Skip to main content
SpringerLink
Log in

From Chloroplasts to Chaperones: How One Thing Led to Another

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Two lessons I have learned during my research career are the importance of following up unexpected observations and realizing that the most obvious interpretation of such observations can be rational but wrong. When you carry out an experiment there is usually an expectation that the result will fall within a range of predictable outcomes, and it is natural to feel pleased when this turns out to be the case. In my view this response is a mistake. What you should be hoping for is a puzzling result that was not anticipated since with persistence and luck further experiments may uncover something new. In this article I give a personal account of how studies of the synthesis of proteins by isolated intact chloroplasts from pea leaves eventually led to the discovery of the chaperonins and the formulation of the general concept of the molecular chaperone function that is now seen to be a fundamental aspect of how all cells work.

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

References

  • Arnon DI, Allen MB and Whatley FR (1956) Photosynthesis by isolated chloroplasts. 4. General concept and comparison of 3 photochemical reactions. Biochim Biophys Acta 20: 449–461

    Article  PubMed  CAS  Google Scholar 

  • Barraclough R and Ellis RJ (1980) Protein synthesis in chloroplasts.IX. Assembly of newly-synthesized large subunits into ribulose bisphosphate carboxylase in isolated intact pea chloroplasts. Biochim Biophys Acta 608: 19–31

    PubMed  CAS  Google Scholar 

  • Bartlett SG, Grossman AR and Chua NH (1982) In vitro synthesis and uptake of cytoplasmically-synthesized chloroplast proteins. In: Edelman M, Hallick RB and Chua NH (eds) Methods in Chloroplast Molecular Biology, pp 1081-1091. Elsevier Biomedical Press, Amsterdam

    Google Scholar 

  • Blair GE and Ellis RJ (1973) Protein synthesis in chloroplasts. I. Light-driven synthesis of the large subunit of fraction I protein by isolated pea chloroplasts. Biochim Biophys Acta 319: 223–234

    PubMed  CAS  Google Scholar 

  • Bloom MV, Milos P and Roy H (1983) Light-dependent assembly of ribulose 1,5-bisphosphate carboxylase. Proc Natl Acad Sci USA 80: 1013–1017

    Article  PubMed  CAS  Google Scholar 

  • Chanda PK, Ono M, Kuwano M and Kung HF (1985) Cloning, sequence, analysis and expression of alteration of the mRNA stability gene (ams+) of Escherichia coli. J Bacteriol 161: 446–449

    PubMed  CAS  Google Scholar 

  • Eaglesham ARJ and Ellis RJ (1974) Protein synthesis in chloroplasts.

  • II. Light-driven synthesis of membrane proteins by isolated pea chloroplasts. Biochim Biophys Acta 335: 396–407

  • Ellis RJ (1977) Protein synthesis by isolated chloroplasts. Biochim Biophys Acta 463: 186–215

    Google Scholar 

  • Ellis RJ (1979) The most abundant protein in the world. Trends Biochem Sci 4: 241–244

    Article  CAS  Google Scholar 

  • Ellis RJ (1981) Chloroplast proteins: synthesis, transport and assembly. Annu Rev Plant Physiol 32: 111–137

    Article  CAS  Google Scholar 

  • Ellis RJ (1987) Proteins as molecular chaperones. Nature 328: 378–379

    Article  PubMed  CAS  Google Scholar 

  • Ellis RJ (1998) Steric chaperones. Trends Biochem Sci 23: 43–45

    Article  PubMed  CAS  Google Scholar 

  • Ellis RJ (1999) Molecular chaperone. In: Creighton TE (ed) Encyclopedia of Molecular Biology. Wiley, New York

    Google Scholar 

  • Ellis RJ (2001a) Macromolecular crowding: obvious but underappreciated. Trends Biochem Sci 26: 597–604

    Article  PubMed  CAS  Google Scholar 

  • Ellis RJ (2001b) Inside and outside the Anfinsen cage. Curr Biol 11: R1038–R1040

    Article  PubMed  CAS  Google Scholar 

  • Ellis RJ and Hartl FU (2003) Protein folding and chaperones. In: Cooper DN (ed) Nature Encyclopedia of the Human Genome, Vol 4, pp 806–810. Nature Publishing Group, London

    Google Scholar 

  • Ellis RJ and Hemmingsen SM (1989) Molecular chaperones: proteins essential for the biogenesis of some macromolecular structures. Trends Biochem Sci 14: 339–342

    Article  PubMed  CAS  Google Scholar 

  • Georgopolous CP, Tilly K and Casgens SR (1983) Lambdoid phage head assembly. In: Hendrix RW, Roberts JW, Stahl FW and Weisberg RA (eds) Lambda II, pp 279–304. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Goloubinoff P, Christeller JP, Gatenby AA and Lorimer GH (1989) Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfolded state depends on two chaperonin proteins and ATP. Nature 342: 884–889

    Article  PubMed  CAS  Google Scholar 

  • Gray JC and Kekwick RGO (1974) An immunological investigation of the structure and function of ribulose 1.5-bisphosphate carboxylase. Eur J Biochem 44: 481–489

    Article  PubMed  CAS  Google Scholar 

  • Haas IG and Wabl M (1983) Immunoglobulin heavy-chain bindingprotein. Nature 306: 387–389

    Article  PubMed  CAS  Google Scholar 

  • Hall DO (1972) Nomenclature for isolated chloroplasts. Nature New Biol 235: 125–126

    Article  PubMed  CAS  Google Scholar 

  • Hartl FU and Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295: 1852–1858

    Article  PubMed  CAS  Google Scholar 

  • Hartley MR and Ellis RJ (1973) Ribonucleic acid synthesis in chloroplasts. Biochem J 134: 249–262

    PubMed  CAS  Google Scholar 

  • Hartley MR, Wheeler A and Ellis RJ (1975) Protein synthesis in chloroplasts. V. Translation of the messenger RNA for the large subunit of fraction I protein in a heterologous cell-free system. J Mol Biol 91: 67–77

    Article  PubMed  CAS  Google Scholar 

  • Hemmingsen SM and Ellis RJ (1986) Purification and properties of the ribulose bisphosphate large subunit binding protein. Plant Physiol 80: 269–276

    Article  PubMed  CAS  Google Scholar 

  • Hemmingsen SM, Woolford C, van der Vies SM, Tilly K, Dennis DT, Georgopoulos CP, Hendrix RW and Ellis RJ (1988) Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 333: 330–334

    Article  PubMed  CAS  Google Scholar 

  • Highfield PE and Ellis RJ (1978) Synthesis and transport of the small subunit of chloroplast ribulose bisphosphate carboxylase. Nature 271: 420–424

    Article  CAS  Google Scholar 

  • James WO and Das VSR (1957) The organisation of respiration in chlorophyllous cells. New Phytol 56: 325–343

    Article  CAS  Google Scholar 

  • Kirk JTO and Tilney-Bassett RAE (1967) The Plastids: Their Chemistry, Structure, Growth and Inheritance. Freeman, London

    Google Scholar 

  • Kochan JA and Murialdo H (1983) Early intermediates in bacteriophage lambda prohead assembly. Virology 131: 100–115

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685

    Article  PubMed  CAS  Google Scholar 

  • Laskey RA, Honda BM, Mills AD and Finch JT (1978) Nucleosomes are assembled by an acidic protein that binds histones and transfers them to DNA. Nature 275: 416–420

    Article  PubMed  CAS  Google Scholar 

  • Leech RM and Ellis RJ (1961) Coprecipitation of mitochondria and chloroplasts. Nature 190: 790–792

    PubMed  CAS  Google Scholar 

  • McMullin TWand Hallberg RL (1988) A highly evolutionarily conserved mitochondrial protein is structurally related to the protein encoded by the Escherichia coli GroEL gene. Mol Cell Biol 8: 371–380

    PubMed  CAS  Google Scholar 

  • Miller PTO (1970) Control of Organelle Development. Symposium No. XXIV of the Society for Experimental Biology. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Musgrove JE and Ellis RJ (1986) The Rubisco large subunit binding protein. Phil Trans R Soc London Ser B 313: 419–428

    CAS  Google Scholar 

  • Musgrove JE, Johnson RA and Ellis RJ (1987) Dissociation of the ribulose bisphosphate binding protein into dissimilar subunits.Eur J Biochem 163: 529–534

    Article  PubMed  CAS  Google Scholar 

  • Ostermann J, Horwich AL, Neupert W and Hartl FU (1989) Protein folding in mitochondria requires hsp60 and ATP hydrolysis. Nature 341: 125–130

    Article  PubMed  CAS  Google Scholar 

  • Pelham HRB (1986) Speculations of the functions of the major heat shock and glucose-regulated proteins. Cell46: 956–971

    Article  Google Scholar 

  • Satoh K (2003) The identification of the Photosystem II reaction center: a personal story. Photosynth Res 76: 233–240

    Article  PubMed  CAS  Google Scholar 

  • Voordouw G, van der Vies SM and Bouwmeister PP (1984) Dissociation of ribulose bisphosphate carboxylase oxygenase from spinach by urea. Eur J Biochem 141: 313–318

    Article  PubMed  CAS  Google Scholar 

  • Walker DA (2003) Chloroplasts in envelopes: CO2 fixation by fully functional intact chloroplasts. Photosynth Res 76: 319–327

    Article  PubMed  CAS  Google Scholar 

  • Wildman SG (2002) Along the trail from Fraction I protein to Rubisco (ribulose bisphosphate carboxylase-oxygenase). Photosynth Res 73: 243–250

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Warwick, Coventry, CV4 7AL, UK

    R. John Ellis

Authors
  1. R. John Ellis
    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

John Ellis, R. From Chloroplasts to Chaperones: How One Thing Led to Another. Photosynthesis Research 80, 333–343 (2004). https://doi.org/10.1023/B:PRES.0000030439.62331.d0

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:PRES.0000030439.62331.d0

Search

Navigation