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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.

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

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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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  2. Emily J. Mockford
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  7. Ken Thompson
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  9. Colin P. Osborne
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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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