Expression of a CO2-permeable aquaporin enhances mesophyll conductance in the C4 species Setaria viridis

Abstract

A fundamental limitation of photosynthetic carbon fixation is the availability of CO2. In C4 plants, primary carboxylation occurs in mesophyll cytosol, and little is known about the role of CO2 diffusion in facilitating C4 photosynthesis. We have examined the expression, localization, and functional role of selected plasma membrane intrinsic aquaporins (PIPs) from Setaria italica (foxtail millet) and discovered that SiPIP2;7 is CO2-permeable. When ectopically expressed in mesophyll cells of S. viridis (green foxtail), SiPIP2;7 was localized to the plasma membrane and caused no marked changes in leaf biochemistry. Gas-exchange and C18O16O discrimination measurements revealed that targeted expression of SiPIP2;7 enhanced the conductance to CO2 diffusion from the intercellular airspace to the mesophyll cytosol. Our results demonstrate that mesophyll conductance limits C4 photosynthesis at low pCO2 and that SiPIP2;7 is a functional CO2 permeable aquaporin that can improve CO2 diffusion at the airspace/mesophyll interface and enhance C4 photosynthesis.

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All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Maria Ermakova

    Australian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Australian National University, Canberra, Australia
    For correspondence
    maria.ermakova@anu.edu.au
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8466-4186
  2. Hannah Osborn

    Australian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Australian National University, Canberra, Australia
    Competing interests
    The authors declare that no competing interests exist.
  3. Michael Groszmann

    Australian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Australian National University, Canberra, Australia
    Competing interests
    The authors declare that no competing interests exist.
  4. Soumi Bala

    Australian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Australian National University, Canberra, Australia
    Competing interests
    The authors declare that no competing interests exist.
  5. Andrew Bowerman

    Australian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Australian National University, Canberra, Australia
    Competing interests
    The authors declare that no competing interests exist.
  6. Samantha McGaughey

    Australian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Australian National University, Canberra, Australia
    Competing interests
    The authors declare that no competing interests exist.
  7. Caitlin Byrt

    Australian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Australian National University, Canberra, Australia
    Competing interests
    The authors declare that no competing interests exist.
  8. Hugo Alonso-cantabrana

    Australian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Australian National University, Canberra, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5462-5861
  9. Steve Tyerman

    ARC Centre of Excellence in Plant Energy Biology, School of Agriculture Food and Wine, University of Adelaide, Adelaide, Australia
    Competing interests
    The authors declare that no competing interests exist.
  10. Robert T Furbank

    ARC Centre of Excellence in Plant Energy Biology, School of Agriculture Food and Wine, Australian National University, Canberra, Australia
    Competing interests
    The authors declare that no competing interests exist.
  11. Robert E Sharwood

    Hawkesbury Institute for the Environment, Western Sydney University, Richmond, Australia
    For correspondence
    robert.sharwood@anu.edu.au
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4993-3816
  12. Suzanne von Caemmerer

    Australian Research Council Centre of Excellence for Translational Photosynthesis, Division of Plant Science, Australian National University, Canberra, Australia
    Competing interests
    The authors declare that no competing interests exist.

Funding

Australian Research Council (Centre of Excellence for Translational Photosynthesis,CE140100015)

  • Maria Ermakova
  • Hannah Osborn
  • Michael Groszmann
  • Soumi Bala
  • Hugo Alonso-cantabrana
  • Robert T Furbank
  • Robert E Sharwood
  • Suzanne von Caemmerer

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

Reviewing Editor

  1. David M Kramer, Michigan State University, United States

Version history

  1. Preprint posted: April 29, 2021 (view preprint)
  2. Received: May 6, 2021
  3. Accepted: November 23, 2021
  4. Accepted Manuscript published: November 29, 2021 (version 1)
  5. Version of Record published: December 6, 2021 (version 2)

Copyright

© 2021, Ermakova 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. Maria Ermakova
  2. Hannah Osborn
  3. Michael Groszmann
  4. Soumi Bala
  5. Andrew Bowerman
  6. Samantha McGaughey
  7. Caitlin Byrt
  8. Hugo Alonso-cantabrana
  9. Steve Tyerman
  10. Robert T Furbank
  11. Robert E Sharwood
  12. Suzanne von Caemmerer
(2021)
Expression of a CO2-permeable aquaporin enhances mesophyll conductance in the C4 species Setaria viridis
eLife 10:e70095.
https://doi.org/10.7554/eLife.70095

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https://doi.org/10.7554/eLife.70095

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