Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds

Nature volume 432, pages 779–782 (2004)Cite this article

Abstract

Efficient storage of carbon in seeds is crucial to plant fitness and to agricultural productivity. Oil is a major reserve material in most seeds1, and these oils provide the largest source of renewable reduced carbon chains available from nature. However, the conversion of carbohydrate to oil through glycolysis results in the loss of one-third of the carbon as CO2. Here we show that, in developing embryos of Brassica napus L. (oilseed rape), Rubisco (ribulose 1,5-bisphosphate carboxylase/oxygenase) acts without the Calvin cycle2 and in a previously undescribed metabolic context to increase the efficiency of carbon use during the formation of oil. In comparison with glycolysis, the metabolic conversion we describe provides 20% more acetyl-CoA for fatty-acid synthesis and results in 40% less loss of carbon as CO2. Our conclusions are based on measurements of mass balance, enzyme activity and stable isotope labelling, as well as an analysis of elementary flux modes.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Metabolic transformation of sugars into fatty acids.
Figure 2: Light-dependent ratio of oil synthesis and CO2 production.

Similar content being viewed by others

References

  1. Levin, D. A. The oil content of seeds: An ecological perspective. Am. Nat. 108, 193–206 (1974)

    Article  Google Scholar 

  2. Bassham, J. A. et al. The path of carbon in photosynthesis. XXI. The cyclic regeneration of carbon dioxide acceptor. J. Am. Chem. Soc. 67, 1760–1770 (1954)

    Article  Google Scholar 

  3. Schwender, J., Ohlrogge, J. & Shachar-Hill, Y. Understanding flux in plant metabolic networks. Curr. Opin. Plant Biol. 7, 309–317 (2004)

    Article  CAS  Google Scholar 

  4. Neuhaus, H. E. & Emes, M. J. Non-photosynthetic metabolism in plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 111–140 (2000)

    Article  CAS  Google Scholar 

  5. King, S. P., Badger, M. R. & Furbank, R. T. CO2 refixation characteristics of developing canola seeds and silique wall. Aust. J. Plant Phys. 25, 377–386 (1998)

    CAS  Google Scholar 

  6. Schwender, J., Ohlrogge, J. B. & Shachar-Hill, Y. A flux model of glycolysis and the oxidative pentose phosphate pathway in developing Brassica napus embryos. J. Biol. Chem. 278, 29442–29453 (2003)

    Article  CAS  Google Scholar 

  7. Ruuska, S. A., Schwender, J. & Ohlrogge, J. B. The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes. Plant Physiol. 136, 2700–2709 (2004)

    Article  CAS  Google Scholar 

  8. Goffman, F. D., Ruckle, M., Ohlrogge, J. B. & Shachar-Hill, Y. Carbon dioxide concentrations are very high in developing oil seeds. Plant Physiol. Biochem. 42, 703–708 (2004)

    Article  CAS  Google Scholar 

  9. Schwender, J. & Ohlrogge, J. Probing in vivo metabolism by stable isotope labeling of storage lipids and proteins in developing Brassica napus embryos. Plant Physiol. 130, 347–361 (2002)

    Article  CAS  Google Scholar 

  10. Schuster, S., Fell, D. & Dandekar, T. A general definition of metabolic pathways useful for systematic organization and analysis of complex metabolic networks. Nature Biotechnol. 18, 326–332 (2000)

    Article  CAS  Google Scholar 

  11. Schuster, S., Dandekar, T. & Fell, D. A. Detection of elementary flux modes in biochemical networks: a promising tool for pathway analysis and metabolic engineering. Trends Biotechnol. 17, 53–60 (1999)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Department of Energy, the National Science Foundation and the USDA. Acknowledgement is also made to the Michigan Agricultural Experiment Station for its support of this research.

Author information

Authors and Affiliations

  1. Plant Biology Department, Michigan State University, East Lansing, Michigan, 48824, USA

    Jörg Schwender, Fernando Goffman, John B. Ohlrogge & Yair Shachar-Hill

Authors
  1. Jörg Schwender
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fernando Goffman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John B. Ohlrogge
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yair Shachar-Hill
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jörg Schwender.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Notes

Contains an analysis of how much carbon dioxide can be assimilated and stored in biomass by carboxylation reactions that produce oxaloacetate. Alternative metabolic routes for converting hexose into acetyl-CoA are described and analysed as elementary flux modes. The labelling experiments using 13CO2 or 13C-labelled alanine are discussed with additional detail. (DOC 354 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schwender, J., Goffman, F., Ohlrogge, J. et al. Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds. Nature 432, 779–782 (2004). https://doi.org/10.1038/nature03145

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03145

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing