Plant Physiol. (1980) 66, 1032-10360032-0889/80/66/ 1032/05/$00.50/0

Effect of CO2, 02, and Light on Photosynthesis andPhotorespiration in Wheat

Received for publication April 10, 1980 and in revised form June 30, 1980

ALAIN GERBAUD AND MARCEL ANDREDepartement de Biologie, Service de Radioagronomie, CEN Cadarache, BP 1, 13115 Saint-Paul-Lez-Durance,France

ABSTRACT

Unidirectional 02 fluxes were measured with 1802 in a whole plant ofwheat cultivated in a controOled environment. At 2 or 21% 02, 02 uptakewas maximum at 60 microliters per liter CO2. At lower CO2 concentrations,it was strongly inhibited, as was photosynthetic 02 evolution. At 2% 02,there remained a substantial 02 uptake, even at high CO2 level; the 02evolution was inhibited at CO2 concentrations under 330 microliters perliter. The 02 uptake increased linearly with light intensity, starting fromthe level of dark respiration. No saturation was observed at high lightinten-sities. No significant change in the gas-exchange patterns occurredduring a long period of the plant life. An adaptation to low light intensitieswas observed after 3 hours illumination. These results are interpreted inrelation to the functioning of the photosynthetic apparatus and point to aregulation by the electron acceptors and a specific action of CO2. Thebehavior of the 02 uptake and the study of the CO2 compensation pointseem to indicate the persistence of mitochondrial respiration during pho-tosynthesis.

20% of P,' independently of CO2 concentration (17, 25).The use of 1 02 gives access to the complementary aspect of

photorespiration, the uptake of 02, as well as to the gross 02evolution. The information obtained is not at all symmetrical withthe preceding one. In particular, the flux rates are much higher,which may be due in part to the difference in reactions involving02 or CO2 and in part to the underestimation of CO2 evolution,which is avoided by the use of 1802 (3, 19, 33).

In spite of this advantage in precision, 1802 was seldom usedafter the first studies on algae (8, 40) or higher plants (27, 38, 39).The main defect of these studies was the lack of CO2 regulation.The problem was reassessed recently on a new technical basis(whole plants grown in automatic culture, computer monitoring,and analysis), revealing the existence of photorespiration at highlight intensity in C4 plants (3) and, in C3 plants, a surprisinglyhigh level of 02 uptake, the competition between 02 and CO2 forreducing power, and the independence of the production of re-ducing power from CO2 level (5, 19, 30). An international teamhas confirmed these results and further explored the influences oflight and 02 concentration (11). The study presented here iscomplementary to theirs and presents new data on the regulationof reducing power production, the continuation ofdark respirationin light, the influence of plant age, and the adaptation to low lightintensity.

Whereas the metabolism of photorespiration has been the sub-ject of numerous studies, relatively few data are available con-cerning the associated gas fluxes in organs or whole plants, al-though such gas-exchange measurements were at the origin of thediscovery of, first, the Warburg effect, then the loss of CO2 (16)and the uptake of 02 in light (8, 22), which are the main expres-sions of photorespiration. Interest in the gas exchanges ebbed afterthese discoveries, as the complexity of the underlying mechanismswas uncovered through biochemistry, challenging the value of gasflux measurements and showing the difficulty of their interpreta-tion.

Nonisotopic methods do not allbw a measurement of photores-piration during photosynthesis; moreover, they are not consistent.For example, the Warburg effect depends on CO2 concentrationbut not on light intensity (6, 34), whereas the evolution of CO2 inC02-free air and the CO2 postillumination burst (14, 37) increasewith light intensity but are independent of CO2 (7). All resultsagree on the stimulating action of 02 on photorespiration.

Isotopic methods also have their flaws. As in the preceding case,several phenomena may be involved. Methods with 14C are usedto measure true photosynthesis (CO2 uptake) (25) or CO2 evolution(41), but contradictions have arisen (13). Unfortunately, the resultsare underestimated because of internal recycling phenomena (10,32) which can only be estimated. However, tests with 14C havebeen used to estimate the photorespiratory loss of CO2 at 10 to

MATERIALS AND METHODS

The experiments were conducted on whole wheat plants (Triti-cum aestivum L var Champlein) grown from the 8th day aftersowing in a "C23A mini-chamber" (volume, 6 to 18 liters). PARduring growth was 175 w/m2 (610 ,IE/m2 s-1), day/night temper-atures were 20 ± lC/15 ± IC, and the CO2 level was kept at 330tdl F'. The root compartment was separated from the aerial part.Techniques were described in detail by Andre et al. (1, 2).The plants were grown for 40 to 70 days. As the plants had not

undergone winter frosts, vegetative growth still continued after 70days without flowering. Apparent photosynthesis was around 100ml/h at the end of the experiments, still increasing by 2 to 4%/day; it was limited mainly by the reciprocal shading and thedisturbance of the ventilation by the leaves.The roots were placed in a beaker containing 2.3 liters nutrient

solution at pH 6.5. This solution was changed every day andanalyzed for nutrient uptake. The volume of solution was enoughto provide a roughly constant concentration of elements, exceptNH4', which was exhausted after a few hours of photosynthesis.The experiments were done in the same growth chamber.

' Abbreviations: P, apparent photosynthesis or net CO2 assimilation; P',apparent or net 02 evolution; E, 02 evolution; U, 02 uptake; PS, netphotosynthesis in standard conditions; R, dark respiration; For clarity thegas fluxes are schematized in Figure 1.

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02 EXCHANGES IN WHEAT

FIG. 1. Scheme of the gas exchanges of a plant, with unidirectional andnet fluxes.

Different light intensities were obtained by the use of the propernumber of lamps or by placing grids under the lamps for lowerintensities. 02 concentration was lowered by sweeping the chamberwith N2 just before the measuring period. After that, the concen-tration increased again; at the end of the period, it ranged from 3to 7% 02- Periods of measurement in nonstandard conditions wereusually limited to 6 to 7 h, separated by 1.5-day "rest" periods toavoid any adaptation or stress of the plant. In doing so, weascertained that the growth curves of the plant were not perturbedby the experiments, which made it possible to interpolate theapparent photosynthesis in standard conditions (175 w/m2, 330Au 1 C02, 21% 02) to the precise time of the measurement; mostof the results here are expressed in per cent of this standardphotosynthesis PS.

Photorespiration was measured through the decrease of theconcentration of the 18018O isotope of 02, compared with that ofan inert reference gas ( 19). The initial concentration of the isotopein the chamber was about 1%. Gaseous concentrations weremeasured with a gas spectrometer Riber QMM 17 and CO2 levelswere measured with an IR gas analyzer (ADC). All raw data were

processed in real time by a Telemecanique T 1600 minicomputer(2).

RESULTS

INFLUENCE OF A LOW 02 PRESSURE

Figure 2 shows the 02 and net CO2 gas exchanges of a wheatplant as a function of the concentration of CO2 at either the 21%(a) or 2% (b) 02 level.Warburg Effect. The lowering of the 02 concentration increases

photosynthesis (Warburg effect) and decreases U. In absolutevalue, the increase in photosynthesis is nearly independent ofCO2(about 40% PS), whereas the decrease in U is greater at low CO2.

Residual Respiration. At 330 Lp1 1-1 C02, reducing the 02 pres-sure 10 times reduces U by less than 4 times. Even at higher C02,U does not fall under 20%o of PS, just the level of R. Theidentification of this reaction with dark respiration will be dis-cussed below.

Competition between 02 and CO2. The increase of U anddecrease of P when CO2 decreases from 300 to 80 ,ul I-, due to thecompetition between 02 and CO2 for reducing power which was

already noticed at 20% 02 (11, 19), also occurs at 2% 02. In thatcase, however, the curves are not symmetrical but are decreasedby the reduction of the available quantity of reducing power.

Inhibition of Electron Transport by Lack of Acceptors. We

0 100 PS~ale(

00 100 200 300 400 500

9I1-1.' CO2

b 2% 62E

C,,p0.

100 P0

0 100 200 300 400 900

11.1 '1 CO2

FIG. 2. Variations of the photosynthesis and oxygen uptake rates of awheat plant as a function of the concentration of CO2 at 21% 02 (a) or 2%02 (b). Light intensity was 175 w m-2 (610 AE m-2 s-'); temperature was20 C; plant age was 45 to 70 days. Standard photosynthesis (PS) is definedas the net photosynthesis at 175 w m-2 light intensity, 21% 02, and 330,u-1 C02.

observed a decrease in the production of 02 at 20% 02 under 120,A I-' CO2 or at 2% 02 under 330 ,ul I` CO2. In both cases, thisoccurs when the availability of acceptors is about 40% lower thannormal, if we take the affinities of the plant for 02 and CO2 intoaccount. Since reducing power, in the form of NADPH, is an endproduct of electron transport, this inhibition could be a simpleend-product regulation of the reaction by mass action law or bythe effect of an allosteric enzyme.

Inhibition of Electron Transport by Lack of CO2. The precedingconsiderations cannot explain why, at still lower CO2 concentra-tions, U becomes inhibited also, in spite of the continuing avail-ability of 02 and diminishing competition from C02; this is clearlya new phenomenon. At both 02 concentrations, E is inhibitedwhen CO2 is less than 60 Ll 1-1. This cannot be due to theexhaustion of the pool of ribulose bisphosphate, the substrate ofthe 02-consuming carboxylase reaction, because the exhaustionwould occur much sooner at 20o than at 2% 02, whereas, remark-ably, the inhibition occurs at the same level of CO2. Therefore, itmust be due to a specific effect of CO2 on the photosyntheticapparatus.

INFLUENCE OF LIGHT INTENSITY

Figure 3 shows the variations in gas exchanges of a young (40days old) wheat plant as a function of light intensity. The valuesof R are those measured on a night following a whole day at thecorresponding light intensity. When a given light intensity wasmaintained for only half a day, the effect on R was similar, but oflower amplitude. The balance of photosynthesis was positive for

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GERBAUD AND ANDRE

C,)0.

100

R -

0 100 200 300 400

Light intensity (W.M-2)

FIG. 3. Effect of light intensity on the gas exchanges of a wheat plantat 330 ill -'; 1 w m-2 = 3.48 ,uE m-2 s-'.

light intensities greater than 12.5 w m-2 (43.5 ,tE m-2 s-') andevolved afterwards following a classical curve. The ratio of P to Uwas highest at 175 w m-2. This means that the reducing powerwas used most efficiently at the standard light intensity, which wasabout half-saturating.At higher intensities, P approached saturation but U continued

growing linearly. Canvin et al. (I 1) have shown that U could evenexceed P at high light intensities in the C3 plant Hirschfeldiaincana Lowe. This indicates that the reaction with 02 has a lowaffinity but a high maximum rate (higher than that of photosyn-thesis), which allows an efficient elimination of excess reducingpower. Nevertheless, we can see that E does not increase linearlywith light intensity; this could be due to a beginning of saturationof the photosystems or of the 02 uptake reaction.

AGE OF PLANT

When the plant grows, mutual shading of leaves increases andthe lighting of central leaves becomes weaker and less homoge-neous, which changes the shapes of gas-exchange curves andmakes comparisons more difficult.The decrease of P and increase of U relative to E that is

observed when the plant ages (Fig. 4) does not exceed 10%Yo. It maybe due in part to the effect of diminished light intensity (Fig. 3).

ADAPTATION

The wheat plant adapts itself to low light intensities (less than60 w m 2 or 210 ,utE m-2 s-'). When a new, lower intensityillumination is given from the beginning of a day, photosynthesis,initially low, begins to increase after 3 h, the light intensityremaining constant (Fig. 5). The variation of photosynthesis [e.g.from 0.5 ml/h initially to 9 ml/h, when the light intensity is 20 wm-2 (70 ,uE m-2 s-1)] is quite small when compared to the standardphotosynthesis of the plant (116 ml/h), but it is worth noticingthat the same increase of photosynthesis would be obtained ifthere were no adaptation at 30 w m-2 (105 ,uE m-2 s-'), that is, a50% increase in light intensity. No reverse effect was observed atthe return to normal lighting. It is possible that the reverseadaptation is fast or that the adaptation is efficient only at lowillumination.The speed of this adaptation process shows the risk of dealing

with a modified or rapidly evolving plant when measurements aremade in apparently steady-state conditions, in particular in wholeplant experiments. All our measurements at low light intensitywere taken during the first 3 h so that the values correspond toplants in their initial standard state. Other measurements corre-spond to half-day or whole-day means, but there was no variationof the gas exchanges during the period of measurement.

4RC.) 10LuA

40 50 60 70PLANT AuE (DAYS)

FIG. 4. Evolution with plant age of the gas exchanges of wheat. As theplot is semilogarithmic, the linear part of the curves (left) corresponds tothe exponential growth period; the flat part of the curves (right) corre-sponds to a linear growth period.

7.5

C)0.0 5

2.5

0 5 10 14

HOURSFIG. 5. Hourly evolution of photosynthesis of a wheat plant during its

adaptation to a low light intensity [20 w m-2 (70 ,uE m-2 s-'), about one-tenth of normal intensity (175 w m-2)]. The average level of U during thesame period was 36 ml/h. Net photosynthesis in normal light intensitywas 116 ml/h. Plant age was 63 days.

ZERO LIGHTING

When zero lighting was realized during the day, U and the CO2evolution rates were near that of the respiration of the precedingnight and a little higher than the extrapolation of R to 0 w m(Fig. 3). No rhythm appeared.

DARK RESPIRATION IN LIGHT

The fact that the variation of U with light follows the equationU = R + k(light intensity) is a clue in favor of the continuationof mitochondrial respiration in the light. Supplementary infor-mation is given by the study of the CO2 compensation point r asa function of the 02 concentration. It is assumed that the level ofdark respiration is independent of 02 concentration between 1and 21% and that the level of photorespiration tends towards zerowith 02 concentration. In this hypothesis, the extrapolation to

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02 EXCHANGES IN WHEAT

zero CO2 of the values of r measured between I and 21%'02depends only on the level of dark respiration in this range (18).Forrester et al. (18) found that, in soybean leaves, r extrapolatedto zero with 02 and concluded that dark respiration was inhibitedin the light. Our result is different: r extrapolated to 10,ul 1-' C02(Fig. 6). If we suppose that the level of the compensation point isapproximately proportional to the rate of CO2 evolution, weroughly estimate that there is 5 times more CO2 evolved at 20%02 than at 2%. This does not make it possible to determine theprecise value of the CO2 evolution rate at r CO2 and 2% 02, butit indicates the existence of a nonnegligible dark respiration in thelight in the conditions of the experiment.

DISCUSSION

Continuation of Dark Respiration in Light. Several points, ofour study suggest the presence of dark respiration during photo-synthesis. This is an important point in the interpretation of all 02uptake measurements.The convergence of U towards the level of R at zero light

intensity (Fig. 3) is best ex?lained by a dark respiration. Similarmeasurements done with 802 with algae (22, 40) have givencontradictory results. More recently, Mulchi et al. (27) came tothe same conclusion as was reached here, whereas Canvin et al.(11) found a convergence of U towards zero. First, it is possiblethat the measurements of Canvin et al. may be slightly underes-timated, as shown by the convergence below zero of several curves;second, as shown below, experimental conditions may be impor-tant in this respect.The convergence ofU towards the level of R either at very high

CO2 concentrations (19) or at high CO2 at 2% 02 (Fig. 2b),conditions which are known to suppress photorespiration, showsthe presence of dark respiration.The convergence of the CO2 compensation point towards 10,tl

1-1 CO2 is consistent with the preceding data. The use of a wholeplant could explain the disagreement with the result of Forrester.

In vitro studies have proven the respiratory. activity of themitochondria in the light (26), this activity being regulated at thelevel of substrates, in particular ADP, or of enzymes (12, 31). Thisregulation of R could be an alternate explanation of the variationsin labeling of the emitted CO2 after a period of photosynthesis in'4Co2. Fock et al. (17) attribute these variations to the participationof carbohydrate reserves in photorespiration.

Because it is not known how to distinguish respiratory from

40

30

~20

10

0 5 10 15 20

% 02FIG. 6. Influence of 02 concentration on the CO2 compensation point

of a wheat plant. The arrows show the order in which the points weredetermined. Rest periods of about 20 min were allowed between thedetermination of each point. Light intensity was 175 w m-2; plant age was48 days.

photorespiratory gas exchanges, all respiration tests are madeunder conditions that inhibit photorespiration, sometimes even inthe absence of photosynthesis (21). It is known that photorespir-ation influences the ADP/ATP ratio and that some of its reactionsoccur in the mitochondria (36). Photorespiration must have aninfluence on respiration, the nature and direction of which are stillunknown. However, such a regulation could hardly act as an on/off switch but, rather, could modulate the level of dark respirationso as to allow a finite rate of activity even under the less favorableconditions and apparently, a rate near that of night respirationunder the experimental conditions reported here.

Regulation of Photosynthetic Apparatus. The observed effectsof 02 and CO2 (Fig. 2) may be related to what is known from thebiochemistry of the photosynthetic apparatus.The functioning of the electron transport chain necessitates that

NADP+ be regenerated from NADPH. This is normally donethrough CO2 and 02 uptake. Inhibition appears when the availa-bility of acceptors is insufficient; this happens at 21% 02 whenCO2 concentration is under 100 d F1-1 or, which is equivalent forthe acceptor efficiency, at 2% 02 when CO2 concentration is under330 [l I-.A specific action of C02, the lack of which inhibits U or E,

regardless of the 02 concentration, has been pointed out. Threemechanisms could explain it. (a) The inhibition of the electrontransport in the absence of CO2 was discovered by Warburg, whobelieved that CO2 was the source of the 02 evolved duringphotosynthesis. It has been found since then that CO2 catalyzesthe transport of electrons (35), but the exact mechanism is still amatter of discussion (20). (b) The transport of electrons needs theregeneration of ADP from ATP, which is assumed by the assimi-lation of CO2 in the Calvin cycle, but not by photorespiration.This hypothesis seems less probable because the inhibition of Ewould then be photosynthesis-dependent rather than C02-de-pendent. (c) The inactivation of the enzyme ribulose bisphosphatecarboxylase-oxygenase at low CO2 level (4) also may play a role,impeding the regeneration of ADP, and, except for the small partthat may be due to the Mehler reaction, of NADP. It is not yetpossible to judge of the relative importance of these three mech-anisms.

Potential Role of Photorespiration. The exact role of plantphotorespiration is still not known, although several functionshave been proposed, most notably the protection of the photosyn-thetic apparatus in the case of various stresses (9, 15, 28).The high maximum rate of U and the regulation of electron

transport could help to protect the plant whenever CO2 assimila-tion cannot cope with the supply of reducing power, e.g. too stronglight, closed stomata (water stress), or cold weather causing aslowing down of photosynthesis. It was observed that strong lightcan actually enhance the damaging effect of cold (23, 24). Thisview is also confirmed by experiments that show a durable inhi-bition of photosynthesis in white mustard (15) or bean (29) aftertreatment at low concentrations of 02 and C02, but we did notobserve it in wheat, which suggests that the regulation of theelectron transport that has been shown here is quite efficient inwheat, but not in white mustard or bean. In a wheat-type plant,efficient regulation could be a necessary component of plantresistance to low temperatures.

Acknowledgments-The authors are grateful to Mr. A. Daguenet and Mrs. J.Massimino for their contributions to the experiments.

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Al

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