Skip to main content
SpringerLink
Log in

Long-term kinetics of the light-dependent regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase activity in plants with and without 2-carboxyarabinitol 1-phosphate

  • Published:
Planta Aims and scope Submit manuscript

Abstract

The light-dependent modulation of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activity was studied in two species: Phaseolus vulgaris L., which has high levels of the inhibitor of Rubisco activity, carboxyarabinitol 1-phosphate (CA1P), in the dark, and Chenopodium album L., which has little CA1P. In both species, the ratio of initial to fully-activated Rubisco activity declined by 40–50% within 60 min of a reduction in light from high a photosynthetic photon flux density (PPFD; >700 μmol · m−2 · s−1) to a low PPFD (65 ± 15 μmol · m−2 · s−1) or to darkness, indicating that decarbamylation of Rubisco is substantially involved in the initial regulatory response of Rubisco to a reduction in PPFD, even in species with potentially extensive CA1P inhibition. Total Rubisco activity was unaffected by PPFD in C. album, and prolonged exposure (2–6 h) to low light or darkness was accompanied by a slow decline in the activity ratio of this species. This indicates that the carbamylation state of Rubisco from C. album gradually declines for hours after the large initial drop in the first 60 min following light reduction. In P. vulgaris, the total activity of Rubisco declined by 10–30% within 1 h after a reduction in PPFD to below 100 μmol · m−2 · s−1, indicating CA1P-binding contributes significantly to the reduction of Rubisco capacity during this period, but to a lesser extent than decarbamylation. With continued exposure of P. vulgaris leaves to very low PPFDs (< 30 μmol · m−2 · s−1), the total activity of Rubisco declined steadily so that after 6–6.5 h of exposure to very low light or darkness, it was only 10–20% of the high-light value. These results indicate that while decarbamylation is more prominent in the initial regulatory response of Rubisco to a reduction in PPFD in P. vulgaris, binding of CA1P increases over time and after a few hours dominates the regulation of Rubisco activity in darkness and at very low PPFDs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

CA1P:

2-carboxyarabinitol 1-phosphate

CABP:

2-carboxyarabinitol 1,5-bisphosphate

kcat :

substrate-saturated turnover rate of fully carbamylated enzyme

PPFD:

photosynthetically active photon flux density (400–700 nm)

Rubisco:

ribulose-1,5-bisphosphate carboxylase/oxygenase

RuBP:

ribulose-1,5-bisphosphate

References

  • Berry, J.A., Lorimer, G.H., Pierce, J., Seemann, J.R., Meeks, J., 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 

  • Butz, N.D., Sharkey, T.D. (1989) Activity ratios of ribulose-1,5-bisphosphate carboxylase accurately reflect carbamylation ratios. Plant Physiol. 89, 735–739

    Google Scholar 

  • Cardon, Z.G., Mott, K.A. (1989) Evidence that ribulose 1,5-bisphosphate (RuBP) binds to inactive sites of RuBP carboxylase in vivo and an estimate of the rate constant for dissociation. Plant Physiol. 89, 1253–1257

    Google Scholar 

  • Collatz, G.J., Badger, M.R., Smith, C., Berry, J.A. (1979) A radioimmune assay for RuP2 carboxylase protein. Carnegie Inst. Washington Yearb. 78, 171–175

    Google Scholar 

  • Holbrook, G.P., Campbell, W.J., Bowes, G. (1987) Effect of light intensity during growth on the activation state of RuBP carboxylase from leaves in the light and dark. Progr. Photosynth. Res. 3, 399–402

    Google Scholar 

  • Holbrook, G.P., Galasinski, S.C., Salvucci, M.E. (1991) Regulation of 2-carboxyarabinitol 1-phosphatase. Plant Physiol. 97, 894–899

    Google Scholar 

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

    Google Scholar 

  • Kobza, J., Seemann, J.R. (1988) Mechanism of 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., Seemann, J.R. (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., Seemann, J.R. (1989b) Regulation of ribulose-1,5-bisphosphate carboxylase activity in response to diurnal changes in irradiance. Plant Physiol. 89, 918–924

    Google Scholar 

  • Lehninger, A.L., Nelson, D.L., Cox, M.M. (1993) Principles of biochemistry, 2nd edn., Worth Publ. Inc., New York

    Google Scholar 

  • Moore, B.d., Seemann, J.R. (1992) Metabolism of 2-carboxyarabinitol in leaves. Plant Physiol. 99, 1551–1555

    Google Scholar 

  • Moore, B.d., Kobza, J., Seemann, J.R. (1991) Measurement of 2-carboxyarabinitol 1-phosphate in plant leaves by isotope dilution. Plant Physiol. 96, 208–213

    Google Scholar 

  • Perchorowicz, J.T., Raynes, J.A., Jensen, R.G. (1981) Light limitation of photosynthesis and activation of ribulose bisphosphate carboxylase in wheat seedlings. Proc. Natl. Acad. Sci. USA 78, 2985–2989

    Google Scholar 

  • Portis, A.R., Jr. (1992) Regulation of ribulose 1,5-bisphosphate carboxylase/oxygenase activity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 415–437

    Google Scholar 

  • Prinsley, R.T., Dietz, K.J., Leegood, R.C. (1986) Regulation of photosynthetic carbon assimilation in spinach leaves after a decrease in irradiance. Biochim. Biophys. Acta. 849, 254–263

    Google Scholar 

  • Sage, R.F. (1990) A model describing the regulation of ribulose-1,5-bisphosphate carboxylase, electron transport, and triose-phosphate use in response to light intensity and CO2 in C3 plants. Plant Physiol. 94, 1728–1734

    Google Scholar 

  • Sage, R.F., Seemann, J.R. (1993) Regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase activity in response to reduced light intensity in C4 plants. Plant Physiol., 102, 21–28

    Google Scholar 

  • Sage, R.F., Sharkey, T.D., Seemann, J.R. (1988) The in-vivo response of the ribulose-1,5-bisphosphate carboxylase activation state and the pool sizes of photosynthetic intermediates to elevated CO2 in Phaseolus vulgaris L. Planta 174, 407–416

    Google Scholar 

  • Sage, R.F., Sharkey, T.D., Seemann, J.R. (1990) Regulation of ribulose-1,5-bisphosphate carboxylase activity in response to light intensity and CO2 in the C3 annuals Chenopodium album L. and Phaseolus vulgaris L. Plant Physiol. 94, 1735–1742

    Google Scholar 

  • Salvucci, M.E., Anderson, J.C. (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 

  • Seemann, J.R., Sharkey, T.D. (1986) Salinity and nitrogen effects on photosynthesis, ribulose-1,5-bisphosphate carboxylase and metabolite pool sizes in Phaseolus vulgaris L. Plant Physiol. 82, 555–560

    Google Scholar 

  • Seemann, J.R., Berry, J.A., Freas, S.M., Krump, M.A. (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, J.R., Kirschbaum, M.U., Sharkey, T.D., Pearcy, R.W. (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, J.R., Kobza, J., Moore, B.d. (1990) Metabolism of 2-carboxyarabinitol 1-phosphate and regulation of ribulose-1,5-bisphosphate carboxylase activity. Photosynth. Res. 23, 119–130

    Google Scholar 

  • Servaites, J.A. (1990) Inhibition of ribulose 1,5-bisphosphate carboxylase /oxygenase by 2-carboxyarabinitol-1-phosphate. Plant Physiol. 92, 867–870

    Google Scholar 

  • Servaites, J.C., Torisky, R.S., Chao, S.F. (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 

  • Servaites, J.C., Parry, M.A., Gutteridge, S., Keys, A.J. (1986) Species variation in the predawn inhibition of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol. 82, 1161–1163

    Google Scholar 

  • Servaites, J.C., Shieh, W., Geiger, D.R. (1991) Regulation of photosynthetic carbon reduction cycle by ribulose bisphosphate and phosphoglyceric acid. Plant Physiol. 97, 1115–1121

    Google Scholar 

  • Sharkey, T.D. (1985) O2-insensitive photosynthesis in C3 plants. Its occurrence and a possible explanation. Plant Physiol. 78, 71–75

    Google Scholar 

  • Sharkey, T.D., Seemann, J.R., Berry, J.A. (1986) Regulation of ribulose-1,5-bisphosphate carboxylase activity in response to changing partial pressures of O2 and light in Phaseolus vulgaris. Plant Physiol. 81, 788–791

    Google Scholar 

  • von Caemmerer, S., Farquhar, G.D. (1981) Some relationships between the biochemistry of photosynthesis and the gas-exchange of leaves. Planta 153, 376–387

    Google Scholar 

  • Wang, Z.Y., Portis, A.R., Jr. (1992) Dissociation of ribulose-1,5-bisphosphate bound to ribulose-1,5-bisphosphate carboxylase/ oxygenase and its enhancement by ribulose-1,5-bisphosphate carboxylase/oxygenase activase-mediated hydrolysis of ATP. Plant Physiol. 99, 1348–1353

    Google Scholar 

  • Woodrow, I.E., Berry, J.A. (1988) Enzymatic regulation of photosynthetic CO2 fixation in C3 plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 533–594

    Google Scholar 

  • Zhu, G., Jensen, R.G. (1990) Status of the substrate binding sites of ribulose bisphosphate carboxylase as determined with 2-C-carboxyarabinitol 1,5-bisphosphate. Plant Physiol. 93, 244–249

    Google Scholar 

Download references

Author information

Author notes

  1. Rowan F. Sage

    Present address: Department of Botany, University of Toronto, 25 Wilcocks Street, M5S 3B2, Toronto, Ontario, Canada

  2. C. D. Reid

    Present address: USD A-Air Quality Lab, 1509 Varsity Drive, 27606, Raleigh, NC, USA

Authors and Affiliations

  1. Department of Botany, University of Georgia, 30602, Athens, GA, USA

    Rowan F. Sage & C. D. Reid

  2. Department of Biochemistry, University of Nevada, 89557, Reno, NV, USA

    Brandon d. Moore & Jeffrey R. Seemann

Authors
  1. Rowan F. Sage
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. D. Reid
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brandon d. Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jeffrey R. Seemann
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sage, R.F., Reid, C.D., Moore, B.d. et al. Long-term kinetics of the light-dependent regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase activity in plants with and without 2-carboxyarabinitol 1-phosphate. Planta 191, 222–230 (1993). https://doi.org/10.1007/BF00199753

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00199753

Key words

Search

Navigation