sign in sign up
<<
Home , Biosynthesis, Photorespiration

32 TIBS - February 1980 Open Question

but again reduced pyridine and What is the physiological role of ATP are consumed. It has been claimed [7] that the of glycolate fuels the ? production of mitochondrial ATP. This refers to the conversion of to U. Heber and G. H. Krause in the mitochondria that yields NADH. hz vitro, NADH can be oxidized in the respiratory chain. In vivo, however, reduc- There is scarcely any that is metaboli- competes with CO2 at the active sites of ing equivalents must be reinvested for the cally more flexible than the mesophyll cell ribulose bisphosphate (RuBP) carboxyl- reduction of hydroxypyruvate and refixa- of plant leaves. Upon illumination, ase. Instead of being carboxylated, RuBP is tion of NH~ liberated during the formation respiratory uptake is rapidly oxygenated to form phosphoglycerate and of serine (Fig. 1). On balance, those reduc- replaced by photosynthetic oxygen evolu- phosphoglycolate. The latter is hydrolysed ing equivalents are therefore unavailable tion which may be up to 100 times faster to glycolate. for ATP production. Apparently the than oxygen uptake in the dark. Often, A peculiar feature of photorespiration is is not incorporated directly into mitochrondrial respiration, which gives that, in contrast to dark respiration, it does glutamate by mitochondrial glutamate rise to oxygen uptake, is suppressed in the not conserve but consumes energy [6]. This dehydrogenase, but rather is ref'Lxed by light. However, in the presence of atmos- becomes apparent from the energy balance synthetase in the or pheric concentrations of oxygen, most of the metabolic cycles depicted in Fig. 1. to form glutamine [8]. In the plants exhibit another type of oxidative The formation of glycolate requires energy chloroplasts, the glutamine reacts with sugar degradation that is not observed in in the form of ATP and reducing equiv- 2-oxoglutarate to glutamate. The latter the dark and is therefore called photo- alents, since it utilizes photosynthetic pathway requires, in addition to reducing respiration [1]. This process has unusual intermediates. Isolated chloroplasts can equivalents, one ATP to re-assimilate one properties. It proceeds at appreciable rates oxidize triosephosphate (TP) via RuBP of NH~. The balance of the inte- only at high oxygen tensions and can there- and the completely to glyco- grated cycles in the scheme in Fig. 1 shows fore be suppressed by a reduction in the late and inorganic [3]. The that evolution of 1 mol CO2 by photorespi- partial pressure of oxygen. In an atmos- energy requirement of the oxidation pro- ration re.quires about twice as much energy phere containing 1-2% oxygen, almost no cess can be derived from a summation of as assimilation of 1 mol CO, in the Calvin photorespiration is observed. the individual reactions involved, yielding: cycle [6]. It is noteworthy that the ratio of The biochemical pathway of photores- reducing equivalents consumed to ATP 2 TW- + 3 O2 + 3 NADPH + 6 ATW- piration has been elucidated mainly by consumed is the same or almost the same in + 6 OH--~ Tolbert and co-workers [2]. In brief, glyco- photorespiratory oxidation 3 glycolate - + 8 Pi ~- + 3 NADP ~ late is formed in the chloroplasts at the as in photosynthetic carbohydrate forma- + 6 ADP 3- + H20 expense of sugar-phosphate intermediates tion. Clearly, energy-dependent oxidation of the Calvin cycle. After export from the Details of the conversion of glycolate to instead of formation of must chloroplasts, the glycolate undergoes a phosphoglycerate are not entirely clear, reduce photosynthetic yield. series of reactions taking place in peroxi- somes, mitochondria and finally again in II II OUTSIDEOF CHLOROPLAST the chloroplasts (Fig. 1). There, phospho- II glycerate is produced, linking glycolate II ATP II metabolism to the Calvin cycle. Formation II and conversion of 2 mol of glycolate to 1 II t P-glyiolote 11 mol of phosphoglycerate lead to the uptake glycolate II of 3 mol O2 and the evolution of 1 mol CO2. IIII , glyc~ If photosynthetic oxygen evolution for II glyoxylote production of requii'ed reducing equiv- II alents is taken into account, an O~/CO2 triose-P II II [ ratio of 1 is obtained for the complete pro- II cess of photorespiration. The key reaction | Calvin cycle ) II -iHz gl~~'-IH]P 171 II of the process - the of glyco- II late in the chloroplasts - has been a con- II 5n/o._ O II troversial issue for several years. It now U pyruvote [~1 appears established [3-5] that .oxygen II 13-ph0 +yc.ro,. glycr~'~'otee 1 ATP NADPH U. Heber and G. tl. Krattse are at the Institute of II and Pharrnaceutical of the University II of Wgtrzburg and Institute of Botany of the University Fig. I. Scl, eme of photosynthetic and photorespiratory pathways showing energy-requiring steps. [It] denotes of Diisseldorf, F.R.G. reduced pyridine . * of glycerate is possible both inside and outside the chloroplasts. El~vier/North-HollandBiomedical Prr 1980 TIBS - February 1980 33

Bjfrkman [12] have suggested that photo- respiratory energy consumption may pro- tect plants from photo-oxidative damage. l | Several mechanisms are available to pre-~ vent light damage to the photosynthetic apparatus [13]. are known to play a role in the protection of chloroplast - - ~-- l rnin, ~(~ L.-..-....~._.~ pigments against photo-bleaching. Super- I' light on oxide dismutase, , ascorbate and glutathione act together to degrade oir. oil. superoxide radicals and Fig. 2. Effects o f gas phase composition on scattering o f a weak beam of 535 nm light by a spinach leaf.. Exciting red formed during reduction of oxygen. It light (intensity 125 W.m=) was switched on aj~er a 2 rain dark period. The gas phase surrounding the leaf was appeared possible that light energy not changed from air to nitrogen and vice versa, both containing 475 ppm C02. Numbers denote steady-state rates of used for could give rise to net photosynthetic CO~ uptake, as recorded with an infrared analyser (hoT,oiling h). destructive reactions which cannot be Dissipation of energy by photores- photorespiration would only be practical handled by the available protective piration can be demonstrated in vivo by when oxygenation of RuBP is selectively deVices. light scattering suppressed without the impairment of Attempts have been made to test this measurements [6]. Upon illumination of carboxylase activity, a task that seems dif- concept. Isolated chloroplasts that are cap- leaves, a proton gradient is established ficult to accomplish. able of photosynthetic rates comparable to across the energy-conserving thylakoid There is the question of why evolu- those shown by the parent leaves were membranes in the chloroplasts. Together tionary pressures have not eliminated a exposed to light in the absence of CO2 [14]. with a light-dependent membrane poten- process as wasteful as photorespiration Oxidizable substrates were also largely tial this is thought to drive ATP synthesis. appears to be. Such pressures seem to have absent from the chloroplasts and little for- The magnitude of the proton gradient can produced insensitivity to oxygen inhibition mation of glycolate was possible during be used as a measure of the energization of of photosynthesis in the group of'Ca plants' illumination. Within only a few minutes of the chloroplast system. Formation of the in which primary photosynthetic CO2 exposure to light, the chloroplasts lost a proton gradient gives rise to an increase jn incorporation occurs into the Ca acid, significant proportion of their capacity to light scattering and a decrease in chloro- oxaloacetate. Even Ca plants are capable of photoreduce CO= (Table I). This loss of phyll fluorescence. Both phenomena'can photorespiration, but photorespiratory activity was irreversible. It seems that in be easily monitored in intact leaves. Fig. 2 rates are low. The rates are probably these chloroplasts, photophosphorylation shows that after a lag phase during which a decreased because Ca plants have a and, to a lesser degree, photosynthetic steady rate of photosynthesis and mechanism whereby CO2 is accumulated at electron transport were partly inactivated. photorespiration in air are established, the site of secondary CO= fixation by RuBP Oxygen appeared to play a role in the inac- light scattering by a leaf is kept at a low carboxylase. In isolated chloroplasts from tivation, as damage increased with increas- value. When photorespiration is suppres- spinach, a (23 plant, glycolate synthesis is ing oxygen concentration. Chloroplasts sed by exchange of air for Na + CO2, light almost completely suppressed by CO2 permitted to assimilate CO2 during illumi- scattering increases, indicating increased [3,4]. In leaves of (23 plants, the ratio of nation at a constant oxygen concentration energization of the membranes. This sup- CO= fixation to photorespiratory CO2 did not lose activity while exposed to light. ports a higher rate of CO2 f'Lxation; energy evolution increases with ambient CO2 con- Rather similar results were obtained that in air was required for photorespirat- centrations, although in apparent contra- with isolated leaf cells suspended in CO2- ory COa evolution is now available for diction to the results found hz vitro, absol- and -free medium, but loss of increased CO~ assimilation. In Ca plants ute rates of photorespiration were little activity during exposure to light was (plants that incorporate CO= first into the affected by COa concentration [10]. slower. Probably, photorespiratory CO2 C3 acid, 3-phosphoglycerate) an increase in Thus photorespiration, a process appar- released during illumination escaped into the net yield of photosynthesis by 50% is ently of universal occurrence in green not uncommon when photorespiration is plants, degrades sugars and additionally TABLE I selectively suppressed by a reduction in Protective effect of bicarbonate on photosynthetic consumes ATP and reducing equivalents, activity of illuminated intact spinach chloroplasts oxygen tension [9]. Under laboratory con- but can be decreased by a reduction in ditions, Ca plants have been shown not only oxygen or an increase in COa levels not Pre-treatment Rate % to photosynthesize faster but also to grow on!y without immediate adverse effects, faster at 2% oxygen than at 21% oxygen. but with actual beneficial effects to the Light, 2 mM KttCO= 138 100 These observations have prompted plants. These results leave all questions Light, no 89 64 attempts to inhibit photorespiration by open regarding a physiological role of Dark, 2 mM KttCO, 117 85 No pre-incubation 129 93 means other than a reduction in the oxygen photorespiration, if indeed there is one. It tension; which is clearly impractical on a has been argued [11] that for mechanistic Samples of physiologically active intact isolated large scale. Considerable finance and reasons oxygenation of RuBP is an un- spinach chloroplasts were pre-incubated for 7 min in research effort has been invested in such avoidable side reaction to white light (500 W.m 2) or dark, with and without attempts, but with little success so far. The and that the photorespiratory conversion KHCOa as substrate. During pre-incubation the O= oxygenation of RuBP is an irreversible of phosphoglycolate back to phosphoglyc- level in the assay medium was kept constant at 0.3 m~.l O2 (corresponding to about 21% O= in air). In the table reaction. Because photosynthesis and crate serves only to salvage, if not all, at the rates of photosynthetic O= evolution in the pres- photorespiration share RuBP carboxylase least 75% of the carbon lost from the Cal- ence of 2 mM KHCO3 observed subsequent to pre- as a common key , inhibition of vin cycle. On the other hand, Osmond and incubation are given in ~mol/mg chlorophyll - h. 34 TIBS - February 1980 the solution. Ref'Lxation was insignificant, deductions contain uncertainties. Ex- Announcing and the photorespiratory pathway was perimentation is necessary to fill gaps in gradually depletedof substrate. Again, our knowledge. In particular, it remains to photoinhibition was completely prevented be established under what environmental by bicarbonate. conditions the protective mechanism might BIOLOGICAL RHYTHMS These results need to be related to the be essential for undisturbed growth or even situation in vivo. In leaves, conditions of survival of plants. The experimental evi- AND THEIR COo depletion are frequently encountered dence available at present may, however, CENTRAL MECHANISM in the light. The green plant must live with justify the warning that selective inhibition the dilemma that both COo and water may of photorespiration in crop plants, if the edited by MASAMI SUDA, be scarce at times, that both are needed for attempts were ever successful, might be OSAMU HAYAISHI and life and conditions thatpermit uptake of disastrous under drought conditions. HACHIRO NAKAGAWA CO~, i.e. open stomata, necessarily entail Finally, it should be emphasized that the loss of water by . When the concept of photorespiration as a wasteful A NATO FOUNDATION SYMPOSIUM water potential of leaf cells drops to low process, forced on the plant by the high O2 values because water uptake by the roots level of the atmosphere [11], is not neces- 1979 480 pages cannot keep up with transpiration, open sarily contradictory to a protective role of Price: US $83.00/Dfl. 170.00 stomata close. This occurs preferably dur- photorespiratory energy dissipation. Poss- ISBN 0-444-80136-7 ing full sunshine. COo in the intercellular ibly, the process has developed in response This book, dealing with one of the most space of the leaves then drops to the CO2 to inevitable glycolate formation as a side exciting subjects in biology and medicine compensation point which is 30-60 ppm reaction of CO2 fixation when the atmos- today, offersthe first rigorousexamination into the sites of "biological clocks" in CO2 in C3 plants and near zero in ~ plants. pheric oxygen concentration increased animals, the mechanisms of action and At the compensation point, photorespirat- because of the photosynthetic activity of their relationships to environmental ory CO2 evolution is as fast as photosyn- the plants. At the same time, due to the factors. thetic CO2 fixation, and CO= cycles be- energy requirement of photorespiration, CONTENTS: Preface. List of Contributors. tween both biochemical pathways. Consid- plants were protected under adverse Chapters I. Principle of circadian or- ganization. S. Pittendrigh. 2. Metabolic erable turnover of photosynthetic energy environmental conditions from oxygen- oscillation. B. Hess, T. Ishikawa, M. Naka- will continue while net gas exchange is dependent photoinduced damage. mura, S. Nakamura, I. Yamazaki and zero. Since both pathways use NADPH K.-N. Yokota. 3. Cellular basis of biological clock. R.B. Alvarez, R. Denison, J.F. and ATP at very similar ratios, the electron References Feldman, G. Gardner, K. Goshima, F. transport chain should be little affected by 1 Zelitch, I. (1971) Photosynthesis, Photorespira- Strumwasser, D.P. VieleandJ.C. Woolum. 4. Avian circadian system. K. Homma, the shifts in carbon metabolism. tion and Plant Productivity, Academic Press, New York M. Menaker, M. Ohta, Y. Sakakibara and Support for this concept has been pro- 2 Tolbert, N. E. (1971) Annu. Rev. Plant Physiol. J.S. Takahashi. 5. Physiological signifi- vided by Powles and Osmond [15] in a cance and control mechanism of pineal 22, 45-74 rhythm in . D. Auer- study of intact bean leaves. When the 3 Kirk, M. R. and Heber, U. (1976) Planta 132, bach, 7". Deguchi, O. Hayaishi, D.C. Klein, leaves were exposed for several hours to 131-141 H.J. Lynch, S. Reppert, L. Tamarkin, J. Weller, R.J. Wurtman, R. Yoshida and strong illumination in the absence of CO= 4 Krause, G. H., Thorne, S. W. and Lorimer, G. tl. (1977)Arch. Biochem. Biophys. 183, 471--479 M. Zatz. 6. Factors entraining circadian in an atmosphere containing 1% O2 in rhythms in mammals. C.A. Czeis/er, 5 Lorimer, G.. H., Woo, K.C., Berry, J.A. and K. Hanada, T. Hiroshige, K.-I. Honma, nitrogen, i.e. when photorespiration was Osmond, C. B. (1978) Photosynthesis '77, Proc. M.C. Moore-Erie, Y. Morimoto, K. Taka- suppressed, the rates of CO2 uptake sub- 4th Internat. Congress on Photosynthesis (Hall, hashi, Y. Takahashi, E.D. Weitzman and sequently measured were severely low- D. O., Coombs, J. and Goodwin, T. W., eds), pp. Y. Yamamura. 7. Control mechanism of circadian rhythms apparently generated ered. This photoinhibition was fully pre- 311-322, The Biochem. Sot., London 6 Krause, G. H., Lorimer, G. H., Heber, U. and in relation to food intake. Y. Abe, Y. vented under conditions that allowed Habara, K. Ishikawa, S. Ishizuka, T. Kirk, M. R. (1978) Photosynthesis "77, Proc. 4th Kanno, K. Kida, J. Mizoguchi, K. Nagai, energy dissipation by photorespiratory or lnternat. Congress on Photosynthesis (Hall, D. O., H. Nakagawa, 1". Nishio, H. Nishino, 1". photosynthetic carbon metabolism to pro- Coombs, J. and Goodwin, T.W., eds), pp. Ono, Y. Oomura, A. Saito, M. Saito, ceed. No inhibition was observed when the 299-310, The Biochem. Sot., London K. Sasaki, N. Shimizu, T. Shimazu, M. Suda. 8. Suprachiasmatic nucleus as the Oxygen tension was raised which leads to 7 Moore, A. L., Jpckson, C., Halliwell, B., Dench, J. E. and Hall, D. O. (1977) Biochem. Biophys. circadian clock in mammals. L.C. David- photorespiratory COo evolution from sen, N. Ibuka, 7". Inouye, H. Kawamura, Res. Commun. 78, 483--491 R.Y. Moore, W.J. Schwartz, Shin-lchi, endogenous carbohydrate reserves, or 8 Keys, A. J., Bird, I. F., Cornelius, M. J., Lea, P. J., C.B. Smith and I. Zucker. 9. Circadian alternatively, when COo was added to the Wallsgrove, R. M. and Miflin, B. J. (1978) Nature rhythms without any possible relation to gas phase giving rise to photosynthetic car- (London) 275,741-743 the suprachiasmatic nucleus. S. Aral, 9 Bj6rkman, O. (1966) Physiol. Plantarurn 19, C.A. Fuller, E. Halberg, F. Halberg, bon turnover. Interestingly, a CO2 con- J. Halberg, M.C. Moore-Ede, 1. Nakayama, 618---633 centration c0rresponding to the intercellu- F.M. Sulzman and K. Yakamoto. 10. 10 Bravdo, B.-A. and Canvin, D. (1979) Plant General Discussion. Subject Index. lar partial pressure at the CO= compensa- Physiol. 63,399--401 tion point in air (65 ppm) was sufficient to 11 Andrews, T. J. and Lorimer, G. H. (1978) FEBS fully prevent photoinhibition. This indi- Left. 90, 1-9 ELSEVIER/NORTH-HOLLAND cates that at the compensation point under 12 Osmond, C. B. and Bj6rkman, O. (1972) Carnegie Institution of Washington, Yearbook 7 l, DMEDICALI PRESS conditions of high light intensities and 141-148 closed stomata, energy-dissipating carbon 13 Halliwell, B. (1978) Progr. Biophys. MoL BioL metabolism may indeed protect the photo- 33, 1-54 P.O. Box 211, Amsterdam, The Netherlands synthetic apparatus from destructive 14 Krause, G. If., Kirk, M., Heber, I3. and Osmond, effects of light. C. B. (1978) Planta 142,229-233 Distributor in the U.S.A. and Canada: 15 Powles, S. B. and Osmond, C. B. (1978) Aust. J. ELSEVIER NORTH-HOLLAND, INC., It must be admitted that the above Plant Physiol. 5,619-629 52 Vanderbilt Ave., New York, NY 10017 The Dutchguilder price is definitive. US $ prices are sub/ect to exchangerate fluctuations. Circle no. 84 on adverb'sing enquiry form