Proc. Natl. Acad. Sci. USA 77 (1980) 1229

Correction. In the article "Organelle DNA variation and sys-tematic relationships in the genus Zea: Teosinte" by D. H.Timothy, C. S. Levings III, D. R. Pring, M. F. Conde, and J. L.Kermicle, which appeared in the September 1979 issue of Proc.Natl. Acad. Sci. USA (76, 4220-4224), the authors request thatthe following corrections be noted. On p. 4220 in the Abstract,the fourth sentence should read "Separation of the teosinte andmaize organelle DNAs into six groups (Guatemala; perennialteosinte; Balsas and Huehuetenango; Central Plateau andChalco; Nobogame; and maize) approximated the biosystematicrelationships of the taxa." On p. 4222, in the right-hand columnunder the heading "Organelle DNA Evolution in Parallel withthe Nuclear System," the third sentence should read, "Thearrangement of these distinct groups into one hierarchicalstructure results in the delineation of six classes which corre-spond to conventionally determined taxonomic entities as fol-lows: (i) race Guatemala, (ii) perennial teosinte, (iii) racesHuehuetenango and Balsas, (iv) races Central Plateau andChalco, (v) race Nobogame, and (vi) several stocks of normalmaize of the U.S. Corn Belt type." On p. 4223 in line 14 of theright-hand column, delete "and maize," and in lines 3 and 4from the bottom, delete "as its ctDNA resembles maize,".

Correction. In the article "Triplet states in photosystem I ofspinach chloroplasts and subehloroplast particles" by Harry A.Frank, Mary B. McLean, and Kenneth Sauer, which appearedin the October 1979 issue of Proc. Natl. Acad. Sci. USA (76,5124-5128), an error occurred in the Proceedings editorialoffice. On p. 5125 in Fig. 2 and on p. 5126 in Fig. 3, the scaleof magnetic field strength, which is now shown to span the re-gion of 3000-3500 G in 100-G increments, should be correctedto span the region of 2750-3750 G in 200-G increments.

Correction. In the article "Effect of interchain disulfide bondon hapten binding properties of light chain dimer of protein315" by Raphael Zidovetzki, Arieh Licht, and Israel Pecht,which appeared in the November 1979 issue of Proc. Natl.Acad. Sci. USA (76,5848-5852), an undetected printer's errorresulted in the misspelling of the first author's surname. Itshould have appeared as "Zidovetzki."

Correction. In the article "Cloning of integrated Moloneysarcoma proviral DNA sequences in bacteriophage A" by G.F. Vande Woude, M. Oskarsson, L. W. Enquist, S. Nomura, M.Sullivan, and P. J. Fischinger, which appeared in the September1979 issue of Proc. Natl. Acad. Sci. USA (76, 4464-4468), theauthors request that the following correction be noted. On page4468 under Note Added in Proof, in line 2 "140-kb" should bechanged to "15.0-kb."

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Proc. Natl. Acad. Sci. USA 77 (1980) 1229

Correction. In the article "Organelle DNA variation and sys-tematic relationships in the genus Zea: Teosinte" by D. H.Timothy, C. S. Levings III, D. R. Pring, M. F. Conde, and J. L.Kermicle, which appeared in the September 1979 issue of Proc.Natl. Acad. Sci. USA (76, 4220-4224), the authors request thatthe following corrections be noted. On p. 4220 in the Abstract,the fourth sentence should read "Separation of the teosinte andmaize organelle DNAs into six groups (Guatemala; perennialteosinte; Balsas and Huehuetenango; Central Plateau andChalco; Nobogame; and maize) approximated the biosystematicrelationships of the taxa." On p. 4222, in the right-hand columnunder the heading "Organelle DNA Evolution in Parallel withthe Nuclear System," the third sentence should read, "Thearrangement of these distinct groups into one hierarchicalstructure results in the delineation of six classes which corre-spond to conventionally determined taxonomic entities as fol-lows: (i) race Guatemala, (ii) perennial teosinte, (iii) racesHuehuetenango and Balsas, (iv) races Central Plateau andChalco, (v) race Nobogame, and (vi) several stocks of normalmaize of the U.S. Corn Belt type." On p. 4223 in line 14 of theright-hand column, delete "and maize," and in lines 3 and 4from the bottom, delete "as its ctDNA resembles maize,".

Correction. In the article "Triplet states in photosystem I ofspinach chloroplasts and subehloroplast particles" by Harry A.Frank, Mary B. McLean, and Kenneth Sauer, which appearedin the October 1979 issue of Proc. Natl. Acad. Sci. USA (76,5124-5128), an error occurred in the Proceedings editorialoffice. On p. 5125 in Fig. 2 and on p. 5126 in Fig. 3, the scaleof magnetic field strength, which is now shown to span the re-gion of 3000-3500 G in 100-G increments, should be correctedto span the region of 2750-3750 G in 200-G increments.

Correction. In the article "Effect of interchain disulfide bondon hapten binding properties of light chain dimer of protein315" by Raphael Zidovetzki, Arieh Licht, and Israel Pecht,which appeared in the November 1979 issue of Proc. Natl.Acad. Sci. USA (76,5848-5852), an undetected printer's errorresulted in the misspelling of the first author's surname. Itshould have appeared as "Zidovetzki."

Correction. In the article "Cloning of integrated Moloneysarcoma proviral DNA sequences in bacteriophage A" by G.F. Vande Woude, M. Oskarsson, L. W. Enquist, S. Nomura, M.Sullivan, and P. J. Fischinger, which appeared in the September1979 issue of Proc. Natl. Acad. Sci. USA (76, 4464-4468), theauthors request that the following correction be noted. On page4468 under Note Added in Proof, in line 2 "140-kb" should bechanged to "15.0-kb."

Corrections

Proc. Natl. Acad. Sci. USAVol. 76, No. 10, pp. 5124-5128, October 1979Biophysics

Triplet states in photosystem I of spinach chloroplasts andsubchloroplast particles

(photosynthesis/digitonin/P-700/electron paramagnetic resonance/chlorophyll)

HARRY A. FRANK, MARY B. MCLEAN, AND KENNETH SAUERLaboratory of Chemical Biodynamics, Lawrence Berkeley Laboratory, and Department of Chemistry, University of California,Berkeley, California 94720

Communicated by Melvin Calvin, June 28,1979

ABSTRACT We report light-induced electron paramagneticresonance triplet spectra from samples of chloroplasts or digi-tonin photosystem I particles that depend upon the dark redoxstate of the bound acceptors of photosystem I. If the reactioncenters are prepared in the redox state P-700 A X- FdB- FdA-,then upon illumination at I1K we observe a polarized chloro-phyll triplet species which we interpret as arising from radicalpair recombination between P-700- and A-. This chlorophylltriplet is apparently the analog of the PR state of photosyntheticbacteria [Parson, W. W. & Cogdell, R. J. (1975) Biochin. Biophys.Acta 416, 105-1491. If the reaction centers are prepared in thedark redox state P-700 A X FdB- FdA-, then upon illuminationat IlK we observe a different triplet species of uncertain origin,possibly pheophytin or carotenoid. This species is closely asso-ciated with the photosystem I reaction center and it traps ex-citation when P-700 is oxidized.

Electron paramagnetic resonance (EPR) detection of tripletstates has provided an effective probe of both the mechanismof the primary light reaction of bacterial photosynthesis andthe structure and geometry of reaction center components (1).The first observation of a triplet state in photosynthetic bacteriaby EPR methods by Dutton et al. (2) has led to a significantadvance in our understanding of the initial charge separationprocess. They showed that intense, spin-polarized triplet EPRsignals arise upon illumination at low temperatures under re-ducing conditions when normal photochemistry is inhibited.Further work in this area has revealed that this triplet state,designated PR, forms on the primary electron donor, P-860, asthe result of a charge recombination reaction between thephotoreduced electron acceptor, I-, and the photooxidizedprimary donor P-860+ (3). However, in green plant and algalpreparations, only low-intensity EPR triplet signals, which mostlikely originate outside the reaction center, have been reported,and no unambiguous assignment of a triplet state to the primaryphotoreactions has been made (4-9). A component of delayedluminescence observed optically by Shuvalov et al. (10, 11) wasattributed to triplet formation dependent upon the redox stateof the reaction center of photosystem I.Our choice of sample conditions for studying EPR triplet

spectra was guided by the current model of the photosystemI reaction center, which may be represented as P-700 A X FdBFdA. P-700 is the primary electron donor (12); FdB and FdA areiron sulfur centers (13, 14); and X is a species of unknownchemical composition that can be observed in its reduced stateby EPR at liquid helium temperatures (15). In samples con-taining reduced FdB and FdA, illumination at liquid heliumtemperature reduces X to X-, which then undergoes a backreaction with P-700+ with a decay time of 130 msec (16). A isan acceptor species that participates as an intermediate in the

light-induced charge separation between P-700 and X (16, 17).When X has been reduced prior to illumination (16,17) or whenX and the iron sulfur centers are chemically inactivated (18,19), a back reaction attributed to P-700+ and A- occurs witha decay time of 1 msec at liquid helium temperatures in pho-tosystem I subchloroplast particles. Under the same redoxconditions in chloroplasts at liquid helium temperatures, twocomponents with half-times of 122 ,gsec and 1.7 msec contributeto the decay (20). Motivated by these new findings, we havedesigned experiments to detect triplet states by EPR in samplesin which the normal photochemistry of photosystem I is blockedimmediately beyond the initial electron acceptor.

MATERIALS AND METHODSChloroplasts were isolated from market spinach in 0.4 M su-crose/10 mM NaCl/10mM Tris buffer, pH 8.0/10 ,gM EDTAand collected by centrifugation at 5000 X g for 5 min.To prepare digitonin photosystem I subchloroplast particles,

we resuspended chloroplasts to a chlorophyll concentration of0.3-0.4 mg ml-l in 50mM Tris buffer (pH 8.0) containing 10mM Mg2+ to assure clean fractionation of photosystem I fromphotosystem 11 (21). Digitonin was added to the chloroplastsuspension as a 10% (wt/vol) solution to give 0.5% (wt/vol) di-gitonin. After incubation for 2 hr at 40C, the detergent incu-bation mixture was centrifuged for 0.5 hr at 30,000 X g. Thesupernatant contained photosystem I particles with the char-acteristics: chlorophyll a/chlorophyll b = 5.6 and chloro-phyll/P-700 = 175.The supernatant was concentrated for EPR studies by pre-

cipitation with protamine sulfate as described by Nelson et al.(22).Treatment with Dithionite. Chloroplasts or digitonin pho-

tosystem I pellets were degassed under reduced pressure andmixed with sodium dithionite in 100 mM glycine buffer (pH10) under a nitrogen atmosphere to give 12 mM dithionite.Treatment with Ferricyanide. Chloroplast or digitonin

photosystem I pellets were mixed with K3Fe(CN)6 in 50 mMTris buffer (pH 8) to give 1 mM ferricyanide.The treated pellets were then combined with an equal vol-

ume of ethylene glycol, sealed in EPR tubes, and stored at 77K.Final chlorophyll concentration of the samples was about 2 mgml-l. Samples prepared in Condition I (described below) wereilluminated by a tungsten lamp for approximately 3 min andfrozen to dry ice/acetone temperature under illuminationbefore they were stored at 77K.EPR measurements were made with a Varian E-109 spec-

trometer at X-band with 100 kHz field modulation andequipped with an Air Products Helitron cryostat. The tripletstate signals were detected by a light modulation technique by

Abbreviation: EPR, electron paramagnetic resonance.

5124

The publication costs of this article were defrayed in part by pagecharge payment. This article must therefore be hereby marked "ad-vertisement" in accordance with 18 U. S. C. §1734 solely to indicatethis fact.

Proc. Natl. Acad. Sci. USA 76 (1979) 5125

which the exciting light was chopped at 33.5 Hz. The outputof the EPR system was fed directly to a PAR (Princeton AppliedResearch, Princeton, NJ) model 210 selective amplifier and thento a PAR model 220 lock-in amplifier that was referenced tothe chopper.

Excitation was provided by an Oriel 1000-W xenon lampfiltered by 5 cm of water. Temperature was measured with agold/chromel thermocouple. No change in the relative signsof the EPR signal occurred when the microwave power wasreduced to 1 AtW, when the chopper frequency was loweredto 11 Hz, or when the detector phase angle on the lock-in am-plifier was altered.

RESULTSCondition 1: Dithionite, pH 10, Frozen under Illumina-

tion. Chloroplasts or digitonin photosystem I particles that werefrozen under illumination in the presence of dithionite gave thedark EPR spectrum shown in Fig. 1A. In the light-modulatedtriplet state spectra for chloroplasts (Fig. 2A) and digitoninphotosystem I particles (Fig. 3A) prepared in condition 1, onemajor triplet, denoted triplet I, was observed. Triplet I has thespin polarization pattern aee aae, where a denotes a signal inabsorption and e denotes a signal in emission. The zero-fieldsplitting parameters of triplet I are ID I = 0.0278 ± 0.0009 cm-land IE I = 0.0039 + 0.0009 cm.- (Table 1).

Condition 2: Dithionite, pH 10, Frozen Dark. Chloroplastsand digitonin photosystem I particles that were frozen dark in

9 2.05 2.00

A

B

1 OOG

1.89 1.78

FIG. 1. EPR spectra of reduced chloroplasts observed in the darkat ilK. Conditions under which the samples were frozen were: (A)Dithionite, illumination while cooling; (B) dithionite, dark. EPRconditions for both spectra were: microwave power, 10 mW; sweep

time, 2 min; time constant, 0.5 sec; modulation amplitude, 16 G;modulation frequency, 100 kHz; microwave frequency, 9.079 GHz;receiver gain, 2500.

3200 3300Magnetic field strength, G

FIG. 2. Light-modulated, triplet state spectra of chloroplasts.Conditions under which the samples were frozen were: (A) dithionite,illumination while cooling; (B) dithionite, dark; (C) ferricyanide. EPRconditions for all three spectra were: microwave power, 1 mW; sweejtime, 1 hr; recorder time constant, 30 sec; modulation amplitude, 1G; modulation frequency, 100 kHz; receiver gain, 80; microwave fre-quency, 9.075 GHz; light modulation frequency, 33.5 Hz.

the presence of dithionite gave the 11K dark EPR spectrumshown in Fig. 1B. Figs. 2B and 3B show the light-induced tripletsignals obtained in condition 2 from chloroplasts and digitoninphotosystem I particles, respectively. One major triplet state,denoted triplet II, was observed. Triplet II has the spin polar-ization pattern eae aea and zero-field splitting parameters IDI= 0.0383 i 0.0013 cm-l and IEI = 0.0040 + 0.0013 cm-l

Biophysics: Frank et al.

Proc. Natl. Acad. Sci. USA 76 (1979)

3000 3100 3200 3300 3400 3500

Magnetic field strength, GFIG. 3. Light-modulated triplet state spectra of digitonin pho-

tosystem I particles. Conditions under which the samples were frozenwere: (A) dithionite, illumination while cooling; (B) dithionite, dark;(C) ferricyanide. EPR conditions for spectra A and B were: microwavepower, 1 mW; sweep time, 1 hr; recorder time constant, 30 sec; mod-ulation amplitude, 16 G; modulation frequency, 100 kHz; receivergain, 20; microwave frequency, 9.075 GHz; light modulation fre-quency, 33.5 Hz. EPR conditions for spectrum C were the same as inA and B except for receiver gain, which was 80.

(Table 1). We made this assignment as follows. The innermostsignals were assigned to the Y+ and Y- transitions because oftheir characteristic shape. The other major features, labeled X+and X, were used with the assignments of Y+ and Y- and therelation (23)

Hx+- Hx- + Hy+- Hy- = Hz+- Hz-

Table 1. Zero-field splitting parameters and electron spinpolarization patterns of observed triplet state signals

PolarizationTriplet IDI,cm-' IEI,cm-' pattern

I 0.0278 + 0.0009 0.0039 + 0.0009 aee aaeII 0.0383 + 0.0013 0.0040 + 0.0013 eae aea

The errors represent the uncertainty in the parameters as deducedfrom the repeatability of the field position measurements. a, Ab-sorption; e, emission.

to calculate the positions of the third transitions, Z+ and Z-. Thecalculated value agrees with small features that appear repro-ducibly in the spectra shown in Figs. 2 and 3.

Condition 3: Ferricyanide, pH 8. Figs. 2C and 3C show thelight-induced triplet signals obtained in condition 3 for chlo-roplasts and digitonin photosystem I particles, respectively.Once again we observe triplet II as the major species, with thepolarization pattern eae aea and zero-field splitting parametersID = 0.0383 + 0.0013 cm-l and El =0.0040 i 0.0013 cm-l(Table 1).

DISCUSSIONThe dark signals at g = 1.78 and g = 1.89 in Fig. 1A indicatethat X and FdB become reduced in samples frozen under illu-mination in the presence of dithionite (24). During subsequentlight-modulation experiments in this redox state, we observelight-induced signals that accompany the process of chargeseparation and recombination (16, 17, 20) which we interpretas

P-700 A X- FdB- FdA- P-700+ A- X- FdB FdA,

T1/2 = 1 msec.

The aee aae polarization pattern of triplet I is characteristicof triplets formed via a charge recombination reaction and isbest explained by the radical pair mechanism (1). Accordingto this mechanism, the system is initially prepared in an excitedsinglet state. After one electron is transferred from a donor toan acceptor, a change in spin correlation occurs between theelectron localized on the acceptor and the one remaining on thedonor. This mixes the singlet state, S, predominantly with themiddle-energy high-field triplet spin sublevel, To. The effectof this process is to drive the population into the To level se-lectively. Hence, all To to T+1 transitions are in absorption andall To to T-1 transitions are in emission. Thus, the aee aaeradical pair polarization pattern is observed in the triplet stateEPR spectrum.The radical pair mechanism explains the observation in the

photosynthetic bacteria of the triplet state, PR, which has theradical pair polarization pattern (3, 25). Also, the radical pairmechanism is known to be operating in photosystem I fromrecent studies of chemically induced dynamic electron polar-ization observed in green plant preparations (26-28), whichwere interpreted by Friesner et al. (29) to arise from a dynamicinteraction between P-700, A, and X. We believe that tripletI, whose spectrum is shown in Figs. 2A and 3A, is the photo-system I analog of the bacterial PR state.The zero-field splitting parameters for triplet I (see Table 1)

are precisely those observed for monomeric chlorophyll a (25,30). The bacterial PR state zero-field splitting parameters areabout 20% smaller than the corresponding monomeric bac-teriochlorophyll a values measured in vitro (1, 25). This isconsistent with the idea that the triplet state, PR, is delocalizedover more than one molecule-i.e., the bacterial reaction centerprimary donor, P-860, is a bacteriochlorophyll dimer (1, 25).

5126 Biophysics: Frank et al.

Proc. Natl. Acad. Sci. USA 76 (1979) 5127

In view of the fact that P-700 is thought to be a chlorophyll adimer (1, 31), the observation of monomeric chlorophyll a IDand E I values for triplet I is puzzling.

If triplet I is not localized on P-700, it could be centered ona chlorophyll a monomer closely associated with the reactioncenter and on which the charge recombination reaction energyis trapped. Such a process would have to occur coherently so thatthe spin polarization is preserved. Alternatively, triplet I mayremain on the acceptor A after charge recombination betweenP-700+ and A- takes place. It has been suggested that A is achlorophyll species (29). We are not aware, however, of anyprecedent for this kind of event.

If triplet I is localized on P-700, then we must explain the factthat the zero-field splitting parameters correspond to mono-meric chlorophyll a values. Clarke et al. (32, 33) have proposeda simple exciton model which they use to calculate the anglebetween the chlorophyll planes of the bacterial dimer, P-860,based on a comparison between monomeric bacteriochlorophyllzero-field splittings measured in vitro and those obtained forseveral species in vivo. Following this reasoning, our resultscould be explained by a plane-parallel P-700 dimer structurewhere the monomeric magnetic axes are all parallel. This pos-sibility was suggested as the model for P-700 by Fong (34).However, this interpretation is not fully consistent with theP-700 circular dichroism spectrum obtained by Philipson et al.(35). Further experimental and theoretical investigations willbe needed to corroborate structural models based on observedtriplet state parameters with those obtained from opticalmeasurements.The signal at g = 1.89 in Fig. 1B indicates that FdA and FdB

are reduced (24), but the absence of a signal at g = 1.78 showsthat X is not reduced when samples are frozen dark in thepresence of dithionite. Subsequent illumination at liquid heliumtemperatures of samples in this redox state causes the rapidtransfer of an electron from P-700 to X. Because the donorsystem to P-700+ does not function at low temperatures (20)and the charge recombination time between P-700+ and X-is 130 msec (16), illumination produces the redox state P-700+A X- FdB- FdA- during light modulation experiments.The eae aea polarization pattern seen in triplet II is one

among many patterns that can arise from a molecular inter-system crossing mechanism populating the lowest triplet stateof an aromatic molecule. Such a mechanism has been studiedin great detail for aromatic hydrocarbons (36-38) and chloro-phylls (23, 39, 40). The eae aea polarization pattern indicatesthat the most populated triplet spin sublevel is the middle-energy zero-field level (39). The population is driven into thislevel as the result of spin-orbit and vibronic coupling betweenthe singlet and triplet manifolds of states of an isolated molecule(41, 42). In contrast to the radical pair mechanism, no chargetransfer-recombination process need be operating for the tripletto be formed. Consequently, spin polarization patterns distinctfrom the radical pair mechanism pattern are observed.

Thus, we believe that triplet II forms while the photosystemI reaction center is in the charge separated P-700+A X- FdB-FdA-state. Because the back reaction time between X- andP-700+ is sufficiently slow (see above), the P-700 trap remainsclosed to excitation during the light-modulation time period.The excess excitation energy incident on the sample is funnelledinto a different trap where molecular intersystem crossing takesplace to form triplet II.

The zero-field splitting parameters of triplet II (see Table 1)are substantially larger than those of either chlorophyll or

pheophytin monomers (25, 43). Similar triplet state parameterswere obtained by Hoff et al. (9), using optical detection ofmagnetic resonance techniques on reduced chloroplasts or di-

gitonin particles prepared without intense illumination whilefreezing (our condition 2). They suggested that the observedsignals arose from a non-chlorophyll species, possibly pheo-phytin. We feel that it is also possible that the signals arise fromcarotenoids. Numerous optical experiments on green plants andbacteria have revealed that carotenoid triplet states serve assinks for excess energy (44-48). However, triplet state EPRspectra of these systems are sparse, presumably due to the dif-ficulty of photoexciting carotenoids directly into their tripletstates (49). Chlorophyll sensitization greatly enhances the ca-rotenoid triplet population (49).Our studies of chloroplasts and digitonin photosystem I

particles treated with ferricyanide confirm the hypothesis thattriplet II appears when the P-700 traps are closed. In the pres-ence of ferricyanide we have the redox state P-700+ A X FdBFdA in the dark. One can see from Figs. 2 B and C and 3 B andC that the same triplet state spectrum, triplet II, arises eitherwhen all P-700 traps are closed by chemical oxidation (condi-tion 3) or when X is not reduced (condition 2). This result pro-vides evidence that triplet II is not localized on one of the maincomponents active in the primary charge transfer events ofphotosystem I, but serves as an energy sink for excess excitationthat never reaches P-700.Our observation of the radical pair polarization of triplet I

is consistent with the observation of a radical pair mechanismpolarizing the EPR signal from P-700+ and giving rise tochemically induced dynamic electron polarization duringnormal forward photochemistry at room temperature inchloroplasts (27-29). Furthermore, the observation of tripletI provides independent corroboration that an electron carrierA mediates in the charge transfer from P-700 to X (16, 17).Our conclusion that triplets I and II are associated with P-700

in the photosystem I reaction center is supported by (i) thelight-induced appearance of triplet I only when X is reducedprior to the EPR experiment; (ii) the disappearance of tripletI and the appearance of triplet II when P-700 is oxidized; and(iii) the observation of these events in a photosystem I-enricheddigitonin fraction.

This research was supported in part by the U.S. Department of-Energy under Contract W-7405-ENG-48 and by National ScienceFoundation Grant PCM 76-5074. H.A.F. is a National Institutes ofHealth Postdoctoral Fellow.

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