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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Christin, P.-A. & Osborne, C. P. The evolutionary ecology of C4 plants. New Phytol. 204, 765–781 (2014).
Sage, R. F., Christin, P.-A. & Edwards, E. J. The C4 plant lineages of planet Earth. J. Exp. Bot. 62, 3155–3169 (2011).
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).
Monteith, J. L. Reassessment of maximum growth rates for C3 and C4 crops. Exp. Agr. 14, 1–5 (1978).
Zhu, X.-G., Long, S. P. & Ort, D. R. Improving photosynthetic efficiency for greater yield. Ann. Rev. Plant Biol. 61, 235–261 (2010).
Snaydon, R. W. The productivity of C3 and C4 plants: a reassessment. Funct. Ecol. 5, 321–330 (1991).
Long, S. P. in C4 Plant Biology (eds Sage, R. F. & Monson, R. K. ) Ch. 7, 215–249 (Academic, 1999).
Ehleringer, J. R. Implications of quantum yield differences on the distributions of C3 and C4 grasses. Oecologia 31, 255–267 (1978).
Ehleringer, J. R., Cerling, T. E. & Helliker, B. R. C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112, 285–299 (1997).
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).
Edwards, E. J., Osborne, C. P. & Stromberg, C. A. The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328, 587–591 (2010).
von Caemmerer, S., Quick, W. P. & Furbank, R. T. The development of C4 rice: current progress and future challenges. Science 336, 1671–1672 (2012).
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).
Grass Phylogeny Working Group II. New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol. 193, 304–312 (2012).
Rees, M. et al. Partitioning the components of relative growth rate: how important is plant size variation? Am. Nat. 176, E152–E161 (2010).
Grime, J. P. et al. Integrated screening validates primary axes of specialisation in plants. Oikos 79, 259–281 (1997).
Black, C. C., Chen, T. M. & Brown, R. H. Biochemical basis for plant competition. Weed Sci. 17, 338–344 (1969).
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).
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).
Taylor, S. H. et al. Ecophysiological traits in C3 and C4 grasses: a phylogenetically controlled screening experiment. New Phytol. 185, 780–791 (2010).
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).
Kiær, L. P., Weisbach, A. N. & Weiner, J. Root and shoot competition: a meta-analysis. J. Ecol. 101, 1298–1312 (2013).
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).
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).
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).
Christin, P. A. et al. Anatomical enablers and the evolution of C4 photosynthesis in grasses. Proc. Natl Acad. Sci. USA 110, 1381–1386 (2013).
Byott, G. S. Leaf air space systems in C3 and C4 species. New Phytol. 76, 295–299 (1976).
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).
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.
Hewitt, E. J. Sand and water culture methods used in the study of plant nutrition (Commonwealth Agricultural Bureaux, 1966).
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.
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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