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Quenching by 02 in Various Algae and Higher Plants Received for Publication March 29, 1983 and in Revised Form July 26, 1983

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Quenching by 02 in Various Algae and Higher Plants Received for Publication March 29, 1983 and in Revised Form July 26, 1983 P1ant Physiol. (1983) 73, 886-888 0032-0889/83/73/0886/03/$00.50/0 Electron Transport-Dependent Chlorophyll-a Fluorescence Quenching by 02 in Various Algae and Higher Plants Received for publication March 29, 1983 and in revised form July 26, 1983 DOUG BRUCE, WILLIAM VIDAVER, KONRAD COLBOW, AND RADOVAN POPOVIC Photobiology Group, Departments ofPhysics and Biological Sciences, Simon Fraser University, Burnaby, British Columbia V5A 1S6 CANADA ABSTRACT aquarium at 15°C with a 16 h photoperiod. Phaseolus vulgaris and Zea mays were greenhouse grown under natural illumina- A comparison of chlorophyll-a fluorescence in brown algae (Macro- tion; plants used were 2 to 4 weeks old. For Fmav' determinations cystis integrfolia, Fucus vesiculosis), green algae (Scenedesmusobliquus, in bean and corn, 8-mm leaf discs were floated on an aqueous Ulva sp.) and higher plants (bean, corn) show differences in the relative solution of IuM DCMU in the dark for 1 h prior to measurement. fluorescence intensities and induction time courses which charcterize To determine Fmav in seaweed, 8-mm discs were suspended in a each type of plant. These differences are not reflected in either the seawater solution of IMm DCMU for I h in the dark; kelp blade maximum fluorescence emission in the presence of 3-(3,4-dichloro- discs were first suspended in seawater for 30 min to allow partial phenyl)-1,1-dimethylurea (F.) or the nonvariable fluorescence (Fo). removal of the mucopolysaccarides which interfere with DCMU Constaucy of F, and F.., suggests functional similarities of photosystem inhibition. All seaweeds were kept at 10 to 1 5C in seawater until II and associated antennae pigments in the various classes of plants. The used. time course differences are observed only in the absence of 343,4- The fluorescence measuring apparatus, stainless steel pressure dichlorophenyl)-1,1-dimethylurea and appear, therefore, to be electron cell, and data acquisition technique have been previously de- transport dependent. During induction, the peak in fluorescence (F,) is scribed ( 12). Blue actinic light (Corning filter 4-96) was adjusted much lower in all ofthe alpe studied than in the higher plants. Exogenous to 10 w m-2 at the sample. 02 strongly quenches F, in all plants studied and our data indicate that All fluorescence determinations were done using dark-adapted the low F, in the alge can be partially accounted for by endogenous 02 samples for more than 1 h. Fo was determined with ~80 ms flash quenching. of actinic light. Results from samples in an 02 atmosphere were independent of the presence of 300 ,l/l CO2. RESULTS Photosynthetic plants can be classified according to the type of pigment system they possess. For example: red, brown, green Typical fluorescence induction curves for bean are seen in algae are so designated because these colors result from the Figure la. The upper trace shows Fmax in the presence ofDCMU; presence of phycoerythrin, fucoxanthin, and Chl-b as their re- lower traces are for untreated leaves under increasing O2 pres- spective accessory pigments. The brown algae also have Chl-c. sures (atm). The bottom trace is for Fo in air, normalized to 1 Only green algae and the terrestrial green plants share a common relative fluorescent unit. Figures lb and lc show the same set of pigment system. Despite this diversity in pigments, its signifi- measurements for Ulva and M. integrifolia, respectively. It is cance is presumably limited to light capture and the basic energy readily apparent that althoughfn - (Fma,. - FO)/FO is similar in conversion steps are believed to be similar for all 02 evolving these plants,fp (F, - Fo)/Fo is lower in the seaweeds, especially plants (1, 6). Chl-a is universally present in all plants which have so in M. integrifolia (Fig. ld). the capacity for water splitting, and there is much evidence to 02 reversibly quenchedf, in all plants studied (Fig. 1, a, b, c). indicate that the function of accessory pigments is to transfer The 02 quenching curves (Fig. 2) show similar half-quenching excitation energy to Chl-a (4). Excitation energy transfer is a 02 pressures of 7 atm for bean, 6 atm for Ulva, and 5 atm for highly effective quencher ofaccessory pigment fluorescence, thus M. integrifolia, suggestive of similar mechanisms for 02 quench- Chl-a fluorescence is indicative of light harvesting by the acces- ing;f, is lower in Ulva than in bean and lowest in M. integrifolia sory pigments as well as by Chl-a. at all 02 pressures. In this work we compare the in vivo Chl-a fluorescence emis- Half-quenching with DCMU present required more than 40 sion of two brown algal species, two green algae, and two higher atm 02 in all three plants, and 02 quenching off, fits the same plants in order to investigate possible differences in absorbed curve for all three (Fig. 2). The result is similar to that previously light energy utilization. We found major differences in both the reported for bean, Scenedesmus obliquus, and chloroplasts from relative fluorescence intensity and the dark adapted time courses. spinach and lettuce (1 1, 12). Using the technique of fluorescence quenching by hyperbaric 02 In Table I, values of fm and f, for various higher plants. (11, 12), we obtained results which suggest that some of the unicellular algae, and seaweeds are compared; fn is similar for difference in fluorescence emission by the various plants can be all ofthe plants, yetf,p is distinctly lower in the algae than in corn accounted for by the influence of 02 on electron transport. or bean. MATERIALS AND METHODS ' Abbreviations: Fma, maximum in variable fluorescence in the pres- Fresh samples of mature Macrocystis integrifolia, Fucus vesi- ence ofDCMU; Fo, 0 level fluorescence; F, peak in variable fluorescence culosis, and Ulva sp. were collected weekly and kept in an during induction of photosynthesis. 886 FLUORESCENCE QUENCHING BY 02 IN ALGAE AND HIGHER PLANTS 887 0 1L '-0 L0M 1 M Xo 10 ms for Fl for Fol 0 0 e == 0 1 time (s) FIG. 1. Fluorescence induction curves, a, bean; b, Ulva sp.; c, M. integrifolia; d, a comparison of the bean, Ulva sp., and M. integrifolia fluorescence induction curves in air. For a, b, and c, Fmox~was measured in the presence of DCMU, the control curve is labeled air, and in the lower traces the numbers refer to 02 pressures in atmospheres. The F0 trace in air is shown on an expanded time scale. Table I. fm andfpfor Higher Plants and Algae Plant fp frfplfn Bean 4.2 4.2 1.0 Corn 3.7 3.9 0.95 Ulva species 2.6 4.2 0.62 Macrocystis integrifolia 1.5 4.1 0.37 Fucus vesiculosis 1.4 3.8 0.37 Scenedesmus obliquus 1.1 3.7 0.30 variable fluorescence yield is determined by changes in the redox state of Q. With the above assumptions, the constancy off,m observed in the diverse plants studied is indicative of a functional similarity 20 in PSII and associated antennae pigments which permits in vivo 02 pressure (atm) comparisons of the relative redox state of Q. However, asf,, is a relative measure, similarities in absolute energy transfer efficien- FIG. 2. 02 quenching Offm.-- -) andfp (-) in bean (0), Ulva sp. cies from antennae to PSII are not implied. In algae not inhibited (E), and M. integrifolia (A). with DCMU, variable fluorescence was seen to be highly quenched. As fm was similar in all the plants, the low fp in the DISCUSSION algae suggests that during induction Q is relatively more oxidized Interpretation ofthe data is made under the following assump- in the algae than in the higher plants. Either less efficient water- tions (7). splitting, more efficient electron transport to PSI, or higher (a) The measured Fo is the minimum fluorescence yield re- oxidation losses from electron transport would result in a lower sulting from the maximum possible rate of energy transfer from f,. A major electron transport loss involves reduction of 02 and antennae pigments to PSII. the subsequent production of H202 (2, 3, 5, 9). We have previ- (b) DCMU changes the absolute fluorescence yield by the ously described the quenching of variable fluorescence by 02 in prevention of Q oxidation via electron transport. higher plants and unicellular algae and suggested that this is most (c) During the initial induction of photosynthesis (5-10 s), the likely due to oxidation of electron carriers near PSI by 02 (11, 888 BRUCE ET AL. Plant Physiol. Vol. 73, 1983 12). It has been reported that Scenedesmus obliquus shows higher brown seaweeds. Biochim Biophys Acta 590: 309-323 rates of 02 uptake (02 reduction) than spinach or soybean (2, 5). 2. BEHRENS PW, TV MARSHO, RJ RADMER 1982 Photosynthetic 02 exchange kinetics in isolated soybean cells. Plant Physiol 70: 179-185 The low variable fluorescence yield of S. obliquus (Table I) 3. EGNEUS H, U HEBER, U MATrHIESEN, M KIcRK 1975 Reduction of oxygen by supports these results if 02 is assumed to be the quencher ofSf. the electron transport chain of chloroplasts during assimulation of carbon We have shown the endogenous quenching off, to be greater in dioxide. Biochim Biophys Acta 408: 252-268 the brown algae than in higher land plants. As 02 is a potent 4. GOEDHEER JC 1972 Fluorescence in relation to photosynthesis. Annu Rev quencher offp in all the plants, it is conceivable that the endog- Plant Physiol 23: 87-112 enous quencher is 02 If so, higher rates of 02 reduction and 5. MARSHOTV, PW BEHRENs, RJ RADMER 1979 Photosynthetic oxygen reduction presumably H202 production are to be expected in the brown in isolated intact chloroplasts and cells from spinach.
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