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Light Reaction Photosyntesis PDF
Light Reaction Photosyntesis PDF
USA
Vol. 68, No. 11, pp. 2883-2892, November 1971
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 from the photodecomposition of C02 recombines with the
or CO2. ATP formation could best be accounted for not
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 of free energy which is trapped C02 + H20 (CH20) + 02 (i)
in the pyrophosphate bonds of ATP.
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 search in photosynthesis, was put forward by van Niel (8).
a light-induced electron transport from water to ferredoxin
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 hydrogen in turn reducing C02 by dark, enzymic reactions:
reaction that is independent of light. ATP, from both
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, H2A is H2S, with the results that oxygen becomes the by-
one (System II) that best uses light of "short" wavelength
(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 distinction between plant and bacterial photosynthesis
by a "dark" electron-transport chain to which is coupled
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
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
1957: NADPH2 +ATP CHLOROPLASTS
First products of photosynthesis:
1962: Fd red
experiments with isolated chloroplasts
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 of
either of the two earlier 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 mV, at pH 7). This finding was followed by several
pentose phosphate cycle), which was convincingly identified other developments which drastically altered the then preva-
with the dark phase of photosynthesis. The chief importance lent ideas about the photosynthetic capacity of isolated
of the carbon cycle to the understanding of the role of light in chloroplasts. These developments (Fig. 1) will now be dis-
photosynthesis lay in revealing which of its component en- cussed in chronological order.
zymic reactions require an input of energy-rich chemical In 1954, a reinvestigation of photosynthesis in isolated
intermediates that must be formed by the light reactions. chloroplasts by different methods yielded evidence for a
As summarized in Fig. 2, the carbon cycle shows that the con- light-dependent assimilation of C02 (ref. 33). Chloroplasts
version of 1 mole of C02 to the level of hexose phosphate re- isolated from spinach leaves assimilated 14CO2 to the level
quires 3 moles of ATP and 2 moles of reduced NADP. Accord- of carbohydrates, including starch, with a simultaneous
ingly, the need for light energy in photosynthesis by green evolution of oxygen (34, 35). When the conversion of 14CO2
plants could now be traced to those photochemical reactions by isolated chloroplasts to sugars and starch was confirmed
that generate ATP and NADPHE2. and extended in other laboratories (36-40), the capacity of
The occurrence of phosphorylated compounds among the chloroplasts to carry on complete extracellular photosyn-
early products of C02 assimilation suggested that light- thesis was no longer open to question.
induced phosphorus assimilation may, in fact, precede carbon Because of the earlier negative results, special experimental
assimilation but experimental evidence for this conclusion safeguards were deemed necessary to establish that chloro-
was lacking in whole cells. When Calvin's group investigated plasts alone, without other organelles or enzyme systems and
the photoassimilation of phosphorus by Scenedesmus cells with light as the only energy source, were capable of a total
with the aid of carrier-free KH232PO4, they found that the synthesis of carbohydrates from C02. The chloroplasts were
shortest exposure to light gave the lowest incorporation of washed and, to eliminate a possible source of chemical energy
32p into ATP and, conversely, that the highest incorporation and metabolites, their isolation was performed not as formerly
of 32p into ATP occurred on short, dark exposure (21). The * Contrary to a widely held belief, this conclusion was not un-
first compound to be labeled proved to be not the expected equivocally documented by experiments with 180 [(see A. H.
ATP but again PGA (21). Other investigations of direct Brown and A. W. Frenkel, Annu. Rev. Plant Physiol., 4, 53
photoassimilation of phosphorus by intact cells also gave (1953)].
Proc. Nat. Acad. Sci. USA 68 (1971) Light Reactions of Photosynthesis 2885
lative ideas based on model systems. The situation changed electrons from water to NADP (or to a nonphysiological
with the discovery of light-induced ATP formation. ATP electron acceptor such as ferricyanide) and a concomitant
is formed in nonphotosynthetic cells at the expense of energy evolution of oxygen. Moreover, ATP formation in this coupled
released by electron transport. The idea that ATP may also system greatly increased the rate of electron transfer from
be formed in photosynthesis through a special light-induced water to ferricyanide (63-65) or to NADP (66) and the rate
electron flow mechanism in chloroplasts now had a high proba- of the concomitant oxygen evolution. It thus became apparent
bility that could be experimentally tested. that the electron transport system of chloroplasts functions
The electron flow hypothesis (58, 59) envisaged that a more effectively when it is coupled, as it would be under
chlorophyll molecule, on absorbing a quantum of light, be- physiological conditions, to the synthesis of ATP. The con-
comes excited and promotes an electron to an outer orbital ventional Hill reaction (25, 26) now appeared to measure a
with a higher energy level. This high-energy electron is then noncoupled electron transport, severed from its normally
transferred to an adjacent electron acceptor molecule, a coupled phosphorylation (63).
catalyst (A) with a strongly electronegative oxidation-reduc- In extending the electron flow concept to this new reaction,
tion potential. The transfer of an electron from excited chloro- it was envisaged (58, 59) that a chlorophyll molecule excited
phyll to this first acceptor is the energy conversion step proper by a captured photon transfers an electron to NADP (or
and terminates the photochemical phase of the process. By to ferricyanide). It was postulated that electrons thus re-
transforming a flow of photons into a flow of electrons, it moved from chlorophyll are replaced by electrons from water
constitutes a mechanism for generating a strongly electronega- (OH-, at pH 7) with a resultant evolution of oxygen. In this
tive reductant at the expense of the excitation energy of manner, light would induce an electron flow from OH- to
chlorophyll. NADP and a coupled phosphorylation. Because of the uni-
Once the strongly electronegative reductant is formed, no directional or noncyclic nature of this electron flow, this
further input of energy is needed. Subsequent electron trans- process was named noncyclic photophosphorylation (58, 59).
fers within the chloroplast liberate energy, since they constitute
an electron flow from the electronegative reductant to elec- Role of ferredoxin
tron acceptors (thought to include chloroplast cytochromes) Further progress in elucidating the role of light in chloroplast
with more electropositive redox potentials (58, 59). Several reactions came from investigations of the mechanism of
of the exergonic electron transfer steps, particularly those NADP reduction and of the identity of the catalyst in cyclic
involving cytochromes, were thought to be coupled with photophosphorylation by chloroplasts.
phosphorylation. At the end of one cycle, the electron origi- Investigations of the mechanism of NADP reduction and
nally emitted by the excited chlorophyll molecule returns cyclic photophosphorylation in chloroplasts led to the recogni-
to the electron-deficient chlorophyll molecule and the tion of the key role of the iron-sulfur protein, ferredoxin. The
quantum absorption process is repeated. A mechanism of name ferredoxin was introduced in 1962 by Mortenson et al.
this kind would account for the observed lack of any oxida- (67) and did not, at first, concern photosynthesis. It referred
tion-reduction change in any external electron donor or ac- to a nonheme, iron-containing protein which they isolated
ceptor. Because of the envisaged cyclic pathway traversed by from Clostridium pasteurianum, an anaerobic bacterium
the emitted electron, the process was named cyclic photo- devoid of chlorophyll and normally living in the soil at a
phosphorylation (58, 59). depth to which sunlight does not penetrate. A connection
e between ferredoxin and photosynthesis was established, also
in 1962, when C. pasteurianum ferredoxin was crystallized
and found to mediate the photoreduction of NADP by spinach
chlorophyll A! cytochrome I cytochrome 2 chloroplasts (68). In this reaction, Clostridium ferredoxin
Ihv _p replaced a native chloroplast protein (known by different
names) that up to then was thought to be peculiar to photo-
A cyclic electron flow that is driven by light and that synthetic cells. Its replaceability by the bacterial ferredoxin
liberates chemical energy, used for the synthesis of the pyro- and other considerations led to renaming the chloroplast pro-
phosphate bonds of ATP, is unique to photosynthetic cells. tein ferredoxin (68). A discussion of the history of ferredoxin,
The idea has been discussed elsewhere (58, 59) that cyclic its occurrence and properties, is given elsewhere (69, 70).
photophosphorylation may be a primitive manifestation of Ferredoxin is now known to play a key role in photosyn-
photosynthetic activity-an activity that is the common thesis-a role that includes (but is not limited to) a catalytic
denominator of plant and bacterial photosynthesis. function in both cyclic and noncyclic photophosphorylation.
Ferredoxin is an electron carrier protein whose reversible
Noncyclic photophosphorylation oxidation-reduction is accompanied by characteristic changes
As already alluded to, there was at first no experimental in its absorption spectrum (Fig. 3). From the standpoint of
evidence linking photophosphorylation to the photoreduction electron transport, the most notable finding (68) was the
of NADP by chloroplasts. In fact, these two photochemical strongly electronegative oxidation-reduction potential of
activities of chloroplasts appeared to be antagonistic (62). ferredoxin, close to that of hydrogen gas (Em = -420 mV,
It was therefore wholly unexpected when a second type of at pH 7) and about 100 mV more electronegative than that
photophosphorylation was discovered in 1957 (ref. 63) that of NADP. Thus, ferredoxin (in its reduced state) emerged
provided direct experimental evidence for a coupling between as the strongest chemically defined reductant that is photo-
photoreduction of NADP and the synthesis of ATP. Here, in chemically generated by, and is isolable from, chloroplasts.
contrast to cyclic photophosphorylation, ATP formation was The existence of stronger reductants in chloroplasts has
stoichiometrically coupled with a light-driven transfer of been suggested on the basis of observations (71-73) that
Proc. Nat. Acad. Sci. USA 68 (1971) Light Reactions of Photosynthesis 2887
-0.4 -
-0.4
NADP '
-0.2 -0.2
0
0
en
0
0
+0.2
-0 +0.2
w
w
+0.4
+0.6 +0.6
+0.8L +0.8
fib
SYSTEMII SYSTEM I
(noncycl c) (cyclic)
FIG 5. Scheme for three light reactions in plant photosynthesis. Explanation in text; fp stands for ferredoxin-NADP reductase.
Discussed elsewhere (93) are the roles of Cl-,manganese, and plastoquinone (PQ) (Knaff and Arnon, ref. 96).
b559 (ref. 100). In contrast, the removal of plastocyanin had of System I. A primary electron acceptor would be expected to
no effect on the photoreduction of cytochrome b559 by Com- undergo reduction by an electron transferred solely as a result
ponent 550, nor on the photoreduction of Component 550 of photon capture at temperatures low enough to inhibit
itself by photoreaction IIb (97). These findings, buttressed chemical reactions. This expectation was fulfilled for photo-
by the observation (99, 96, 100) that cytochrome b5i9, unlike reaction IIb when the photoreduction of Component 550 was
cytochrome f, is photooxidized effectively only by System II indeed found to occur at liquid-nitrogen temperature (Fig. 6).
(short-wavelength) light, account for the proposed sequence Evidence for the photoreduction of ferredoxin at 770K was
of electron carriers in System II (Fig. 5). sought by electron paramagnetic resonance spectroscopy-a
Cytochromes b6 and f have previously been assigned to technique that, unlike absorption spectrophotometry, would
cyclic photophosphorylation (92, 93) and are now also con- permit detection of ferredoxin reduction without the inter-
sidered components of System I. The present concept places ference of chlorophyll or chloroplast cytochromes. When whole
cytochrome f and P700 in System I and, in contrast to the spinach chloroplasts were illuminated at 770K from 10 to 50
older hypothesis, predicts that neither would be required for
the photoreduction of ferredoxin-NADP by water via System
II. [P700 represents a small component part of the total
chlorophyll a and has in situ an absorption peak at 700 nm;
P700 is considered to act as the terminal trap for the light s ASPINA H
k.) ,6
S0
0)
k 4
3
v
1
w
--"" 19~~~ 2
550 600 650 700 730 550 600 650 700 730
wavelength (nm)
FIG. 8. Quantum requirements of light-induced electron
transport by System II (H20NADP) and System I (DPIPH2
- NADP) in monochromatic light of different wavelengths.
3200 3300 34
(Data of B. D. McSwain.)
Magnetic field (gauss)
FIG. 7. Low-temperature light-induced EPR signals in spinach one photoact in System I, its light-induced electron transport
chloroplasts. Illumination: 770K; EPR: 250K (Malkin and would have a theoretical quantum requirement of one quan-
Bearden, ref. 121). tum per electron.
Fig. 8 shows experimental measurements close to two quanta
min and examined by EPR spectroscopy at 250K, light-in- per electron for System II and one quantum per electron for
duced changes in the EPR spectrum were observed (121). System I. The quantum requirement measurements in Fig. 8
Fig. 7 shows the EPR spectrum of chloroplasts in the dark demonstrate again the contrasting responses of Systems II and
and when illuminated for 20 min at 770K. Illumination in- I to monochromatic light: increasing quantum efficiency for
duced increased EPR absorption at g-values of 1.86, 1.94, and System II and decreasing quantum efficiency for System I at
2.05. No other light-induced absorptions were detected when the shorter wavelengths and a reverse situation at the longer
the scanning range was widened to include g-values from 1.5 wavelengths. Similar results, despite many variations in condi-
to 6. The large (off-scale) signal- in the g = 2.00 region, which tions and experimental design, have been obtained by other
occurred in both the light and dark samples, was due to free investigators (123-129).
radicals (not associated with ferredoxin) previously observed Since the assimilation of one molecule of CO2 to the level of
in photosynthetic systems by the EPR technique (122). hexose via the reductive pentose phosphate cycle requires two
It appears that the light-induced EPR spectrum of chloro- molecules of NADPH2 and three molecules of ATP (Fig. 2), it
plasts was produced by a bound type of plant ferredoxin differ- becomes possible to arrive at the maximum theoretical quan-
ent from the soluble ferredoxin contained in whole chloroplasts. tum efficiency of photosynthesis from measurements of the
Illumination at 770K of broken chloroplasts, prepared by respective quantum efficiencies for cyclic and noncyclic elec-
osmotically disrupting whole chloroplasts and washing to re- tron transport. A requirement of two quanta per electron for
move any remaining soluble ferredoxin, gave an EPR spectrum System II means that eight quanta would be required to
similar to that observed with whole chloroplasts (121). The produce two NADPH2 and two ATP (accompanied by evolu-
absence of soluble ferredoxin in this chloroplast preparation tion of one 02) via noncyclic photophosphorylation. Two addi-
was evidenced by its inability (without added ferredoxin) to tional quanta assigned to generate one ATP via cyclic photo-
reduce NADP photochemically with either water or reduced phosphorylation would give a total requirement of about ten
dye as the hydrogen donor. quanta per molecule of CO2 assimilated or 02 liberated-a
value in good agreement with measurements of the overall
Quantum efficiency of photosynthesis quantum efficiency of photosynthesis in intact cells.
Few questions in photosynthesis have received more intensive
theoretical and experimental study and led to more contro- The experimental work from the author's laboratory cited
herein was supported, in part, by National Science Foundation
versy than the efficiency of the quantum conversion process. Grant GB-23796.
The extensive literature on this subject, which is beyond the
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(V. Nyon, Paris, 1804).
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