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C4 photosynthesis boosts growth by altering physiology, allocation and size

Nature Plants volume 2, Article number: 16038 (2016) Cite this article

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Abstract

C4 photosynthesis is a complex set of leaf anatomical and biochemical adaptations that have evolved more than 60 times to boost carbon uptake compared with the ancestral C3 photosynthetic type1–3. Although C4 photosynthesis has the potential to drive faster growth rates4,5, experiments directly comparing C3 and C4 plants have not shown consistent effects1,6,7. This is problematic because differential growth is a crucial element of ecological theory8,9 explaining C4 savannah responses to global change10,11, and research to increase C3 crop productivity by introducing C4 photosynthesis12. Here, we resolve this long-standing issue by comparing growth across 382 grass species, accounting for ecological diversity and evolutionary history. C4 photosynthesis causes a 19–88% daily growth enhancement. Unexpectedly, during the critical seedling establishment stage, this enhancement is driven largely by a high ratio of leaf area to mass, rather than fast growth per unit leaf area. C4 leaves have less dense tissues, allowing more leaves to be produced for the same carbon cost. Consequently, C4 plants invest more in roots than C3 species. Our data demonstrate a general suite of functional trait divergences between C3 and C4 species, which simultaneously drive faster growth and greater investment in water and nutrient acquisition, with important ecological and agronomic implications.

The repeated emergence of C4 photosynthesis across multiple independent plant lineages transformed plant evolutionary history, and represents a remarkable example of convergent evolution1,2. Despite accounting for only 3% of extant plant species, C4 lineages today dominate warm, open environments and account for 25% of terrestrial carbon fixation9,10. C4 grasses include some of the world's most important food and energy crops, and C4 grassy savannahs provide critical ecosystem services for more than a billion people13. Understanding how the C4 photosynthetic pathway changes plant growth is therefore crucially important for plant evolution, crop production and ecosystem ecology.

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Figure 1: Relative growth rate of the sampled species.
Figure 2: Relative growth rate.
Figure 3: Components of growth.

References

  1. Christin, P.-A. & Osborne, C. P. The evolutionary ecology of C4 plants. New Phytol. 204, 765–781 (2014).

    Article  CAS  Google Scholar 

  2. Sage, R. F., Christin, P.-A. & Edwards, E. J. The C4 plant lineages of planet Earth. J. Exp. Bot. 62, 3155–3169 (2011).

    Article  CAS  Google Scholar 

  3. Hatch, M. D. & Slack, C. R. Photosynthesis by sugar-cane leaves. A new carboxylation reaction and the pathway of sugar formation. Biochem. J. 101, 103–111 (1966).

    Article  CAS  Google Scholar 

  4. Monteith, J. L. Reassessment of maximum growth rates for C3 and C4 crops. Exp. Agr. 14, 1–5 (1978).

    Article  CAS  Google Scholar 

  5. Zhu, X.-G., Long, S. P. & Ort, D. R. Improving photosynthetic efficiency for greater yield. Ann. Rev. Plant Biol. 61, 235–261 (2010).

    Article  CAS  Google Scholar 

  6. Snaydon, R. W. The productivity of C3 and C4 plants: a reassessment. Funct. Ecol. 5, 321–330 (1991).

    Article  Google Scholar 

  7. Long, S. P. in C4 Plant Biology (eds Sage, R. F. & Monson, R. K. ) Ch. 7, 215–249 (Academic, 1999).

    Book  Google Scholar 

  8. Ehleringer, J. R. Implications of quantum yield differences on the distributions of C3 and C4 grasses. Oecologia 31, 255–267 (1978).

    Article  Google Scholar 

  9. Ehleringer, J. R., Cerling, T. E. & Helliker, B. R. C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112, 285–299 (1997).

    Article  Google Scholar 

  10. Still, C. J., Berry, J. A., Collatz, G. J. & DeFries, R. S. Global distribution of C3 and C4 vegetation: carbon cycle implications. Global Biogeochem. Cycles 17, 1006 (2003).

    Article  Google Scholar 

  11. Edwards, E. J., Osborne, C. P. & Stromberg, C. A. The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328, 587–591 (2010).

    Article  CAS  Google Scholar 

  12. von Caemmerer, S., Quick, W. P. & Furbank, R. T. The development of C4 rice: current progress and future challenges. Science 336, 1671–1672 (2012).

    Article  CAS  Google Scholar 

  13. Parr, C. L., Lehmann, C. E. R., Bond, W. J., Hoffmann, W. A. & Andersen, A. N. Tropical grassy biomes: misunderstood, neglected, and under threat. Trends Ecol. Evolut. 29, 205–213 (2014).

    Article  Google Scholar 

  14. Grass Phylogeny Working Group II. New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol. 193, 304–312 (2012).

    Article  Google Scholar 

  15. Rees, M. et al. Partitioning the components of relative growth rate: how important is plant size variation? Am. Nat. 176, E152–E161 (2010).

    Article  Google Scholar 

  16. Grime, J. P. et al. Integrated screening validates primary axes of specialisation in plants. Oikos 79, 259–281 (1997).

    Article  Google Scholar 

  17. Black, C. C., Chen, T. M. & Brown, R. H. Biochemical basis for plant competition. Weed Sci. 17, 338–344 (1969).

    CAS  Google Scholar 

  18. Sage, R. F. & Pearcy, R. W. The nitrogen use efficiency of C3 and C4 Plants. 1. Leaf nitrogen, growth, and biomass partitioning in Chenopodium album (L) and Amaranthus retroflexus (L). Plant Physiol. 84, 954–958 (1987).

    Article  CAS  Google Scholar 

  19. Poorter, H., Remkes, C. & Lambers, H. Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiol. 94, 621–627 (1990).

    Article  CAS  Google Scholar 

  20. Taylor, S. H. et al. Ecophysiological traits in C3 and C4 grasses: a phylogenetically controlled screening experiment. New Phytol. 185, 780–791 (2010).

    Article  CAS  Google Scholar 

  21. Ghannoum, O., Von Caemmerer, S., Ziska, L. H. & Conroy, J. P. The growth response of C4 plants to rising atmospheric CO2 partial pressure: a reassessment. Plant Cell Environ. 23, 931–942 (2000).

    Article  CAS  Google Scholar 

  22. Kiær, L. P., Weisbach, A. N. & Weiner, J. Root and shoot competition: a meta-analysis. J. Ecol. 101, 1298–1312 (2013).

    Article  Google Scholar 

  23. Atkinson, R. R. L., Burrell, M. M., Osborne, C. P., Rose, K. E. & Rees, M. A non-targeted metabolomics approach to quantifying differences in root storage between fast- and slow-growing plants. New Phytol. 196, 200–211 (2012).

    Article  CAS  Google Scholar 

  24. Ghannoum, O., Evans, J. & von Caemmerer, S. in C4 Photosynthesis and Related CO2 Concentrating Mechanisms Vol. 32 Advances in Photosynthesis and Respiration (eds Raghavendra, A. S. & Sage, R. F. ) Ch. 8, 129–146 (Springer Netherlands, 2011).

    Google Scholar 

  25. Shipley, B. & Vu, T.-T. Dry matter content as a measure of dry matter concentration in plants and their parts. New Phytol. 153, 359–364 (2002).

    Article  Google Scholar 

  26. Christin, P. A. et al. Anatomical enablers and the evolution of C4 photosynthesis in grasses. Proc. Natl Acad. Sci. USA 110, 1381–1386 (2013).

    Article  CAS  Google Scholar 

  27. Byott, G. S. Leaf air space systems in C3 and C4 species. New Phytol. 76, 295–299 (1976).

    Article  Google Scholar 

  28. Stata, M. et al. Mesophyll cells of C4 plants have fewer chloroplasts than those of closely related C3 plants. Plant Cell Environ. 37, 2587–2600 (2014).

    Article  CAS  Google Scholar 

  29. Ocheltree, T. W., Nippert, J. B. & Vara Prasad, P. V. A safety vs efficiency trade-off identified in the hydraulic pathway of grass leaves is decoupled from photosynthesis, stomatal conductance and precipitation. New Phytol. 210, 97–107.

  30. Hewitt, E. J. Sand and water culture methods used in the study of plant nutrition (Commonwealth Agricultural Bureaux, 1966).

    Google Scholar 

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Acknowledgements

This work was funded by a Natural Environment Research Council grant (NE/I014322/1) awarded to C.P.O., M.R., R.P.F. and K.T. P.A.C. thanks The Royal Society for support from a University Research Fellowship.

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Authors and Affiliations

  1. Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK

    Rebecca R. L. Atkinson, Emily J. Mockford, Christopher Bennett, Pascal-Antoine Christin, Robert P. Freckleton, Ken Thompson, Mark Rees & Colin P. Osborne

  2. Department of Ecology and Evolutionary Biology, Yale University, New Haven, 06520-8105, Connecticut, USA

    Elizabeth L. Spriggs

Authors
  1. Rebecca R. L. Atkinson
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Contributions

C.P.O., R.P.F., K.T. and M.R. conceived the project. R.R.L.A., R.P.F., K.T., M.R. and C.P.O. designed the experiments. R.R.L.A., E.J.M. and C.B. carried out the experiments and compiled the data. P.A.C. and E.L.S. sequenced DNA and built the phylogeny. R.R.L.A. and M.R. analysed experimental data. R.R.L.A., M.R. and C.P.O. wrote the paper. All authors interpreted the results and commented on the paper.

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Correspondence to Colin P. Osborne.

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The authors declare no competing financial interests.

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Atkinson, R., Mockford, E., Bennett, C. et al. C4 photosynthesis boosts growth by altering physiology, allocation and size. Nature Plants 2, 16038 (2016). https://doi.org/10.1038/nplants.2016.38

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