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The controversy over the minimum quantum requirement for oxygen evolution

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Abstract

During the early- to mid-twentieth century, a bitter controversy raged among researchers on photosynthesis regarding the minimum number of light quanta required for the evolution of one molecule of oxygen. From 1923 until his death in 1970, Otto Warburg insisted that this value was about three or four quanta. Beginning in the late 1930s, Robert Emerson and others on the opposing side consistently obtained a value of 8–12 quanta. Warburg changed the protocols of his experiments, sometimes in unexplained ways, yet he almost always arrived at a value of four or less, except eight in carbonate/bicarbonate buffer, which he dismissed as “unphysiological”. This paper is largely an abbreviated form of the detailed story on the minimum quantum requirement of photosynthesis, as told by Nickelsen and Govindjee (The maximum quantum yield controversy: Otto Warburg and the “Midwest-Gang”, 2011); we provide here a scientific thread, leaving out the voluminous private correspondence among the principal players that Nickelsen and Govindjee (2011) examined in conjunction with their analysis of the principals’ published papers. We explore the development and course of the controversy and the ultimate resolution in favor of Emerson’s result as the phenomenon of the two-light-reaction, two-pigment-system scheme of photosynthesis came to be understood. In addition, we include a brief discussion of the discovery by Otto Warburg of the requirement for bicarbonate in the Hill reaction.

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Notes

  1. John F. Allen told us about his recollection of an exchange at a Photochemistry Discussion Group meeting at London's Royal Institution in 1975. Sir George Porter was organizer and chair. Helmut Metzner had just given a talk on the possible role of bicarbonate/CO2 in the Hill reaction. Porter addressed Robin Hill in the audience, “But, CO 2 is not required for your reaction; is it? Robin replied “Yes, it is.” (See Shevela et al. 2012 for a complete perspective on this issue.)

References

  • Arnold W (1935) Investigations on photosynthesis. PhD Thesis, Harvard University, Cambridge, Massachusetts, USA

  • Arnold W (1949) A calorimetric determination of the quantum yield in photosynthesis. In: Franck J, Loomis WE (eds) Photosynthesis in plants. Iowa State College Press, Ames, pp 273–276

    Google Scholar 

  • Arnon DI, Barber J (1990) Photoreduction of NADP+ by isolated reaction centers of photosystem II: requirement for plastocyanin. Proc Natl Acad Sci USA 87:5930–5934

    PubMed  CAS  PubMed Central  Google Scholar 

  • Arnon DI, Knaff DB, McSwain BD, Chain RK, Tsujimoto HY (1971) Three light reactions and the two photosystems of plant photosynthesis. Photochem Photobiol 14:397–425

    CAS  Google Scholar 

  • Baker NR, Bradbury M, Farage PK, Ireland CR, Long S (1989) Measurements of quantum yield of carbon assimilation and chlorophyll fluorescence for assessment of photosynthetic performance of crop plants in the field. Phil Trans Royal Soc B 323: 295–308

  • Bannister TT (1972) The careers and contributions of Eugene Rabinowitch. Biophys J 12:707–718

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bassham JA (2003) Mapping the carbon reduction cycle: a personal retrospective. Photosynth Res 76:35–52

    PubMed  Google Scholar 

  • Bassham JA, Benson AA, Kay LD, Harris AZ, Wilson AT, Calvin M (1954) The path of carbon in photosynthesis. XXI. The cyclic regeneration of carbon dioxide acceptor. J Am Chem Soc 76:1760–1770

    CAS  Google Scholar 

  • BBC movie “Botany: a Blooming History, Episode 2, The Power of Plants” (2010) http://www.bbc.co.uk/programmes/b011wz4q (Not currently available on BBC iplayer); contact Govindjee (e-mail: gov@illinois.edu) for further information

  • Benson AA (2002) Following the path of carbon in photosynthesis: a personal story. Photosynth Res 73:29–49

    PubMed  CAS  Google Scholar 

  • Benson AA (2010) Last days in the old radiation laboratory (ORL), Berkeley, California, 1954. Photosynth Res 105:209–212

    PubMed  CAS  PubMed Central  Google Scholar 

  • Blackman FF (1905) Optima and limiting factors. Ann Bot 19:281–296

    Google Scholar 

  • Blankenship RE (2014) Molecular mechanisms of photosynthesis, 2nd edn. Wiley-Blackwell, Oxford

    Google Scholar 

  • Blankenship RE, Tiede DM, Barber J, Brudvig GW, Fleming G, Ghirardi M, Gunner MR, Junge W, Kramer DM, Melis A, Moore TA, Moser CC, Nocera DG, Nozik AJ, Ort DR, Parson WW, Prince RC, Sayre RT (2011) Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332:805–809

    PubMed  CAS  Google Scholar 

  • Bolton JR, Hall D (1991) The maximum efficiency of photosynthesis. Photochem Photobiol 53:545–548

    CAS  Google Scholar 

  • Brown HT, Escombe F (1905) Researches on some of the physiological processes of green leaves, with special reference to the interchange of energy between the leaf and its surroundings. Proc R Soc Lond Ser B 76:29–111

    CAS  Google Scholar 

  • Buchanan BB (2012) A conversation with Andrew Benson: reflections on the discovery of the Calvin-Benson Cycle. YouTube video http://www.youtube.com/watch?v=GfQQJ2vR_xE. Accessed 1 March 2014

  • Buchanan BB, Wong JH (2013) A conversation with Andrew Benson: reflections on the discovery of the Calvin-Benson cycle. Photosynth Res 114:207–214

    CAS  Google Scholar 

  • Bücher T (1983) Otto Warburg: a personal recollection. In: Sund H, Ullrich V (eds) Biological oxidations. Springer, Berlin, pp 1–29

    Google Scholar 

  • Burk D, Hendricks S, Korzenovsky M, Schocken V, Warburg O (1949) The maximum efficiency of photosynthesis: a rediscovery. Science 110:225–229

    PubMed  CAS  Google Scholar 

  • Burk D, Cornfield J, Schwartz M (1951) The efficient transformation of light into chemical energy in photosynthesis: an application of the Einstein law of photochemical equivalence to living organisms. Sci Mon 73:213–223

    CAS  Google Scholar 

  • Calvin M, Bassham JA, Benson AA (1950) Chemical transformations of carbon in photosynthesis. Proc Fed Am Soc Exp Biol 9:524–534

    CAS  Google Scholar 

  • Duysens LNM (1952) Transfer of excitation energy in photosynthesis. Doctoral thesis, University of Utrecht, The Netherlands

  • Duysens LNM (1958) The path of light in photosynthesis. Brookhaven Symp Biol 11:18–25

    Google Scholar 

  • Duysens LNM (1962) A note on efficiency for conversion of light energy. Plant Physiol 37:407–408

    PubMed  CAS  PubMed Central  Google Scholar 

  • Einstein A (1912a) Thermodynamische Begründung des photochemischen Aequivalentgesetzes. Ann Physik 37:832–838

    CAS  Google Scholar 

  • Einstein A (1912b) Nachtrag zu meiner Arbeit: thermodynamische Begründung des photochemischen Aequivalentgesetzes. Ann Physik 38:881–884

    Google Scholar 

  • El-Shintinawy F, Govindjee (1990) Bicarbonate effect in leaf discs from spinach. Photosynth Res 24:189–200

    PubMed  CAS  Google Scholar 

  • Emerson R (1958) The quantum yield of photosynthesis. Annu Rev Plant Physiol 9:1–24

    CAS  Google Scholar 

  • Emerson R, Arnold W (1932) The photochemical reaction in photosynthesis. J Gen Physiol 16:191–205

    PubMed  CAS  PubMed Central  Google Scholar 

  • Emerson R, Chalmers R (1955) Transient changes in cellular gas exchange and the problem of maximum efficiency of photosynthesis. Plant Physiol 30:504–529

    PubMed  CAS  PubMed Central  Google Scholar 

  • Emerson R, Chalmers R (1958) Speculations concerning the function and phylogenetic significance of the accessory pigments of algae. Phycol Soc News Bull 11:51–56

    Google Scholar 

  • Emerson R, Lewis CM (1939) Factors influencing the efficiency of photosynthesis. Am J Bot 26(10):808–822

    CAS  Google Scholar 

  • Emerson R, Lewis CM (1941) Carbon dioxide exchange and the measurement of the quantum yield of photosynthesis. Am J Bot 28:789–804

    CAS  Google Scholar 

  • Emerson R, Lewis CM (1943) The dependence of the quantum yield of Chlorella photosynthesis on wave length of light. Am J Bot 30:165–178

    CAS  Google Scholar 

  • Emerson R, Rabinowitch E (1960) Red drop and role of auxiliary pigments in photosynthesis. Plant Physiol 35:477–485

    PubMed  CAS  PubMed Central  Google Scholar 

  • Emerson R, Chalmers R, Cederstrand CN (1957) Some factors influencing the long-wave limit of photosynthesis. Proc Natl Acad Sci USA 43:133–143

    PubMed  CAS  PubMed Central  Google Scholar 

  • Franck J (1949) An interpretation of the contradictory results in measurements of the photosynthetic quantum yields and related phenomena. Arch Biochem 23:297–314

    PubMed  CAS  Google Scholar 

  • Gaffron H, Wohl K (1936) Zur Theorie der Assimilation. Naturwissenschaften 24(81–90):103–107

    Google Scholar 

  • Golbeck JH (ed) (2006) Photosystem I: the light-driven plastocyanin:ferredoxin oxidoreductase. Advances in photosynthesis and respiration, vol 24. Springer, Dordrecht

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Govindjee (2001) Lighting the path: a tribute to Robert Emerson (1903–1959). In: Proceedings of the 12th international congress on photosynthesis (PS2001), Brisbane. CSIRO Publishing

  • Govindjee (2004) Robert Emerson and Eugene Rabinowitch: understanding photosynthesis. In: Hoddeson L (ed) No boundaries: University of Illinois Vignettes. University of Illinois Press, Urbana/Chicago, pp 181–194

    Google Scholar 

  • Govindjee (2010) Celebrating Andrew Alm Benson’s 93rd birthday. Photosynth Res 105:201–208

    PubMed  CAS  Google Scholar 

  • Govindjee, Bjorn LO (2012) Dissecting oxygenic photosynthesis: the evolution of the Z-scheme for thylakoid membranes. In: Itoh S, Mohanty S, Guruprasad KN (eds) Photosynthesis: overviews on recent progress and future perspective. I. K. International Publishers, New Delhi, pp 1–27

    Google Scholar 

  • Govindjee, Krogmann D (2004) Discoveries in oxygenic photosynthesis (1727–2003): a perspective. Photosynth Res 80:15–57

    PubMed  CAS  Google Scholar 

  • Govindjee, Rabinowitch E (1960) Two forms of chlorophyll a in vivo with distinct photochemical functions. Science 132:355–356

    PubMed  CAS  Google Scholar 

  • Govindjee, Srivastava N (2014) William Archibald Arnold (December 6, 1904–October 26, 2001) Biographical Memoirs of the National Academy of Sciences, USA, Washington, DC. http://www.nasonline.org/publications/biographical-memoirs/memoir-pdfs/arnold-william.pdf

  • Govindjee, van Rensen JJ (1978) Bicarbonate effects on the electron flow in isolated broken chloroplasts. Biochim Biophys Acta 505:183–213

    PubMed  CAS  Google Scholar 

  • Govindjee, Owens OvH, Hoch G (1963) A mass spectroscopic study of the Emerson enhancement effect. Biochim Biophys Acta 75:281–284

    PubMed  CAS  Google Scholar 

  • Govindjee, Munday JC Jr., Papageorgiou GC (1967) Fluorescence studies with algae: Changes with time and preillumination. In: Olson, JM (ed.) Energy Conversion by the Photosynthetic Apparatus, Brookhaven Symposia in Biology 19:434–445

  • Govindjee, Knox RS, Amesz J (eds) (1996) Photosynthetic unit: antenna and reaction centers, a special issue dedicated to William A. Arnold. Photosynth Res 48 (1 and 2):1–319

  • Govindjee, Beatty JT, Gest H, Allen JF (eds) (2005) Discoveries in photosynthesis. Advances in photosynthesis and respiration, vol 20. Springer, Dordrecht

  • Govindjee R(ajni), Thomas JB, Rabinowitch EI (1960) “Second Emerson effect” in the Hill reaction of Chlorella cells with quinine as oxidant. Science 132:421

    PubMed  CAS  Google Scholar 

  • Govindjee R(ajni), Govindjee, Hoch G (1962) The Emerson enhancement effect in TPN-photoreduction by spinach chloroplasts. Biochem Biophys Res Commun 9:222–225

    CAS  Google Scholar 

  • Govindjee R(ajni), Govindjee, Hoch G (1964) Emerson enhancement effect in chloroplast reactions. Plant Physiol 39:10–14

    PubMed  CAS  PubMed Central  Google Scholar 

  • Govindjee R(ajni), Rabinowitch EI, Govindjee (1968) Maximum quantum yield and action spectrum of photosynthesis and fluorescence in Chlorella. Biochim Biophys Acta 162:539–544

    PubMed  CAS  Google Scholar 

  • Greenbaum E, Lee JW, Tevault CV, Blankinship SL, Mets LJ (1995) CO2 fixation and photoevolution of H2 and O2 in a mutant of Chlamydomonas lacking photosystem I. Nature 376:438–441

    CAS  Google Scholar 

  • Hendricks SB (1953) A discussion of photosynthesis. Science 117:370–373

    PubMed  CAS  Google Scholar 

  • Hill R (1937) Oxygen evolved by isolated chloroplasts. Nature 139:881–882

    CAS  Google Scholar 

  • Hill R (1939) Oxygen produced by isolated chloroplasts. Proc R Soc Lond Ser B 127:192–210

    CAS  Google Scholar 

  • Hill JF (2012) Early pioneers of photosynthesis research. In: Eaton-Rye JJ, Sharkey TD, Tripathy BC (eds) Photosynthesis: perspectives on plastid biology, energy conversion and carbon metabolism. Advances in photosynthesis and respiration, vol 34. Springer, Dordrecht, pp 771–800

    Google Scholar 

  • Hill R, Bendall F (1960) Function of the two cytochrome components in chloroplasts: a working hypothesis. Nature 186:136–137

    CAS  Google Scholar 

  • Höxtermann E (1992) Fundamental discoveries in the history of photosynthesis research. Photosynthetica 26:485–502

    Google Scholar 

  • Höxtermann E (2007) A comment on Warburg’s early understanding of biocatalysis. Photosynth Res 92:121–127

    PubMed  Google Scholar 

  • Höxtermann E, Sucker U (1989) Otto Warburg (Biographien hervorragender Naturwissenschaftler, Techniker und Mediziner) (Book 91) Vieweg + Teubner Verlag, Springer Fachmedien Wiesbaden GmbH

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

    PubMed  CAS  Google Scholar 

  • Kamen MD (1989) Onward into a fabulous half-century. Photosynth Res 21:139–144

    PubMed  CAS  Google Scholar 

  • Kamen MD (1995) Liebling’s law (“ILL”). Proc Am Philos Soc 139:358–367

    Google Scholar 

  • Klimov V, Allakhverdiev SI, Feyziev YM, Baranov SV (1995) Bicarbonate requirement for the donor side of photosystem II. FEBS Lett 363:251–255

    PubMed  CAS  Google Scholar 

  • Knox RS (1969) Thermodynamics and the primary processes of photosynthesis. Biophys J 9:1351–1362

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kok B (1948) A critical consideration of the quantum yield of Chlorella-photosynthesis. Enzymologia 13:1–5

    CAS  Google Scholar 

  • Koroidov S, Shevela D, Shutova T, Samuelsson G, Messinger J (2014) Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation. Proc Natl Acad Sci USA 111(17):6299–6304

    PubMed  CAS  PubMed Central  Google Scholar 

  • Krebs HA (1972) Otto Heinrich Warburg. Biogr Mem Fellows R Soc 18:628–699

    Google Scholar 

  • Krebs HA (1981) Otto Warburg: cell physiologist, biochemist, and eccentric. Clarendon Press, Oxford

    Google Scholar 

  • Ley AC, Mauzerall DC (1982) Absolute absorption cross-sections for photosystem II and the minimum quantum requirement for photosynthesis in Chlorella vulgaris. Biochim Biophys Acta 680:95–106

    CAS  Google Scholar 

  • Magee JL, de Witt TW, Smith EC, Daniels F (1939) A photocalorimeter: the quantum efficiency of photosynthesis in algae. J Am Chem Soc 61:3529–3533

    CAS  Google Scholar 

  • Manning WM, Stauffer JF, Duggar BM, Daniels F (1938) Quantum efficiency of photosynthesis in Chlorella. J Am Chem Soc 60:266–274

    CAS  Google Scholar 

  • Mauzerall D (2013) Thermodynamics of primary photosynthesis. Photosynth Res 116:363–366

    PubMed  CAS  PubMed Central  Google Scholar 

  • McGrath JM, Long SP (2014) Can the cyanobacterial carbon-concentrating mechanism increase photosynthesis in crop species? A theoretical analysis. Plant Physiol. doi:10.1104/pp.113.232611

    PubMed  PubMed Central  Google Scholar 

  • Mohr H, Schopfer P (1995) Plant physiology (Translated from the German by Lawlor G, Lawlor DW). Springer, Berlin

  • Myers J (1974) Conceptual developments in photosynthesis, 1924–1974. Plant Physiol 54:420–426

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ng K-S, Bassham JA (1968) The quantum requirement of photosynthesis in Chlorella. Biochim Biophys Acta 162:254–264

    PubMed  CAS  Google Scholar 

  • Nickelsen K (2007) Otto Warburg’s first approach to photosynthesis. Photosynth Res 92:109–120

    PubMed  CAS  Google Scholar 

  • Nickelsen K (2009a) Of light and darkness: modeling photosynthesis 1840–1960. Habilitation. University of Bern, Bern, Switzerland

  • Nickelsen K (2009b) The construction of a scientific model: Otto Warburg and the building block strategy. Stud Hist Philos Biol Biomed Sci 40:73–86

    PubMed  Google Scholar 

  • Nickelsen K (2012) From the red drop to the Z-scheme of photosynthesis. Ann Phys (Berlin) 524:A157–A160

    CAS  Google Scholar 

  • Nickelsen K (2014) Explaining photosynthesis: models of biochemical mechanisms. Springer, Dordrecht, pp 1840–1960 (Series: history, philosophy and theory of the life sciences)

    Google Scholar 

  • Nickelsen K, Govindjee (2011) The maximum quantum yield controversy: Otto Warburg and the “Midwest-Gang.” Bern studies in the history and philosophy of science, University of Bern, Bern, Switzerland

  • Nishimura MS, Whittingham CP, Emerson R (1951) The maximum efficiency of photosynthesis: a critique of certain manometric techniques used for measuring rates of photosynthesis. Carbon dioxide fixation and photosynthesis: symposia of society for experimental biology 5. Cambridge University Press, Cambridge, pp 176–210

    Google Scholar 

  • Orr L, Govindjee (2013) Photosynthesis web resources. Photosynth Res 115:179–214

    PubMed  CAS  Google Scholar 

  • Osborne BA, Geider RJ (1987) The minimum photon requirement for photosynthesis. New Phytol 106:631–644

    CAS  Google Scholar 

  • Parson WW (1978) Thermodynamics of the primary reactions of photosynthesis. Photochem Photobiol 28:389–393

    CAS  Google Scholar 

  • Pirt SJ (1986) The thermodynamic efficiency (quantum demand) and dynamics of photosynthetic growth. New Phytol 102:3–37

    Google Scholar 

  • Rabinowitch EI (1945) Photosynthesis and related processes, vol I: chemistry of photosynthesis, chemosynthesis and related processes in vitro and in vivo. Interscience Publishers, New York. http://www.life.illinois.edu/govindjee/g/Books.html. Accessed 1 March 2014

  • Rabinowitch EI (1951) Photosynthesis and related processes, vol II, Part 1. Interscience Publishers, New York. http://www.life.illinois.edu/govindjee/g/Books.html. Accessed 1 March 2014

  • Rabinowitch EI (1959) Robert Emerson, 1903–1959. Plant Physiol 34:179–184

    Google Scholar 

  • Rabinowitch EI (1961) Robert Emerson (1903–1959). Biogr Mem Natl Acad Sci USA 25:112–131

    Google Scholar 

  • Rabinowitch E, Govindjee (1961) Different forms of chlorophyll a in vivo and their photochemical function. In: McElroy WD, Glass B (eds) A symposium on light and life. The Johns Hopkins Press, Baltimore, pp 378–386

    Google Scholar 

  • Rabinowitch E, Govindjee (1969) Photosynthesis. Wiley, New York. http://www.life.illinois.edu/govindjee/g/Books.html; and http://www.life.illinois.edu/govindjee/photosynBook.html. Accessed 1 March 2014

  • Rieke FF (1939) On the quantum efficiency of photosynthesis. J Chem Phys 7:238–244

    CAS  Google Scholar 

  • Rieke FF (1949) Quantum efficiencies for photosynthesis and photoreduction in green plants. In: Franck J, Loomis WE (eds) Photosynthesis in plants. Iowa State College Press, Ames, pp 251–272

    Google Scholar 

  • Ross RT, Calvin M (1967) Thermodynamics of light emission and free energy storage in photosynthesis. Biophys J 7:595–614

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ruben S, Randall M, Kamen M, Hyde JL (1941) Heavy oxygen (18O) as a tracer in the study of photosynthesis. J Am Chem Soc 63:877–879

    CAS  Google Scholar 

  • Ryder AW (1957) The Panchatantra (of India), English translation, University of Chicago Press, 1957, p 9

  • Senger H, Bishop NI (1967) Quantum yield of photosynthesis in synchronous Scenedesmus cultures. Nature 214:140–142

    PubMed  CAS  Google Scholar 

  • Sharp RE, Matthews MA, Boyer JS (1984) Kok effect and the quantum yield of photosynthesis: light partially inhibits dark respiration. Plant Physiol 75:95–101

    PubMed  CAS  PubMed Central  Google Scholar 

  • Shevela D, Eaton-Rye JJ, Shen JR, Govindjee (2012) Photosystem II and unique role of bicarbonate: A historical perspective. Biochim Biophys Acta 1817:1134–1151

  • Skillman JB (2008) Quantum yield variation across the three pathways of photosynthesis: not yet out of the dark. J Exp Bot 59:1647–1661

    PubMed  CAS  Google Scholar 

  • Stemler A (1982) The functional role of bicarbonate in photosynthetic light reaction II. In: Govindjee (ed) Photosynthesis. Academic Press, New York, pp 513–538

    Google Scholar 

  • Stemler A, Babcock GT, Govindjee (1974) The effect of bicarbonate on photosynthetic oxygen evolution in flashing light in chloroplast fragments. Proc Natl Acad Sci USA 71:4679–4683

    PubMed  CAS  PubMed Central  Google Scholar 

  • The Nobel Prize in Physiology or Medicine (1931). Nobelprize.org. Nobel Media AB 2013. http://www.nobelprize.org/nobel_prizes/medicine/laureates/1931/. Accessed 30 Apr 2014

  • Umbreit WW, Burris RH, Stauffer JF (1957) Manometric techniques: a manual describing methods applicable to the study of tissue metabolism. Burgess Publ Co, Minneapolis

    Google Scholar 

  • Van Niel CB (1932) On the morphology and physiology of the purple and green sulphur bacteria. Arch Mikrobiol 3:1–112

    Google Scholar 

  • Van Niel CB (1941) The bacterial photosyntheses and their importance for the general problem of photosynthesis. Adv Enzymol Relat Areas Microbiol 1:263–328

    Google Scholar 

  • Van Rensen JJS, Xu C, Govindjee (1999) Role of bicarbonate in photosystem II, the water-plastoquinone oxido-reductase of plant photosynthesis. Physiol Plant 105:585–592

    Google Scholar 

  • Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324(5930):1029–1033

    PubMed  CAS  PubMed Central  Google Scholar 

  • Walker D (1992) Energy, plants and man. Oxygraphics, East Sussex

    Google Scholar 

  • Wang QJ, Singh A, Li H, Nedbal L, Sherman LA, Govindjee, Whitmarsh JC (2012) Net light-induced oxygen evolution in photosystem I deletion mutants of the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1817:792–801

    PubMed  CAS  Google Scholar 

  • Warburg E (1917) Über die anwendung der Quantenhypothese auf de photochemie. Naturwissenschaften 5(30):489–494

    Google Scholar 

  • Warburg O (1919) Über die Geschwindigkeit der photochemischen Kohlensäurezersetzung in lebenden Zellen I. Biochem Zeitschrift 100:230–270

    CAS  Google Scholar 

  • Warburg O (1920) Über die Geschwindigkeit der photochemischen Kohlensäurezersetzung in lebenden Zellen II. Biochem Zeitschrift 103:188–217

    CAS  Google Scholar 

  • Warburg O (1921) Theorie der Kohlensäureassimilation. Naturwissenschaften 9:354–358

    CAS  Google Scholar 

  • Warburg O (1928) Uber die Katalytischen Wirkungen der Lebendigen Substanz: Arbeiten aus dem Kaiser Wilhelm-Institut für Biologie Berlin-Dahlem. Springer, Berlin

    Google Scholar 

  • Warburg O (1945) Über den Quantenbedarf der Kohlensäureassimilation. Naturwissenschaften 33:122

    Google Scholar 

  • Warburg O (1948) Assimilatory quotient and photochemical yield. Am J Bot 35:194–204

    PubMed  CAS  Google Scholar 

  • Warburg O (1958) Photosynthesis. Science 128:68–73

    PubMed  CAS  Google Scholar 

  • Warburg O, Burk D (1950) The maximum efficiency of photosynthesis. Arch Biochem 25:410–443

    PubMed  CAS  Google Scholar 

  • Warburg O, Krippahl G (1958) Hill-Reakionen. Z Naturforsch 13b:509–514

  • Warburg O, Negelein E (1922) Über den Energieumsatz bei der Kohlensäureassimilation. Z Phys Chem 102:235–266

    Google Scholar 

  • Warburg O, Negelein E (1923) Über den Einfluss der Wellenlänge auf den Energieumsatz bei der Kohlensäureassimilation. Z Phys Chem 106:191–218

    CAS  Google Scholar 

  • Warburg O, Burk D, Schocken V, Hendricks SB (1950) The quantum efficiency of photosynthesis. Biochim Biophys Acta 4:335–348

    PubMed  CAS  Google Scholar 

  • Warburg O, Krippahl G, Schröder W (1954) Katalytische Wirkung des blaugrünen Lichts auf den Energieumsatz bei der Photosynthese. Z Naturforsch 9b:667–675

    CAS  Google Scholar 

  • Warburg O, Krippahl G, Schröder W (1955) Wirkungsspektrum eines Photosynthese-Fermentes. Z Naturforsch 10b:631–639

    CAS  Google Scholar 

  • Warburg O, Krippahl G, Lehman A (1969) Chlorophyll catalysis and Einstein’s law of photochemical equivalence in photosynthesis. Am J Bot 56:961–971

    CAS  Google Scholar 

  • Willstätter R, Stoll A (1918) Untersuchungen über die assimilation der kohlensäure. Sieben Abhandlungen, Springer, Berlin

    Google Scholar 

  • Wydrzynski TJ, Satoh K (eds) (2005) Photosystem II—the light-driven water: plastoquinone oxidoreductase. Advances in photosynthesis and respiration, vol 22. Springer, Dordrecht

    Google Scholar 

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Acknowledgments

J. F. Hill thanks William A. Hill and Anita Baker-Blocker for invaluable comments on early drafts of this paper. J. F. Hill and Govindjee are thankful to Ekkehard Höxtermann for help with the figures and to Kärin Nickelsen, Ekkehard Höxtermann, and John F. Allen for reading and making valuable comments and suggestions on an earlier version of this Historical Corner paper. We are highly thankful to Alexendrina (Sandra) Stirbet for Figs. 1, 6, and 7, used in this paper.

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Hill, J.F., Govindjee The controversy over the minimum quantum requirement for oxygen evolution. Photosynth Res 122, 97–112 (2014). https://doi.org/10.1007/s11120-014-0014-8

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