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1978. 7:393-434

Annu. Rev. Biophys. Bioeng. 1978.7:393-434. Downloaded from www.annualreviews.org by University of Tennessee - Knoxville - Hodges Library on 04/09/13. For personal use only.

CHLOROPHYLL FUNCTION IN THE PHOTOSYNTHETIC

.9118

REACTION CENTER 1.2 Joseph J. Katz, James R. Norris, Lester L. Shipman, Marion C. Thurnauer, and Michael R. Wasielewski Chemistry Division, Argonne National Laboratory, Argonne, Illinois 60439

INTRODUCTION The chlorophylls are a small group of compounds with closely related structures that are universally acknowledged to be the indispensible photoreceptors in plant and bacterial photosynthesis. Photosynthesis is the process whereby the energy of sunlight is converted to chemical oxidizing and reducing capacity, which can then be used to drive chemical oxidation-reduction reactions that would otherwise not proceed spontaneously. Only organisms that contain chlorophyll are able to carry out photosynthesis as we define it here, and no organism that lacks chlorophyll is known to do so. The chlorophylls are intimately involved in all aspects of the primary events of photosynthesis: light harvesting, energy transfer, and light energy conversion. In

1932,

it was recognized by Emerson & Arnold

(48, 49)

that chloro­

phyll function in photosynthesis is a cooperative phenomenon that requires the participation of many chlorophyll molecules to effect conversion of a single photon. The great majority of the chlorophyll molecules in the photosynthetic apparatus constitute a light-harvesting apparatus that acts as the initial photoreceptor. Elec­ tronic excitation energy that results from absorption of a photon is then transferred by the light-harvesting or antenna chlorophyll to a small number of chlorophyll molecules in a photoreaction center

(46,47,96,97), where the electronic excitation

energy is trapped and converted to an electron (reducing capacity) and a positive hole (oxidizing capacity). The antenna and photoreaction center, together with auxiliary pigments and electron transport chains, constitute a photosynthetic unit 1.2 The Argonne work described in this paper was carried out under the auspices of the Division of Basic Energy Sciences of the U.S. Department of Energy. 2 The U.S. Government has the right to retain a nonexclusive, royalty-free license in and to any copyright covering this article.

393 0084-6589/78/0615-0393$1.00

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394

KATZ ET AL

(PSU). Much of the research in photosynthesis since then has been an effort to establish the details of the structure and function of the antenna and photoreaction­ center chlorophylls in the PSU. In green plants, the electrons used for carbon dioxide reduction originate in water. The transfer of electrons from water (oxidation) forms molecular oxygen, and all organisms, without exception, that produce oxygen by photosynthesis con­ tain chlorophyll a (Chla) (Figure 1). Antenna Chla in the photosynthetic apparatus of oxygen-producing organisms is accompanied by auxiliary light-harvesting pig­ ments, e.g. chlorophyll b in higher green plants and green algae (123), phycobilins ( 1 1 7) in blue-green algae, chlorophylls CI and Cz (141) in diatoms and many marine algae, and carotenoids and xanthophylls (99) that are present in all (wild type) photosynthetic organisms. With the possible exception of chlorophyll b, which may also be implicated in photoreaction-center activity that leads to the oxidation of water in green plants, all of the auxiliary photosynthetic pigments appear to be primarily involved in light-harvesting and subsequent energy transfer from the antenna to the photoreaction center and are only indirectly involved in the charge separation step. It is generally accepted that green plant photosynthesis involves two different photoreaction centers: (a) Photosystem I (pS I) reaction centers that are the primary source of electrons for the reduction of carbon dioxide; and (b) Photosystem II (PS II) reaction centers (10, 1 24) that generate the oxidation power required for the abstraction of electrons from water. PS I and II are considered to act in series in the familiar two photosystem Z scheme (10). Associated with the photo-

30 CH3

4bCH3

4bCH

I

CH2 40

/

3

CHz 40

H

2

H

50

CH3

0

C-phy 2

phy= Figure 1

C-phyl!C-phy3

-�Hz,, ITII>' and 17;,>. which correspond to the interaction of the electrons along the three magnetic axes x. y, and z. In the high magnetic field of an EPR experiment (-3500 G). the spins are aligned along the external magnetic field, and the eigen-functions of the triplet spin states are given by IT+I>. ITo>. and IT-I>' These can be related to those at zero field by mixing coefficients that depend on the strength and direction of the magnetic field. For instance, when a

422

KATZ ET AL

molecule in the triplet state is placed in a magnetic field such that a spin axis, say

z,

is aligned along the field, then the other two levels (in this case

are mixed by the field, and these two energy levels are split giving

IT_ I > The energy of the IT..> level (in this case) remains r I To> level. The same pattern occurs when each of the other

x

and

I T+I>

y)

and

constant giving the two triplet

axes are

Annu. Rev. Biophys. Bioeng. 1978.7:393-434. Downloaded from www.annualreviews.org by University of Tennessee - Knoxville - Hodges Library on 04/09/13. For personal use only.

oriented along the applied magnetic field. Each orientation gives a set of two

A B

I I

; Zi i J101+31EI I­ �-----'2 IDI \IOI -3 IEI I I

I I

I

ZI Xn

'fn

YI

2

I

XiI Zn

Figure 1 4 Triplet EPR Spectra. (A) EPR spectrum o f a randomly oriented triplet system.

The spectrum is displayed in absorption mode. This is the intensity pattern expected for a triplet with a normal Boltzmann distribution of spin populations of the three triplet energy levels. (B) Derivative of the absorption mode presented in (A). This is the usual presentation of triplet EPR spectra. (C) Absorption mode triplet EPR spectrum observed in the bacteria

Rhodospirillum rubrum. (D) Triplet EPR spectrum (derivative of the absorption mode) ob­ R. rubrum. The ZFS parameters D and E can be taken directly from the spectrum.

served in

The labeling at the bottom corresponds to the transitions observed for a given triplet axis along the magnetic field. a, Absorption; e, emission.

CHLOROPHYLL IN PHOTOSYNTHESIS

EPR I::J. m

transitions (one from

=

I T-I> to I To> and one from �I> to I To»

423

known as

± l transitions. A typical spectrum is shown in Figure l 4B. The peaks are

labeled to show how each set of two transitions corresponds to a given orientation along the magnetic field. The zero field splitting (ZFS) of the triplet state is characterized by the two

ZFS parameters D and E. D gives a measure of the average distance between

the two unpaired electrons. As D increases, the electrons in a triplet are on the

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average closer together. E gives a measure of the deviation of a molecule from axial symmetry. Thus, the relative magnitudes of D and E provide a means to

study molecular structural properties. As can be seen in Figure 14, these parameters

can be taken directly from a triplet

EPR

spectrum.

To deduce information from the triplet state that can be generated in bacterial reaction centers, it is necessary to understand the magnetic properties of the triplet state of the pure chlorophylls as observed in vitro in solution. Several workers have recently undertaken such studies by both

149)

and optically detected magnetic resonance

EPR spectroscopy (68, 94, 101, (27, 28). The two properties of

interest are the ZFS parameters and the kinetics of populating and depopulating of the triplet state. There has been reasonable agreement (with minor variatibns because of solvent effects) between the various groups with respect to the magni­ tudes of the ZFS of the various chlorophyUs. ZFS parameters for a number of in vitro chlorophylls and in vivo systems are given in Table

3.

In general, the

ZFS are fairly small for the chlorophylls, which reflects the substantial extent of

electron delocalization in these large macrocycles. The BChia triplet in intact

Rhodospirillum rubrum and Rhodopseudomonas spheroides cell have an even smaller D value than any of the in vitro chlorophyll systems (Table

the decrease in D in the in vivo systems is only

20%,

3).

Although

it nevertheless is a reduction

sufficiently large to preclude the possibility that a single BChia could be the site

of the triplet. Delocalization of the triplet over more than one BChia macmcycJe is indicated by the sign and magnitUde of the ZFS, and it is plausible that in this triplet state the excitation energy is shared between the two molecules of the BChlsp and probably has at least some charge-transfer character. The second important source of information deducible from triplet spectra is the kinetics of the population and depopulation of the triplet states. A major

Table 3

ZFS parameters for in vitro and in vivo triplet states

Species Chla Pheophytin a Chl b

Pheophytin b BChia Bpheoa Rhodospiril/ium rubrum cells Rhodopseudomonas spheroides cells

I D I (cm-I)

I E I (cm-I)

0.0273 0.0342 0.0293 0.0347 0.0224 0.0259

0.0040 0.0033 0.0052 0.0038 0.0053 0.0046

0.0185

0.0033

0.0182

0.0035

424

KATZ ET AL

Annu. Rev. Biophys. Bioeng. 1978.7:393-434. Downloaded from www.annualreviews.org by University of Tennessee - Knoxville - Hodges Library on 04/09/13. For personal use only.

difference is observed between the population kinetics of in vitro monomeric chloro­ phyll and in vivo bacterial reaction-center bacterio-chlorophyll. All chlorophyll triplet EPR spectra show electron spin polarization. i.e. a non-Boltzmann distri­ bution of populations of the triplet levels. which arises from unequal rates of population and depopulation of the triplet state (Figure 1 5). Although all chloro-

W

I

W2 (1+ o )

I

IX >

Wj WI (1+ 0 )

;\ �\ K\

W3(l+2o)

IY,

W2

II)

S

o

Figure 15

Intersystem crossing in SI

+

To. After a molecule is excited from So to SI. the

rates of intersystem crossing (Pr• py• and p.) to the three energy levels of TI are unequal. The rates of depopulation and

(kx,

(x, y,

and

kyo k.) are likewise unequal. The rates WI.

z)

Wz.

WJ are the spin lattice relaxation times. All these processes contribute to the non-Boltzman

distribution of populations observed in the triplet state of the cWorophylls.

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CHLOROPHYLL IN PHOTOSYNTHESIS

425

phyll triplet EPR spectra show this feature, the polarization of the in vivo triplet spectra differs in a very important respect from the polarization observed in in vitro chlorophyll triplets and, indeed, is unique in that invariably it is only the middle of the three Zeeman levels that has excess spin population. In all other known triplet states that have been studied by EPR, the middle energy level may have a smaller spin population than either the upper or lower triplet sublevels. In the in vivo triplet, it is the middle To level that is overpopulated for all orienta­ tions of the triplet in the magnetic field, which gives rise to an EPR triplet spectrum with unusual polarization (Figure 14B). Such a population pattern cannot be ob­ tained by the usual spin orbit-induced inter-system crossing mechanism. In fact, it must involve more than one molecule. Thus, in principle a study of the unique features of the population-depopulation kinetics of the in vivo triplet state can provide important clues on BChlsp structure and function. An interpretation of the unusual spin polarization of in vivo bacterial triplets in terms of a radical pair intermediate is consistent with the available data. But before the mechanistic aspects of BChlsp are addressed, some general comments on the possible roles of chlorophyll triplets in normal photosynthesis may be useful.

Chlorophyll Triplet States in Normal Photosynthesis Because so much of the photochemistry of organic molecules involves excited triplet states (I SS), many investigators have considered possible roles for chloro­ phyll triplets in photosynthesis (1 54). Various photochemical reactions of chloro­ phyll in vitro clearly involve the monomeric triplet state ( 1 32). Establishing a role for triplet chlorophyll in normal in vivo photosynthesis, however, has not been successful. There are a number of considerations that make triplet chlorophyll participation in photosynthesis unlikely. (a) Although monomeric Chla.L1 absorbs at "'665 nm, Chla (presumably in monomeric form) phosphoresces at 950 nm ( 105). Thus, intersystem crossing from 81 to the lowest energy triplet state in Chla results in a loss of about 30% of the energy of the first excited singlet. In BChla, it has been estimated that 3BChia has between 0.7 to 0.5 the energy of the first excited singlet (J. Connolly, personal communication). Large energy losses cannot be avoided if passage through the chlorophyll triplet state in photosynthesis is obligatory. (b) All (wild type) photosynthetic organisms contain carotenoids. Although the energy of the first excited singlet state is higher than that of the first excited Chla"L1 state, the energy of the carotenoid triplet is lower than that of triplet chlorophyll. Thus, light absorbed by �-carotene in green plants can be efficiently transferred to Chla, but any Chla triplet would immediately transfer its excitation energy to /3-carotene. This in fact is the basis for the widely held view that carotenoid function in the photosynthetic apparatus is to prevent the formation of long-lived excited chlorophyll states (99, 126). To our knowledge, no triplet chlorophyll signal has ever been detected by EPR in a green plant in the course of normal photosynthesis, nor in photosynthetic bacteria or reaction­ center preparations except under conditions where the normal pathway for photo­ synthetic electron transfer is blocked. Blankenship et al (12, 140) and McIntosh & Bolton (109), however, have carried out time-resolved EPR experiments that have led them to conclude that a triplet state may be on the main pathway of

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426

KATZ ET AL

normal photosynthesis. In our opinion, a radical pair mechanism may be a more satisfactory interpretation (see below). Recently a mechanism for photosynthesis has been proposed on theoretical grounds that makes participation of triplet Chl.p obligatory on the normal pathway of photosynthesis (59-61). This is a singlet-triplet (Sl-T1) anihilation scheme and goes by the name of upconversion. Upconversion essentially is an hypothesis for Chl.p function. In the upconversion hypothesis, the Chl.p is excited to the first excited singlet state, *Chl.p, which undergoes intersystem crossing to 3Chlspo From symmetry considerations, Fong (59-61) concluded that the 3Chlsp state would be split into a short-lived symmetric and a long-lived antisymmetric state. The postulated long-lived antisymmetric triplet state (with a postulated lifetime of sec­ onds to days) lives sufficiently long to receive another photon, which by anihilation of the triplet raises the BChl.p to a higher, excited charge-transfer state from which electron transfer occurs. Subsequent to electron transfer, a dark process restores the long-lived metastable triplet special pair and the cycle is repeated. The theoretical basis for upconversion has a number of serious problems. (a) In the deduction of the existence of a long-lived triplet state for a Chl.p with C2 symmetry, Fong used an inappropriate (atomic) Hamiltonian. This Hamiltonian is valid for isolated atoms, but not for molecules in a condensed phase and thus it cannot be used to draw conclusions about Chl.p in the photosynthetic apparatus at room temperature. If the appropriate Hamiltonian is used, then it can be shown rigorously ( 1 8) that a chlorophyll special pair triplet cannot have a lifetime longer than that of the monomers from which it is constituted, i.e. in the low milli­ second range at the most. Thus no theoretical basis for the prediction of a long­ lived triplet Chl.p state exists. (b) The argument from C2 symmetry in the Chl.p is that an anti-symmetric lowest triplet exciton state is produced from which radia­ tionless transitions to the ground state are both spin and symmetry forbidden, and so a Chl.p sufficiently long-lived to be upconverted by singlet excitation from the antenna persists. This conclusion disregards the well-known fact that the first­ order splittings between triplet states that are degenerate at zero order are generally quite small compared to kT at room temperature. We consider it unreasonable to expect that coherence between very weakly coupled triplet excitations on the two molecules can be maintained for times sufficiently long to permit upconversion from a coherent antisymmetric triplet exciton state. The coherence should be quickly broken by the intermolecular collisions that occur in a condensed phase on a very short time scale, and as soon as coherence is broken, radiationless processes are no longer prevented from returning the triplet to the ground state (134) (c) Warden (1 56) has carried out experiments designed to detect the presence of a long-lived Chl.p triplet with results that do not support its presence in green plants. By using very weak light (there are 1()4 ChI.p present for each photon absorbed) and a series of nonsaturating, 200-nsec light flashes (-620 nm), it was found that the first flash is sufficient to form Chls,,t. The experiment revealed no evidence for upconversion and does not support the upconversion hypothesis that photooxidation of the reaction center should occur only after the second flash. (d) Menzel (1 10) has shown that the steady-state rate equations used by Fong

CHLOROPHYLL IN PHOTOSYNTHESIS in the early version of the upconversion hypothesis

(60)

427

lead to predictions on

the relationship between light flux intensity and fluorescence yield in disagreement with experiment.

(e) Upconversion in its latest form (62) requires that the quantum

requirement for O2 evolution in green plant photosynthesis should have a minimum value of

12

to

16

quanta. The experimentally determined minimum quantum re­

quirement for O2 production is

8

quanta/02, and a value of

10

quanta/02 is

observed under circumstances where cyclic phosphorylation occurs in vivo. Reliable experimental determinations of the quantum requirements for P700 or P870 oxida­

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tion and for oxygen evolution disagree with the requirements of Fong's version of upconversion

(157, 1 63).

In our judgement, there is little or no support at this

time for the view that chlorophyll triplets are involved in the main pathway of normal forward photosynthesis.

Radical Pair Mechanism for Triplet Formation When the primary electron acceptor (i.e. an Fe-ubiquinone complex) in bacterial reaction centers is chemically reduced, exciting the primary donor in the reaction

center (Le. BChl.p indicated schematically in the present discussion as [BB)) trans­ fers an electron to the so-called preprimary electron acceptor, probably bacterio­

pheophytin (BPheo). The electron is captured by BPheo to form BPheo-. With normal continued electron transfer impossible, the electron returns to the original BChlspo Return of the electron to the special pair forms a triplet state of the special pair forms, which is observable by EPR. Only the To (BChlsp) sublevel is populated to any great extent, thereby leaving the T+ 1 and T-l sublevels of 3BChl.p essentially unpopulated. This unusual population pattern has been inter­ preted by a simple dynamical model called the radical pair mechanism

(147).

We start with a reaction center in which the special pair [BB] is in its lowest singlet state and the primary acceptor (X) is reduced. Excitation raises the special pair to its lowest excited singlet state. The first step is the transfer of an electron 1 from * [BB] to P (the preprimary acceptor bacteriopheophytin (5 1), which creates a singlet radical pair state in which one unpaired electron is on the special pair and the other is on P-. Initially the spins are antiparallel [Le. a singlet state,

Sl(RP)]. The radical pair also has a triplet state (parallel spins) with the three triplet-spin sublevels, which at high magnetic field are the spin quantized states To(RP), T+(RP), and T_(RP). Because the two unpaired spins in the radical pair are well separated, the Sl(RP) and To(RP) are essentially degenerate in energy,

whereas the T-(RP) and T+(RP) are lower and higher in energy, respectively. Under the conditions of high magnetic field and spin separation, small local mag­ netic inhomogeneities bring about a mixing of the To(RP), T+l(RP), T-1(RP), and Sl(RP) states. The extent of mixing is much greater between To(RP) and Sl(RP) states than between the other triplet states and Sl(RP) because To(RP) and Sl(RP) are essentially degenerate in energy. In dynamic terms, the spin on the special pair and the spin on the bacteriopheophytin are precessing at different frequencies about the applied magnetic field because of local differences in their magnetic environments. This difference in spin precessional frequency takes the description of the radical pair state between the Sl(RP) and To(RP) descriptions.

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428

KATZ ET AL

Before sufficient time has passed for the T+1(RP) and T-l(RP) states to become populated to any considerable extent :by way of out-of-resonance mixing with the other levels, back transfer of the electron occurs via the To{RP) - To(BChlsp) path to form the observed To(BChls�) state, which leaves the T+l and T-l levels of the special pair essentially unpopulated. This sequence of events is summarized in Scheme 1 . The symbols [BB] stand for the BChl.p, P stands for the preprimary electron acceptor, probably bacterio­ pheophytin, and X- stands for reduced ubiquinone-Fe complex. as, f3T, and 'YeT are coefficients for the fraction of singlet, triplet, and charge transfer character, respectively. The triplet observed by EPR arises from structure IV. This structure implies a triplet excitation shared between the two molecules of the BChl.p and some percentage of charge transfer character. However, other workers ( 1 1 1) believe that the observed triplet is a biradical state (BChl+-BChl-) and therefore has 100% charge transfer character. Formated via a radical pair precursor with the predominant intersystem crossing populating the To level, a species such as IV accounts for the unusual spin polarization of the EPR triplet spectra. Thus, the properties of the triplet state provide information about its radical pair precursor that cannot be observed directly by EPR. Furthermore, in principle the triplet state kinetic data can provide structural information about the special pair (22-24, 7 1 , 146). but the present data on population and depopulation is still too tentative to permit firm structural conclusions to be drawn. Recent experiments on the magnetic field dependence on the yield of the triplet state in bacteria support the radical pair nature of an intermediate state which leads to its formation (13, 74). On the other hand, it is not clear whether or not this mechanism is supported by magnetic field effects on fluorescence in these systems (26). Nanosecond and picosecond spectroscopy are complementary to the magnetic resonance studies of the triplet state in these systems, since these techniques allow workers to look directly at the optical transients associated with the primary events in bacterial photosynthesis. Parson et al (121) measured the optical absorption changes after flash excitation in reaction centers in which the electron acceptor is reduced. Two transient species were observed. One called pF appears in less than 10 psec after flash excitation and decays in nanoseconds with the formation

I

([BBj PX-)

lhv

II

l*([BBj PX-)

III

[as l([BBj+P-X-) + {3T 3([BBj+P-X-)]

IV

1

!

[( 1 - 'YCT, - 'YCT.) (P*BBjPX- + [B3*BjPX-) + 'YCT,([BB]+P-X-) + 'YCT.([B+B-jPX-)j SCHEME 1

CHLOROPHYLL IN PHOTOSYNTHESIS

429

I

II

Annu. Rev. Biophys. Bioeng. 1978.7:393-434. Downloaded from www.annualreviews.org by University of Tennessee - Knoxville - Hodges Library on 04/09/13. For personal use only.

III

IV

[BB]+PX-

1

Etc

SCHEME 2

of a second species called pI/. Subsequently, by using picosecond spectroscopy Rockley et a1 ( 127) and Kaufmann et a1 (93) were able to show in reaction centers where the primary acceptor (ubiquinone-Fe complex) is not reduced prior to excita­ tion that the state pF is on the main photosynthetic pathway (see Scheme 2). On the other hand, pR is not formed under these conditions, which puts it on an alternative pathway when the main photosynthetic route is blocked. The identity of the two transient species was uncertain. It was suggested that pR could be identified with the lowest excited triplet state of the BChl complex in the reaction center. In Scheme 1 , pR is identified with structure IV. As in the triplet EPR experiments, transfer of an electron from one of the four bacteriochloro­ phyll molecules to another or to a bacteriopheophytin molecule was suggested for the identity of PI'. Subsequently Fajer et al (5 1) suggested that the optical spectrum observed for pF could be simulated by a superposition of the spectral differences (P870t-P870) + (BPheoa--BPheoa). Thus, the most likely candidate for pF is a radical pair between the oxidized special pair and reduced bacteriopheo­ phytin (structure III in Scheme 1). Recently, it was shown by Tiede et a1 ( 1 1 1, 1 5 1) that the acceptor molecule in pF can be reduced chemically. Under these conditions the triplet EPR signal is significantly reduced in intensity. The optical changes that accompany this proc­ ess show that the acceptor may not simply be bacteriopheophytin but may involve an electron sharing with the two bacteriochlorophylls in the reaction center other than the special pair (P800). Several workers are using magnetic resonance techni­ ques as an approach to identifying the species (52, 57, 146).

Chlorophyll Special Function in Normal Photosynthesis The EPR, picosecond, and optical spectroscopic results described in the foregoing can be used to suggest a mechanism for normal (unblocked) forward photosynthesis (Scheme 2). As no firm triplet information is available yet for green plants, our proposed radical pair scheme for chlorophyll special pair function is discussed in terms of bacterial photosynthesis. Again [BB] is the BChlsl>' P is the first electron acceptor, and X is the second member of the electron transport chain. P may be bacteriopheophytin and X may be a ubiquinone-Fe complex in photosynthetic

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430

KATZ ET AL

bacteria. The primary acceptor in green plant photosynthesis is still a subject of investigation. Although the exact identity of the members of the electron transport chains are different in green plants and bacteria, the essential features of Chlsp and BChl.p are assumed to be the same in Scheme 2. The intermediate in normal photosynthesis is III, a radical pair in its first excited state with both singlet (as) and triplet (I3T) character. Indicated by dotted arrows is the possible formation of a radical pair intermediate in the special pair itself from which electron transfer occurs to the first acceptor. Step IV shows the special pair in its doublet state. If, as in Scheme I, electron transfer from P to X is prevented, then a long-lived triplet will be generated from III. In Scheme 2, Etc includes all of the steps that lead to NaDPH formation and the restoration of the electron to the doublet state Chlspt. Chlsp function in this scheme is a I -quantum event and involves only the first excited state. This state is a radical pair, and the proposed scheme invokes a radical pair mechanism as a necessary intermediate. [The results of Blankenship et al (12) and of McIntosh & Bolton (109) that suggest a role for the triplet state on the main path of photosynthesis can probably also be explained by a radical pair mechanism, but not necessarily the radical pair of Scheme 2.] Hoff et a1 (72) and Haberkorn & Michel-Beyerle (67) have reached similar conclusions about the role of radical pairs in normal photosynthesis. Although there are many details that must be clarified and choices between different alternatives to be made, we believe that most of the experimental features of primary electron donor function in green plant and bacterial photosynthesis, at least in general terms, are accounted for by the radical pair Schemes 1 and 2.

Literature Cited 1. 2.

3.

4.

5. 6. 7. 8.

9.

10.

Anderson, A. F. R., Calvin, M. 1964. Arch. Biochem. Biophys. 107:251-59 Androes, G. M., Singleton, M. F., Cal­ vin, M. 1962. Proc. Natl Acad. Sci. USA 48:1022-3 1 Anton, J. A., Kwong, J., Loach, P. A. 1976. J. Heterocyclic Chem. 1 3:717-25 Ballschmiter, K., Cotton, T. M., Strain, R. R., Katz, J. J. 1969. Biochim. Biophys. Acta 180:347-59 Ballschmiter, K., Katz, J. J. 1968. Nature 220: 123 1-33 Ballschmiter, K., Katz, J. J. 1 969. J. Am. Chem. Soc. 9 1 :2661 Ballschmiter, K., Katz, J. J. 1972. Biochim. Biophys. Acta 256:307-27 Ballschmiter, K., Truesdell, K., Katz, J. J. 1969. Biochim. Biophys. Acta 1 84:604-13 Baum, S. J., Burnham, B. F., Plane, R. A. 1964. Proc. NatL Acad. Sci. USA 62:1439 Bearden, A. J., Malkin, R. 1975. Q. Rev. Biophys. 7: 1 3 1-77

1 1.

12.

13.

14.

15. 16.

17.

18. 19. 20.

Beinert, R., Kok, B., Roch, G. 1962. Biochem. Biophys. Res. Commun. 7:209-1 2 Blankenship, R., McGuire, A . , Sauer, K. 1975. Proc. Natl Acad. Sci. USA 72:4943-47 Blankenship, R. E., Schaafsma, T. J., Parson, W. W. 1977. Biochim. Bio­ phys. Acta 46l :297-305 Bolton, J. R., Clayton, R. K., Reed, D. W. 1969. Photochem. Photobiol. 9:209- 1 8 Bolton, J. R., Warden, J. T. 1976. Ann. Rev. Plant Physiol 27:375-83 Borg, D. c., Fajer, J., Felton, R. R., Dolphin, D. 1970. Proc. Nat! Acad. Sci. USA 67:8 1 3-20 Boucher, L. J., Strain, R. R., Katz, J. J. 1966. J. Am. Chern. Soc. 88: 1 34146 Bowman, M. K., Norris, J. R. Chem. Phys. Lett. In press Boxer, S. G., Closs, G. L. 1976. J. Am. Chem. Soc. 98:5406-8 Boxer, S. G., Closs, G. L., Katz, J. J.

43 1

CHLOROPHYLL IN PHOTOSYNTHESIS

21.

22. 23.

24.

1974. J.

97:7230-37 Clarke, R. H.,

Annu. Rev. Biophys. Bioeng. 1978.7:393-434. Downloaded from www.annualreviews.org by University of Tennessee - Knoxville - Hodges Library on 04/09/13. For personal use only.

90:7058-66

Connors, R. E.

Chern. Phys. Lett.

42:69-72

1976.

Clarke, R. H., Connors, R. E., Frank, H. A. 1976. Biochern. Biophys. Res.

Commun.

43.

Dutton, P. L., Leigh, J. S., Seibert, M. 1972. Biochem. Biophys. Res. Com­

44 .

Dutton, P. L., Leigh, I . S., Seibert, M. 1972. Biochern. Biophys. Res. Corn­

45.

Duysens, L. N. M.

46.

PhD thesis. Univ. Utrecht, The Neth­ erlands. 96 pp. Duysens, L. N. M. 1954. Nature

7 1 :67 1-75

Clarke, R. H., Connors, R. E., Frank, H. A., Hoch, I. C. 1977. Chern. Phys.

Lett.

25. 26.

Arn. Chem. Soc.

Chow, H.-C., Serlin, R., Strouse, C. E. 1975. J. Arn. Chern. Soc.

45:523-28

Deleted in proof. Clarke, R. H., Connors, R. E., Kee­ gan, I. 1977. J. Chern. Phys. 66:358-

28. 29. 30. 31. 32.

Clarke, R. H., Connors, R. E., Schaafsma, T. J., Kleibeuker, J. F., Platenkamp, R. J. 1 976. J. Am. Chem.

Soc.

98:3674-77

1975. J. 6 1 :4582-87 Clayton, R. K. 1963. Biochim. Bio­ phys. Acta 74: 3 1 2-23 Clayton, R. K. 1971. Adv. Chern. Phys. 19:353-78 Clayton, R. K. 1973. Ann. Rev. Bio­ phys. Bioeng. 2 : 1 3 1-56 Clayton, R. K., Wang, R. T. 1971. Methods Enzyrnol 23:696-704

Clarke, R. H., Hofeldt, R. J.

Chem. Phys.

48. 49. 50. 51.

52.

56.

35.

Commoner, B., Heise, J. J., Lippin­ cott, B. B., Norberg, R. E., Passon­ neau, J. V., Townsend, J. 1957. Science

57.

36.

1 26:57-63

Commoner, B., Heise, I. I., Townsend,

I. 1956. Proc. Natl. Acad. Sci USA 42:710-18

37.

38.

39.

40.

41.

42.

Cotton, T. M., Loach, P. A., Katz, J. J., Ballschmiter, K. 1977. Photo­ chem. Photobiol. In press Cotton, T. M., Trifunac, A. D., Ballschmiter, K., Katz, I. I. 1974.

Biochim. Biophys. Acta 368 : 1 8 1-98

Dougherty, R. C., Crespi, H. L., Strain, H. H., Katz, J. J. 1966. J. Am.

Chern. Soc.

88:2854-55

Dougherty, R. C., Sphon, I., Dreyfus, P., Katz, I. 1. 1977. Submitted for publication Dutton, P. L., Kaufmann, K. I., Chance, B., Rentzepis, P. M. 1975.

FEBS Lett.

292:654-64

Natl Acad. Sci USA

1977.

Abstr. Biophys. J. 1 7 : 1 50a 1956. Phy. Rev. 103:834-

72:4956-

Fajer, J., Davis, M. S., Forman, A. 35

14:373-87

1 97 1 .

Photochern. Photobiol.

Acad.

Sci. 244:239-59

Abstr.

1 3:61

Feher, G., Hoff, A. J., Isaacson, R. A., McElroy, J. D. 1973. Biophys. Soc.

58.

Feher, G., Isaacson, R. A., Okamura, M. Y. 1977. Abstr. Biophys. J. 17: 149a Feher, G., Okamura, M. Y. 1976.

59.

Fong, F. K.

60.

Brookhaven Syrnp. BioL 28: 183-94 1974. Proc. Natl Acad. Sci. USA 7 1 :3692-95 Fong, F. K. 1 974. J. Theor. Biol

46:407

Fong, F. K.

1975.

62.

Fong, F. K.

63.

1976. J.

Fong, F. K., Koester, V. J.

1976.

Fuhrhop, I.-H., Mauzerall, D.

1969.

61.

64. 65.

66.

60:275-80

Dutton, P. L., Leigh, I. S., Reed, D. W. 1973. Biochirn. Biophys. Acta

Proc. 60

Feher, G., Hoff, A. I., Isaacson, R. A., Ackerson, L. C. 1975. Ann. NY

Collman, J. P., Elliott, C. M., Halbert, T. R., Tovrog, B. S. 1977. Proc. Natl 74: 1 8-22

Fajer, I., Brune, D. C., Davis, M. S., Forman, A., Spaulding, L. D. 1975.

Feher, G.

34.

Acad. Sci. USA

Symp. Bioi.

54. 55.

85:3809-2 1

1958. Brookhaven 1 1 : 10-25 Emerson, R., Arnold, W. 193 1-1932. J. Gen. Physiol. 1 5:39 1-420 Emerson, R., Arnold, W. 1932-1933. J. Gen. Physioi. 1 6 :1 9 1-205 Evans, T. A., Katz, J. J. 1975. Biochim. Biophys. Acta 396:414-26

Duysens, L. N. M.

Feher, G.

Closs, G. L., Katz, J. J., Pennington, F. C., Thomas, M. R., Strain, H. H.

Am. Chern. Soc.

1952. Transfer of excitation energy in photosynthesis.

53.

33.

1963. J.

rnun. 46:406-13

173:692-93

47.

59 27.

mun. 46:406-1 3

66

98:7840-43

Appl. Phys.

6 :1 51-

Am. Chem. Soc.

Biochim. Biophys. Acta 423:52-64 J. Am. Chern. Soc. 9 1 :4174-8 1

Gaines, G. L. Ir., Bellamy, W. D., Tweet, A. G. 1964. J. Chern. Phys. 4 1 :2572-73

Garcia-Morin, M., Uphaus, R. A., Norris, J. R., Katz, J. J. 1969. J. Phys.

Chern.

73:1066-70

67.

Haberkorn, R., Michel-Beyerle, M. E.

68.

Hagele, W., Drissler, F., Schmid,

1977.

FEBS Lett.

75:5-8

432

KATZ ET AL

D.,

Wolf, H. C. 1976. ESR studies of the photoexcited triplet states of chlorophyll a and chlorophyll b in poly(methyl methacrylate) and methyl tetrahydrofuran at 4.2 K Presented at

69.

Annu. Rev. Biophys. Bioeng. 1978.7:393-434. Downloaded from www.annualreviews.org by University of Tennessee - Knoxville - Hodges Library on 04/09/13. For personal use only.

70.

Third Int. Seminar on Excitation En­ ergy Transfer in Condensed Matter, Prague, Czechoslovakia Hall, R. L., Kung, M. C., Fu, M., Hales, B. J., Loach, P. A. 1973. Pho­ tochem. Photobiol

Henry,

1 8:505-20

Int. CNRS

Grondelle, R., Duysens, L. N. M.

76. 77.

78. 79. 80. 81.

82.

83.

84. 85. 86. 87.

1977. Biochim. Biophys. Acta 460:54754 Hoff, A. J., van der Waals, J. H. 1976. Biochim. Biophys. Acta 423:615-20 Holt, A. S., Jacobs, E. E. 1955. Plant Physiol 30:553-59

Kagan, N. E., Mauzerall, D., Merri­ field, R. B. 1977. J. Am. Chem. Soc.

99:5484-86

Katz, J. J. 1968. Dev. Appl Spectrosc.

6:201-18

Katz, J. J. 1973. In Inorganic Bio­ chemistry, ed. G. L. Eichhorn, II: 1022-66. Amsterdam: Elsevier Katz, J. J., Ballschmiter, K. 1968.

Angew, Chern. Int. Ed. Engl.

80:283; Angew. 7:286-87

Chem.

Katz, J. J., Ballschmiter, K., Garcia­ Morin, M., Strain, H. H., Uphaus, R. A. 1968. Proc. Natl Acad. Sci. USA

60: 100-7

Katz, J. J., Closs, G. L., Penning­ ton, F. C., Thomas, M. R., Strain, H. H. 1963. J. Am. Chem. Soc.

85:380 1-9

Katz, J. J., Dougherty, R. C., Boucher, L. J. 1966. In The Chloro­ phy/ls, ed. L. P. Vernon, G. R. Seely, pp. 185-25 1. New York: Academic Katz, J. J., Dougherty, R. C., Crespi, H. L., Strain, H. H. 1966. J. Am. Chem. Soc.

88:2856-57

Katz, J. J., Janson, T. R. 1973. Ann. NY Acad. Sci.

206;579-603

Katz, J. J., Janson, T. R., Kostka, A. G., Uphaus, R. A., Closs, G. L. 1972.

J. Am. Chem. Soc. 94;2883-85 Katz, J. J., Norman, G. D., Svec, W. A., Strain, H. H. 1968. J. Am. Chem. Soc.

Katz, J. J., Norris, J. R., 1973. Curro

89.

Katz, J. J., Norris, J. R., Shipman, L. L. 1976. Brookhaven Symp. BioL

90.

90;6841-45

Top. Bioeng.

5:41-75

28:16-55

Katz, J. J., Oettmeier, W., Norris, J. R. 1976. Phi/os. Trans. R. Soc. London

Ser. B 273:227-53 91. Katz, J. J., Shipman, L. L., Cotton, T. M., Janson, T. R. 1977. In The Por­

Dolphin. New York: Academic. In press Katz, J. J., Strain, H. H., Leussing, D. L., Dougherty, R. C. 1968. J. Am.

phyrins, ed. D.

M., Leicknam, J.-P. 1970. Coli.

191:317-33 71. Hoff, A. J. 1976. Biochim. Biophys. Acta 44:765-71 72. Hoff, A. J., Gast, P., Romijn, J. C. 1977. FEBS Lett. 73:185-90 73. Hoff, A. J., Govindjee, Romijn, J. C. 1977. FEBS Lett 73:191-95 74. Hoff, A. J., Rademaker, H., Van

75.

88.

92. 93. 94. 95.

Chem. Soc.

90:784-91

Kaufmann, K. J., Dutton, P. L., Net­ zel, T. L., Leigh, J. S., Rentzepis, P. M. 1975. Science 1 88:1301-4 Kleibeuker, J. F., Schaafsma, T. J.

1974.

Chem. Phys. Lett.

29: 1 16-22

Kohl, D. H., Townsend, J., Com­ moner, B., Crespi, H. L., Dougherty, R. C., Katz, J. J. 1965. Nature

206:1 105-10 Kok, B. 1956. 22:399-401 97. Kok, B. 1957.

96.

Biochim. Biophys. Acta

98.

Kratky, C., Dunitz, J. D. 1977. J. MoL

99. 100.

Bioi.

Nature

179:583-84

1 13:43 1-42

Krinsky, N. I. 1971. In Carotenoids, ed. O. Isler, pp. 686-98. Basle: Berk­ hauser Verlag Leigh, J. S., Dutton, P. L. 1974.

Biochim. Biophys. Acta 357:67-77 H., Scherz, A. 1975. Chem. Phys. Lett. 3 1 : 1 19-24 Loach, P. A., Hales, B. J. 1976. In Free Radicals in Biology, ed. W. J.

101. Levanon, 102.

103.

Pryor, pp. 199-237. New York: Academic Loach, P. A., Sekura, D. L. 1967.

104.

Lubimenko, V. N. 1927. Rev. Gen.

105.

Photochem. Photobiol. Bot

6:381-93

39:547-59

Mau, A. W. H., Puza, M. 1977. Photochem. Photobiol

25:601-3

106.

McElroy, J. D.,.:Feher, G., Mauzerall, D. C. 1969. Biochim. Biophys. Acta

107.

McElroy, J. D., Feher, G., Mauzerall, D. C. 1972. Biochim. Biophys. Acta

172: 180-83

267:363-74 108. McElroy, J. D., Mauzerall, D. C., Feher, G. 1974. Biochim. jJiophys. . Acta 333:261-78 109. McIntosh, A. R., Bolton, J. R. 1976. Nature 263:443-45 1 10. Menzel, E. .R. 1976. J. Theor. Biol 56:401-16 1 1 1. Netzel, T. L., Rentzepis, P. M., Tiede, .

D. M., Prince, R. C., Dutton, P. L.

433

CHLOROPHYLL IN PHOTOSYNTHESIS

1977. Biochim. Biophys. Acta460:46779

1 12. 1 13. 1 14.

Annu. Rev. Biophys. Bioeng. 1978.7:393-434. Downloaded from www.annualreviews.org by University of Tennessee - Knoxville - Hodges Library on 04/09/13. For personal use only.

1 15. 1 16. 1 17.

1 1 8. 1 19. 120.

121. 122.

123. 124.

Norris, J. R., Druyan, M. E., Katz, J. J. 1973. J. Am. Chem. Soc. 95:168082 Norris, J. R., Scheer, H., Druyan, M. E., Katz, J. J. 1974. Proc. Natl.

Acad. Sci USA 71 :4897-900

Norris, J. R., Scheer, H., Katz, J. J. 1975. Ann. NY Acad. Sci. 244:261-80 Norris, J. R., Uphaus, R. A., Crespi, H. L., Katz, J. J. 197 1 . Proc. NatL Acad. Sci USA 68:625-28 Norris, J. R., Uphaus, R. A., Katz, J. J. 1972. Biochim. Biophys. Acta

Soc. 98:8222-30

.

137.

Okamura, M. Y., Steiner, L. A., Feher, G. 1974. Biochemistry 13:1394-

141.

403

Parson, W. W. 1974. Ann. Rev. Micro­

bioi. 28:41-59

Phys. Chem. 8 1:577-8 1

Shipman, L. L., Norris, J. R., Katz, J. J. 1976. J. Phys. Chem 80:877-

82

Shipman, L. L., Owicki, J. C., Scher­ aga, H. A. 1974. J. Phys. Chem.

78:2055-60

142.

Smith, G. E., Blankenship, R. E., Klein, M. P. 1977. Rev. Sci Instrum 48:282-86 Strain, H. H., Cope, B. T., McDonald, G. N., Svec, W. A., Katz, J. J. 197 1 . Phytochemistry 10:1 109-14 Strouse, C. E. 1973. Proc. Natl. Acad.

143.

Strouse, C. E.

Parson, W. W., Clayton, R. K., Cog­ dell, R. 1. 1975. Biochim. Biophys. Acta 387:265-78 Parson, W. W., Cogdell, R. J. 1975. Biochim. Biophys. Acta 416: 105-49 Rabinowitch, E. I. 1945. Photosyn­ thesis, Vol. I, p. 402. New York: Interscience Radmer, R., Kok, B. 1975. Ann. Rev.

Sci USA 71 :325-28 1976. Prog. Inorg. Chem 22: 159-77 144. Thornber, J. P. 1975. Ann. Rev. Plant PhysioL 26:127-58 145. Thornber, J. P., Alberte, R. S. 1976. In The Enzymes of Biological Mem­ branes, ed. A Martonosi, pp. 163-90.

Biochem 44:409-33

146.

Biochem. Biophys. Res.

Commun.

Biophys. Acta 460:47-57

Rockley, M. G., Windsor, M. W., Cogdell, R. J., Parson, W. W. 1975. Proc. NatL Acad. Sci USA 72:225155 Rosilio, A., Leicknam, J.-P. 1970. Rev.

GAMS 6:1 32-37

129. Scheer, H., Katz, J. J. 1975. In Porphyrins and Metal/oporphyrins, ed.

132.

Shipman, L. L., Janson, T. R., Ray, G. J., Katz, J. J. 1975. Proc NatL Acad. Sci USA 72:2873-76 Shipman, L. L., Katz, J. J. 1977. J.

140.

126.

131.

136.

Ogoshi, H., Sugimoto, H., Yoshida, Z. I. 1 977. Tetrahedron Lett. 2:169-

30:471-75 Renger, G., Wolff, C. 1 977. Biochim.

1 30.

Shipman, L. L., Cotton, T. M., Norris, J. R., Katz, J. J. 1976. J. Am. Chem.

139.

72

Acad. Sci. USA 73:1791-94

1 35.

Chemistry and Biochemistry of Plant Pigments, ed. T. W. Goodwin, 1:32876. New York: Academic

O'Carra, P., O'hEocha, C. 1976. In

523-68. New York: Academic Serlin, R., Chow, H.-C., Strouse, C. E. 1975. J. Am. Chem. Soc. 97:7237-42 Shipman, L. L., Cotton, T. M., Norris, J. R., Katz, J. J. 1976. Proc Natl. .

138.

Reed, D. W., Clayton, R. K. 1968.

128.

134.

275:161--ti8

125.

127.

133.

K. M. Smith, pp. 399-524, Amster­ dam: Elsevier Scheer, H., Katz, J. J., Norris, J. R. 1977. J. Am. Chem. Soc. 99:1 37281 Schwarz, F . P., Gouterman, M., Mul­ jiani, Z., Dolphin, D. H. 1972.

Bioinorg. Chem. 2:1-32 Seely, G. R. 1 966. In The Chlorophyl/s, ed. L. P. Vernon

and G. R. Seely, pp.

147.

148. 149. 1 50.

New York: Plenum Thurnauer, M. C., Bowman, M. K., Johnson, K. W., Clilft, E. B., Norris, J. R. 1977. Am. Chem Soc. 1 74th NatL Meet., Chicago, Abstr. No. P43 Thurnauer, M. C., Katz, J. J., Norris, J. R. 1975. Proc. NatL Acad. Sci. USA

72:3270-74

Thurnauer, M. C., Norris, J. R. 1976.

Biochem Biophys. Res.

Commun.

73:501-6 Thumauer, M. C., Norris, J. R. 1977. Chem. Phys. Lett. 47:1 00-5 Thurnauer, M. C., Smith, U. H., Bow­ man, M. K., Norris, J. R. 1977. Am.

Chem Soc. 1 74th NatL Meet. Chicago,

151.

152. 153.

Abstr. No. P44 Tiede, D. M., Prince, R. C., Dutton, P. L. 1976. Biochim. Biophys. Acta

449:447-67 Trebst, A. 1974. Ann. Rev. Plant. Phy­ sioL 25:423-58

Van der Bent, S. J., Schaafsma, T. J., Goedheer, J. C. 1 976. Biochem. Bio­ phys. Res. Commun. 7 1 : 1 147-52

434 1 54. 155.

Annu. Rev. Biophys. Bioeng. 1978.7:393-434. Downloaded from www.annualreviews.org by University of Tennessee - Knoxville - Hodges Library on 04/09/13. For personal use only.

156.

KATZ ET AL

D.

Van der Meulen, L., Govind­ jee. 1973. J. Sci Indus. Res. 32:62-

160.

69

Wagner, P. J., Hammond, G. S. 1968.

161.

Sci USA 73:2773-75

162.

Adv. Photochem. 5:21-156

Warden, J. T. 1976. Proc. Natl. Acad.

157. Warden, J. T., Bolton, J. R. 1972. J. Am. Chem. Soc. 94:435 1-52 158. Warden, J. T., Bolton, J. R. 1974. Acc. Chem. Res. 7:189-95 159. Warden, J. T. Jr., Bolton, J. R. 1973. J. Am. Chern. Soc. 95:6435-36

Wasielewski, M. R., Smith, U. H., Cope, B. T., Katz, 1. 1. 1977. J. Am.

Chern. Soc. 99:4172-73

Wasielewski, M. R., Studier, M. H., Katz, J. J. 1976. Proc. Natl. Acad. Sci.

USA 73:4282-86

163.

Worcester, D. L., Katz, J. J. 1977. Submitted for publication Wraight. C. A., Clayton, R. K. 1973.

Biochim. Biophys. Acta 333:246--60

164.

Wraight, C. A., Leigh, J. S., Dutton, P. L., Clayton, R. K. 1974. Biochim.

Biophys. Acta 333:401-8