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Metabolism of 2-carboxyarabinitol 1-phosphate and regulation of ribulose-1,5-bisphosphate carboxylase activity

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Abstract

Metabolism of 2′-carboxy-D-arabinitol 1-phosphate (CA1P) is an important component in the light-dependent regulation of ribulose-1,5-bisphosphate carboxylase (Rubisco) activity and whole leaf photosynthetic CO2 assimilation in many species, and functions as one mechanism for regulating Rubisco activity when photosynthesis is light-limited. Species differ in their capacity to accumulate CA1P, ranging from those which can synthesize levels of this compound approaching or in excess of the Rubisco catalytic site concentration, to those which apparently lack the capacity for CA1P synthesis. CA1P is structurally related to the six carbon transition state intermediate of the carboxylation reaction and binds tightly to the carbamylated catalytic site of Rubisco, making that site unavailable for catalysis. Under steady-state, the concentration of CA1P in the leaf is highest at low photon flux density (PFD) or in the dark. Degradation of CA1P and recovery of Rubisco activity requires light and is stimulated by increasing PFD. The initial degradation reaction is catalyzed by an enzyme located in the chloroplast stroma, CA1P phosphatase, which yields carboxyarabinitol (CA) and inorganic phosphate as its products. The pathway of CA metabolism in the plant remains to be determined. Synthesis of CA1P occurs in the dark, and in Phaseolus vulgaris this process has been shown to be stimulated by low PFD. The pathway of CA1P synthesis and its relationship to the degradative pathway remains unknown at the present time. The discovery of the existence of this previously unknown carbon pathway in photosynthesis indicates that we still have much to learn concerning the regulation of Rubisco activity and photosynthesis.

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Abbreviations

CA:

2′-carboxy-D-arabinitol

CA1P:

2′-carboxy-D-arabinitol 1-phosphate

CABP:

2′-carboxy-D-arabinitol-1,5-bisphosphate (transition state analog)

PFD:

photon flux density

P1 :

inorganic phosphate

Rubisco:

ribulose-1,5-bisphosphate carboxylase/oxygenase (EC 4.1.1.39)

RuBP:

ribulose-1,5-bisphosphate

References

  • Ashton AR (1982) A role for ribulose-1,5-bisphosphate carboxylase as a metabolite buffer. FEBS Letts 145: 1–7

    Google Scholar 

  • Bahr JT and Jensen RG (1978) Activation of intact chloroplasts by CO2 and light. Arch Biochem Biophys 185: 39–48

    Google Scholar 

  • Beck E, Scheibe R and Reiner J (1989) An assessment of the rubisco inhibitor. 2-carboxyarabinitol-1-phosphate and D-hamamelonic acid 2-phosphate are identical compounds. Plant Physiol 90: 13–16

    Google Scholar 

  • Beck E, Stransky H and Furbinger M (1971) Synthesis of hamamelose diphosphate by isolated spinach chloroplasts. FEBS Letts 13: 229–234

    Google Scholar 

  • Berry JA, Lorimer GH, Pierce J, Seemann JR, Meeks J and Freas S (1987) Isolation, identification, and synthesis of 2-carboxyarabinitol 1-phosphate, a diurnal regulator of ribulose-bisphosphate carboxylase activity. Proc Natl Acad Sci (USA) 84: 734–738

    Google Scholar 

  • Besford RT (1984) Some properties of ribulose bisphosphate carboxylase from tomato leaves. J Exp Bot 153: 495–504

    Google Scholar 

  • Bowes G and Holbrook GP (1988) Species, cultivar, and developmental variation in the production of 2-carboxyarabinitol 1-phosphate by leaves during darkness. Plant Physiol 86: s5

  • Brooks A and Portis AR (1988) Protein-bound ribulose bisphosphate correlates with deactivation of ribulose bisphosphate carboxylase in leaves. Plant Physiol 87: 244–249

    Google Scholar 

  • Brooks A, Portis AR and Sharkey TD (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

    Google Scholar 

  • Butz ND and Sharkey TD (1989) Activity ratios of ribulose-1,5-bisphosphate carboxylase accurately reflect carbamylation ratios. Plant Physiol 89: 735–739

    Google Scholar 

  • Cardon ZG and Mott KA (1989) Evidence that RuBP binds to inactive sites of RuBP carboxylase in vivo and an estimate of the rate constant of dissociation. Plant Physiol 89: 1253–1257

    Google Scholar 

  • Chazdon RL and Pearcy RW (1986) Photosynthetic responses to light variation in rain forest species. II. Carbon gain and photosynthetic efficiency during lightflecks. Oecologia 69: 524–531

    Google Scholar 

  • Farineau J, Suzuki A and Morot-Gaudry JF (1988) Changes in the activation state of Rubisco in bean leaves in relation to recovery of photosynthetic activity after various treatments. Plant Sci 55: 191–198

    Google Scholar 

  • Fong FK and Butcher KA (1987) Photoreductive path of carbon fixation in green plant photosynthesis. Reaction pathway of six-carbon ribulose 1,5-bisphosphate carboxylation adduct intermediate. Biochem Biophys Res Comm 142: 732–737

    Google Scholar 

  • Foyer C (1986) Discovery of the most abundant inhibitor in the world? Nature 324: 211

    Google Scholar 

  • Furbank RT, Foyer CH and Walker DA (1987) Interactions between ribulose-1,5-bisphosphate carboxylase and stromal metabolites. II. Corroboration of the role of this enzyme as a metabolite buffer. Biochim Biophys Acta 894: 165–173

    Google Scholar 

  • Grisebach H (1980) Branched-chain sugars: occurrence and biosynthesis. In: Preiss J (ed) The Biochemistry of Plants, a Comprehensive Treatise, Vol 3, Carbohydrates: structure and function, pp. 171–197. New York: Academic Press

    Google Scholar 

  • Gutteridge S, Parry MAJ, Burton S, Keys AJ, Mudd A, Feeney J, Servaites JC and Pierce J (1986) A nocturnal inhibitor of carboxylation in leaves. Nature 324: 274–276.

    Google Scholar 

  • Gutteridge S, Reddy GS and Lorimer G (1989) The synthesis and purification of 2′-carboxy-D-arabinitol-1-phosphate; a natural inhibitor of ribulose bisphosphate carboxylase investigated by 31P NMR. Biochem J, in press

  • Holbrook GP, Bowes G and Salvucci ME (1989) Degradation of 2-carboxyarabinitol 1-phosphate by a specific chloroplast phosphatase. Plant Physiol, 90: 673–678

    Google Scholar 

  • Johal S, Partridge BF and Chollet R (1985) Structural characterization and determination of negative cooperativity in the tight binding of 2-carboxyarabinitol bisphosphate to higher plant ribulose bisphosphate carboxylase. J Biol Chem 260: 9894–9904

    Google Scholar 

  • Jordan DB and Chollet R (1983) Inhibition of ribulose bisphosphate carboxylase by substrate ribulose-1,5-bisphosphate. J Biol Chem 258: 13752–13758

    Google Scholar 

  • Kobza J, Moore Bd and Seemann JR (1989) Isolation of photosynthetically active protoplasts and chloroplasts from Phaseolus vulgaris. Plant Sci, in press

  • Kobza J and Seemann JR (1988) Mechanisms for the light regulation of ribulose-1,5-bisphosphate carboxylase activity and photosynthesis in intact leaves. Proc Natl Acad Sci (USA) 85: 3815–3819

    Google Scholar 

  • Kobza J and Seemann JR (1989a) Light-dependent kinetics of 2-carboxyarabinitol 1-phosphate metabolism and ribulose-1,5-bisphosphate carboxylase activity in vivo. Plant Physiol 89: 174–179

    Google Scholar 

  • Kobza J and Seemann JR (1989b) Regulation of ribulose-1,5-bisphosphate carboxylase activity in response to diurnal changes in irradiance. Plant Physiol 89: 918–924

    Google Scholar 

  • Ku SB, Prickril BC, Reger RJ and Pallas JE (1982) Diurnal fluctuation of RuBP carboxylase activity in peanut leaves. Possible regulation by photosynthetic metabolites. Plant Physiol 69: s51

  • McDermott DK, Zeiher CA and Porter CA (1983) Physiological activity of RuBP carboxylase in soybeans. In: Randall DD, Blevins DG and Larson R (eds) Current Topics in Plant Biochemistry and Physiology, Vol I, p. 230. Columbia: Univ Missouri

    Google Scholar 

  • Miziorko HM and Lorimer GH (1983) Ribulose-1,5-bisphosphate carboxylase-oxygenase. Annu Rev Biochem 52: 507–535

    Google Scholar 

  • Moore Bd, Kobza J and Seemann JR (1989) Metabolism of 2-carboxyarabinitol 1-phosphate in bean. Plant Physiol 89: s75

  • Mott KA, Jensen RG, O'Leary JW and Berry JA (1984) Photosynthesis and ribulose 1,5-bisphosphate concentrations in intact leaves of Xanthium strumarium L. Plant Physiol 76: 968–971

    Google Scholar 

  • Mulligan RM, Houtz RL and Tolbert NE (1988) Reaction-intermediate analogue binding by ribulose bisphosphate carboxylase/oxygenase causes specific changes in proteolytic sensitivity: The amino-terminal residue of the large subunit is acetylated proline. Proc Natl Acad Sci (USA) 85: 1513–1517

    Google Scholar 

  • Perchorowicz JT, Raynes DA and Jensen RG (1981) Light limitation of photosynthesis and activation of ribulose bisphosphate carboxylase in wheat seedlings. Proc Natl Acad Sci (USA) 78: 2985–2989

    Google Scholar 

  • Pierce J, Tolbert NE and Barker R (1980) Interaction of ribulosebisphosphate carboxylase/oxygenase with transition state analogues. Biochemistry 19: 934–942

    Google Scholar 

  • Portis AR, Salvucci ME and Ogren WL (1986) Activation of ribulosebisphosphate carboxylase/oxygenase at physiological CO2 and ribulose bisphosphate concentrations by rubisco activase. Plant Physiol 82: 967–971

    Google Scholar 

  • Robinson SP and Portis AR (1988a) Release of the nocturnal inhibitor, carboxyarabinitol-1-phosphate, from ribulose bisphosphate carboxylase/oxygenase by rubisco activase. FEBS Letts 233: 413–416

    Google Scholar 

  • Robinson SP and Portis AR (1988b) Involvement of stromal ATP in the light activation of ribulose 1,5-bisphosphate carboxylase/oxygenase in intact chloroplasts. Plant Physiol 86: 293–298

    Google Scholar 

  • Robinson SP, Streusand VJ, Chatfield JM and Portis AR (1989) Purification and assay of rubisco activase from leaves. Plant Physiol 88: 1008–1014

    Google Scholar 

  • Sage RF, Sharkey TD and Seemann JR (1988) The in-vivo response of ribulose-1,5-bisphosphate carboxylase activation and pool sizes of photosynthetic metabolites to elevated CO2 in Phaseolus vulgaris L. Planta 174: 407–416

    Google Scholar 

  • Salvucci ME and Anderson JC (1987) Factors affecting the activation state and the level of total activity of ribulose bisphosphate carboxylase in tobacco protoplasts. Plant Physiol 85: 66–71

    Google Scholar 

  • Salvucci ME and Holbrook GP (1989) Purification and properties of 2-carboxy-D-arabinitol 1-phosphate. Plant Physiol, 90: 679–685

    Google Scholar 

  • Salvucci ME, Holbrook GP, Anderson JC and Bowes G (1988) NADPH-dependent metabolism of the ribulose bisphosphate carboxylase/oxygenase inhibitor 2-carboxyarabinitol 1-phosphate by a chloroplast protein. FEBS Letts 231: 197–201

    Google Scholar 

  • Salvucci ME, Portis AR and Ogren WL (1985) A soluble chloroplast protein catalyzes activation of ribulosebisphosphate carboxylase/oxygenase in vivo. Photosynth Res 7: 193–201

    Google Scholar 

  • Salvucci ME, Portis AR and Ogren WL (1986) Light and CO2 response of ribulose-1,5-bisphosphate carboxylase/oxygenase activation in Arabidopsis leaves. Plant Physiol 80: 655–659

    Google Scholar 

  • Salvucci ME, Werneke JM, Ogren WL and Portis AR (1987) Purification and species distribution of Rubisco activase. Plant Physiol 84: 930–936

    Google Scholar 

  • Schloss JV and Lorimer GH (1982) The stereochemical course of ribulosebisphosphate carboxylase. Reductive trapping of the 6-carbon reaction-intermediate. J Biol Chem 257: 4691–4694

    Google Scholar 

  • Seemann JR, Berry JA, Freas SM and Krump MA (1985) Regulation of ribulose bisphosphate carboxylase activity in vivo by a light-modulated inhibitor of catalysis. Proc Natl Acad Sci (USA) 82: 8024–8028

    Google Scholar 

  • Seemann JR, Kirschbaum MUF, Sharkey TD and Pearcy RW (1988) Regulation of ribulose-1,5-bisphosphate carboxylase activity in Alocasia macrorrhiza in response to step changes in irradiance. Plant Physiol 88: 148–152

    Google Scholar 

  • Seemann JR and Kobza J (1988) Genetic variation in the regulation of ribulose-1,5-bisphosphate carboxylase activity. Plant Physiol Biochem 26: 461–471

    Google Scholar 

  • Seemann JR and Sharkey TD (1987) The effect of abscisic acid and other inhibitors on photosynthetic capacity and the biochemistry of CO2 assimilation. Plant Physiol 84: 696–700

    Google Scholar 

  • Servaites JC (1985) Binding of a phosphorylated inhibitor to ribulose bisphosphate carboxylase/oxygenase during the night. Plant Physiol 78: 839–843

    Google Scholar 

  • Servaites JC, Torisky RS and Chao SF (1984) Diurnal changes in ribulose-1,5-bisphosphate carboxylase activity and activation state in leaves of field grown soybeans. Plant Sci Lett 35: 115–121

    Google Scholar 

  • Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: Physics, physiology and rate limitations. Bot Rev 51: 53–105

    Google Scholar 

  • Sharkey TD, Seemann JR and Berry JA (1986) Regulation of ribulose-1,5-bisphosphate carboxylase in response to changing partial pressure of O2 and light in Phaseolus vulgaris. Plant Physiol 81: 788–791

    Google Scholar 

  • Smrcka AV and Jensen RG (1988) HPLC separation and indirct ultraviolet detection of phosphorylated sugars. Plant Physiol 86: 615–618

    Google Scholar 

  • Taylor SE and Terry N (1984) Limiting factors in photosynthesis V. Photochemical energy supply colimits photosynthesis at low values of intercellular CO2 concentration. Plant Physiol 75: 82–86

    Google Scholar 

  • Vu JCV, Allen LH and Bowes G (1983) Effects of light and elevated atmospheric CO2 on the ribulose bisphosphate carboxylase activity and ribulose bisphosphate level of soybean leaves. Plant Physiol 73: 729–734

    Google Scholar 

  • Vu JCV, Allen LH and Bowes G (1984) Dark/light modulation of ribulose bisphosphate carboxylase activity in plants from different photosynthetic categories. Plant Physiol 76: 834–845

    Google Scholar 

  • Vu JCV, Allen LH and Bowes G (1986) Properties of ribulose 1,5-bisphosphate carboxylase from dark- and light-exposed soybean leaves. Plant Sci 44: 119–123

    Google Scholar 

  • Werneke JM, Chatfield HM and Ogren WL (1988) Catalysis of ribulosebisphosphate carboxylase/oxygenase activation by the product of a rubisco activase cDNA clone expressed in Escherichia coli. Plant Physiol 87: 917–920

    Google Scholar 

  • Williams JW and Morrison JF (1979) The kinetics of reversible tight-binding inhibition. Methods Enzymol 63: 437–467

    Google Scholar 

  • Woodrow IE and Berry JA (1988) Enzymatic regulation of photosynthetic CO2 fixation in C3 plants. Ann Rev Plant Physiol Plant Mol Biol 39: 533–594

    Google Scholar 

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  1. Department of Biochemistry, University of Nevada, 89557, Reno, Nevada, USA

    Jeffrey R. Seemann, John Kobza & Brandon d. Moore

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  1. Jeffrey R. Seemann
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  2. John Kobza
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  3. Brandon d. Moore
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Seemann, J.R., Kobza, J. & Moore, B.d. Metabolism of 2-carboxyarabinitol 1-phosphate and regulation of ribulose-1,5-bisphosphate carboxylase activity. Photosynth Res 23, 119–130 (1990). https://doi.org/10.1007/BF00035005

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