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:

Kranz anatomy is not essential for terrestrial C4 plant photosynthesis

Nature volume 414, pages 543–546 (2001)Cite this article

Abstract

An important adaptation to CO2-limited photosynthesis in cyanobacteria, algae and some plants was development of CO2-concentrating mechanisms (CCM)1. Evolution of a CCM occurred many times in flowering plants, beginning at least 15–20 million years ago, in response to atmospheric CO2 reduction, climate change, geological trends, and evolutionary diversification of species2. In plants, this is achieved through a biochemical inorganic carbon pump called C4 photosynthesis, discovered 35 years ago3. C4 photosynthesis is advantageous when limitations on carbon acquisition are imposed by high temperature, drought and saline conditions. It has been thought that a specialized leaf anatomy, composed of two, distinctive photosynthetic cell types (Kranz anatomy), is required for C4 photosynthesis4. We provide evidence that C4 photosynthesis can function within a single photosynthetic cell in terrestrial plants. Borszczowia aralocaspica (Chenopodiaceae) has the photosynthetic features of C4 plants, yet lacks Kranz anatomy. This species accomplishes C4 photosynthesis through spatial compartmentation of photosynthetic enzymes, and by separation of two types of chloroplasts and other organelles in distinct positions within the chlorenchyma cell cytoplasm.

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: Light microscopy of leaves (transverse sections).
Figure 2: Immunolocalization of photosynthetic enzymes in leaves of Borszczowia aralocaspica by confocal laser scanning microscopy.
Figure 3: The response of photosynthesis to varying atmospheric levels of CO2.

Similar content being viewed by others

References

  1. Badger, M. R. & Spalding, M H. in Photosynthesis: Physiology and Metabolism (eds Leegood, R. C., Sharkey, T. D. & von Caemmerer, S.) 369–397 (Kluwer Academic, Netherlands, 2000).

    Book  Google Scholar 

  2. Sage, R. F. Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biol. 3, 202–213 (2001).

    Article  CAS  Google Scholar 

  3. Hatch, M. D. in Photosynthesis and Photorespiration (eds Hatch, M. D., Osmond, C. B. & Slatyer, R. O.) 139–152 (Wiley-Interscience, New York, 1971).

    Google Scholar 

  4. Sage, R. F. & Monson, R. K. C4 Plant Biology (Academic, San Diego, 1999).

    Google Scholar 

  5. Edwards, G. E. & Walker, D. A. C3,C4: Mechanisms, and Cellular and Environmental Regulation, of Photosynthesis (Blackwell Scientific, Oxford, 1983).

    Google Scholar 

  6. Edwards, G. E., Furbank, R. T., Hatch, M. D. & Osmond, C. B. What does it take to be C4? Lessons from the evolution of C4 photosynthesis. Plant Physiol. 125, 46–49 (2001).

    Article  CAS  Google Scholar 

  7. Winter, K. & Smith, J. A. C. Crassulacean Acid Metabolism (Springer, New York, 1996).

    Book  Google Scholar 

  8. Freitag, H. & Stichler, W. A remarkable new leaf type with unusual photosynthetic tissue in a central asiatic genus of Chenopodiaceae. Plant Biol. 2, 154–160 (2000).

    Article  Google Scholar 

  9. Carolin, R. C., Jacobs, S. W. L. & Vesk, M. The structure of the cells of the mesophyll and parenchymatous bundle sheath of the Gramineae. Bot. J. Linn. Soc. 66, 259–275 (1973).

    Article  Google Scholar 

  10. Voznesenskaya, E. V., Franceschi, V. R., Pyankov, V. I. & Edwards, G. E. Anatomy, chloroplast structure and compartmentation of enzymes relative to photosynthetic mechanisms in leaves and cotyledons of species in the tribe Salsoleae (Chenopodiaceae). J. Exp. Bot. 50, 1779–1795 (1999).

    Article  CAS  Google Scholar 

  11. Voznesenskaya, E. V. & Gamaley, Y. V. The ultrastructural characteristics of leaf types with Kranz-anatomy. Bot. Zh. 71, 1291–1307 (1986) (in Russian).

    Google Scholar 

  12. Pyankov, V. I. et al. Occurrence of C3 and C4 photosynthesis in cotyledons and leaves of Salsola species (Chenopodiaceae). Photosynth. Res. 63, 69–84 (2000).

    Article  CAS  Google Scholar 

  13. Kanai, R. & Edwards, G. in C4 Plant Biology (eds Sage, R. F. & Monson, R. K.) 49–87 (Physiological Ecology series, Academic, San Diego, 1999).

    Book  Google Scholar 

  14. Pyankov, V. I. et al. Features of photosynthesis in Haloxylon species of Chenopodiaceae that are dominant plants in Central Asian deserts. Plant Cell Physiol. 40, 125–134 (1999).

    Article  CAS  Google Scholar 

  15. Farquhar, G. D. On the nature of carbon isotope discrimination in C4 species. Aust. J. Plant Physiol. 10, 205–226 (1983).

    CAS  Google Scholar 

  16. Laing, W. A., Ogren, W. L. & Hageman, R. H. Regulation of soybean net photosynthetic CO2 fixation by the interaction of CO2, O2, and ribulose 1,5-diphosphate carboxylase. Plant Physiol. 54, 678–685 (1974).

    Article  CAS  Google Scholar 

  17. Maroco, J. P., Ku, M. S. B. & Edwards, G. E. Utilization of O2 in the metabolic optimization of C4 photosynthesis. Plant Cell Environ. 23, 115–121 (2000).

    Article  CAS  Google Scholar 

  18. Cerling, T. E., Quade, J. & Wang, Y. Expansion and emergence of C4 plants. Nature 371, 112 (1994).

    Article  ADS  Google Scholar 

  19. Pagani, M., Freeman, K. H. & Arthur, M. A. Late Miocene atmospheric CO2 concentrations and the expansion of C4 grasses. Science 285, 876–878 (1999).

    Article  CAS  Google Scholar 

  20. Sheehy, J. E., Mitchell, P. L. & Hardy, B. Redesigning Rice Photosynthesis to Increase Yield (IRRI and Elsevier Science, Makati City, Philippines, 2000).

    Google Scholar 

  21. Matsuoka, M., Furbank, R. T., Fukayama, H. & Miyao, M. Molecular engineering of C4 photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 297–314 (2001).

    Article  CAS  Google Scholar 

  22. Maurino, V. G., Drincovich, M. F. & Andreo, C. S. NADP-malic enzyme isoforms in maize leaves. Biochem. Mol. Biol. Int. 38, 239–250 (1996).

    CAS  PubMed  Google Scholar 

  23. Long, J. J., Wang, J.-L. & Berry, J. O. Cloning and analysis of the C4 photosynthetic NAD-dependent malic enzyme of amaranth mitochondria. J. Biol. Chem. 269, 2827–2833 (1994).

    CAS  PubMed  Google Scholar 

  24. Voznesenskaya, E. V. et al. Salsola arbusculiformis, a C3–C4 intermediate in Salsoleae (Chenopodiaceae). Ann. Bot. 88, 337–348 (2001).

    Article  Google Scholar 

  25. Akhani, H., Trimborn, P. & Ziegler, H. Photosynthetic pathways in Chenopodiaceae from Africa, Asia and Europe with their ecological, phytogeographical and taxonomical importance. Plant Syst. Evol. 206, 187–221 (1997).

    Article  Google Scholar 

  26. Dai, Z., Ku, M. S. B. & Edwards, G. E. Oxygen sensitivity of photosynthesis in C3, C4, and C3–C4 intermediate species of Flaveria. Planta 198, 563–571 (1996).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the Electron Microscope Center of Washington State University for use of facilities and staff assistance. We thank N. Ogar and H. Akhani for supply of viable seeds, and S. Huber, C. A. Ryan and T. Okita for comments on the manuscript. This work was supported by the National Science Foundation (G.E.E.) and the DFG (H.F.).

Author information

Authors and Affiliations

  1. Laboratory of Anatomy and Morphology, V. L. Komarov Botanical Institute of Russian Academy of Sciences, Prof. Popov Street 2, St Petersburg, 197376, Russia

    Elena V. Voznesenskaya

  2. School of Biological Sciences, Washington State University, Pullman, 99164-4236, Washington, USA

    Vincent R. Franceschi, Olavi Kiirats & Gerald E. Edwards

  3. Morphologie u. Systematik der Pflanzen, Universität Gesamthochschule Kassel, FB19, Kassel, D-34109, Germany

    Helmut Freitag

Authors
  1. Elena V. Voznesenskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vincent R. Franceschi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Olavi Kiirats
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Helmut Freitag
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gerald E. Edwards
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gerald E. Edwards.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Voznesenskaya, E., Franceschi, V., Kiirats, O. et al. Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature 414, 543–546 (2001). https://doi.org/10.1038/35107073

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35107073

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