Abstract
Chronological recognition of the intermediates and mechanisms involved in photosynthetic carbon dioxide fixation is delineated. Sam Ruben and Martin Kamen's development of application of radioactive carbon for the study of carbon dioxide fixation provided impetus and techniques for following the path of carbon in photosynthesis. Discovery The identity of the primary carboxylation enzyme and its identity with the major protein of photosynthetic tissues (`Fraction 1' protein of Sam Wildman) is reviewed. Memories are dimmed by sixty years of exciting discoveries exploration in newer fields [see Benson 2002 (Annu Rev Plant Biol 53: 1–25), for research and perspectives beyond the early Berkeley days].
References
Andrews TJ, Lorimer GH and Tolbert NE (1973) (Year 1971 in the text. Pls check) Ribulose diphosphate oxygenase I. Synthesis of phosphoglycolate by fraction 1 protein of leaves. Biochemistry 12: 11–18
Aubert J-P, Milhaud G and Millet J (1955) Metabolisme du carbone dans la chimioautotrophie. Mode d'incorporation de l'anhydride carbonique. C R Seances Acad Sci 240: 2178–2179
Baly ECC (1940) Photosynthesis. Van Nostrand, New York
Baly ECC and Hood NR (1929) The photosynthesis of naturally occurring compounds: IV. The compounds: IV. The temperature coefficient of the photosynthesis of carbohydrates from carbonic acid. Proc R Soc London Ser A 122: 393–398
Baly ECC, Stephen WE and Hood NR (1927) The photosynthesis of naturally occurring compounds: II. The photosynthesis of carbohydrates from carbonic acid by means of visible light. Proc R Soc London Ser A 122: 212–219
Barltrop JA, Hayes PM and, Calvin M (1954) The Chemistry chemistry of 1,2-dithiolane (trimethylene disulfide) as a Model model for the primary quantum conversion act in photosynthesis. J Am Chem Soc 76: 4348–4367
Bassham JA (1964) Kinetic studies of the photosynthetic carbon reduction cycle. Annu Rev Plant Physiol 15: 101–120
Bassham JA and Calvin M (1957) The Path of Carbon in Photosynthesis. Englewood Cliffs, New Jersey
Bassham JA and Kirk M (1963) Synthesis of compounds from C14O2 in the dark by preilluminated Chlorella. In: Japanese Society of Plant Physiologists (ed) Studies on Microalgae and Photosynthetic Bacteria (special issue of Plant and Cell Physiology), pp 493–503. The University of Tokyo Press, Tokyo
Bassham JA, Benson AA, Kay LD, Harris AZ, Wilson AT and Calvin M(1954) The path of carbon in photosynthesis. XXI. The cyclic regeneration of carbon dioxide acceptor. J Am Chem Soc 76: 1760–1770
Benson AA (1951) Identification of ribulose in C14O2 photosynthesis products. J Am Chem Soc 73: 2971
Benson AA (1952) Mechanism of biochemical photosynthesis. Z Elektrochem 56: 848–854
Benson AA (1977) Philosophy of the tracer method. Radioisotopes 26: 348–356
Benson AA (1981) Molecular exploration in unknown metabolic worlds. In: Kagayama M, Nakamura K, Oshima T, Uchida T (eds) Science and Scientists, pp 207–212. Japan Scientific Societies Press, Tokyo
Benson AA (1982) Tracers in biology. In: Kaplan NO and Robinson A (eds) From Cyclotrons to Cytochromes, pp 59–65. Academic Press, New York
Benson AA (1987a) Carboxylation from Ruben to rubisco. Presented at the Oji International Seminar (October 20-24, 1986, Kashiko-jima, Mie, Japan) on 'New Aspects of Plant Cell Biology and Molecular Biology,' sponsored by the Japan Society for the Promotion of Science (JSPS) and the Fujihara Science Foundation (Tokyo), and organized by Takashi Akazawa, Masahiro Sugiura, Tatsuo Sugiyama, Akira Watanabe and Tetsuko Takabe, see book of abstracts, p 8
Benson AA (1987b) Radiochromatographic exploration. J Am Oil Chemists Soc 64: 1309–1314
Benson AA (1990) Photosynthesis in the dark ages before regulation. In: Kanai R, Katoh S and Miyachi S (eds) Regulation of Photosynthetic Processes. Bot Mag Tokyo (special issue)
Benson AA (1995) Saga of a great theory of photosynthesis. Am Soc Plant Physiol Newslett 22: 5–6
Benson AA (1996) Naïve steps along the path. C R Acad Sci Paris Life Sci 319: 843–847
Benson AA (1998) The path of carbon in photosynthesis: 1942-1955. In: Kung S-D and Yang S-F (eds) Discoveries in Plant Biology, Vol 1, pp 197–213. World Scientific Publishing, Singapore
Benson AA (2002) Paving the path. Annu Rev Plant Biol 53: 1–25
Benson AA and Calvin M (1947) The dark reductions of photosynthesis. Science 105: 648–649
Benson AA and Calvin M (1948) The path of carbon in photosynthesis. Cold Spring Harbor Symp Quant Biol 13: 6–10
Benson AA and Calvin M (1950a) Path of carbon in photosynthesis VII. Respiration and photosynthesis. J Exp Bot 1: 63–68
Benson AA and Calvin M (1950b) Carbon dioxide fixation by green plants. Annu Rev Plant Physiol 1: 25–42
Benson AA and Miyachi S (1992) Interview. Cell Sci (Japan) 8: 55–69
Benson AA, Calvin M, Haas VA, Aronoff S, Hall AG, Bassham JA and Weigl JW (1949) C14 in photosynthesis. In: Franck J and Loomis WE (eds) Photosynthesis in Plants, pp 381–401. Iowa State College Press, Ames, Iowa
Benson AA, Bassham JA, Calvin M, Goodale TC, Hass VA and Stepka W (1950) Paper chromatography and radioautography of the products. J Am Chem Soc 72: 1710–1718
Benson AA, Bassham JA and Calvin M (1951) Sedoheptulose in photosynthesis by plants. J Am Chem Soc 73: 2970
Benson AA, Bassham JA, Calvin M, Hall AG, Hirsch HE, Kawaguchi S and Tolbert NE (1952a) The path of carbon in photosynthesis XV. Ribulose and sedoheptulose. J Biol Chem 196: 703–715
Benson AA, Kawaguchi S, Hayes P and Calvin M (1952b) The path of carbon in photosynthesis XVI. Kinetic relationships of the intermediates in steady state photosynthesis. J Am Chem Soc 74: 4477–4482
Benson AA, Daniel H and Wiser R (1959) A sulfolipid in plants. Proc Natl Acad Sci USA 45: 1582–1587
Blackman FF (1905) Optima and limiting factors. Ann Bot LXXIV: 281–295
Brown AH, Fager EW and Gaffron H (1948) Assimilation of tracer carbon in the alga Scenedesmus. Arch Biochem 19: 407–428
Brown AH, Fager EW and Gaffron H (1949) Kinetics of a photochemical intermediate in photosynthesis. In: Franck J and Loomis WE (eds) Photosynthesis in Plants, pp 403–422. Iowa State College Press, Ames, Iowa
Burr GO, Hartt CE, Brodie HW, Tanimoto T, Kortschak HP, Takahashi D, Ashton FM and Coleman RE (1957) The sugarcane plant. Annu Rev Plant Physiol 8: 275–308
Calvin M (1949) The Path of Carbon in Photosynthesis, VI. J Chem Educ 26: 639–657
Calvin M (1954) Chemical and photochemical reactions of thioctic acid and related disulfides. Fed Proc 13: 697–711
Calvin M (1956) The photosynthetic carbon cycle. In: Liébecq C (ed) Proceedings of the Third International Congress in Biochemistry, pp 211–225. Academic Press, New York
Calvin M (1992) Following the trail of light: a scientific odyssey. In: Seeman JE (ed) Profiles, Pathways and Dreams, p 178. American Chemistry Society, Washington, DC
Calvin M and Benson AA (1948). The path of carbon in photosynthesis. Science 107: 476–480
Calvin M and Massini P (1952) The path of carbon in photosynthesis. XX. The steady state. Experientia VIII: 445–457
Calvin M, Bassham JA and Benson AA (1950) Chemical transformations in photosynthesis. Fed Proc 9: 524–534
Chan PH, Sakano K and Wildman S (1972). Crystalline fraction 1 protein. Preparation in large yield. Science 176: 1145–1146.
Dent CE, Stepka W and Steward FC (1947). Detection of the free amino-acids of plant cells by partition chromatography. Nature 160: 682–683
Dorner RW, Kahn A and Wildman S (1957) The proteins of green leaves. VII. Synthesis and decay of the cytoplasmic proteins during the life of a tobacco leaf. J Biol Chem 229: 945–952
Emerson R (1929) On the behavior of nickel carbonate in relation to photosynthesis. J Gen Physiol 13: 163–168
Fager EW (1949) Chemical studies of early fixation products with C14O2. In: Franck J and Loomis WE (eds) Photosynthesis in Plants, pp 423–436. Iowa State College Press, Ames, Iowa
Fager EW and Rosenberg JL (1950) Phosphoglyceric acid in photosynthesis. Science 112: 617–618
Fager EW, Rosenberg JL and Gaffron H (1950) Intermediates in photosynthesis. Fed Proc 9: 535–542
Franck J and Loomis WE (eds) (1949) Photosynthesis in Plants. Iowa State College Press, Ames, Io
Fuller RC (1998) Photosynthetic carbon metabolism in the green and purple bacteria. In: Clayton RK and Sistrom WR (eds) The Photosynthetic Bacteria, pp 691–705. Plenum Press, New York
Fuller RC (1999) Forty years of microbial photosynthesis research: where it came from and what it led to. Photosynth Res 62: 1–29
Govindjee (1999) On the requirement of minimum number of four versus eight quanta of light for the evolution of one molecule of oxygen in photosynthesis: a historical note. Photosynth Res 59: 249–254
Hartt CE (1943) The synthesis of sucrose in the sugar cane plant III. The effects of specific inhibitors upon the interconversion of glucose and fructose and formation of sucrose in detached blades of the sugar cane plant. Hawaian Plant Rec 47: 223–255
Hartt CE (1944) The synthesis of sucrose in the sugar cane plant. IV. Concerning the mechanism of sucrose synthesis in the sugar cane plant. Hawaian Plant Rec 48: 31–42
Horecker BL, Hurwitz J and Weissbach A (1954). Pentose phosphate and carbon dioxide fixation with spinach extracts. J Am Chem Soc 76: 3611–3612
Johnston HS (2002) A Bridge Not Attacked. World Scientific Publishing, Singapore/Imperial College Press, London (in press)
Kamen MD (1985) Radiant Science, Dark Politics. A Memoir of the Nuclear Age. University of California Press, Berkeley, California
La Forge FB and and Hudson CS (1917) Sedoheptose, a new sugar from Sedum spectabile. J Biol Chem 30: 61–77
Lorimer GH, Andrews TJ, Pierce J and Schloss JV (1986) 2'-carboxy-3-keto-D-arabinitol 1,5-bisphosphate, the six-carbon intermediate of the ribulose bisphosphate carboxylase reaction. Phil Trans R Soc London Ser B 313: 397–407
Maruo B and Akazawa T (1997) Ruben and Kamen. Chem Biol (KASEAA) 35: 808–814 [in Japanese]
Mayaudon J (1957) Study of association between the main nucleo-protein of green leaves and carboxydismutase. Enzymologia 18: 345–354
Mayaudon J, Benson AA and Calvin M (1957) Ribulose-1,5-diphosphate from and CO2 fixation by Tetragonia expansa leaves extract. Biochim Biophys Acta 23: 342–351
Nonomura AM and Benson AA (1992) The path of carbon in photosynthesis. XXIV. Improved crop yields with methanol. Proc Natl Acad Sci USA 89: 9794–9798
Quayle JR, Fuller RC, Benson AA and Calvin M (1954) Enzymatic carboxylation of ribulose diphosphate. J Am Chem Soc 76: 3610–3612
Ruben S (1943) Photosynthesis and phosphorylation. J Am Chem Soc 65: 279–282
Ruben S and Benson AA (1945) The physiological action of phosgene. Report prepared on October 22, 1943 by TH Norris and CN Rice, 10 pp. In: Committee of Gas Casualties, 'Fasiculus on Chemical Warfare Medicine,' National Research Council Committee on Treatment of Gas Casualties. Vol 2: Respiratory Tract, p 327 and p 641. Washington, DC
Ruben S and Kamen MD (1940) Photosynthesis with radioactive carbon. IV. Molecular weight of the intermediate products and a tentative theory of photosynthesis. J Am Chem Soc 62: 3451–3455
Ruben S and Kamen MD (1941) Long-lived radioactive carbon: C14. Phys Rev 59: 349–354
Ruben S, Kamen MD, Hassid WZ and DeVault DC (1939) Photosynthesis with radio-carbon. Science, 90: 570–571
Saltman P, Kunitake G, Spolter H and Stitt C (1956) The dark fixation of CO2 by succulent leaves: the first products. Plant Physiol 31: 464–468
Smyrniotis PZ and Horecker BL (1956). Preparation of sedoheptulose diphosphate. J Biol Chem 218: 745–752
Stoppani AOL, Fuller RC and Calvin M (1955) Carbon dioxide fixation by Rhodopsuedomonas capsulatus. J Bacteriol 69: 491–495
Takamiya A (1990) Hiroshi Tamiya, life and work. In: Hase E, Iwamura T and Miyachi S (eds) Daishowa Publ Co, Tokyo
Tamiya H and Huzisige H (1949) Effect of oxygen on the dark reaction of photosynthesis. Acta Phytochim 15: 83–104
Tolbert NE (1997) The C2 oxidative photosynthetic carbon cycle. Annu Rev Plant Physiol 48: 1–25
van Niel CB, Ruben S, Carson SF, Kamen MD and Foster JW (1942) Radioactive carbon as an indicator of carbon dioxide utilization. VIII. The role of carbon dioxide in cellular metabolism. Proc Natl Acad Sci USA 28: 8–15
Wildman SG (1998) Discovery of Rubisco. In: Kung S-D and Yang S-F (eds) Discoveries in Plant Biology, Chapter 12, pp 163–173. World Scientific Publishing, Singapore
Willstätter R and Stoll A (1913) Untersuchungen über Chlorophyll, Methoden und Ergebnisse. Julius Springer-Verlag, Berlin
Willstätter R and Stoll A (1918) Untersuchungen über die Assimilation der Kohlensäure. Julius Springer-Verlag, Berlin
Wilson AT and Calvin M (1955) The photosynthetic cycle. CO2 dependent transients. J Am Chem Soc 77: 5948–5957
Witkop B (1992) Remembering Heinrich Wieland (1877-1957). Portrait of an organic chemist and founder of modern biochemistry. Med Res Rev 12: 195–274
Yoshikawa H and Kauffman J (1994) Science has no Borders. Harry C. Kelly and the Reconstruction of Science and Technology in Postwar Japan. MIT Press, Cambridge, Massachusetts/Mita Press, Tokyo
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Benson, A.A. Following the path of carbon in photosynthesis: a personal story. Photosynthesis Research 73, 29–49 (2002). https://doi.org/10.1023/A:1020427619771
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DOI: https://doi.org/10.1023/A:1020427619771