The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria

Elife. 2014 Jun 16:3:e02478. doi: 10.7554/eLife.02478.


C4 photosynthesis represents a most remarkable case of convergent evolution of a complex trait, which includes the reprogramming of the expression patterns of thousands of genes. Anatomical, physiological, and phylogenetic and analyses as well as computational modeling indicate that the establishment of a photorespiratory carbon pump (termed C2 photosynthesis) is a prerequisite for the evolution of C4. However, a mechanistic model explaining the tight connection between the evolution of C4 and C2 photosynthesis is currently lacking. Here we address this question through comparative transcriptomic and biochemical analyses of closely related C3, C3-C4, and C4 species, combined with Flux Balance Analysis constrained through a mechanistic model of carbon fixation. We show that C2 photosynthesis creates a misbalance in nitrogen metabolism between bundle sheath and mesophyll cells. Rebalancing nitrogen metabolism requires anaplerotic reactions that resemble at least parts of a basic C4 cycle. Our findings thus show how C2 photosynthesis represents a pre-adaptation for the C4 system, where the evolution of the C2 system establishes important C4 components as a side effect.

Keywords: 4; Flaveria; evolution; evolutionary biology; genomics; plant biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biological Evolution*
  • Carbon / metabolism
  • Cell Respiration / radiation effects
  • Flaveria / genetics
  • Flaveria / physiology*
  • Flaveria / radiation effects*
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant / radiation effects
  • Light*
  • Models, Biological
  • Photosynthesis / radiation effects*
  • Plant Leaves / genetics
  • Plant Leaves / radiation effects
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism


  • RNA, Messenger
  • Carbon

Associated data

  • SRA/SRP036880
  • SRA/SRP036881
  • SRA/SRP036883
  • SRA/SRP036884
  • SRA/SRP036885
  • SRA/SRP037526
  • SRA/SRP037527
  • SRA/SRP037528
  • SRA/SRP037529

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.