1. Cell Biology
  2. Plant Biology
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Stromule extension along microtubules coordinated with actin-mediated anchoring guides perinuclear chloroplast movement during innate immunity

  1. Amutha Sampath Kumar
  2. Eunsook Park
  3. Alexander Nedo
  4. Ali Alqarni
  5. Li Ren
  6. Kyle Hoban
  7. Shannon Modla
  8. John H McDonald
  9. Chandra Kambhamettu
  10. Savithramma P Dinesh-Kumar  Is a corresponding author
  11. Jeffrey Lewis Caplan  Is a corresponding author
  1. University of Delaware, United States
  2. University of California, Davis, United States
Research Article
  • Cited 36
  • Views 5,060
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Cite this article as: eLife 2018;7:e23625 doi: 10.7554/eLife.23625

Abstract

Dynamic tubular extensions from chloroplasts called stromules have recently been shown to connect with nuclei and function during innate immunity. We demonstrate that stromules extend along microtubules (MTs) and MT organization directly affects stromule dynamics since stabilization of MTs chemically or genetically increases stromule numbers and length. Although actin filaments (AFs) are not required for stromule extension, they provide anchor points for stromules. Interestingly, there is a strong correlation between the direction of stromules from chloroplasts and the direction of chloroplast movement. Stromule-directed chloroplast movement was observed in steady-state conditions without immune induction, suggesting it is a general function of stromules in epidermal cells. Our results show that MTs and AFs may facilitate perinuclear clustering of chloroplasts during an innate immune response. We propose a model in which stromules extend along MTs and connect to AF anchor points surrounding nuclei, facilitating stromule-directed movement of chloroplasts to nuclei during innate immunity.

Article and author information

Author details

  1. Amutha Sampath Kumar

    Delaware Biotechnology Insititute, University of Delaware, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Eunsook Park

    Department of Plant and The Genome Center, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2984-3039
  3. Alexander Nedo

    Delaware Biotechnology Insititute, University of Delaware, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Ali Alqarni

    Delaware Biotechnology Insititute, University of Delaware, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Li Ren

    Department of Plant and Soil Sciences, University of Delaware, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Kyle Hoban

    Delaware Biotechnology Institute, University of Delaware, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Shannon Modla

    Delaware Biotechnology Institute, University of Delaware, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. John H McDonald

    Department of Biological Sciences, University of Delaware, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Chandra Kambhamettu

    Department of Plant and Soil Sciences, University of Delaware, Newark, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Savithramma P Dinesh-Kumar

    Department of Plant and The Genome Center, University of California, Davis, Davis, United States
    For correspondence
    spdineshkumar@ucdavis.edu
    Competing interests
    The authors declare that no competing interests exist.
  11. Jeffrey Lewis Caplan

    Delaware Biotechnology Institute, University of Delaware, Newark, United States
    For correspondence
    jcaplan@udel.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3991-0912

Funding

National Institutes of Health (R01 GM097587)

  • Savithramma P Dinesh-Kumar
  • Jeffrey Lewis Caplan

National Institutes of Health (P20 GM103446)

  • Jeffrey Lewis Caplan

National Institutes of Health (S10 OD016361)

  • Jeffrey Lewis Caplan

National Institutes of Health (S10 RR027273)

  • Jeffrey Lewis Caplan

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

Reviewing Editor

  1. Jean T Greenberg, University of Chicago, United States

Publication history

  1. Received: November 24, 2016
  2. Accepted: January 16, 2018
  3. Accepted Manuscript published: January 17, 2018 (version 1)
  4. Version of Record published: February 16, 2018 (version 2)

Copyright

© 2018, Kumar 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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