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The Light Reactions of Photosynthesis

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The Light Reactions of Photosynthesis Proc. Nat. Acad. Sci. USA Vol. 68, No. 11, pp. 2883-2892, November 1971 The Light Reactions of Photosynthesis DANIEL I. ARNON Department of Cell Physiology, University of California, Berkeley, Berkeley, Calif. 94720 ABSTRACT Historically, the role of light in photo- (4) and Willsttfiter (5); its last great contemporary protago- svnthesis has been ascribed either to a photolysis of carbon nist was Otto Warburg (6). After de Saussure (7) showed that dioxide or to a photolysis of water and a resultant rear- rangement of constituent atoms into molecules of oxy- water is a reactant in photosynthesis, the C02 cleavage hy- gen and glucose (or formaldehyde). The discovery of photo- pothesis readily accounted for the deceptively simple overall phosphorylation demonstrated that photosynthesis in- photosynthesis equation (Eq. i): the C: 2H: 0 proportions cludes a light-induced phosphorus metabolism that in the carbohydrate product fitted the idea that the carbon precedes, and is independent from, a photolysis of water recombines with the or CO2. ATP formation could best be accounted for not from the photodecomposition of C02 by a photolytic disruption of the covalent bonds in C02 elements of water. or water but by the operation of a light-induced electron h 0 2 flow that results in a release offree energy which is trapped C02 + H20 + 02 (i) in the pyrophosphate bonds of ATP. (CH20) Photophosphorylation is now divided into (a) a non- A different hypothesis,, one that profoundly influenced re- cyclic type, in which the formation of ATP is coupled with in was forward van Niel a light-induced electron transport from water to ferredoxin search photosynthesis, put by (8). and a concomitant evolution of oxygen and (b) a cyclic After elucidating the nature of bacterial photosynthesis, he type which yields only ATP and produces no net change in proposed (8) that bacterial and plant photosynthesis are the oxidation-reduction state of any electron donor or special cases of a general process in which light energy is used acceptor. Reduced ferredoxin formed in (a) serves as an to photodecompose a hydrogen donor, H2A, with the released electron donor for the reduction of NADP by an enzymic reaction that is independent of light. ATP, from both hydrogen in turn reducing C02 by dark, enzymic reactions: cyclic and noncyclic photophosphorylation, and reduced hp NADP jointly constitute the assimilatory power for the C02 + 2H2A -- (CH20) + H20 + 2A (ii) conversion of C02 to carbohydrates (3 moles of ATP and 2 moles of reduced NADP are required per mole of C02). The hypothesis envisaged that in plant photosynthesis Investigations, mainly with whole cells, have shown that H2A is water, whereas in green sulfur bacteria (for example) photosynthesis in green plants involves two photosystems, with the results that becomes the one (System II) that best uses light of "short" wavelength H2A is H2S, oxygen by- (X < 685 nm) and another (System I) that best uses product of plant photosynthesis and elemental sulfur the light of "long" wavelength (X > 685 nm). Cyclic photo- by-product of bacterial photosynthesis. phosphorylation in chloroplasts involves a System I In later formulations (9, 10) van Niel no longer considered photoreaction. Noncyclic photophosphorylation is widely the photodecomposition of water as being unique to plant held to involve a collaboration of two photoreactions: a short-wavelength photoreaction belonging to System II photosynthesis but postulated that "the photochemical reac- and a long-wavelength photoreaction belonging to System tion in the photosynthetic process of green bacteria, purple I. Recent findings, however, indicate that noncyclic photo- bacteria, and green plants represents, in all cases, a photo- phosphorylation may include two short-wavelength, Sys- decomposition of water" (10). According to this concept, the tem II, photoreactions that operate in series and are joined by a "dark" electron-transport chain to which is coupled distinction between plant and bacterial photosynthesis a phosphorylation site. turned on the events that followed the photodecomposition of water into H and OH. H was used for C02 reduction and OH formed a complex with an appropriate acceptor. In plant Early concepts photosynthesis, the acceptor was regenerated when the com- The first hypothesis about the role of light in photosynthesis plex was decomposed by liberating molecular oxygen. In came very appropriately from Jan Ingenhousz, who some bacterial photosynthesis, oxygen was not liberated and the years earlier had made the epochal discovery that it is "the acceptor could be regenerated only when the OH-acceptor influence of the light of the sun upon the plant" (1) that is complex was reduced by the special hydrogen donor, H2A, responsible for the "restorative" effect of vegetation on that is always required in bacterial photosynthesis. "bad" air-an observation first made in 1771 by Joseph The concept of photodecomposition of C02 or photodecom- Priestley without reference to light (2). In 1796, Ingenhousz position of water provided, each in its own historical wrote that the green plant absorbs from "carbonic acid in period, a broad, general perspective on the role of light in the the sunshine, the carbon, throwing out at that time the oxygen overall events of photosynthesis. In the last two decades, alone, and keeping the carbon to itself as nourishment" (3). however, the focus in photosynthesis research shifted toward The idea that light liberates oxygen by photodecomposing the isolation, identification, and characterization of the C02 had, with some modifications, persisted for well over a specific reactions and mechanisms by which light energy century. It seemed to have had a special attraction for some drives the photosynthetic process. This approach has led to of the most illustrious chemists in their day, e.g., von Baeyer new perspectives on the mechanisms by which light energy is 2883 Downloaded by guest on September 26, 2021 2884 Amnon Proc. Nat. Acad. Sci. USA 68 (1971) EXPERIMENTALLY IDENTIFIED FIRST results that were at best suggestive [see review (22)1. In PRODUCTS OF PHOTOSYNTHESIS short, experiments with whole cells proved, for reasons dis- I1862: STARCHWHL cussed below, incapable of yielding evidence for an indepen- 11883: SUCROSE, GLUCOSE CELLS dent light-induced phosphorus metabolism. Its occurrence in photosynthesis was discovered not in whole cells but in 1951: NADPH2 isolated chloroplasts. 1954: AT P First products of photosynthesis: 1957: NADPH2 +ATP CHLOROPLASTS experiments with isolated chloroplasts 1962: Fd red 1964: Fd red + AT P Chloroplasts were once widely believed to be the site of com- plete photosynthesis but this view was not supported by FIG. 1. critical evidence (23, 24) and was largely abandoned after Hill (25, 26) demonstrated that isolated chloroplasts could used in photosynthesis and to a finding, inadmissible under evolve oxygen but could not assimilate C02. [The failure either of the two earlier of hypotheses, that the photosynthetic isolated chloroplasts to fix C02 was also reported with the apparatus can convert light energy into a stable form of sensitive 14CO2 technique (27).] In the oxygen-producing reac- chemical energy, independently of the splitting of either water tion, which became known as the Hill reaction, isolated or C02. chloroplasts evolved oxygen only in the presence of artificial First products of photosynthesis: oxidants with distinctly positive oxidation-reduction poten- experiments with whole cells tials, e.g., ferric oxalate, ferricyanide, benzoquinone. In chemical terms, an insight into the role of light in photo- The Hill reaction established that the photoproduction of synthesis could come from identification of the first chemically oxygen by chloroplasts is basically independent of C02 as- defined products that are formed under the influence of light. similation. This provided strong support for the view that the In the 19th century (Fig. 1) this approach established that source of photosynthetic oxygen is water.* Left in doubt was starch is the first product of photosynthesis in chloroplasts the role of chloroplasts in the energy-storing reactions needed (11)-a conclusion that was later revised in favor of soluble for C02 assimilation. The photochemical generation by iso- carbohydrates (ref. 12). In the modern period, the powerful lated chloroplasts of a strong reductant capable of reducing new techniques of 14C (ref. 13), paper chromatography (14), C02 was deemed unlikely on experimental and theoretical and radioautography (15) aided in the identification of phos- grounds (26, 28). The first experiments with the sensitive 82p phoglyceric acid (PGA) as the first stable product of photo- technique to test the ability of isolated chloroplasts to form synthesis, formed only after a few seconds of illumination ATP, on illumination, also gave negative results (29). (16). Aside from PGA, phosphate esters of two sugars, ribulose A different perspective on the photosynthetic capacity and sedoheptulose, were soon added to the list of early prod- of isolated chloroplasts began to emerge in 1951 when three ucts of photosynthesis in green cells (17, 18). laboratories (30-32), independently and simultaneously, The discovery of PGA and other early intermediates of found that isolated chloroplasts could photoreduce NADP C02 assimilation led Calvin and his associates (19, 20) to the despite its strongly electronegative redox potential (Em = formulation of a photosynthetic carbon cycle (reductive -320
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