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Evolution of the Z-scheme of photosynthesis: a perspective

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Abstract

The concept of the Z-scheme of oxygenic photosynthesis is in all the textbooks. However, its evolution is not. We focus here mainly on some of the history of its biophysical aspects. We have arbitrarily divided here the 1941–2016 period into three sub-periods: (a) Origin of the concept of two light reactions: first hinted at, in 1941, by James Franck and Karl Herzfeld; described and explained, in 1945, by Eugene Rabinowitch; and a clear hypothesis, given in 1956 by Rabinowitch, of the then available cytochrome experiments: one light oxidizing it and another reducing it; (b) Experimental discovery of the two light reactions and two pigment systems and the Z-scheme of photosynthesis: Robert Emerson’s discovery, in 1957, of enhancement in photosynthesis when two light beams (one in the far-red region, and the other of shorter wavelengths) are given together than when given separately; and the 1960 scheme of Robin Hill & Fay Bendall; and (c) Evolution of the many versions of the Z-Scheme: Louis Duysens and Jan Amesz’s 1961 experiments on oxidation and reduction of cytochrome f by two different wavelengths of light, followed by the work of many others for more than 50 years.

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(modified from Fig. 2 in Demeter and Govindjee 1989)

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Acknowledgements

We are highly indebted to Robert Blankenship, Wim Vermaas, John Raven, and four reviewers of this manuscript, who helped us improve the presentation of this historical educational paper. We thank P. Lester Dutton for looking at our Fig. 6 and for bringing to our attention reviews on the primary photochemistry of photosynthesis. Govindjee thanks Rajni Govindjee for her support during the preparation of this paper; he is grateful to the excellent staff of the offices of Information Technology (Life Sciences), Plant Biology, Biochemistry, and Biophysics & Quantitative Biology of the University of Illinois at Urbana-Champaign for their cooperation and help in all what he does. The proofs were corrected on January 14, 2017, when Govindjee was visiting the laboratories of Ashwani Pareek and Baishnab Tripathy at Jawaharlal Nehru University, New Delhi, India.

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Authors and Affiliations

  1. Department of Plant Biology, Department of Biochemistry, and Center of Biophysics & Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Govindjee

  2. Department of Chemistry, Chemical Biological Centre, Umeå University, 90187, Umeå, Sweden

    Dmitriy Shevela

  3. Department of Biology, Molecular Cell Biology, Lund University, Sölvegatan 35, 22362, Lund, Sweden

    Lars Olof Björn

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  1. Govindjee
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  2. Dmitriy Shevela
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  3. Lars Olof Björn
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Correspondence to Govindjee.

Additional information

Submitted for publication in honor of Nathan Nelson, a world leader in the field of photosynthesis, and of T. Nejat Veziroglou, a world leader in the field of hydrogen evolution (see Tsygankov et al. 2016; also see pdfs at http://www.life.illinois.edu/govindjee/honorsfrom.html).

John Raven sent the following comment on this paper: “The history of the concept of the ‘Z scheme’ analysed in this manuscript by Govindjee and colleagues is timely and accurate. The sequence of publications cited, and the discussion of these publications, show how theoretical and experimental work led to our present concept of linear electron transport in oxygenic photosynthesis”.

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Appendix

Appendix

The following example shows that science is a self-correcting enterprise, no matter who the authors are, and that even the top scientists make mistakes. James Franck, together with Gustav Ludwig Hertz, received the 1925 Nobel Prize in Physics in 1926 for “for their discovery of the laws governing the impact of an electron upon an atom”. Later, he became known for the “Franck–Condon Principle”, which states that upon light absorption, a molecule goes into an excited state, but in a higher vibrational state. (See Rice and Jortner (2010) for all the major contributions, and life, of Franck.) Franck contributed extensively to photosynthesis (see Rosenberg 2004; also see Franck and Rosenberg 1964). Unfortunately, some of his thoughts, which may have been physically sound, turned out to be incorrect. Examples are: instead of using realistic 3-dimensional structure of the “antenna”, Franck and Teller (1938) calculated excitation energy transfer as if the pigments were located in one dimension; with these results, they challenged the concept of “photosynthetic unit”, but when two-dimensional and multidimensional approaches were used, their conclusions could not be accepted (see e.g., Bay and Pearlstein 1963; Robinson 1967). In the same manner, explanation by Franck (1958) of the “red drop” (Emerson and Lewis 1943) and the Emerson Enhancement Effect (Emerson et al. 1957), by double excitation (“up-conversion”) of the same chlorophyll a molecules was also incorrect.

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Govindjee, Shevela, D. & Björn, L.O. Evolution of the Z-scheme of photosynthesis: a perspective. Photosynth Res 133, 5–15 (2017). https://doi.org/10.1007/s11120-016-0333-z

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