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

Abstract

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.

Article and author information

Author details

  1. Julia Mallmann

    Heinrich-Heine-Universität, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. David Heckmann

    Heinrich-Heine-Universität, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Andrea Bräutigam

    Heinrich-Heine-Universität, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Martin J Lercher

    Heinrich-Heine-Universität, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Andreas PM Weber

    Heinrich-Heine-Universität, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Peter Westhoff

    Heinrich-Heine-Universität, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Udo Gowik

    Heinrich-Heine-Universität, Düsseldorf, Germany
    For correspondence
    gowik@uni-duesseldorf.de
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Detlef Weigel, Max Planck Institute for Developmental Biology, Germany

Version history

  1. Received: February 6, 2014
  2. Accepted: June 14, 2014
  3. Accepted Manuscript published: June 16, 2014 (version 1)
  4. Version of Record published: July 22, 2014 (version 2)

Copyright

© 2014, Mallmann et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Julia Mallmann
  2. David Heckmann
  3. Andrea Bräutigam
  4. Martin J Lercher
  5. Andreas PM Weber
  6. Peter Westhoff
  7. Udo Gowik
(2014)
The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria
eLife 3:e02478.
https://doi.org/10.7554/eLife.02478

Share this article

https://doi.org/10.7554/eLife.02478

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