Abstract
Sugar beets (Beta vulgaris L. cv. F58-554H1) were cultured hydroponically in growth chambers at 25°C, with a photon flux density of 500 μmol m-2s-1. Measurements were made of net CO2 exchange, leaf adenylates (ATP, ADP and AMP), and leaf nicotinamide nucleotides (NAD+, NADP+, NADH, NADPH), over the diurnal period (16h light/8 h dark) and during photosynthetic induction. All the measurements were carried out on recently expanded leaves from 5-week-old plants. When the lights were switched on in the growth chamber, the rate of photosynthetic CO2 uptake, and the levels of leaf ATP and NADPH increased to a maximum in 30 min and remained there throughout the light period. The increase in ATP over the first few minutes of illumination was associated with the phosphorylation of ADP to ATP and the increase in NADPH with the reduction of NADP+; subsequently, the increase in ATP was associated with an increase in total adenylates while the increase in NADPH was associated with an accumulation of NADP+ and NADPH due to the light-driven phosphorylation of NAD+ to NADP+. On return to darkness, ATP and NADPH values decreased much more slowly, requiring 2 to 4 hours to reach minimum values. From these results we suggest that (i) the total adenylate and NADPH and NADP+ (but not NAD+ and NADH) pools increase following exposure to light; (ii) the increase in pool size is not accompanied by any large change in the energy or redox states of the system; and (iii) the measured ratios of ATP/ADP and NADPH/NADP+ for intact leaves are low and constant during steady-state illumination.
Similar content being viewed by others
Abbreviations
- AEC:
-
adenylate energy charge
- DHAP:
-
dihydroxyacetone phosphate
- MTT:
-
3-(4,5-dimethylthiazolyl-2)-2,5-diphenyltetrazolium bromide
- PES:
-
phenazine ethosulfate
- PEP:
-
phosphoenolpyruvate
- PGA:
-
3-phosphoglycerate
- PFD:
-
photon flux density
- Ru5P:
-
ribulose-5-phosphate
- Rubisco:
-
ribulose 1,5-bisphosphate carboxylase/oxygenase
References
Bonzon M, Hug M, Wagner E and Greppin H (1981) Adenine nucleotides and energy charge evolution during the induction of flowering in spinach leaves. Planta 152: 189–914
Bonzon M, Simon P, Greppin H and Wagner E (1983) Pyridine nucleotides and redox-charge evolution during the induction of flowering in spinach leaves. Planta 159: 254–260
Brooks A, Portis A R and Sharkey T D (1988) Effects of irradiance and methyl viologen treatment on ATP, ADP and activation of ribulose bisphosphate carboxylase in spinach leaves. Plant Physiol 88: 850–853
Champigny M L (1978) Adenine nucleotides and the control of photosynthetic activities. In: Hall D O, Coombs J and Goodwin T W (eds) Proc IVth Int cong on Photosyn, pp 479–488, Biochem Soc, London
Fader G M and Koller H R (1984) Relationships between respiration rate and adenylate and carbohydrate pools of the soybean fruit. Plant Physiol 75: 694–699
Gans P and Rebeille F (1988) Light inhibition of mitochondrial respiration in a mutant of Chlamydomonas reinhardtii devoid of ribulose-1,5-bisphosphate carboxylase/oxygenase activity. Arch Biochem Biophys 260: 109–117
Hampp R, Goller M and Ziegler H (1982) Adenylate levels, energy charge, and phosphorylation potential during dark-light and light-dark transition in chloroplasts, mitochondria, and cytosol of mesophyll protoplasts from Avena sativa L. Plant Physiol 69: 448–455
Hampp R, Goller M and Fullgraf H (1984) Determination of compartmented metabolite pools by a combination of rapid fractionation of oat mesophyll protoplasts and enzyme cycling. Plant Physiol 75: 1017–1921
Hampp R, Goller M, Fullgraf H and Eberle J (1985) Pyridine and adenine nucleotide status, and pool sizes of a range of metabolites in chloroplasts, mitochondria and the cytosol/vacuole of Avena mesophyll protoplasts during dark/light transition: Effect of pyridoxal phosphate. Plant Cell Physiol 26: 99–108
Heber U, Takahama U, Neimanis S and Shimizu-Takahama M (1982) Transport as the basis of the Kok effect. Levels of some photosynthetic intermediates and activation of light-regulated enzymes during photosynthesis of chloroplasts and green leaf protoplasts. Biochim Biophys Acta 679: 287–299
Heber U, Niemanis S, Dietz K J and Viil J (1986) Assimilatory power as a driving force in photosynthesis. Biochim Biophys Acta 852: 144–155
Jarrett H W, Brown C J, Black C C and Cormier M J (1982) Evidence that calmodulin is in the chloroplast of peas and serves a regulatory role in photosynthesis. J Biol Chem 257: 13795–13804
Kacser H (1987) Control of metabolism. In: Davies DD (ed) The Biochemistry of Plants: A Comprehensive Treatise, Vol. II, pp 39–67. San Diego: Academic Press
Kobayashi Y, Inoue Y, Shibata K and Heber U (1979) Control of electron flow in intact chloroplasts by the intrathylakoid pH, not by the phosphorylation potential. Planta 146: 481–486
Kobayashi Y, Koster S and Heber U (1982) Light scattering, chlorophyll fluorescence and state of the adenylate system in illuminated spinach leaves. Biochim Biophys Acta 682: 44–54
Kondo T and Nakashima H (1979) Content of adenosine phosphate compounds in a long-day duckweed, Lemma gibba G3, under different light and nutritional conditions. Physiol Plant 45: 357–362
Leegood R C, Walker D A and Foyer C H (1985) Regulation of the Benson-Calvin cycle. In: Barber J and Baker N R (eds) Topics in Photosynthesis: Photosynthetic Mechanisms and the Environment, Vol 6, pp 189–258. Amsterdam-New York-Oxford: Elsevier
Lilley R, Chon C J, Mosbach A and Heldt H W (1977) The distribution of metabolites between spinach chloroplasts and medium during photosynthesis in vitro. Biochim Biophys Acta 460: 259–272
Lüttge U and Ball E (1976) ATP levels and energy requirements of ion transport in cells of slices of greening barley leaves. Z Pflanzenphysiol 80: 50–59
Lüttge U, Ball E and Willert K V (1971) Gas exchange and ATP levels of green cells of leaves of higher plants as affected by FCCP and DCMU in in vitro experiments. Z Pflanzenphysiol 65: 326–335
Maciejewska U and Kacperska A (1987) Changes in the level of oxidized and reduced pyridine nucleotides during cold acclimation of winter rape plants. Physiol Plant 69: 687–691
Miginiac-Maslow M and Hoarau A (1979) The adenine nucleotide levels and the adenylate energy charge values of different Triticum and Aegilops species. Z Pflanzenphysiol 93: 387–394
Muto S, Miyachi S, Usuda H, Edwards G E and Bassham J A (1981) Light-induced conversion of nicotinamide adenine dinucleotide to nicotinamide adenine dinucleotide phosphate in higher plant leaves. Plant Physiol 68: 324–328
Pradet A and Raymond P (1983) Adenine nucleotide ratios and adenylate energy charge in energy metabolism. Annu Rev Plant Physiol 34: 199–224
Raymond P, Gidrol X, Salon C and Pradet A (1987) Control involving adenine and pyridine nucleotides. In: Davies DD (ed) The Biochemistry of Plants: A Comprehensive Treatise, Vol 11, pp 129–176. San Diego: Academic Press
Santarius K A and Heber U (1965) Changes in the intracellular levels of ATP, ADP, AMP, and Pi and regulatory function of the adenylate system in leaf cells during photosynthesis. Biochim Biophys Acta 102: 39–54
Sharkey T D (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Bot Rev 51: 53–105
Stitt M, Lilley R and Heldt H W (1982) Adenine nucleotide levels in cytosol, chloroplasts and mitochondria of wheat leaf protoplasts. Plant Physiol 70: 971–977
Terry N (1980) Limiting factors in photosynthesis I. Use of iron stress to control photochemical capacity in vivo. Plant Physiol 65: 114–120
Terry N (1983) Limiting factors in photosynthesis IV. Iron stress-mediated changes on light-harvesting and electron transport capacity and its effects on photosynthesis in vivo. Plant Physiol 71: 855–860
Ulrich-Eberius C I, Novacky A and Ball E (1983) Effect of cyanide in dark and light on the membrane potential and ATP level of young and mature green tissues of higher plants. Plant Physiol 72: 7–15
VanBel A J E, VanLeeuwenkamp P and Van DerSchoot C (1981) Amino acid uptake by various tissues of the tomato plant. Effects of the external pH and light. Z Pflanzenphysiol 104: 117–128
Walton J D, Dearle E, Yoder O C and Spanswick R M (1979) Reduction of ATP levels in susceptible maize mesophyll protoplasts by Helminthosporium maydis Race T toxin. Plant Physiol 63: 806–810
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Madhusudana Rao, J., Raviraj Arulanantham, A. & Terry, N. Diurnal changes in adenylates and nicotinamide nucleotides in sugar beet leaves. Photosynth Res 23, 205–212 (1990). https://doi.org/10.1007/BF00035011
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00035011