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Oecologia

, Volume 187, Issue 4, pp 941–966 | Cite as

Some like it hot: the physiological ecology of C4 plant evolution

  • Rowan F. Sage
  • Russell K. Monson
  • James R. Ehleringer
  • Shunsuke Adachi
  • Robert W. Pearcy
Special Topic

Abstract

The evolution of C4 photosynthesis requires an intermediate phase where photorespiratory glycine produced in the mesophyll cells must flow to the vascular sheath cells for metabolism by glycine decarboxylase. This glycine flux concentrates photorespired CO2 within the sheath cells, allowing it to be efficiently refixed by sheath Rubisco. A modest C4 biochemical cycle is then upregulated, possibly to support the refixation of photorespired ammonia in sheath cells, with subsequent increases in C4 metabolism providing incremental benefits until an optimized C4 pathway is established. ‘Why’ C4 photosynthesis evolved is largely explained by ancestral C3 species exploiting photorespiratory CO2 to improve carbon gain and thus enhance fitness. While photorespiration depresses C3 performance, it produces a resource (photorespired CO2) that can be exploited to build an evolutionary bridge to C4 photosynthesis. ‘Where’ C4 evolved is indicated by the habitat of species branching near C3-to-C4 transitions on phylogenetic trees. Consistent with the photorespiratory bridge hypothesis, transitional species show that the large majority of > 60 C4 lineages arose in hot, dry, and/or saline regions where photorespiratory potential is high. ‘When’ C4 evolved has been clarified by molecular clock analyses using phylogenetic data, coupled with isotopic signatures from fossils. Nearly all C4 lineages arose after 25 Ma when atmospheric CO2 levels had fallen to near current values. This reduction in CO2, coupled with persistent high temperature at low-to-mid-latitudes, met a precondition where photorespiration was elevated, thus facilitating the evolutionary selection pressure that led to C4 photosynthesis.

Keywords

C4 photosynthesis C3–C4 intermediate Flaveria Photorespiration Photosynthetic evolution 

Notes

Acknowledgements

We thank Perlina Lim for assistance with manuscript preparation. Preparation of this review was supported by funding from the Natural Science and Engineering Research Council of Canada to RFS.

Author contribution statement

RFS outlined the review and wrote the initial draft, and prepared all figures. RKM revised the draft with new input. JRE and RWP provided critical feedback on multiple drafts. SA measured all new data for Fig. 3 and provided editorial feedback on the final draft.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

442_2018_4191_MOESM1_ESM.pdf (756 kb)
Supplementary material 1 (PDF 756 kb)

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of TorontoTorontoCanada
  2. 2.Department of Ecology and Evolutionary Biology and Laboratory of Tree Ring ResearchUniversity of ArizonaTucsonUSA
  3. 3.School of Biological SciencesUniversity of UtahSalt Lake CityUSA
  4. 4.Institute of Global Innovation ResearchTokyo University of Agriculture and TechnologyFuchuJapan
  5. 5.Section of Evolution and Ecology, College of Biological SciencesUniversity of CaliforniaDavisUSA

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