Skip to main content

Thank you for visiting 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.

Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants


Most plants are known as C3 plants because the first product of photosynthetic CO2 fixation is a three-carbon compound1. C4 plants, which use an alternative pathway in which the first product is a four-carbon compound, have evolved independently many times and are found in at least 18 families2,3. In addition to differences in their biochemistry, photosynthetic organs of C4 plants show alterations in their anatomy and ultrastructure4. Little is known about whether the biochemical or anatomical characteristics of C4 photosynthesis evolved first. Here we report that tobacco, a typical C3 plant, shows characteristics of C4 photosynthesis in cells of stems and petioles that surround the xylem and phloem, and that these cells are supplied with carbon for photosynthesis from the vascular system and not from stomata. These photosynthetic cells possess high activities of enzymes characteristic of C4 photosynthesis, which allow the decarboxylation of four-carbon organic acids from the xylem and phloem, thus releasing CO2 for photosynthesis. These biochemical characteristics of C4 photosynthesis in cells around the vascular bundles of stems of C3 plants might explain why C4 photosynthesis has evolved independently many times.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it


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

Figure 1: Distribution of chlorophyll in petioles of celery and tobacco.
Figure 2: Incorporation of 14C into insoluble material in cells around the vascular system of celery and tobacco.
Figure 3: Photosynthesis around the veins of C3 and C4 plants.


  1. Calvin, M. et al. Carbon dioxide assimilation in plants. Symp. Soc. Exp. Biol. 5, 284–305 (1951).

    CAS  Google Scholar 

  2. Moore, P. D. Evolution of photosynthetic pathways in flowering plants. Nature 310, 696 (1982).

    Google Scholar 

  3. Sage, R. F., Li, M. & Monson, R. K. in C4 Plant Biology (eds Sage, R. F. & Monson, R. K.) 551–584 (Academic, San Diego, 1999).

    Book  Google Scholar 

  4. Hatch, M. D. C4 photosynthesis; a unique blend of modified biochemistry, anatomy and ultrastructure. Biochem. Biophys. Acta 895, 81–106 (1987).

    CAS  Google Scholar 

  5. Reinfelder, J. R., Kraepiel, A. M. L. & Morel, F. M. Unicellular C4 photosynthesis in a marine diatom. Nature 407, 996–999 (2000).

    Article  ADS  CAS  Google Scholar 

  6. Monson, R. K. in C4 Plant Biology (eds Sage R. F. & Monson, R. K.) 377–410 (Academic, San Diego, 1999).

    Book  Google Scholar 

  7. Rawsthorne, S. C3–C4 intermediate photosynthesis: linking physiology to gene expression. Plant J. 2, 267–274 (1992).

    Article  CAS  Google Scholar 

  8. Rawsthorne, S., Hylton, C. M., Smith, A. M. & Woolhouse, H. W. Photorespiratory and immunogold localization of photorespiratory enzymes in leaves of C3 and C3–C4 intermediate species of Moricandia. Planta 173, 298–308 (1988).

    Article  CAS  Google Scholar 

  9. Rawsthorne, S., Hylton, C. M., Smith, A. M. & Woolhouse, H. W. Distribution of photorespiratory enzymes between bundle sheath and mesophyll cells in leaves of the C3–C4 intermediate species Moricandia arvensis (L.) DC. Planta 176, 527–532 (1988).

    Article  CAS  Google Scholar 

  10. Keeley, J. E. CAM photosynthesis in submerged aquatic plants. Bot. Rev. 64, 121–175 (1998).

    Article  Google Scholar 

  11. Keeley, J. E., Osmond, C. B. & Raven, J. A. Stylites, a vascular land plant without stomata absorbs CO2 via its roots. Nature 310, 694–695 (1984).

    Article  ADS  CAS  Google Scholar 

  12. Hibberd, J. M. et al. Localization of photosynthetic metabolism in the parasitic angiosperm Cuscuta reflexa. Planta 205, 506–513 (1998).

    Article  CAS  Google Scholar 

  13. Esau, K. Plant Anatomy 2nd edn (John Wiley, New York, 1965).

    Google Scholar 

  14. Kinsman, E. A. & Pyke, K. A. Bundle sheath cells and cell-specific plastid development in Arabidopsis leaves. Development 125, 1815–1822 (1998).

    CAS  Google Scholar 

  15. Nilsen, E. T. in Plant Stems (ed. Gartner, B. L.) 223–240 (Academic, San Diego, 1995).

    Book  Google Scholar 

  16. Raven, J. A. Long-term functioning of enucleate sieve elements: possible mechanisms of damage avoidance and damage repair. Plant Cell Environ. 14, 139–146 (1991).

    Article  Google Scholar 

  17. Gerendas, J. & Schurr, U. Physicochemical aspects of ion relations and pH regulation in plants—a quantitative approach. J. Exp. Bot. 50, 1101–1114 (1999).

    CAS  Google Scholar 

  18. Cramer, M. D. & Richards, M. B. The effect of rhizosphere dissolved inorganic carbon on gas exchange characteristics and growth rates of tomato seedlings. J. Exp. Bot. 50, 79–87 (1999).

    Article  CAS  Google Scholar 

  19. Cramer, M. D., Gao, Z. F. & Lips, S. H. The influence of dissolved inorganic carbon in the rhizosphere on carbon and nitrogen metabolism in salinity treated tomato plants. New Phytol. 142, 441–450 (1999).

    Article  CAS  Google Scholar 

  20. Vuorinen, A. R., Rossi, P. & Vapaavuori, E. M. Combined effect of inorganic carbon and different nitrogen sources in the growth media on biomass production and nitrogen uptake in young willow and birch plants. J. Plant Physiol. 147, 236–242 (1995).

    Article  CAS  Google Scholar 

  21. Pate, J. S. in Encylopedia of Plant Physiology Vol. 1 (eds Zimmerman, M. H. & Milburn, J. A. ) 451–473 (Springer, Heidelberg, 1975).

    Google Scholar 

  22. Raven, J. A. & Smith, F. A. Nitrogen assimilation and transport in vascular land plants in relation to intracellular pH regulation. New Phytol. 76, 415–431 (1976).

    Article  CAS  Google Scholar 

  23. Ben Zioni, A., Vaadia, Y. & Lips, S. H. Nitrate uptake by roots as regulated by nitrate reduction products of the shoot. Physiol. Plant. 24, 288–290 (1971).

    Article  CAS  Google Scholar 

  24. Hibberd, J. M., Quick, W. P., Press, M. C., Scholes, J. D. & Jeschke, W. D. Solute fluxes from tobacco to the parasitic angiosperm Orobanche cernua and the influence of infection on host carbon and nitrogen relations. Plant Cell Environ. 22, 937–947 (1999).

    Article  CAS  Google Scholar 

  25. Ashton, A. R., Burnell, J. N., Furbank, R. T., Jenkins, C. L. D. & Hatch, M. D. in Methods in Plant Biochemistry, Vol. 3 (ed. Lea, P. J.) 39–72 (Academic, San Diego, 1990).

    Google Scholar 

  26. Lea, P. J. & Leegood, R. C. Plant Biochemistry and Molecular Biology (Wiley, Chichester, 1999).

    Google Scholar 

  27. Schaaf, J., Walter, M. H. & Hess, D. Primary metabolism in plant defence. Plant Physiol. 108, 949–960 (1995).

    Article  CAS  Google Scholar 

  28. Gao, Z., Sagi, M. & Lips, M. Assimilate allocation priority as affected by nitrogen compounds in the xylem sap of tomato. Plant Physiol. Biochem. 34, 807–815 (1996).

    CAS  Google Scholar 

  29. Thomas, J. C., De Armond, R. L. & Bohnert, H. J. Influence of NaCl on growth, proline and phosphoenolpyruvate carboxylase levels in Mesembryanthemum crystallinum suspension cultures. Plant Physiol. 98, 626–631 (1992).

    Article  CAS  Google Scholar 

  30. Walker, R. P., Trevanion, S. J. & Leegood, R. C. Phosphenolpyruvate carboxykinase from higher plants: Purification from cucumber and evidence of rapid proteolytic cleavage in extracts from a range of plant tissues. Planta 196, 58–63 (1995).

    Article  CAS  Google Scholar 

Download references


We thank J. C. Gray and W. D. Jeschke for discussions. J.M.H. thanks the BBSRC for a Sir David Phillips Research Fellowship.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Julian M. Hibberd.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hibberd, J., Quick, W. Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature 415, 451–454 (2002).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

This article is cited by


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.


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