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Is There a Triplet State in Photosynthesis?

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Is There a Triplet State in Photosynthesis? 'it Reprinted from the Jozrr+~alof Scie?~tzfic6- Ivzdustvznl Research, 1973, Val 32, KO. 2, pp. 62-69 Is There a Triplet State in Photosynthesis? D. L. VAXDER MEULEN & GOVINDJEE Departments of Botany & Biophysics, University of Illinois, Urbana, Illinois 61801, USA RONI spectrophotometric (and other) work ration. In 1936, Gaffron and WohlI3 postulated igz vivo, and studies on the photochemistry that a metastable state of chlorophyll acts in some F of chlorophyll in solutions, this pigment mole- step of photosensitized reactions. The fact that cule has long bee11 thought to have a significant role many organic molecu!es can indeed be excited to in the primary events of photosyntnesisl. Chloro- a metastable level with a high yield was shown by W phyll has been shown to be an efficient photo- Porter14, using intense flashes of light. The catalyst, acting as a mediator ill various in vitro absorption spectrum of the lowest triplet state of oxidation-reduction reactions, oiten involving the chlorophyll was recorded by Livingston15 and storage of incoming light. In 1952, DuysensQb- Linschitz16 in 0,-free organic solvents. In the pre- served a reversible bleaching of the long-wdve sent communication, some of the studies of triplet absorption band of the bacteriochlorophyll fourAd states in vitvo and in preparations closer to the living in photosynthetic bacteria; only a very small frac- state are reviewed. The existence of a triplet state tion of the total pigment was involved. Similarly, in vivo has not yet been convincingly demonstrated. in green plants K0k3 discotered a light-induced (The techniques of difference and flash spectroscopy, absorbance decrease centred at about 700 nm due dek.yed light emission and electron paramagenetic to a small fraction of a special form of ch1orop;lyll resonance have been used for these studies.) a (Chl a) labelled P700; this was later shown to be Beyond being an assemblage of pertinent informa- due to the oxidation of P700 (~ef.4). Recently, tion, this article attempts to present a picture Doring et al.5 and Govindjee et ~1.~have shown a consistent witn the available data. One of the aims second light-induced absorbance change centred of this article is to encourage investigators to at 682 nm (P682). These two changes (P700 and reinvestigate the role of Clil triplets in vivo. P682) are suggested to originate in separate energy traps (or reactioll centres) of the two pigment sys- Characteristics of the Triplet State tems of photosynthesis7. The light ellergy absorbed Excited electionic states are due to the promo- by various pigments in vivo must be transferred tion of an electron from tne ground state distribu- efficiently to the reaction centre chlorophyll mole- tion, changlng the electron density configuration cules for photosynthesis to take places. When tne to one of higher energy. The excited singlet state photochenlistry of photosynthetic system is blocked is generally short-lived (10-8-10-9 sec) witn the or poisoned, it is noted that the fluorescence of valence electrons having opposite spi~s. [Lifetimes chlorophyll increases, suggesting a relationship be- of Chl singlet excited states in vitro aad in vivo, first tween photochenistry and Chl fluorescenceg~lO. measured by Brody and Rabinowitch17, were 15 This relationship holds good when singlet states and 1 nsec respectivelyls; and excited sisglet are lnvolved in phot~chemistry~~'~~. (S*) to grouiid state (G) transition leads to fluores- Chlorophyll molecules can exist in the excited cence (S*-+Gf hv').] An excited triplet state electronic state either in a singlet or triplet configu- is longer-lived (milliseconds cr more) wlth the two C VESDER JIEULES & GOVISDJEE. IS THERE -1 TRIPLET STATE IS PHOTOSYNTHESIS? electrons hav~ngparallel spms. Slnce the singlet solutions. At concentrations of chlorophyll greater and triplet states or molecules are of different than about 0.5 ;*,If, the biniolecular mode of multiplicity (i.e. spin quantum numbers S = 0 and quenchilig is observed to dominate. However, as 1, and therefore 2Sf 1 = 1 and 3 respectively), the Li~ingston'~points cut, if low intensity light is used, transitions between then1 are strictly forbidder:. chis decay mechanism will not be significant, due But irlteracticns (mixing) of the electro~ispin and to low triplet concentrations; this condition may orbital parts of the total angular monientum allcw hold good for much or all of in situ photochemistry. such transitiol~s[e.g. intersystem crossliig (S*_CST, As the concentration exceeds 500 pM, kg and hence where T = triplet) and phosphorescence (T--+ self-quenching increases2,$24. L GLhv", where hv" = phosphorescence)]. [We note PorteF5 measured k, to he about 1010 L mole-1 here that the energy gap between S* and G is usually sec-l in fluid solvents. This implies that there is nigher than betweerl T and G, and thus phospho- a nlechanism for the protection of the excited rescence is at a loriger wavelength than fluorescence triplet state from oxygen, since it is detected in (E .= hclh, wkere E is epergy; h, Planck's constant; solution, although fhe data do not ensure that such c, velocity of light; and A, the wavelength of light.] a process is important for photosynthesis itz vivo. Triplet states acquire a small compor:ent of singlet An oxygen concentration of only 1 pM will decrease character and singlets likewise become partially the triplet lifetime in benzene by a factor of two. triplet in natu~e. The spin-orbit coupling depends Fujimori and LivingstonZ6 recorded the effects of inversely on the elleigy gap (AE) between the two various added substances or1 the triplet decay rate states (S* and Tj, a11d on the synlmetries of the of chlorophyll in benzene. The oxidizing agents triplet and singlet states with respect to each 9-quinone and oxygen, as well as caroteI~es,some other. Spin-orbit coupling, and hence the prob- carotenoids and m-dinitrobenzene are efficient ability cf populating tile tiiplet state, also increases quenchers, with k, = 10gM-l sec-l. Quenching with atomic number; for example, substituting by transition group elements was observed by Lin- heavy atoms into aromacic rn~IecuIes or just into schitz and PekkarinenZ7. But since Mn2+ has little the solvent environment can often augment the quenching action in comparison with the other singlet-triplet nixing (internal and external heavy transition metal elements, one would conclude that atom effect respectivelylg). Heavy atorn impurity the k, effect is not related to the magnetic moment qbenching, in conjunctioi~ with flasi photolysis, of an ion. On the other hand, if the hydration of has been used to detein~ine tiiplet quantum the io11 was increased, k, decreased without any yields20. change in the magnetic moment. One might Most electrol~ic transitions in the :~,olecules suggest that iv~viva s~zppressionof the chlorophyll involved in photochemistly are eitiler xn* or nx* triplet state is due to some factor other than, the trai~sitions,d~~e to the excitation of an electron from environment of the water side of photosystem I1 a x-ring system or a localized non-bo~idi~ign orbital (Mn2+-enzyme complex) ; CheniaeZ8 has reviewed to a n* antibonding orbital respectively. The zx* the role of Mn2+ in 0, evolution by photosynthesis. promotion gives stlong absorptiorl bands, resulting Care must be tzken, however, in applying in vitvo in part from the symmetiical overlap be tween tne results to photosynthesis. 7c and x* orbitals; triplet zz* excited states have If the triplet state of chlorophyll is significant in lifetimes of about lo-, sec. The nn* is less piobable, the photosynthetic processes of living organisms important to since t+e spatial crerlap bctween the localized 12 arid is to be well understood, it seems orbital (e.g. on an 0 or N atom of chlorophyll) and acquire a kr-owledge of the characceristics of the the delocalized n* cibital :s sn~~ll;the triplet nx* chlorophyll triplet in more controlled slid well- intrinsic lifetime is 10-l-lO-L sec. The long lifetime defined conditions. In 1918, Calvin and Doro~gh~~ and high polarization (large elect1011 displaceme~lt) reported phosphorescence at 865 nlil from chloro- of the nn* state makes it a l~kelycandidate for being pllyll b in highly viscous solutions at low tempera- a reactive partner in electron transfer reactions. ture; this was later confirmed by Becker and Intermolecular quenching is also more likely fol this Eiasha30. The quantum yield for this luminescence transition, however, and will tend to reduce the was low the half-time of decay was about act~~allifetimeL1. 3x sec. Using pheophorbide a (a derivative of Chl, without Mg2+ and phytol tail), the ' heavy Chlorophyll Triplet in Solution atom eflect ' was observed by replacing the Mg2+ The kinetics of chlorophyll triplet decay in with copper; a quenching of the strong fluoiescence solution can be approximated by and an intensification of the phosphorescence band at 867 nm was observed31. 4CT) Chlorophyll e5,ciently sensitizes various oxidatioa- dt - ~I(CT)S~~(CT)V~B,(CT)(C)S~,(CT)(Q)reduction reactions in many different ~olvents~~3~~. .. (1) Auto-oxidations involving the following components are observed (Krasncvsky reaction33): (hydrazine, where CT, C and Q are the chlorophyll triplet, Chl ground state and external quencher concentrations cysteine, glutathione, thiourea, ascorbate, etc.)---t respectively, with their associated rate constants. (viologens, flavins, NAD, etc.). ~ivirtgston~~notes In benzene or pyridine2" kl N lo3 set-I, k, =109 L "Comparison of tne quantum yield of chlorophyll- mole-l sec-I and k, =lo7 L mole-1 sec-l. In the sensitized auto-oxidations with the quantum yield rigid, glassy state, k, is very small; phcsphorescence of fluorescence and its quenching demonstrates un- is observed. With higher concentrations, k, be- equivocally that a long-lived excited state is an comes more important.
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