Photosynthetica, 2015 (vol. 53), issue 2

Photosynthetica 2015, 53(2):161-167 | DOI: 10.1007/s11099-015-0112-7

Benson-Bassham-Calvin cycle contribution to the organic life on our planet

K. Biel1,2,*, I. Fomina1,2
1 Institute of Basic Biological Problems, Russian Academy of Sciences, Pushchino, Moscow Region, Russia
2 Biosphere Systems International Foundation, Tucson, USA

The review is devoted to the outstanding contributions to the path of carbon in photosynthesis by Professor Emeritus Andrew A. Benson, on the occasion of his death at the age of 97, on January 16, 2015. Benson is the legendary co-discoverer of the photosynthetic reductive pentose phosphate cycle, known to every student of photosynthesis as the Benson-Bassham-Calvin cycle. This pathway evolved into the dominant assimilation mechanism for atmospheric carbon into metabolites. The fundamental ecological and biochemical optimization and evolutionary stability of this mechanism unfolded elegantly in Benson's hands, as he was the first to recognize the building blocks for the synthesis of essential organic compounds that satisfy the energetic needs and demands of most life forms. Photosynthetic carbon metabolism together with other energy and oxidative reactions and secondary biosynthetic processes are critical for the formation of organic matter; and, thereby, the Benson-Bassham-Calvin cycle ensures maintenance of the biosphere.

Keywords: autotrophic organisms; eukaryotes; photosynthesis; prokaryotes

Received: February 3, 2015; Accepted: March 11, 2015; Published: June 1, 2015Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Biel, K., & Fomina, I. (2015). Benson-Bassham-Calvin cycle contribution to the organic life on our planet. Photosynthetica53(2), 161-167. doi: 10.1007/s11099-015-0112-7.
Download citation

References

  1. Adrianov A.V., Vaskovsky V.E., Pudovkin A.I. et al.: On the 90th anniversary of Andrew Alm Benson great scientist and excellent man. - Russ. J. Mar. Biol. 33: 343-346, 2007. Go to original source...
  2. Bassham J.A., Benson A.A., Kay L.D. et al.: The path of carbon dioxide in photosynthesis. XXI. The cyclic regeneration of carbon dioxide acceptor. - J. Am. Chem. Soc. 76: 1760-1770, 1954. Go to original source...
  3. Bassham J.A., Buchanan B.B.: Carbon dioxide fixation pathways in plants and bacteria. - In: Govindjee (ed.): Photosynthesis. Vol. 2: Development, Carbon Metabolism, and Plant Productivity. Pp. 141-189. Academic Press, New York 1982. Go to original source...
  4. Benson A.A.: Mechanism of biochemical photosynthesis. - Z. Elektrochem. 56: 848-854, 1952.
  5. Benson A.A.: Paving the Path. - Annu. Rev. Plant Biol. 53: 1-25, 2002a. Go to original source...
  6. Benson A.A.: Following the path of carbon in photosynthesis: a personal story. - Photosynth. Res. 73: 29-49, 2002b. Go to original source...
  7. Benson A.A., Bassham J.A., Calvin M. et al.: The path of carbon in photosynthesis. 5. Paper chromatography and radioautography of the products. - J. Am. Chem. Soc. 72: 1710-1718, 1950. Go to original source...
  8. Benson A.A., Calvin M.: Carbon dioxide fixation by green plants. - Annu. Rev. Plant Phys. 1: 25-42, 1950a. Go to original source...
  9. Benson A.A., Calvin M.: The path of carbon in photosynthesis. VII. Respiration and photosynthesis. - J. Exp. Bot. 1: 63-68, 1950b. Go to original source...
  10. Benson A.A, Muscatine L.: Wax in coral mucus: Energy transfer from corals to reef fishes. - Limnol. Oceanogr. 19: 810-814, 1974. Go to original source...
  11. Benson A.A., Nonomura A.M.: The path of carbon in photosynthesis: Methanol inhibition of glycolic acid accumulation. - In: Murata N. (ed.): Research in Photosynthesis 1, Proceedings of the IX International Congress on Photosynthesis. P-522. Kluver, Nagoya 1992. Go to original source...
  12. Benson A.A., Nonomura A.M., Gerard V.A.: The path of carbon in photosynthesis. XXV. Plant and algal growth responses to glycopyranosides. - J. Plant Nutr. 32: 1185-1200, 2009. Go to original source...
  13. Benson A.A., Patton J.S., Abraham S.: Energy exchange in coral reef ecosystems. - Atoll Res. Bull. 220: 33-54, 1978. Go to original source...
  14. Biel K. Y.: [Ecology of Photosynthesis.] Pp. 1-221. Nauka, Moscow 1993. [In Russian]
  15. Biel K.Y., Fomina I.R., Nazarova G.N. et al.: Untangling metabolic and spatial interactions of stress tolerance in plants. 1. Patterns of carbon metabolism within leaves. - Protoplasma 245: 49-73, 2010. Go to original source...
  16. Biel K.Y., Fomina I.R., Yensen N.P. et al.: Complex Biological Systems: Adaptation and Tolerance to Extreme Environments. Pp. 1-343. Gorod, Pushchino-Krasnoyarsk 2014.
  17. Biel K.Y., Nonomura A.M., Benson A.A., Nishio J.N.: The path of carbon in photosynthesis. XXVI. Uptake and transport of methylglucopyranoside throughout plants. - J. Plant Nutr. 33: 902-913, 2010. Go to original source...
  18. Bil' K.Y., Gedemov T.: Structural and functional properties of assimilation apparatus in Suaeda arcuata Bunge (Chenopodiaceae) related to cooperative photosynthesis. - Proc. Acad. Sci. USSR 250: 9-13, 1980.
  19. Bil' K.Y., Lyubimov V.Y., Demidova R.N., Gedemov T.: [Assimilation of CO2 by plants of the family Chenopodiaceae with three types of autotrophic tissues in the leaves.] - Soviet Plant Physiol. 28: 1119-1127, 1981. [In Russian]
  20. Bil' K.Y., Lyubimov V.Y., Trusov M. F. et al.: [Participation of three types of autotrophic tissues in diurnal dynamics of assimilation CO2 in some plants of Chenopodiaceae family.] - Bot. Zhurnal 68: 54-61, 1983. [In Russian]
  21. Blanquet R.S., Nevenzel J.C., Benson A.A.: Acetate incorporation into the lipids of the sea anemone Anthopleura elegantissima and its associated zooxanthellae. - Mar. Biol. 54: 185-194, 1979. Go to original source...
  22. Buchanan B.B., Arnon D.I.: A reverse Krebs cycle in photosynthesis: consensus at last. - Photosynth. Res. 24: 47-53, 1990. Go to original source...
  23. Buchanan B.B., Sirevåg R.: Ribulose-l,5-diphosphate carboxylase and Chlorobium thiosulfatophilum. - Arch. Microbiol. 109: 15-19, 1977. Go to original source...
  24. Buchanan B.B., Wong J.H.: A conversation with Andrew Benson: reflections on the discovery of the Calvin-Benson cycle. - Photosynth. Res. 114: 207-214, 2013. Go to original source...
  25. Calvin M., Benson A.A.: The path of carbon in photosynthesis. - Science 107: 476-480, 1948. Go to original source...
  26. Doman N.G.: [A question about the nature of rapidly labeled photosynthetic products.] - Dokl. Akad. Nauk SSSR 84: 1017-1019, 1952. [In Russian]
  27. Doman N.G., Khadzhi-Murat L.N., Demina S.E.: [Unities and peculiarities of carbon assimilation pathway(s) in different plant species.] - Dokl. Akad. Nauk SSSR 122: 111-113, 1958. [In Russian]
  28. Evans M.C.W., Buchanan B.B., Arnon D.I.: A new ferredoxindependent carbon reduction cycle in a photosynthetic bacterium. - P. Natl. Acad. Sci. USA 55: 928-934, 1966. Go to original source...
  29. Fomina I.R., Biel K.Y.: [Photosynthetic carbon metabolism: Strategy of adaptation.] - In: Allakhverdiev S.I., Rubin A.B., Shuvalov V.A. (ed.): [Contemporary Problems of Photosynthesis. Vol. 2.] Pp. 415-484. Institute of Computer Science, Moscow-Izhevsk 2014. [In Russian]
  30. Guralnick L.J., Edwards G.E., Ku M.S.B. et al.: Photosynthetic and anatomical characteristics in the C4/CAM-cycling species, Portulaca grandiflora. - Funct. Plant Biol. 29: 763-773, 2002. Go to original source...
  31. 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...
  32. Hartt C.E., Kortschak H.P., Burr G.O.: Photosynthesis by sugar cane fed radioactive carbon dioxide. - P. Hawaii Acad. Sci. 13-14, 1953.
  33. Herter S., Fuchs G., Bacher A., Eisenreich W.: A bicyclic autotrophic CO2 fixation pathway in Chloroflexus aurantiacus. - J. Biol. Chem. 277: 20277-20283, 2002. Go to original source...
  34. Karpilov Y.S.: [Distribution of 14C among the photosynthetic products of maize.] - Trudy Kazan. Sel'skokhoz. Inst. 41: 15-24, 1960. [In Russian]
  35. Karpilov Y.S.: [Features of the functions and structure of the photosynthetic apparatus of some plant species of tropical origin.] - Trudy Mold. N.I.I. Orosh. Zemledel. Ovoshchevod. 11: 1-35, 1969. [In Russian]
  36. Kluge M.: Crassulacean acid metabolism (CAM): CO2 and water economy. - In: Lange O.L., Kappen L., Schulze E.-D. (ed.): Water and Plant Life: Problems and Modern Approaches. Ecological Studies. Vol. 19. Pp. 313-322. Springer, Berlin Heidelberg 1976. Go to original source...
  37. Kondratieva E.N.: [Photosynthetic Bacteria.] Pp. 1-314. Izd. AN SSSR, Moscow 1963. [In Russian]
  38. Kondratieva E.N.: [Autotrophic Prokaryotes.] Pp. 1-304. Publ. Moscow University, Moscow 1996. [In Russian]
  39. Kortschak H.P., Hartt C.E., Burr G.O.: Carbon dioxide fixation in sugarcane leaves. - Plant Physiol. 40: 209-213, 1965. Go to original source...
  40. Lichtenthaler H.K., Buchanan B.B., Douce R.: Honoring Andrew Benson in Paris. A tribute on his 90th birthday. - Photosynth. Res. 96: 181-183, 2008. Go to original source...
  41. Marakushev S.A.: Transformation of hydrocarbons into components of archaic chemoautotrophic CO2 fixation cycle. - Doklady Biochem. Biophys. 418: 18-23, 2008. Go to original source...
  42. Marakushev S.A., Belonogova, O.V.: Emergence of the chemoautotrophic metabolism in hydrothermal environments and the origin of ancestral bacterial taxa. - Doklady Biochem. Biophys. 439: 161-166, 2011. Go to original source...
  43. Mokronosov A.T.: [Ontogenetic Aspects of Photosynthesis.] Pp. 1-196. Nauka, Moscow 1981. [In Russian]
  44. Mokronosov A.T.: [Genotypic and phenotypic factors in the determination of photosynthetic carbon metabolism] - In: Mokronosov A.T. (ed.): [Photosynthetic Carbon Metabolism.] Pp. 7-23. Uralskii Rabochii, Sverdlovsk 1983. [In Russian]
  45. Monson R.K., Edwards G.E., Ku M.S.B.: C3-C4 intermediate photosynthesis in plants. - Bio. Sci. 34: 563-574, 1984.
  46. Nezgovorova L.A.: [To a question about the products of photosynthesis.] - Soviet Plant Physiol. 3: 497-507, 1956. [In Russian]
  47. Nezgovorova L.A.: [Influence of water regime of plants on the receipt and distribution of carbon in photosynthesis.] - Soviet Plant Physiol. 4: 440-449, 1957. [In Russian]
  48. Nichiporovich A.A.: Photosynthetic products and the physiological function of the photosynthetic apparatus of plants. - Trudy Inst. Fiziol. Rast. AN SSSR 8: 3-41, 1953. [In Russian]
  49. Nishio J.N., Ting I.P.: Carbon flow and metabolic specialization in the tissue layers of the Crassulacean acid metabolism plant, Peperomia camptotricha. - Plant Physiol. 84: 600-604, 1987. Go to original source...
  50. Nonomura A.M., Benson A.A.: The path of carbon in photosynthesis: Improved crop yields with methanol. - P. Natl. Acad. Sci. USA 89: 9794-9798, 1992. Go to original source...
  51. Nonomura A.M., Benson A.A., Biel K.Y.: The path of carbon in photosynthesis. XXVII. Sugar-conjugated plant growth regulators enhance general productivity. - J. Plant Nutr. 34: 653-664, 2011. Go to original source...
  52. Nonomura A.M., Benson A.A.: The path of carbon in photosynthesis - XXX - α-mannosides. - In: Dubinsky Z. (ed.): Photosynthesis. Pp. 3-22. InTech, Rijeka 2013.
  53. Nonomura A.M., Benson A.A.: The path of carbon in photosynthesis. XXXI. The role of lectins. - J. Plant Nutr. 37: 785-794, 2014. Go to original source...
  54. Osmond C.B.: Crassulacean acid metabolism: A curiosity in context. - Annu. Rev. Plant Physiol. 29: 379-414, 1978. Go to original source...
  55. Osmond C.B., Allaway W.G.: Pathway of CO2 fixation in the CAM plant Kalanchoe daigremontiana. I. Patterns of 14CO2 fixation in the light. - Aust. J. Plant Physiol. 1: 503-511, 1974. Go to original source...
  56. Shomer-Ilan A., Nissenbaum A., Waisel Y.: Photosynthetic pathway and ecological distribution of the Chenopodiaceae in Israel. - Oecologia 48: 244-248, 1981. Go to original source...
  57. Tarchevsky I.A.: [Photosynthesis and Drought.] Pp. 1-198. Publ. Kazan University, Kazan 1964 [In Russian]
  58. Tarchevsky I.A.: [Mechanisms of drought effects on photosynthetic absorption of CO2.] - In: Nichiporovich, A.A. (ed.): Physiology of Photosynthesis. Pp. 118-129. Nauka, Moscow 1982. [In Russian]
  59. Titlyanov E.A., Titlyanova T.V.: Andy Benson in Russia and at Home. - Russian J. Mar. Biol. 33: 347-348, 2007.
  60. Tolbert N.E.: Metabolic pathways in peroxisomes and glyoxysomes. - Annu. Rev. Biochem. 50: 133-157, 1981. Go to original source...
  61. Tolbert N.E.: The C2 oxidative photosynthetic carbon cycle - Annu. Rev. Plant Phys. 48: 1-25, 1997. Go to original source...
  62. Vacquier V.D., Aguilera M., Nonomura A.: Obituary Notice: Andrew Benson: World-Renowned Scripps Plant Biochemist. https://scripps.ucsd.edu/news/obituary-notice-andrew-benson-world-renowned-scripps-plant-biochemist, 2015.
  63. Winter K., Troughton J.H.: Carbon assimilation pathway in Mesembryanthemum nodiflorum under natural conditions. - Z. Pflanzenphysiol. 88: 153-162, 1978. Go to original source...
  64. Zarzycki J., Brecht V., Müller M., Fuchs G. Identifying the missing steps of the autotrophic 3-hydroxypropionate CO2 fixation cycle in Chloroflexus aurantiacus. - P. Natl. Acad. Sci. USA 106: 21317-21322, 2009. Go to original source...
  65. Zelitch I.: The photooxidation of glyoxylate by envelope-free spinach chloroplasts and its relation to photorespiration. - Arch. Biochem. Biophys. 150: 698-707, 1972. Go to original source...
  66. Zelitch I.: Alternate pathways of glycolate synthesis in tobacco and maize leaves in relation to rates of photorespiration. - Plant Physiol. 51: 299-305, 1973. Go to original source...