Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin

Abstract

Microtubules (MTs) and actin filaments (F-actin) function cooperatively to regulate plant cell morphogenesis. However, the mechanisms underlying the crosstalk between these two cytoskeletal systems, particularly in cell shape control, remain largely unknown. Here, we show that introduction of the MyTH4-FERM tandem into KCBP (Kinesin-like Calmodulin-Binding Protein) during evolution conferred novel functions. The MyTH4 domain and the FERM domain in the N-terminal tail of KCBP physically bind to MTs and F-actin, respectively. During trichome morphogenesis, KCBP distributes in a specific cortical gradient, and concentrates at the branching sites and the apexes of elongating branches, which lack MTs but have cortical F-actin. Further live-cell imaging and genetic analyses revealed that KCBP acts as a hub integrating MTs and actin filaments to assemble the required cytoskeletal configuration for the unique, polarized diffuse growth pattern during trichome cell morphogenesis. Our findings provide significant insights into the mechanisms underlying cytoskeletal regulation of cell shape determination.

Article and author information

Author details

  1. Juan Tian

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Libo Han

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Zhidi Feng

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Guangda Wang

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Weiwei Liu

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Yinping Ma

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Yanjun Yu

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Zhaosheng Kong

    State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China
    For correspondence
    zskong@im.ac.cn
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Sheila McCormick, University of California-Berkeley & USDA Agricultural Research Service, United States

Version history

  1. Received: June 11, 2015
  2. Accepted: August 18, 2015
  3. Accepted Manuscript published: August 19, 2015 (version 1)
  4. Version of Record published: September 18, 2015 (version 2)

Copyright

© 2015, Tian 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. Juan Tian
  2. Libo Han
  3. Zhidi Feng
  4. Guangda Wang
  5. Weiwei Liu
  6. Yinping Ma
  7. Yanjun Yu
  8. Zhaosheng Kong
(2015)
Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin
eLife 4:e09351.
https://doi.org/10.7554/eLife.09351

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https://doi.org/10.7554/eLife.09351

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