Skip to main content
Log in

Chloroplasts in envelopes: CO2 fixation by fully functional intact chloroplasts

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Dan Arnon, Bob Whatley, Mary Belle Allen, and their colleagues, were the first to obtain evidence for `complete photosynthesis by isolated chloroplasts' albeit at rates which were 1% or less of those displayed by the intact leaf. By the 1960s, partly in the hope of confirming full functionality, there was a perceived need to raise these rates to the same order of magnitude as those displayed by the parent tissue. A nominal figure of 100 μmol/mgċchlorophyll/h (CO2 assimilated or O2 evolved) became a target much sought after. This article describes the contributions that Dick Jensen and Al Bassham [(1966) Proc Natl Acad Sci USA 56: 1095–1101], and my colleagues and I, made to the achievement of this goal and the way in which it led to a better understanding of the role of inorganic phosphate in its relation to the movement of metabolites across chloroplast envelopes.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allen JF (2002) Photosynthesis of ATP-electrons, protons pumps, rotors, and poise. Cell 110: 273–276

    Article  PubMed  CAS  Google Scholar 

  • Allen MB, Arnon DI, Capindale JB, Whatley FR, and Durham LJ (1955) Photosynthesis by isolated chloroplasts III. Evidence for complete photosynthesis. J Am Chem Soc 77: 4149–4155

    Article  CAS  Google Scholar 

  • Arnon DI (1961) Cell-free photosynthesis and the energy conversion process. In: McElroy WD and Glass B (eds) Light and Life, pp 489–566.Johns Hopkins Press, Baltimore, Maryland

    Google Scholar 

  • Arnon DI, Allen MB and Whatley FR (1954a) Photosynthesis by isolated chloroplasts. Nature 174: 394–396

    Article  PubMed  CAS  Google Scholar 

  • Arnon DI, Whatley FR and Allen MB (1954b) Photosynthesis by isolated chloroplasts II. Photosynthetic phosphorylation, the conversion of light into phosphate bond energy. J Am Chem Soc 76: 6324–6329

    Article  CAS  Google Scholar 

  • Arnon DI Whatley FR and Allen MB (1958) Assimilatory power in photosynthesis. Photosynthetic phosphorylation by isolated chloroplasts is coupled to TPN reduction. Science 127: 1026–1034

    CAS  PubMed  Google Scholar 

  • Baldry CW, Bucke C and Walker DA (1966a) Incorporation of inorganic phosphate into sugar phosphates during carbon dioxide fixation by illuminated chloroplasts. Nature 210: 793–796

    Article  CAS  Google Scholar 

  • Baldry CW, Walker DA and Bucke C (1966b) Calvin-cycle intermediates in relation to induction phenomena in photosynthetic carbon dioxide fixation by isolated chloroplasts. Biochem J 101: 642–646

    PubMed  CAS  Google Scholar 

  • Bamberger ES and Gibbs M (1963) Studies on photosynthetic carbon fixation by whole spinach chloroplasts. Plant Physiol 38 x–xi

    Google Scholar 

  • Bassham JA (2003) Mapping the carbon reduction cycle: a personal retrospective. Photosynth Res 76: 35–52 (this issue)

    Article  PubMed  Google Scholar 

  • Beevers H and Walker DA (1956) The oxidative activity of particulate fractions from germinating castor beans. Biochem J 62: 114–120

    PubMed  CAS  Google Scholar 

  • Bendall DS (1994) Robert Hill. Biographical Memoirs of Fellows of the Royal Society, Vol 40, pp 141–171. Royal Society, London

    Google Scholar 

  • Benson AA (2002) Following the path of carbon in photosynthesis: a personal story. Photosynth Res 73: 29–49

    Article  PubMed  CAS  Google Scholar 

  • Bucke C, Walker DA and Baldry CW (1966) Some effects of sugars and sugar phosphates on carbon dioxide fixation by isolated chloroplasts. Biochem J 101: 636–641

    PubMed  CAS  Google Scholar 

  • Bucke C, Baldry CW and Walker DA (1967) Photosynthetic carbon dioxide fixation by isolated chloroplasts in Good's buffers. Phytochemistry 6: 495–497

    Article  CAS  Google Scholar 

  • Cockburn W, Baldry CW and Walker DA (1967a) Oxygen evolution by isolated chloroplasts with carbon dioxide as the hydrogen acceptor. A requirement for orthophosphate or pyrophosphate. Biochim Biophys Acta 131: 594–596

    Article  PubMed  CAS  Google Scholar 

  • Cockburn W, Baldry CW and Walker DA (1967b) Photosynthetic induction phenomena in spinach chloroplasts in relation to the nature of the isolating medium. Biochim Biophys Acta 143: 606–613

    Article  PubMed  CAS  Google Scholar 

  • Cockburn W, Baldry CW and Walker DA (1967c) Some effects of inorganic phosphate on O2 evolution by isolated chloroplasts. Biochim Biophys Acta 143: 614–624

    Article  PubMed  CAS  Google Scholar 

  • Cockburn W, Walker DA and Baldry CW (1968a) Photosynthesis by isolated chloroplasts. Reversal of orthophosphate inhibition by Calvin-cycle intermediates. Biochem J 107: 89–95

    PubMed  CAS  Google Scholar 

  • Cockburn W, Walker DA and Baldry CW (1968b) The isolation of spinach chloroplasts in pyrophosphate media. Plant Physiol 43: 1415–1418

    PubMed  CAS  Google Scholar 

  • Delieu T and Walker DA (1972) An improved cathode for the measurement of photosynthetic oxygen evolution by isolated chloroplasts. New Phytol 71: 201–225

    Article  CAS  Google Scholar 

  • Edwards GE and Walker DA (1983) Chloroplast isolation and criteria for intactness. In: Edwards GE and Walker DA (eds) C3, C4, Mechanisms, and Cellular and Environmental Regulation of Photosynthesis, pp 496–511. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Edwards GE, Robinson SP, Tyler NJC and Walker DA (1978) Photosynthesis by isolated protoplasts, protoplast extracts and chloroplasts of wheat. Influence of orthophosphate, pyrophosphate and adenylates. Plant Physiol 62: 313–319

    PubMed  CAS  Google Scholar 

  • Emmett JM and Walker DA (1969) Thermal uncoupling in chloroplasts. Biochim Biophys Acta 180: 424–425

    Article  PubMed  CAS  Google Scholar 

  • Gibbs M and Bamberger ES (1962) Studies on photosynthetic carbon dioxide fixation by whole spinach chloroplasts Plant PhysiolSuppl 37: lxiii

    Google Scholar 

  • Gibbs M and Cynkin MA (1958) Conversion of carbon-14 dioxide to starch glucose during photosynthesis by spinach chloroplasts. Nature (London) 182: 1241–1242

    Article  PubMed  CAS  Google Scholar 

  • Heldt HW and Rapley L (1970) Specific transport of inorganic phosphate, 3–phosphoglycerate dihydroxyacetonephosphate and of dicarboxylates across the inner envelope of spinach chloroplasts FEBS Lett 10: 143–148

    Article  PubMed  CAS  Google Scholar 

  • Hill R (1937) Oxygen evolution by isolated chloroplasts Nature (London) 139: 881–882

    CAS  Google Scholar 

  • Hill R and Walker DA (1959) Pyocyanine and phosphorylation with chloroplasts Plant Physiol 34: 240–245

    CAS  Google Scholar 

  • Jagendorf AT (2002) Photophosphorylation and the chemiosmotic perspective. Photosynth Res 73: 233–241

    Article  PubMed  CAS  Google Scholar 

  • Jensen RG and Bassham JA (1966) Photosynthesis by isolated chloroplasts. Proc Natl Acad Sci USA 56: 1095–1101

    Article  PubMed  CAS  Google Scholar 

  • Lilley RMcC, Fitzgerald MP, Rienits KG and Walker DA (1975) Criteria of intactness and the photosynthetic activity of spinach chloroplast preparations. New Phytol 75: 1–10

    Article  CAS  Google Scholar 

  • Robinson SP and Walker DA (1979) Rapid separation of the chloroplast and cytoplasmic fractions from intact leaf protoplasts. Arch Biochem Biophys 196: 319–323

    Article  PubMed  CAS  Google Scholar 

  • Robinson SP, Edwards GE and Walker DA (1979) Established methods for the isolation of intact chloroplasts. In: Reid E (ed) Methodological Surveys In Biochemistry Plant Organelles, Vol 9, pp 13–24. Ellis Horwood, Chichester, UK

    Google Scholar 

  • Stiller M (1962) The path of carbon in photosynthesis. Annu Rev Plant Physiol 13: 151–170

    Article  CAS  Google Scholar 

  • Walker DA (1956) Malate synthesis in a cell-free extract from a Crassulacean plant. Nature 178: 593–594

    Article  CAS  Google Scholar 

  • Walker DA (1964) Improved rates of carbon dioxide fixation by illuminated chloroplasts. Biochem J 92: 22c–23c

    PubMed  CAS  Google Scholar 

  • Walker DA (1965) Correlation between photosynthetic activity and membrane. integrity in isolated pea chloroplasts. Plant Physiol 40: 1157–1161

    PubMed  CAS  Google Scholar 

  • Walker DA (1967) Photosynthetic activity of isolated pea chloroplasts. In: Goodwin TW (ed) Biochemistry of the Chloroplast. Proc NATO Adv Study Inst Aberystwyth 1965, Vol 2, pp 53–69. Academic Press, New York

    Google Scholar 

  • Walker DA (1969) Permeability of the chloroplast envelope. In: Metzner H (ed) Progress in Photosynthesis Research, Vol 1, pp 250–257. Institut fur Chemische Pflanzenphysiologie, Tübingen, Germany

    Google Scholar 

  • Walker DA (1971) Chloroplasts (and grana) - aqueous (including high carbon fixation ability). In: San Pietro A (ed) Methods in Enzymology, Vol 23, pp 211–220. Academic Press, London/New York

    Google Scholar 

  • Walker DA (1974) Chloroplast and cell - the movement of certain key substances etc across the chloroplast envelope. In: Northcote DH (ed) Med Tech Publ Int Rev. Science Biochem Ser 1, Vol 11, pp 1–49. Butterworths, London

    Google Scholar 

  • Walker DA (1977) In vitro photosynthesis. In: Castellani A (ed) Research in Photobiology. Proc 7th International Congress in Biology, Rome, pp 153–167. Plenum Publishing, New York

    Google Scholar 

  • Walker DA (1987) The Use of the Oxygen Electrode and Fluorescence Probes in Simple Measurements of Photosynthesis, pp 1–145. Oxygraphics Limited, Sheffield, UK

    Google Scholar 

  • Walker DA (1992) Robert Hill. Photosynth Res 34: 337–338

    Article  Google Scholar 

  • Walker DA, (1997) ‘Tell me where all past years are.’ Photosynth Res 51: 1–26

    Article  Google Scholar 

  • Walker DA (2000) What drives photosynthesis? In: Like Clockwork, pp 83–84. Oxygraphics, Sheffield, UK

    Google Scholar 

  • Walker DA (2002a) The Z-scheme-down hill all the way. Trends Plant Sci 7: 183–185

    Article  PubMed  CAS  Google Scholar 

  • Walker DA (2002b) ‘And whose bright presence’ - an appreciation of Robert Hill and his reaction. Photosynth Res 73: 51–54

    Article  PubMed  CAS  Google Scholar 

  • Walker DA and Beevers H (1956) Some requirements for pyruvate oxidation by plant mitochondrial preparations. Biochem J 62: 120–127

    PubMed  CAS  Google Scholar 

  • Walker DA and Herold A (1977) Can the chloroplast support photosynthesis unaided? In: Fujita Y, Katoh S, Shibata K and Miyachi S (eds) Photosynthetic Organelles: Structure and Function. Special Issue of Plant and Cell Physiol, pp 295–310. Japanese Society of Plant Physiologists & Center for Academic Publications, Japan

    Google Scholar 

  • Walker DA and Hill R (1958) Phosphorylation by illuminated chloroplast preparations. Biochem J 69: 57–57

    Google Scholar 

  • Walker DA and Hill R (1967) The relation of oxygen evolution to carbon assimilation with isolated chloroplasts. Biochim Biophys Acta 131: 330–333

    Article  PubMed  CAS  Google Scholar 

  • Walker DA and Robinson SP (1978) Chloroplast and Cell. A contemporary view of photosynthetic carbon assimilation. Ber Deutsch Bot Ges 91: 513–526

    CAS  Google Scholar 

  • Walker DA, Cockburn W and Baldry CW (1967) Photosynthetic oxygen evolution by isolated chloroplasts in the presence of carbon cycle intermediates. Nature 216: 597–599

    Article  CAS  Google Scholar 

  • Walker DA, Baldry CW and Cockburn W (1968) Photosynthesis by isolated chloroplasts, simultaneous measurement of carbon assimilation and oxygen evolution. Plant Physiol 43: 1419–1422

    Article  PubMed  CAS  Google Scholar 

  • Walker DA, McCormick AV, Stokes DM (1971) CO2 dependent oxygen evolution by envelope-free chloroplasts. Nature 223: 346–347

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Alan Walker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Walker, D.A. Chloroplasts in envelopes: CO2 fixation by fully functional intact chloroplasts. Photosynthesis Research 76, 319–327 (2003). https://doi.org/10.1023/A:1024962328483

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1024962328483

Navigation