipzig 1904.

    Google Scholar 

  • 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.

    Google Scholar 

  • Hatch, M.D.: C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure.-Biochim. Biophys. Acta 895: 81–106, 1987.

    CAS  Google Scholar 

  • Hatch, M.D.: I can’t believe my luck.-Photosynth. Res. 33: 1–14, 1992a.

    Article  CAS  Google Scholar 

  • Hatch, M.D.: C4 photosynthesis: an unlikely process full of surprises.-Plant Cell Physiol. 33: 333–342, 1992b.

    CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Hatch, M.D., Slack, C.R.: Photosynthetic CO2-fixation pathways.-Annu. Rev. Plant Physiol. 21: 141–162, 1970.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Hesketh, J.D.: Limitations to photosynthesis responsible for differences among species.-Crop Sci. 3: 493–496, 1963.

    Article  Google Scholar 

  • Hesketh, J.D., Moss, D.N.: Variation in the response of photosynthesis to light.-Crop Sci. 3: 107–110, 1963.

    Article  Google Scholar 

  • Hesketh, J. D.: Musgrave R.B. (Photosynthesis under field conditions). IV. Light studies with individual corn leaves.-Crop Sci. 2: 311–315, 1962.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Huzisige, H., Ke, B.: Dynamics of the history of photosynthesis research.-Photosynth. Res. 38: 185–209, 1993.

    Article  CAS  Google Scholar 

  • 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.)

  • Irvine, J.E.: Evidence for photorespiration in tropical grasses.-Physiol. Plant. 23: 607–612, 1970.

    Article  CAS  Google Scholar 

  • Jackson, W.A., Volk, R. J.: Oxygen uptake by illuminated maize leaves.-Nature 222: 269–271, 1969.

    Article  PubMed  CAS  Google Scholar 

  • Jackson, W.A., Volk. R. J.: Photorespiration.-Annu. Rev. Plant Physiol. 21: 385–432, 1970.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, B.L., Henderson, T.L.: Water use patterns of grain amaranth in the northern Great Plains.-Agron. J. 94: 1437–1443, 2002.

    Google Scholar 

  • Kamukondiwa, W.: Alternative food crops to adapt to potential climate change in southern Africa.-Clim. Res. 6: 153–155, 1996.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Google Scholar 

  • Kimball, B.A., Kobayashi, K., Bindi, M.: Responses of agricultural crops to free air CO2 enrichment.-Adv. Agron. 77: 293–368, 2002.

    Article  Google Scholar 

  • Kortschak, H.P., Hart, C.E., Burr, G.O.: Carbon dioxide fixation in sugarcane leaves.-Plant Physiol. 40: 209–213, 1965.

    Article  PubMed  CAS  Google Scholar 

  • Krenzer, E.G., Jr., Moss, D.N., Crookston, R.K.: Carbon dioxide compensation points of flowering plants.-Plant Physiol. 56: 194–206, 1975.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Ku, M.S.B., Edwards, G. E.: Oxygen inhibition of photosynthesis in the C4 species Amaranthus graecizans L.-Planta 147: 277–282, 1980.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Laetsch, W. M.: C4 syndrome: structural analysis.-Annu. Rev. Plant Physiol. 25: 27–52, 1974.

    Article  CAS  Google Scholar 

  • Laing, W.A., Forde, B.J.: Comparative photorespiration in Amaranthus, soybean and corn.-Planta 98: 221–231, 1971.

    Article  CAS  Google Scholar 

  • Langdale, J.A., Nelson, T.: Spatial regulation of photosynthetic development.-TIG 7: 191–196, 1991.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Leopold, A.C.: Citation classic-plant growth and development.-Curr. Cont./Agr. Biol. Environ. 22: 20, 1988.

    Google Scholar 

  • Lester, J.N., Goldsworthy, A.: The occurrence of high CO2-compensation points in Amaranthus species.-J. Exp. Bot. 24: 1031–1034, 1973.

    Article  CAS  Google Scholar 

  • Lieckfeldt, E.: Importance of leaf anatomy for characterization of primary leaf photosynthetic efficiency in different genotypes of wheat (Triticum).-Photosynthetica 23: 63–70, 1989.

    Google Scholar 

  • Lin, Z.F., Ehleringer, J.: Phosoynthetic characteristics of Amaranthus tricolor, a C4 tropical leafy vegetable.-Photosynth. Res. 4: 171–178, 1983.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Loomis, R.S., Connor, D. J.: Crop Ecology: Productivity and Management in Agricultural Systems. Cambridge Univ. Press, Cambridge 1992.

    Google Scholar 

  • Loomis, R.S., Williams, W.A., Hall, A.E.: Agricultural productivity.-Annu. Rev. Plant Physiol. 22: 431–468, 1971.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Mansfield, T.A.: Carbon dioxide compensation points in maize and pelargonium.-Physiol. Plant. 21: 1159–1162, 1968.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Meidner, H.: Minimum intercellular-space CO2 concentration (Γ) of maize leaves and its influence on stomatal movement.-J. Exp. Bot. 13: 284–293, 1962.

    Article  CAS  Google Scholar 

  • Monteith, J.L.: Reassessment of maximum growth rates for C3 and C4 crops.-Exp. Agric. 14: 1–5, 1978.

    Article  CAS  Google Scholar 

  • 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.

  • Moss, D.N.: The limiting carbon dioxide concentration for photosynthesis.-Nature 193: 587, 1962.

    Article  PubMed  CAS  Google Scholar 

  • Moss, D.N., Musgrave, R.B.: Photosynthesis and crop production.-Adv. Agron. 23: 317–336, 1971.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Nasyrov, Y.S.: Genetic-control of photosynthesis and improving of crop productivity.-Annu. Rev. Plant Physiol. 29: 215–237, 1978.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Nelson, N.D.: Woody plants are not inherently low in photosynthetic capacity.-Photosynthetica 18: 600–605, 1984.

    Google Scholar 

  • Nelson, T., Langdale, J.A.: Pattern of leaf development in C4 plants.-Plant Cell 1: 3–13, 1989.

    Article  PubMed  CAS  Google Scholar 

  • Nelson, T., Langdale, J.A.: Developmental genetics of C4 photosynthesis.-Annu. Rev. Plant Physiol. Plant Mol. Biol. 43: 25–47, 1992.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Oaks, A.: Efficiency of nitrogen utilization in C3 and C4 cereals.-Plant Physiol. 106: 407–414, 1994.

    PubMed  CAS  Google Scholar 

  • Ogren, W.L.: Photorespiration: pathways, regulation, and modification.-Annu. Rev. Plant Physiol. 35: 415–442, 1984.

    Article  CAS  Google Scholar 

  • Ogren, W. L., Bowes, G.: Ribulose diphosphate carboxylase regulates photorespiration.-Nature 230: 159–160, 1971.

    CAS  Google Scholar 

  • Osada, A.: Studies on the photosynthesis of indica rice.-Proc. Crop Sci. Soc. Japan 33: 69–76, 1964.

    Google Scholar 

  • 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.

    Google Scholar 

  • Parker, J.: Photosynthesis of Picea excelsa in winter.-Ecology 34: 605–609, 1953.

    Article  CAS  Google Scholar 

  • Parkhurst, D.F.: A three-dimensional model for CO2 uptake by continuously distributed mesophyll in leaves.-J. Theoretical Biol. 67: 471–478, 1977.

    Article  CAS  Google Scholar 

  • Parkhurst, D.F.: Adaptive significance of stomatal occurrence on one or both surfaces of leaves.-J. Ecol. 66: 367–383, 1978.

    Article  Google Scholar 

  • Patton, L., Jones, M.B.: Some relationships between leaf anatomy and photosynthetic characteristics of willows.-New Phytol. 111: 657–661, 1989.

    Article  Google Scholar 

  • Pearcy, R.W., Ehleringer, J.: Comparative ecophysiology of C3 and C4 plants.-Plant Cell Environ. 7: 1–13, 1984.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Pettigrew, W.T, Gerik, T.J.: Cotton leaf photosynthesis and carbon metabolism.-Adv. Agron 94: 209–236, 2007.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Rabinowitch, E.: Photosynthesis and related processes. Vol. I,II/1,II/2. Intersci. Publ., New York 1945, 1951, 1955.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Rosenzweig, C., Parry, M.L.: Potential impact of climate-change on world food-supply.-Nature 367: 133–138, 1994.

    Article  Google Scholar 

  • Ruhland, W. (ed.): Encyclopedia of Plant Physiology.-Vol. V. Springer-Verlag, Berlin 1960.

    Google Scholar 

  • Sage, R.F.: The evolution of C4 photosynthesis.-New Phytol. 161: 341–370, 2004.

    Article  CAS  Google Scholar 

  • Sage, R.F., Monson, R.K. (ed.): C4 Plant Biology.-Academic Press, London-New York-San Diego 1999.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Salisbury, F. B., Ross, C. W.: Plant Physiology. 2nd Ed.-Wadsworth Publish. Comp., Belmont 1978.

    Google Scholar 

  • Šesták, Z., Čatský, J., Jarvis, P.G. (ed.): Plant Photosynthetic Production. Manual of Methods.-Dr. W. Junk Publ., The Hague 1971.

    Google Scholar 

  • Shantz, H.L., Piemeisel, L.N.: The water requirements of plants at Akron, CO.-J. Agric. Res. (Washington) 34: 1093–1190, 1927.

    Google Scholar 

  • Sheen, J.: C4 gene expression.-Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 187–217, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Shomer-Ilan, A., Beer, S., Waisel, Y.: Suaeda monoica, a C4 plant without typical bundle sheath.-Plant Physiol. 56: 676–679, 1975.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Stanhill, G.: Water use efficiency.-Adv. Agron. 39: 53–85, 1986.

    Article  Google Scholar 

  • 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).

    Article  Google Scholar 

  • 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/)

    Google Scholar 

  • Strogonova, L.E.: Photosynthesis in corn under field conditions.-Biol. Abs. 45: 7029, 1964.

    Google Scholar 

  • 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.

    Google Scholar 

  • Terashima, I.: Anatomy of non-uniform leaf photosynthesis.-Photosynth. Res. 31: 195–212, 1992.

    Article  CAS  Google Scholar 

  • Todd, G.W.: Effect of ozone and ozonated 1-hexene on respiration and photosynthesis of leaves.-Plant Physiol. 33: 416–420, 1958.

    Article  PubMed  CAS  Google Scholar 

  • Tolbert, N.E.: Microbodies-peroxisomes and glyoxysomes.-Annu. Rev. Plant Physiol. 22: 45–74, 1971.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Tregunna, E.B., Downton, J.: Carbon dioxide compensation in members of the Amaranthaceae and some related families.-Can. J. Bot. 45: 2385–2387, 1967.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Turrell, F.M.: The area of the internal exposed surface of dicotyledon leaves.-Am. J. Bot. 23: 255–264, 1936.

    Article  Google Scholar 

  • Verduin, J.: A table of photosynthesis rates under optimal, near natural conditions.-Am. J. Bot. 40: 675–679, 1953.

    Article  CAS  Google Scholar 

  • Verduin, J., Whitwer, E.E., Cowell, B.C.: Maximal photosynthetic rates in nature.-Science 130: 268–269, 1959.

    Article  PubMed  CAS  Google Scholar 

  • Volk, R.J., Jackson, W.A.: Photorespiratory phenomena in maize. Oxygen-uptake, isotope discrimination, and carbon-dioxide efflux.-Plant Physiol. 49: 218–223, 1972.

    Article  PubMed  CAS  Google Scholar 

  • von Caemmerer, S., Furbank, R. T. (ed.): C4 photosynthesis: 30 (or 40) years on.-Aust. J. Plant Physiol. 24: 409–555, 1997.

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Waggoner, P.E., Moss, D.N., Hesketh, J.D.: Radiation in the plant environment and photosynthesis.-Agron. J. 55: 36–39, 1963.

    Article  Google Scholar 

  • Wardlaw, I.F.: Control of carbon partitioning in plants.-New Phytol. 116: 341–381, 1990.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Williamson, D.E.: The double-beam infrared gas analyzer of John Tyndall.-Am. Scientist 39: 672–681, 1951.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Yoshida, S.: Physiological aspects of grain yield.-Annu. Rev. Plant Physiol. 23: 437–464, 1972.

    Article  Google Scholar 

  • Yoshida, S., Cock, J. H., Parao, F.T.: Physiological aspects of high yields.-In: Rice Breeding. Pp. 455–469. IRRI, Los Baños 1972.

    Google Scholar 

  • Zelitch, I.: The close relationship between net photosynthesis and crop yield.-BioScience 32: 796–802, 1982.

    Article  Google Scholar 

  • Zelitch, I.: Photosynthesis, Photorespiration, and Plant Productivity.-Academic Press, New York-London 1971.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

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  1. M. A. El-Sharkawy

    Present address: , A.A. 26360, Cali, Valle, Colombia

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The author is a physiologist/breeder [B.S.(honor) in agronomy, University of Alexandria, Egypt, 1958; MSc. in plant breeding and genetics, Louisiana State University, Baton Rouge,1962; PhD in crop physiology, The University of Arizona, Tucson, 1965]. For more than four decades, he has contributed to research in field crop production, breeding, and physiology of cotton, cereal crops and the root tropical crop cassava. He took a leading role in establishing a faculty of agriculture, Tripoli University, Libyan Arab Republic, and participated in the pioneering agricultural development projects under irrigation in the semiarid and arid ecosystems of North Africa and the Sahara.

This review is dedicated to the memory of Dr. Zdeněk Šesták (4 August 1932–14 November 2008), Editor-in-Chief of Photosynthetica (1991–2008), renowned plant physiologist and world leader in the field of photosynthesis research for five decades. Photosynthetica, Dr. Šesták’s inspired brainchild born in 1967, was the first international journal of its kind dedicated to the dissemination of the findings of original research, in various languages, in all aspects of plant photosynthesis, ranging from molecular to plant community levels, basic and applied, conducted by researchers across continents without discrimination. The environment surrounding the home-base of Photosynthetica was known, at an early time, for its rich tradition in many activities and development of methodology in photosynthesis and plant physiology. Before the initiation of this journal, research findings on plant photosynthesis were normally published in a diverse net of journals that covered many areas such as chemical, biological, botanical, and agronomical research. In our case as agronomists, our early photosynthetic research reviewed here was mainly published in the then new journal Crop Science, USA, that was dominated by plant genetic and breeding publications. There, we felt as outlaw or off-type at the time!. Since I and my colleagues have contributed several articles to Photosynthetica in the past 20 years covering some of our research on cassava conducted at CIAT, Colombia, I became an admirer of the personal qualities of Dr. Šesták as an eminent scientist, efficient communicator, as well as an inspiration to fellow scientists, particulary those in Third World countries who are increasingly publishing in Photosynthetica. His sharp intellect, fairness, unbiased judgement and constructive criticism during the reviewing process, as Editor-in-Chief, were crucial in encouraging us publishing in Photosynthetica. The invaluable editorial inputs provided by him and his staff at Prague to our publications were fundamental in improving the clarity, readability and quality of the submitted manuscripts. I personally have lost, and surely along with me the rest of the international community in the field of photosynthesis reseacrh, a great scientist, a friend and an honest collaborator. I humbly dedicate this review to his memory. We are surely following your green footsteps, Dr. Šesták, on earth and in heaven.

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El-Sharkawy, M.A. 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. Photosynthetica 47, 163–183 (2009). https://doi.org/10.1007/s11099-009-0030-7

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