Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle

  1. Timothy J Ross-Elliott
  2. Kaare H Jensen
  3. Katrine S Haaning
  4. Brittney Michaelle Wager
  5. Jan Knoblauch
  6. Alexander H Howell
  7. Daniel L Mullendore
  8. Alexander G Monteith
  9. Danae Paultre
  10. Dawei Yan
  11. Sofia Otero-Perez
  12. Matthieu Bourdon
  13. Ross Sager
  14. Jung-Youn Lee
  15. Ykä Helariutta
  16. Michael Knoblauch  Is a corresponding author
  17. Karl John Oparka  Is a corresponding author
  1. Washington State University, United States
  2. Technical University of Denmark, Denmark
  3. Oxford Brookes University, United Kingdom
  4. University of Edinburgh, United Kingdom
  5. University of Cambridge, United Kingdom
  6. University of Delaware, United States

Abstract

In plants, a complex mixture of solutes and macromolecules is transported by the phloem. Here we examined how solutes and macromolecules are separated when they exit the phloem during the unloading process. We used a combination of approaches (non-invasive imaging, 3D-electron microscopy, and mathematical modelling) to show that phloem unloading of solutes in Arabidopsis roots occurs through plasmodesmata by a combination of mass flow and diffusion (convective phloem unloading). During unloading, solutes and proteins are diverted into the phloem-pole pericycle, a tissue connected to the protophloem by a unique class of 'funnel plasmodesmata'. While solutes are unloaded without restriction, large proteins are released through funnel plasmodesmata in discrete pulses, a phenomenon we refer to as 'batch unloading'. Unlike solutes, these proteins remain restricted to the phloem-pole pericycle. Our data demonstrate a major role for the phloem-pole pericycle in regulating phloem unloading in roots.

Article and author information

Author details

  1. Timothy J Ross-Elliott

    School of Biological Sciences, Washington State University, Pullman, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Kaare H Jensen

    Department of Physics, Technical University of Denmark, Lyngby, Denmark
    Competing interests
    The authors declare that no competing interests exist.
  3. Katrine S Haaning

    Department of Physics, Technical University of Denmark, Lyngby, Denmark
    Competing interests
    The authors declare that no competing interests exist.
  4. Brittney Michaelle Wager

    School of Biological Sciences, Washington State University, Pullman, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Jan Knoblauch

    School of Biological Sciences, Washington State University, Pullman, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Alexander H Howell

    School of Biological Sciences, Washington State University, Pullman, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Daniel L Mullendore

    School of Biological Sciences, Washington State University, Pullman, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Alexander G Monteith

    Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1731-0446
  9. Danae Paultre

    Institute of Molecular Plant Science, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. Dawei Yan

    Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  11. Sofia Otero-Perez

    Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  12. Matthieu Bourdon

    Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  13. Ross Sager

    Department of Plant and Soil Sciences, University of Delaware, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Jung-Youn Lee

    Department of Plant and Soil Sciences, University of Delaware, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  15. Ykä Helariutta

    Sainsbury Laboratory, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  16. Michael Knoblauch

    School of Biological Sciences, Washington State University, Pullman, United States
    For correspondence
    knoblauch@wsu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0391-9891
  17. Karl John Oparka

    Institute of Molecular Plant Science, University of Edinburgh, Edinburgh, United Kingdom
    For correspondence
    karl.oparka@ed.ac.uk
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Science Foundation (1146500)

  • Michael Knoblauch

Biotechnology and Biological Sciences Research Council

  • Karl John Oparka

Carlsbergfondet

  • Kaare H Jensen

Villum Fonden (13166)

  • Kaare H Jensen

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

Reviewing Editor

  1. Christian S Hardtke, University of Lausanne, Switzerland

Version history

  1. Received: December 10, 2016
  2. Accepted: February 17, 2017
  3. Accepted Manuscript published: February 23, 2017 (version 1)
  4. Version of Record published: March 24, 2017 (version 2)
  5. Version of Record updated: November 13, 2017 (version 3)

Copyright

© 2017, Ross-Elliott 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. Timothy J Ross-Elliott
  2. Kaare H Jensen
  3. Katrine S Haaning
  4. Brittney Michaelle Wager
  5. Jan Knoblauch
  6. Alexander H Howell
  7. Daniel L Mullendore
  8. Alexander G Monteith
  9. Danae Paultre
  10. Dawei Yan
  11. Sofia Otero-Perez
  12. Matthieu Bourdon
  13. Ross Sager
  14. Jung-Youn Lee
  15. Ykä Helariutta
  16. Michael Knoblauch
  17. Karl John Oparka
(2017)
Phloem unloading in Arabidopsis roots is convective and regulated by the phloem-pole pericycle
eLife 6:e24125.
https://doi.org/10.7554/eLife.24125

Share this article

https://doi.org/10.7554/eLife.24125

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