uptakein thelightin chlamydomonas · 02uptake in the light in chlamydomonas time (min) sham 0 ou...

Plant Physiol. (1985) 79, 225-2300032-0889/85/79/0225/06/$0 1.00/0

02 Uptake in the Light in ChlamydomonasEVIDENCE FOR PERSISTENT MITOCHONDRIAL RESPIRATION

Received for publication February 26, 1985

GILLES PELTIER* AND PIERRE THIBAULTDepartement de Biologie, Service de Radioagronomie, CEN de Cadarache, B.P. No. 1, F-13115 Saint-Paul-Lez-Durance, France

ABSTRACT

The nature of the process responsible for the stationary 02 uptakeoccurring in the light under saturating CO2 concentration in Chkmydo-momns reiahardii has been investipted. For this purpose, a mass spec-trometer with a membrane inlet system was used to measure 02 uptakeand evolution in the algal suspension. First, we observed that the 02uptake rate was constant (about 0.5 micromoles of 02 per milligramchlorophyll per minute) during a light to dark transition and was notaffected by 3-(3,4-dichlorophenyl)-1,1-dimethylurea. Salicylhydroxamicacid had no effect on 02 uptake in the dark or in the light, but was foundto have the same inhibitory effect either in the dark or in the light whenadded to cyanide-treated algae. The stimulation of the 02 uptake ratedue to the uncoupling effect of carbonyl cyanide m-chlorophenylhydra-zone was about the same in the dark or in the light. From these results,we conclude that mitochondrial respiration is maintained during illumi-nation and therefore is not inhibited by high ATP levels. Anotherconclusion is that in conditions where photorespiration is absent, no otherlight-dependent 02 uptake process occurs. If Mehler reactions are in-volved, in Chlamydomoms, under conditions where both photosyntheticcarbon oxidation and reduction cycles cannot operate (as in cyanide-treated algae), their occurrence in photosynthesizin algae either undersaturating C02 concentration or at the CO2 compensation point appearsvery unlikely. The comparison with the situation previously reported inScenedesmus (R. J. Radmer and B. Kok 1976 Plant Physiol 58: 336-340) suggests that different 02 uptake processes might be present inthese two algal species.

uptake still occurs (7, 14, 25). The nature of this remaining 02uptake is at present unknown.

Mitochondrial dark respiration could be responsible for thisCO-insensitive 02 uptake (14). However, the first isotope exper-iments on microalgae and cyanobacteria illuminated by low lightintensities were interpreted as showing an inhibition by light ofdark respiration (18). On the other hand, reports of studies ofthe labeling of tricarboxylic acid cycle intermediates (16), or ofthe correlation between CO2 compensation point and CO2 effiuxfrom respiration (2), concluded that tricarboxylic acid cycle wasnot affected by light. Hence, the question is whether or not thereducing power which should continue to be produced withinthe mitochondria in the light is reoxidized through the mito-chondrial respiratory chain.

It has also been shown that direct 02 photoreduction (i.e.Mehler reactions) can be involved in 02 uptake processes in thelight (22). Such reactions could play an important role in greencells in supplying sufficient ATP for CO2 fixation (10, 23).However, in spite of the occurrence of Mehler reactions inisolated chloroplasts (10, 22), their existence in intact cells re-mains questionable (23).Thus, the participation ofmitochondrial respiration or Mehler

reactions to 02 uptake in the light are presently not elucidated.The aim of this work was to determine, in the green algaChlamydomonas reinhardii, the nature of the 02 uptake proc-esses present in the light under CO2 saturation when no photo-respiration occurs. For this purpose, we studied the effects on 02exchanges of respiratory oxidase inhibitors and of an uncouplerof oxidative phosphorylation. Our results provide evidence thatdark respiration is not inhibited by light and that Mehler reac-tions do not occur during CO2 fixation.

Mass isotope studies using 1802 provided evidence that 02uptake was occurring during photosynthesis both in algae (6, 15,18, 26) and in higher plants (7, 13). This 02 uptake process wasrecognized to be of a different nature from that taking place indark respiration ( 18, 19). Oxygenase activity of Rubisco' and theassociated metabolism of glycolate were shown to be involved inthis light 02 consumption (1, 4, 9). The effects of CO2 concen-tration on oxygenase activity in vitro (3) and metabolite fluxthrough the glycolate pathway (4, 25) allow the conclusion thatthese reactions (termed the photorespiratory glycolate pathwayor photosynthetic carbon oxidation cycle) are responsible for thatpart of the 02 uptake which is sensitive to CO2 concentration (7,13, 25). In the light, under saturating CO2 concentration, con-ditions where the oxygenase activity of Rubisco should be com-pletely inhibited and the glycolate pathway stopped, residual 02

'Abbreviations: CCCP, carbonyl cyanide m-chlorophenylhydrazone;Rubisco, ribulose-1,5 bisphosphate carboxylase/oxygenase; DCMU, 3-(3,4-dichlorophenyl)- 1, I-dimethylurea; SHAM, salicyl hydroxamic acid.

MATERIALS AND METHODS

Chlamydomonas reinhardii (wild type 137 c) was grown ax-enically and phototrophically as previously described (24). Airwas bubbled through the culture at a flow rate of about 20 1.h-'. Cells were harvested by centrifugation and then resuspendedin the culture medium lacking NH4'. The pH of the mediumwas 6.0. Chl concentration was between 25 and 40 ;tg Chl-ml['.Algal suspension was bubbled with air in a thermostated (25°C)flask, under a light intensity of 1000 uE-m-2s-' (400-700 nm),for at least 60 min. Then, the cell suspension was transferred toa thermostated (25C) reaction vessel (a cylindrical cavity madeof Plexiglas). The vessel was stirred with a magnetic bar andilluminated with incandescent light to obtain an incident quan-tum flux of 1000 ,AE-m-2-s-' (400-700 nm). A polypropylenemembrane at the bottom ofthe reaction vessel allowed dissolvedgases to be introduced into the mass spectrometer (MAT AtlasCH4). After bubbling the algal suspension with N2 in the light,1802(98.1% 180 from CEA Saclay, France) was injected to obtainan initial 02 concentration of about 20% 02. Then, the reaction

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PELTIER AND THIBAULT

vessel was closed, and NaHCO3 was added (10-2 M final concen-tration). The response time of the system was about 25 s. 02evolution and uptake were measured by alternately recording1602 (m/e = 32) and 1802 (m/e = 36). Each cycle lasted about30 s. 02 uptake rate (Uo) and gross 02 evolution rate (Eo) werecalculated from the expressions:

'O=A[801_180] ____02_____16_0

A( t k['802] [180 1])

/A[1602 16 16__02Eo (At

k['602]) + Uc 1 6021+ )[021

where k is the rate constant of 02 decrease due to the massspectrometer consumption. This rate constant was measured inthe absence of algae and was equal in our experimental condi-tions to 0.01 1 min-'. The mass spectrometer signal was calibratedon the basis of the equilibrium with air (258 Mm at 25°C). [16021and ['802 represent, respectively, the amounts ofeach molecularspecies expressed in ,mol 02-mg-' Chl, and A means that thedifference between two successive values (time interval At) wasused in the calculations.

For the experiment performed only in the dark, the algalsuspension was bubbled with air, then the vessel was closed.Respiration rates were measured by recording 1602 (m/e = 32)and were calculated from the expression:

R =A-'602] k['602]At

In one experiment carried out to determine the optimal CCCP'concentration, dark respiration and net photosynthesis weremeasured with a Clark-type 02 electrode (Rank Brothers). Chlcontent was determined after extraction with 90% methanol (v/v) as previously described (24).

RESULTS

In a previous study on Chlamydomonas (25), we reported thatafter switching on the light, the02 uptake rate decreased froman initial value ofabout 2,umol 02-mg' Chl. min-' to a station-ary value. The stationary level was reached about 1 h after thebeginning of illumination and was shown to depend on the CO2concentration. On the other hand, the process responsible forthe initial decreasing 02 uptake is insensitive to CO2 concentra-tion and will be studied later. Here, we are interested in thenature of the stationary uptake that remains even under saturat-ing CO2 concentrations. For this purpose, algae were pretreatedat least 1 h in the light in order to suppress the decreasing 02uptake process. Algal suspension was then transferred into anilluminated vessel and 02 exchanges were measured as describedin "Materials and Methods."

Figure 1 shows02 uptake (Uo) and gross evolution rates (Eo)in the light and in the following dark period. Stationary 02evolution rate was about 2 Mmol 02* mg-' Chl* min-'. 02 uptakerate in the light was 0.5,mol 02-mg-' Chl-min-' and nosignificant change was observed after switching off the light.Addition of DCMU (50Mm final concentration) in the light wasfound to have the same effect on02 exchanges as switching offthe light in the control. Such a continuity in the 02 uptake ratesuggests that the same process occurs in the light and in the darkand that this process does not depend on photosynthetic electrontransport. Mitochondrial respiration is known to be the mainprocess responsible for02 uptake in the dark. In order to test thehypothesis that such respiration persists in the light, we studiedthe effects of mitochondrial respiration inhibitors (cyanide andSHAM) on02 exchanges in the light in comparison with their

effects in the dark.

In the dark (Fig. 2), cyanide (1 mm final concentration) wasshown to inhibit 02 uptake rate by about 20%, whereas SHAM(1 mm final concentration) alone had no effect. When SHAMwas added to cyanide-treated algae, respiration rate was inhibitedby about 80% of the initial rate. The extent of the SHAM-induced decrease in 02 uptake was 0.30 MAmol 02Mmg ' Chl.min-'.

In the light (Fig. 3), addition of cyanide first stimulated 02uptake rate to a value of about 0.9 ,umol 02 mg ' Chl. min-',and then 02 uptake decreased and stabilized at a level of about0.6 Amol 02.mg-' Chl.min-'. After a short lag period, 02evolution rate was progressively reduced to the same level as the02 uptake rate. From this moment net 02 evolution was com-pletely inhibited. Addition ofSHAM (1 mm final concentration)to cyanide-treated algae was found to inhibit 02 evolution and02 uptake to the same extent. The decrease due to SHAMaddition was about 0.35 Amol 02-mg-' Chl min-'. Addition ofSHAM to untreated algae was found to have no effect on 02exchanges (Fig. 4). We note that after cyanide and SHAMadditions, residual 02 uptake rate in the dark was very low (about0.08 MAmol 02* mg' Chl* min-'; Fig. 2), whereas in the light (Fig.3) it remained at a relatively high value (about 0.3 Amol02Mmg-' Chl- min-'). This remaining 02 uptake was completelysuppressed by addition of 50 AM DCMU to the algal suspension(Fig. 5).The effect of the uncoupler CCCP on 02 exchanges was studied

in the dark and in the light. The first experiment was performedto determine the CCCP concentration which could induce amaximum uncoupling effect in the dark with a minimal effecton net 02 evolution in the light. To avoid any memory effect oflight on the uncoupling by CCCP, algae were preincubated inthe dark for at least 1 h. In this condition, basal respiration ratewas found to be lower (0.22 Amol 02 mg' Chl* min-') than theone observed after 1 h of illumination (Figs. 1 and 2). Anuncoupling effect on dark respiration was significant for a CCCPconcentration of 0.1 Mm and was maximum at 2 Mm, correspond-ing to an increase of the dark respiration rate of about 0.33 Amol02* mg ' Chl - min-' (Fig. 6). CCCP concentrations higher than2 gM strongly decreased the respiration rate. Inhibitory effect ofCCCP on net 02 evolution was first observed at a concentrationof 1 gM. We, therefore, chose a CCCP concentration of 1 ,M toperform experiments on 02 exchanges in the light. Figure 7shows that CCCP stimulated 02 uptake from 0.54 up to 0.80AMmol 02-mg' Chl -min-' without effect on gross 02 evolution.The stimulation (0.26 Amol 02-mg' Chl- min-') was about thesame as that observed in the dark (Fig. 6).

DISCUSSIONMany contradictory reports have been published on the ques-

tion of the persistence of 'dark' respiration in green cells in thelight. This topic has been recently reviewed by Graham (16).Initial studies on the blue-green alga Anacystis concluded thatthe dark respiration was inhibited by low light intensities whereashigh light intensities induced an increase in the 02 uptake rate.The increase was later attributed to photorespiration (18). In thesame way, the Kok effect was considered to be the consequenceof the inhibition of dark respiration bylight due to an increasein the ATP/ADP ratio (18). However, this later interpretationwas contested by Healey and Myers (17) who observed thatCCCP did not inhibit the Kok effect in Chlamydomonas.The aim of our work was to reconsider the question of the

participation of mitochondrial respiration to 02 uptake in thelight under conditions where any complication due to the pres-ence of photorespiratory 02 uptake was eliminated. Therefore,we performed our experiments under high CO2 concentrations.Under such conditions, the glycolate pathway was previouslyreported to be completely inhibited (25). We first observed that

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02 UPTAKE IN THE LIGHT IN CHLAMYDOMONAS

Time (min)

SHAM

0 ou 1 .0°

Dark

5 10 15

SHAM

FIG. 1. 02 exchanges at saturating CO2 concentrationduring a light to dark transition. Eo: gross 02 evolutionrate; Uo: 02 uptake rate. Initial 02 concentration was22% 02; initial NaHCO3 concentration was 10 mM; Chlconcentration was 23.7 Ag.ml-'. Similar results wereobtained when DCMU (50 gM final concentration) wasadded instead of switching off the light.

FIG. 2. Effects of cyanide and SHAM on dark 02uptake. Final concentrations of cyanide and SHAMwere I mM. Initial 02 concentration was 21% 02; Chlconcentration was 31.5 yggml-'.

20

Time (min)

the 02 uptake rate measured in light-pretreated Chlamydomonaswas the same in the light, in the dark, or in the presence ofDCMU. This suggests that in conditions where photorespirationdoes not take place, 02-consuming processes involved in the lightare only due to mitochondrial respiration.

This assumption was tested by studying the effects of mito-chondrial oxidase inhibitors on 02 exchanges. Cyanide was foundto act differently in the light than in the dark. In the dark, thetreatment of algae by cyanide gives a measurement of the maxi-mum capacity fo the alternative pathway (8), which was about80% of the total respiration rate in our conditions. BecauseSHAM alone had no effect on the respiration rate (Fig. 2), wecan conclude that the maximum rate of the Cyt path is at leastthe measured respiration rate. Thus, the effects of cyanide andSHAM in the dark can be easily interpreted in terms of the Cytand alternative pathways.

In the light, the effect of cyanide appears to be more complex.Complete inhibition of net 02 evolution was probably the con-

sequence of Rubisco inhibition by cyanide (20). If Calvin cycleis stopped, reducing power which continues to be producedcannot be used to fix C02 and can be diverted to 02. Thisexplains the cyanide-02 uptake stimulation observed at the onsetofillumination. Such a competition between CO2 and 02 towardsutilization of the reducing power generated by the photosystemshas been reported earlier to occur in the green alga Scenedesmus(26). However, 02 was unable to maintain the electron transportat the same rate as C02, as shown by an eventual decrease in the02 uptake rate. The reason for this regulation is unknown.

In spite of this complex effect of cyanide, SHAM, when addedto cyanide-treated algae was shown to have the same inhibitoryeffect on 02 uptake rate in the light and in the dark. Thisobservation supports the proposal that mitochondrial respirationis probably present in Chlamydomonas in the light. Surprisingly,SHAM was found to inhibit 02 evolution in the same extent as02 uptake in cyanide-treated algae. Because SHAM had no effecton 02 exchanges (Fig. 4), when added to untreated algae, we can

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conclude that this product does not directly inhibit photosyn-thetic electron transport. A possible explanationfor these coupledinhibitions would be to consider that in these conditions thereducing power used by mitochondrial respiration originatesfrom the chloroplast via the metabolic shuttles. In such condi-tions, the inhibition of the mitochondrial oxidations would leadto an accumulation ofthe reducing power within the chloroplastand therefore to an inhibition of 02 evolution because no moreelectron, acceptors are available. On the other hand, the occur-rence, in the light, after cyanide and' SHAM additions of aDCMU-sensitive 02 uptake confirms that cyanide can induce adifferent type of02 uptake process which was absent in untreatedalgae. This is supported by the fact that DCMU had no effect on02 uptake in' untreated algae (Fig. 1). Thus, the DCMU-sensitive02 uptake process, which' requires the photosynthetic electrontransfer could be due to Mehler reactions induced by cyanideaddition.The uncoupler CCCP was shown to induce about the same

increase in the 02 uptake rate measured in the dark (increase of

FIG. 3. Effects of cyanide and SHAM on 02 exchangesin the light at saturating CO2 concentration. Eo: gross 02evolution rate; Uo: 02 uptake rate. Final concentrationof cyanide and SHAM were I mm. Initial 02 concentra-tion was 22% 02; initial NaHCO3 concentration was 10mM; Chl concentration was 41.4 tg-ml-'.

FIG. 4. Effect ofSHAM (I mM) on 02 exchanges inthe light at saturating C02 concentration. Ed. gross 02

evolution rate; Uo: 02 uptake rate. Initial 02 concentra-tion was 18% 02; initial NaHCO3 concentration was 10mM; Chl concentration was 32.1 ug-ml-'.

20

0.33 ;mol 02.mg- Chl * min-') and in the light (increase of0.26Amol 02 * mg-' Chl * min-'. This similar effect ofCCCP providesa further argument that mitochondrial respiration continues inthe light and therefore is not inhibited by high levels of ATPgenerated by the chloroplast.The conclusion that in Chlamydomonas cells, mitochondrial

respiration is not inhibited by light, apparently disagrees withthe interpretation of-Hoch et al. (18). However, if inhibition was'observed in the cyanobacteria Anacystis, these authors failed toshow it in the green alga Scenedesmus. Moreover, it is nowconsidered that inhibition of dark respiration by light in cyano-bacteria (27) as well as in photosynthetic bacteria (29) is due tothe interaction between the respiratory and the photosyntheticchains present in the same membrane. In green algae, espiration

is sequestered in the mitochondria. The only interactions be-,tween chloroplasts and mitochondria must be thrgh metabolic

shuttles (11). On the basis ofATP measurements some authors

have concluded that mitochondrial espiration shod be in-hibited by ATP production within the chloroplast (2i, 28). Our

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Eo

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Uo

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SHAM

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02 UPrAKE IN THE LIGHT IN CHLAMYDOMONAS

FIG. 5. Effect of DCMU (50 pM) on residual 02uptake observed in the presence ofcyanide and SHAM.Eo: gross 02 evolution rate; Uo: 02 uptake rate. Finalconcentrations of cyanide and SHAM were I mm.Initial 02 concentration was 17% 02; initial NaHCO3concentration was 10 mM; Chl concentration was 34.3jg-ml1'.

0

Eim0

2.01

A5S)

.1

CCCP (M)

FIG. 6. Effect of CCCP on dark respiration and net 02 evolution. 02

concentrations were measured using an 0241ectrode chamber, algae weredarkened at least I h prior to the measurements; initial NaHC03 con-

centration was 10 mM; initial 02 concentration was 21% 02; Chl concen-

tration was 24 sAg.ml-'.

results are in conflict with this interpretation. Rather, we confirmthe pioneering isotope studies of Brown (5) who observed nolight inhibition of 02 uptake in Chlorella, in conditions wherephotorespiration was absent (8% 02 and 0.8% C02).Another conclusion which can be drawn from these experi-

ments is that in Chiamydomonas no other 02 uptake processlike Mehler reactions are present in the light under saturatingC02 concentrations. Moreover, even at the C02 compensationpoint, such reactions are very unlikely. This comes from the factthat the overall C02-sensitive 02 uptake measured in Chlamy-domonas was previously reported to be entirely due to theglycolate pathway (25). Therefore, ifMehler reactions are presentin Chlamydomonas, their existence is probably limited to con-ditions where both photosynthetic carbon reduction and oxida-tion cycles are inhibited (as in cyanide-treated algae).

This situation appears to be quite different in the green algaScenedesmus. In this species, Radmer and Kok (26) reported adirect and complete competition between 02 and C02 towardsthe utilization of the photosynthetically generated reducingpower. The use of inhibitors allowed the authors to concludethat a high capacity oxidase (possibly involving ferredoxin) dis-tinct from Rubisco was responsible for this process. In Chlamy

C)

;

.,1C

E

0

0

E

1.51

0.5

0 5 10 iS 20

Time (min)

FIG. 7. Effect ofCCCP on 02 exchanges in the light at saturating C02concentration. Eo: gross 02 evolution rate; Uo: 02 uptake rate. Finalconcentration of CCCP was I M; initial 02 concentration was 20% 02;

initial NaHCO3 concentration was 10 mM; Chl concentration was 28.9jig-ml-'.

domonas, the competition is not complete (12, 25): only about15% of the maximum electron flow (measured as gross 02

evolution) occurring at CO2 saturation can be diverted to 02 atthe C02 compensation point (see Table I in reference 25), and isentirely due to the photosynthetic carbo a oxidation cycle. Thesignificance of such differences concerning the 02 uptake proc-esses and the regulation ofthe electron flow under different CO2levels in these two algal species remains to be elucidated.

Acknowledgments-The authors thank Dr. B. Dumon for perfecting the dataacquisition and processing system and Dr. F. Rebeille for helpful discussions.Technical assistance of Mrs. A. Le Mouellic is gratefully acknowledged.

LITERATURE CITED

1. ANDREWS TJ, GH LORIMER, NE TOLBERT 1971 Incorporation of molecularoxygen into glycine and serine during photorespiration in spinach leaves.Biochemistry 10: 4777-4782

2. AzcoN-BIETo J, CB OSMOND 1983 Relationship between photosynthesis andrespiration. Plant Physiol 71: 574-581

3. BADGER MR, TJ ANDREWS 1974 Effects of C02, 02 and temperature on ahigh-affinity form of ribulose diphosphate carboxylse/oxygenase from spin-

,,

C

E.,aE

N

0

E:k

Time (min)

CCCPfi Light

0 0 000 00 o00000 0 E

*. 0 ~~00 S

** * Uo

229




ach. Biochem Biophys Res Commun 60:204-2104. BERRY JA, CB OSMOND, GH LORIMER 1978 Fixation of 802 during photores-

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oxygen. Am J Bot 40: 719-7296. BROWN AH, D WEIS 1959 Relation between respiration and photosynthesis in

the green alga Ankistrodesmus brauni. Plant Physiol 34: 224-2347. CANVIN DT, JA BERRY, MR BADGER, H FoCK, CB OSMOND 1980 Oxygen

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pathways in plants: the interaction of cyanide-resistant respiration with thecyanide-sensitive pathway. In DD Davies, ed, The Biochemistry of Plants,Vol 2. Academic Press, New York, pp 197-241

9. DiMoN B, R GERSTER, P TOURNIER 1977 Photoconsommation d'oxygene etbiosynthese de la glycine et de la serine chez Zea Mays. C R Acad Sci Paris284: 297-299

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Physiol 47: 373-37918. HocH G, OVH OWENS, B KOK 1963 Photosynthesis and respiration. Arch

Biochem Biophys 101: 171-18019. JACKSON WA, RJ VOLK 1970 Photorespiration. Annu Rev Plant Physiol 21:

385-43220. LORIMER GH, TJ ANDREWS, NE TOLBERT 1973 Ribulose diphosphate oxygen-

ase II. Further proof of reaction products and mechanism of action. Bio-chemistry 12: 18-23

21. MANGAT BS, WB LEWIN, RGS BIDWELL 1974 The extent of dark respirationin illuminated leaves and its control by ATP levels. Can J Bot 52: 673-681

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24. PELTIER G, P THIBAULT 1983 Ammonia exchange and photorespiration inChlamydomonas. Plant Physiol 71: 888-892

25. PELTIER G, P THIBAULT 1985 Light-dependent oxygen uptake, glycolate, andammonia release in L-methionine sulfoximine-treated Chiamydomonas.Plant Physiol 77: 281-284

26. RADMER RJ, B KOK 1976 Photoreduction of 02 primes and replaces CO2assimilation. Plant Physiol 58: 336-340

27. SANDMANN G, R MALKIN 1984 Light inhibition of respiration is due to a dualfunction of the cytochrome b6-fcomplex and the plastocyanine/cytochromec-553 pool in Aphanocapsa. Arch Bioch Biophys 234: 105-111

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