Photosynthesis Research I0: 2 3 3 - 2 4 2 (1986) © Martinus N i j h o f f Publishers, Dordrecht - Printed in the Netherlands





NICHOLAS E. GEACINTOV a, JACQUES BRETON b and ROBERT S. KNOX c achemistry Department, New York University, New York, NY 10003, bServlce de Biophysique, Departement de Biologle, C.E.N. Saclay, 9 1 1 9 1 G i f sur Yvette, cedex, France, and CDepartment of Physics and Astronomy, The University of Rochester, Rochester, NY 14627 Key words: chloroplasts, fluorescence decay components, reaction charge recombination and fluorescence


Abstr~t. The possible origins of the different fluorescence decay components in green plants are discussed in terms of a random walk and Butler's bipartite model. The interaction of the excitations with the photosystem II reaction centers and, specifically, the regeneration of theses excitations by charge recombination within the reaction centers, are considered. Based on comparisons between fluorescence decay profiles, timedependent exciton annihilation and photoelectric phenomena, it appears that the fast 200 ps decay component corresponds to primary energy transport from the antenna to the reaction centers and is dominant in filling the photosystem II reaction centers.

Introductlon In spite of much theoretical and experimental research, the details of exciton migration and trapping in photosynthetic systems are still not completely understood. In this overview we summarize recent advances in this field, and attempt to integrate the results obtained by different experimental approaches to this problem. The central question is: how long does it take for an exciton to reach a reaction center and to give rise to the primary act of charge separation at that reaction center? Different experimental approaches have been utilized in attempts to answer this question; these include (I) time-resolved fluorescence decay profile measurements, (2) direct measurement~ of the kinetics of the appearance of ionic species in the reaction centers by differential absorption spectroscopy, and (3) rapid kinetic measurements of the transmembrane electric field which arises because of the separation of electric charges within the reaction centers. The availability of picosecond pulse lasers and other technological advances have provided an important impetus to this field. Recently, most of the activity in this area of photosynthesis research has centered on accurate measurements of fluorescence decay profiles in green plants and the interpretation of the multi-exponential decays in terms of exclton migration and the known mechanisms of fluorescence. Butler's

Models of Energy Transfer

and F l u o r e s o e a e e




In the 1970's, using steady-state measurements of fluorescence parameters, Butler and his co-workers developed a model of the photosynthetic apparatus and provided important insights into the mechanisms of fluorescence (reviewed in [I]). In Butler's bipartite model, the light harvesting chlorophyll a/b protein complexes and the P S I I core chlorophyll a antenna molecules are considered to be tightly coupled by excitation transfer. These two types of chlorophyll - protein complexes thus represent, approximately, a single species of fluorescence - emitting antenna molecules. Energy transfer from the antenna to the reaction centers (RC) occurs with rate constant kT, where energy can either be returned to the antenna (rate constant k t) or undergo charge separation (photochemical conversion) with a rate constant kp, according to the following scheme: kA fluorescence


kT. A ~'-~RC kt


charge separation


where A represents the antenna, and k A the rate constant for decay of excltons within the antenna. The bipartite model provides a reasonable explanation of steady-state fluorescence data [ I ] . Nevertheless, this model is known to represent an oversimplification, particularly since the coupling between the light-harvesting antenna molecules and PS II core antenna chlorophyll a molecules may be less than 100% efficient. This factor is taken into account in Butler's tripartite model [I]. Evidence has since been provided about an additional type of heterogeneity of the photosynthetic apparatus of green plants, namely the existence of ot and subunlts [2]. Each type of P S I I unit may be characterized by different bipartite fluorescence kinetics, thus further increasing the complexity of the fluorescence [3].

Multi-exponential fluorescence decay p r o f i l e s The heterogeneity of the fluorescence manifests itself in terms of multiexponential decay profiles at low temperatures [4,5] and at room temperature [6,7,8,9]. The latter work, utilizing mode-locked, synchronously pumped dye lasers and time-correlated single photon counting methods, provides the most detailed description of the time dependent fluorescence decay profiles F(t) at ambient temperatures. These decay profiles can be described by a sum of 3 (or more) exponentials: F(t) = Z A i e x p ( - t / ~ i )


where the terms A i (i=1,2,3) correspond to the initial amplitudes of the individual components, the decays of which are characterized by the lifetimes ~i" When the sums of the amplitudes are normalized such that ~ A i = 1.0, these amplitudes are proportional to the fraction of pigment molecules of each type excited at t = 0. The time integrated fluorescence yield of each component is given by the product Ai~i, and the relative contr~butlon of each component to the steady state fluorescence is Ai1~i(~Ai~i )-1. In chloroplasts and green algae, lifetimes of about 100-200 ps, 400-600 ps, and 1.2 - 2.5 ns are generally found. These decay times are termed the fast, intermediate or middle, and slow components, respectively. The fast



eomponent has been shown to be comprised of a 50-80 ps component and a 150 - 200 ps component [ 6 , 9 ] . Relating these d i f f e r e n t components to the various e x c i t a t i o n e n e r g y d i s t r i b u t i o n models of the photosynthetie apparatus has proven to be quite d i f f i e u l t . Before discussing the various interpretations of the kinetic fluorescence data, we consider two theoretical approaches, the random walk and the kinetic model. The ram4~m walk model The migration of exeitons is assumed to occur by a series of transfers from molecule to molecule by the "hopping" F~rster energy transfer mechanism [10]. In a simple model, the different fluorescence components can be assigned to a particular pigment pool, e.g. PSI and PSII and their associated antenna pigment systems. In the simplest model of this type, N antenna molecules and one reaction center are considered to form a regular lattice such that [N]>>[RC]. The excitons, created with uniform probability anywhere within this array, perform a random walk until they are captured by the RC; the excited RC undergoes photochemical conversion (rate constant k_), or an exciton is returned to the antenna. The details of such exciton m~tion have been described in detail by Pearlstein [11-13]. Under certain restrictive, but physically realistic conditions [13], the decay time "C of the excitons is mono-exponential and is given by:

= e(N1~

+ Nkp -I


where,( is a term which depends on the lattice parameters. The first term is the "first passage time", ~'FPT, the time required for an exelton to reach the RC for the first time; the second term is the lifetime of the exoiton which starts a random walk at the reaction center. Thus, if the trap does not photoconvert efficiently, the exciton has a longer lifetime because it has a finite probability to be returned to the antenna. If ~'FPT >> N/k_, the time of photoconversion at the trap is much faster than the diffusion time of the exciton to the trap, and the kinetics of exciton diffusion and trapping are said to be "diffusion controlled". In the opposite ease, the kinetics are said to be "trap-llmlted". In the above treatment, it is assumed that there is only one exclton in the array of N antenna molecules. A more complex random walk approach including energy transfer, trapping, and bimolecular exciton-exeiton annihilation processes which can occur at high excitation intensities, has been recently described [14,15]. The coupled k l n e t . t e r a t e equation model In-this approach the details of the random walk of the excitons, as well as all other mieroscopic parameters, are neglected. The energy transfer between different pigment systems, or between the array of antenna molecules and the reaction centers, is described by macroscopic kinetic rate constants. The instantaneous fluorescence of each subsystem can usually be taken as an indication of the population of exeitons in that subsystem. In order to illustrate this approach, we consider two coupled (by energy transfer), distinct pools of fluorescence-emitting pigment systems, containing N I and N 2 molecules, respectively. The time dependence of the excitation is described by the functions S1(t) and S2(t), each of whieh



depends on the absorption cross section per molecule and on N I and N 2, respectively..Under l~w-intensity excitation conditions, the excited state populations N I and N 2 obey the kinetic equations: dN1*/dt =

S1(t) - (K +q~1-1)N1 * + K'N2*


dN2*/dt =

S2(t) + KNI* - (K' + q~2-1)N2 *


K is the overall rate constant of excitation transfer from pool I to pool 2, and K' the overall rate constant for exc~ton transfer from pool 2 to pool 1. The rate constants ~ I - " and "~2-" are equal to the reciprocal excitation lifetimes in each pool, respectively, in the limit of complete decoupllng (K = K' = 0). In the limit of narrow pulse excitation, and for times t such that S1(t) and S2(t) = O, the decay of the excltons in each pool is governed by the two equations: N1*(t) = A I exp(- ~ i t) + A 2 exp(- ~ 2 t )


N2*(t) = A 3 exp(- ~ I t) + A 4 exp(- ~ 2 t)


The quantities 71 and 7 2 are eigenvalues of a kinetic matrix constructed from the coefficients of equations (4) and (5) [3], and are equal to:

~I-1, 2 = 1/2 [ a ±tJ'b"l ] where








+ ~'2 - 1 ,


and b = (K + ~1~1-1 - K' - q~'2-1) 2 + qKK'.

In general, it is evident that the fluorescence decay of each pigment pool is double-exponential. Furthermore, the experimentally observable decay parameters ~I and 4 ~ are complicated functions of the kinetic parameters K, K ' , ~ I -I and ~ 2 -~. The amplitudes A i are determined by the boundary conditions of the problem, e.g. the initial concentrations of each fluorescence-emltting species at t : O. We now discuss the issue of fluorescence yield rise times which can occur under certain conditions. If one of the emitters is largely non-absorbing, its population, just after a short excitation pulse, is virtually zero. The fluorescence signal due to this emitter is proportional to

F ( t ) ~ " exp ( - ')-lt) - e x p

( - "~,2t)


a factor which is sometimes said to contain an "exponential rise time". An example of a fluorescent component fairly well described by this time dependence is the fluorescence emitted from PSI at 735 nm at low temperatures (F735). Equation (9) was used in early work to describe the time-dependent increase in F7351bY Camplllo et al [16], and more recently by others [4,5]. The time ~ 2 is related to the transfer tlme .between the two comDonents, but is not a simple rise time (example= if ~ o -= = 200 ps and ~ 1 -I = 100 ps, F(t) in equation (9) reaches a maximum at ~39 ps and has a I0-90% risetime of 78 ps). The way a factor, such as (9), arises in formal n- component kinetics is through the eigenvectors of a kinetic matrix [3]. In the two-component case, the eigenvectors are precisely such that the rising component will have a value of zero at t = 0 (A 3 = -A 4 in



eq. 7). When experimental d a t a with rise times are subjected to an nexponential fit (fluorescence decay profiles at low temperatures), a negative component appears, but no attempt has been made to explain such negative pre-exponential amplitudes in terms of kinetic models [4]. As we have stressed earlier [5], it is both possible and desirable to proceed directly with a numerical integration of model kinetic equations of the type shown above (eqs. 4 and 5), and to determine realistic values of parameters by trial and error. The direct integration method solves the problems of risetimes, the interpretations of the experimentally observed parameters ~I and ~2 in terms of kinetic model parameters, and eliminates explicit deconvolutions.

Analyse8 o f experimental f l u o r e s c e n c e decay p r o f i l e s Current interpretations of the experimental data are based on the following models: (I) each of the lifetime components is qualitatively associated with excitons in a particular pigment system, or pool, (2) coupled kinetic rate equations, and (3) random walk parameter~. A detailed examination of the excitation and emission wavelength dependence of each of the amplitudes A i (eq. 2) has been particularly helpful in attributing the origins of the different components to light harvesting antenna containing chlorophyll b and associated with PS II reaction centers, and to chlorophyll a antenna molecules associated with P S I and PS II [9]. The long-standing problem of whether, and how much, P S I contributes to the overall fluorescence of green plants at ambient temperatures appears to be solved. The fastest fluorescence decay component with lifetimes in the range of 50-80 ps [6,9] is attributed to PS I fluorescence. The fluorescence yield of this component at ambient temperatures is small, and its excitation and emission wavelength characteristics correspond to the longer wavelength forms of chlorophyll a [9]. Additional evidence pointing to the P S I origin of this fast fluorescence component stems from studies with mutants which lack P S I [6,17,18], and its lack of sensitivity on (I) the state of PS II reaction centers, (2) the pH, and (3) the presence of cations [8]. The origins of the other, longer lifetime components are more difficult to explain. The observed lifetimes depend on the state of the PS II reaction centers. Butler et al [3], as well as Karukstls and Sauer [19], ini~ially suggested that the origins of the intermediate lifetime components can be explained in terms of the ~ a n d ~ heterogeneity of the photosynthetic units [2]. Holzwarth et al [9] have proposed the most explicit explanation of fluorescence decay kinetics based on this concept. A fast 180 ps component in the Fo:state (PS II reaction centers open) is attributed to o( units, and is converted to a 2.2-2.4 ns lifetime in the Fmax state (reaction centers closed). A t h i r d 500-600 ps l i f e t i m e in the F o state is attributed to the ~ units, and is transformed to a 1.2-1.4 ns component in the Fma X state. While this model is self-consistent, there are some difficulties; the antenna size of ~ units is larger than that of units [20] and thus, according to the random walk model (eq.3) a longer lifetime should be observed in the W units. However, the opposite is observed in the F o state; therefore the model of Holzwarth et al [9] requires some additional assumptions about differences in exciton quenching efficlencles of PS II reaction centers in the ~ and ~ units (in the F o state),



and about differences in the interunit excitation transfer efflciencies the Fma x state.


Butler et al [3], Berens et al [21], as well as Schatz and Holzwarth [22], account for the multiplicity of lifetimes by utilizing the coupled differential equations kinetic approach (eqs. 5 and 6) based on Bytler's bipartite model (eq. I). The [email protected] flyorescence decay times are identified with the parameters ~i -i and ~ 2 -], where: ~1'2 = -I/2[ k A + kp + k T + k t ± V ( k A

+ k T - kp - kt)2 + 4kTkt'] (10)

where the + sign is associated with ~I and the - slgn with ~2" It is important to note that this approach predicts a double-exponential decay, even though the emission occurs from a single pigment pool, the antenna pigment system in the bipartite model. On the other hand, in the random walk model discussed earlier, a single decay component is predicted; the reasons for these different predictions of the two models are not immediately apparent and deserve further investigation. The different lifetime components in the F o and Fma x states are attributed by Berens et al [21] to either the fast or the long reciprocal eigenvalues (eq. 10) of the kinetic matrix, originating either in eg or ~ units of PS II. This heterogeneous bipartite model seems to provide a more adequate description of the fluorescence decay characteristics than the more complex tripartite model [21].

OrXgim o f t h e long f l u o r e s o e n e e component, v a r i a b l e f l u o r e s c e n c e , and Kltmov r e c o m b i n a t i o n meohanlsm


Klimov and his co-workers advanced the hypothesis that the variable PS II fluorescence, which is observed when the reaction centers are closed , is due to a recombination luminescence mechanism described as follows [23]: Exciton + P680-I-Q--->P680+-I--Q--->P680*-I-Q--->P680-I-Q- + exciton


The acceptor is denoted by Q, as usual, while I is an intermediate electron acceptor identified as a pheophytin molecule. Haehnel et al [24] first attributed the longest fluorescence component to the charge recombination mechanism; the yield of this component increases by a factor of 20 as the PS II reaction centers are closed. Both the lifetime and amplitude of this long component increase in the Fma x state, the former presumably because of interunit transfer of excitons. Subsequently [9,25] doubts were raised about this interpretation based on the observation that the amplitude (and yield) of the fast 180 ps fluorescence decay component, attributed to PS II, is strongly decreased in the Fma x state. It was reasoned that the amplitude and lifetime of this component should be constant in the F o and Fma x states since the primary trapping and photochemical conversion should be the same in the P680-I-Q and P680-I-Q- states. Since this is not observed, it is argued that the 180 ps component is transformed to a longer lifetime in the Fma x state because of a decreased excitation quenching rate constant. However this alternative explanation in itself does not constitute a strong argument against the Klimov mechanism. In the random walk model, the Klimov recombination can be viewed as a reduced efficiency of photochemical conversion at the trap (lower k D in eq. 3); thus the 180 ps lifetime in the F o state is transformed into ~ longer, but still mono-



exponential decay phase in the Fm_ x state, due to the re-injection excitation from the RC into the antenna.



The fastest fluorescence decay phases of 50-80 ps attributed to PS I, and the 150-180 ps attributed to PS II, could well correspond to primary energy transfer and reaction center trapping events. However, some of the slower fluorescence decay components have also been attributed to the same phenomenon. It is evident Chat fluorescence techniques alone cannot provide unequivocal information about the rates of primary exciton trapping and conversion at the reaction centers. Additional information can, in principle, be obtained from absorption and photoelectric measurements related to the appearance of charged species in the reaction centers.

K i n e t i c s o f a b s o r p t i o n changes due t o charge s e p a r a t i o n i n r e a c t i o n c e n t e r s Because there is only one reaction center per 100 - 250 antenna molecules, it is difficult to measure the rate of appearance of oxidized P680 or P700 molecules in intact membranes. However, such measurements have been performed with reaction center-enriched sub-chloroplast particles. Fenton et al [26] found that charge separation occurs within I0 ps of excitation in PSI particles in which the CHIa/P700 ratio is 30-40. Kamogawa et al [27] using highly enriched PSI reaction center particles (8I0 Chla/P700), found a tl/e risetime of P700 + of about 25 ps. The fluorescence of these particles, under low intensity excitation such that exciton-exclton annihilation processes were excluded, displayed similar decay kinetics [28]. Ii'ina et al [29] found a risetime of 15-30 ps for P700 + in PSI-enriched particles with Chla/P700 of ~ 60. In intact chloroplasts a fluorescence decay phase of 50-80 ps [6,9] was attributed to the decay and capture of excitons in PSI. This lifetime is about 2-3 times longer than the photoconversion time measured by absorption techniques in PSI-enriched particles. This difference is consistent with larger antenna sizes in intact chloroplasts, giving rise to a larger number of exciton transfer steps before trapping, and thus Co a longer lifetime according to eq. 3. The interpretation of the fast 50-80 ps fluorescence lifetime in terms of primary excitation trapping in P S I is thus entirely reasonable. Using the random walk model (eq. 3) and a trapping time of 53 ps, Gulotty et al [6] have estimated a molecule to molecule hopping race ~'j = 0.I - 0.7 ps.

P h o t o e l e c t r i c measure~ent~ o f p r l . ~ r y

charge s e p a r a t i o n i n r e a e t i o n c e n t e r s

Still another extremely fruitful and newly developed approach involves the measurement of the rate of appearance of photovoltages on subnanosecond time scales in chloroplasts following excitation with picosecond laser flashes [30]. The photoelectric signal, which is due to PSI and PSII photosynthetic transmembrane eharge separation, occurs within less than 175 ps after excitation with a 30 ps laser pulse. Trissl and Kunze concluded that the mean exciton trapping time in both photosystems leading Co charge separation is thus equal to, or shorter than 175 ps. There was no evidence for an intermediate rising phase of the photovoltage in the time range of 400 ps Co 4 ns. Fluorescence decay kinetics provide information on all types of excitons, including those decaying within a time interval comparable to the first



passage time, excitons which have visited the t r a p s without initiating photochemistry, and excitons which are generated by Klimov-type recombination processes and which have been returned to the antenna. As Trissl and Kunze point out, the power of the photoelectric method lies in the fact that only those exciton phases are detected which give rise to charge separation in the reaction centers. Their results thus suggest that only the first fluorescence decay phase (the < 200 ps components associated with PSI and PSII antenna fluorescence) should be attributed to primary exciton trapping events. The longer-lived fluorescence decay components may arise from excitons which have already visited the reaction centers and whose lifetimes are somehow prolonged by their interactions with the reaction centers. In open PS II reaction centers near the F o level, one such mechanism could involve ultrafast charge recombination as proposed by Breton [31] and by Klimov [23]: P680+-I--Q ---> P680w-I-Q ---> P680-1-Q + exciton


In this model, the lifetime of the exciton could be limited by the P680+-I -Q ---> P680+-I-Q - charge stabilization on the accepter Q. The time for such a process is estimated as ~ 200 ps. If this model and the associated time scale of ~ 200 ps are correct, then it becomes more difficult to rationalize the experimentally observed longer ( > 200ps ) fluorescence decay phases. However, it appears intuitively that an expanded and more complex bipartite kinetic scheme taking such processes into account explicitly, could account for the experimental observations in which the observed decay times are complex functions of the model parameters as in eq. 10. The fast flucI'eseenee decay phase, and eompetltlom between a n n : t h I l a t t o n and t r a p p i n g by r e a c t i o n centers


In an effort to correlate the different fluorescence decay phases with capture of excitons by PS II reaction centers, high intensity picosecond laser excitation double pulse experiments were devised [32]. In these experiments it was found that only the initial 150 ps exciton decay phase produced by the first pulse was active in quenching excitons produced by the second pulse (F state). The intermediate second phase of the first pulse, even though i~ dominates the overall fluorescence yield [24,25], is not active in annihilating excitons generated by the second pulse; the intermediate fluorescence decay phase in the F o state was thus attributed to relatively immobile excitons, in contrast to the short-lived ( < 200 ps) excitods [32]. A detailed comparison of the closing of PSII reaction centers induced by single picosecond laser pulses of variable intensities, with the decrease in the overall fluorescence yield produced by the same laser pulses, lead to the startling conclusion that exciton-exciton annihilation processes are not accompanied by decreases in the efficiencies of exciton trapping by PS II reaction centers [33]. It was concluded that the fast exciton decay component displays a relatively low sensitivity towards bimolecular annihilation processes because of rapid trapping by PS II reaction centers. This observation is consistent with the results of the double-pulse experiments, and the fast photovoltage kinetics [30]. The intermediate and longer fluorescence decay phases appear to be due to photophysical events other than primary exeiton trapping, and may be due to excitons



which have already visited the RC, or have been re-injected from the RC into the antenna; because of their longer lifetimes, these excitons are susceptible to bimolecular exciton-exciton annihilations, thus giving rise to a decrease in the integrated fluorescence yield as the laser pulse excitation energy is increased (for a review of exciton annihilation, s e e [343). Finally, it is interesting to point out that in purple photosynthetic bacteria, competition between exciton-exciton annihilation and exciton trapping by reaction centers is indeed effective; because of this competition the efficiency of trapping decreases as the intensity of picosecond lasers is increased [ 35]. Thus, the topological details of the reaction centers embedded within the array of antenna complexes is probably quite different in green plants than in photosynthetic bacteria. Coucltwtoem

Recent, accurate measurements of fluorescence decay profiles in green plants have provided a new impetus to studies of primary energy transfer processes in green plants. The decay profiles are usually represented by a sum of 3-4 exponentials with positive amplitudes. These different decay components are attributed to exciton decay in the light harvesting antenna complexes containing chlorophyll b associated with PS II, or chlorophyll a antenna systems associated with P S I and PS II. Heterogeneity of photosynthetic units ( ~ and ~ units} has been invoked in order to account for the complexities of the decay profiles utilizing either random walk or kinetic coupled differential equations based on Butler's heterogeneous bipartite model. Photoelectric and exciton-exciton annihilation experiments suggest that only the fast fluorescence decay components ( < 200 ps) are directly involved in primary energy transfer involving the migration of excitons from the antenna to the reaction centers, followed by charge separation at the reaction centers.

Ao,knowledKenent;s This work was supported by National Science Foundation grants PCM-83-08190 to N.E.G. at New York University, and U.S. Department of Agriculture grant 82-CRCR-1-1129 to R.S.K. at the University of Rochester. References I. 2. 3. 4. 5. 6. 7. 8.

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Energy migration and exciton trapping in green plant photosynthesis.

The possible origins of the different fluorescence decay components in green plants are discussed in terms of a random walk and Butler's bipartite mod...
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