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Confined-microtubule assembly shapes three-dimensional cell wall structures in xylem vessels

Author

Listed:
  • Takema Sasaki

    (Nagoya University, Furo-cho, Chikusa-ku)

  • Kei Saito

    (National Institute of Genetics
    SOKENDAI University)

  • Daisuke Inoue

    (Kyusyu University)

  • Henrik Serk

    (Umeå University)

  • Yuki Sugiyama

    (Nagoya University, Furo-cho, Chikusa-ku
    Nagoya University, Furo-cho, Chikusa-ku)

  • Edouard Pesquet

    (Umeå University
    Environment and Plant Sciences (DEEP), Stockholm University)

  • Yuta Shimamoto

    (National Institute of Genetics
    SOKENDAI University)

  • Yoshihisa Oda

    (Nagoya University, Furo-cho, Chikusa-ku)

Abstract

Properly patterned deposition of cell wall polymers is prerequisite for the morphogenesis of plant cells. A cortical microtubule array guides the two-dimensional pattern of cell wall deposition. Yet, the mechanism underlying the three-dimensional patterning of cell wall deposition is poorly understood. In metaxylem vessels, cell wall arches are formed over numerous pit membranes, forming highly organized three-dimensional cell wall structures. Here, we show that the microtubule-associated proteins, MAP70-5 and MAP70-1, regulate arch development. The map70-1 map70-5 plants formed oblique arches in an abnormal orientation in pits. Microtubules fit the aperture of developing arches in wild-type cells, whereas microtubules in map70-1 map70-5 cells extended over the boundaries of pit arches. MAP70 caused the bending and bundling of microtubules. These results suggest that MAP70 confines microtubules within the pit apertures by altering the physical properties of microtubules, thereby directing the growth of pit arches in the proper orientation. This study provides clues to understanding how plants develop three-dimensional structure of cell walls.

Suggested Citation

  • Takema Sasaki & Kei Saito & Daisuke Inoue & Henrik Serk & Yuki Sugiyama & Edouard Pesquet & Yuta Shimamoto & Yoshihisa Oda, 2023. "Confined-microtubule assembly shapes three-dimensional cell wall structures in xylem vessels," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42487-w
    DOI: 10.1038/s41467-023-42487-w
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    References listed on IDEAS

    as
    1. Yuki Sugiyama & Yoshinobu Nagashima & Mayumi Wakazaki & Mayuko Sato & Kiminori Toyooka & Hiroo Fukuda & Yoshihisa Oda, 2019. "A Rho-actin signaling pathway shapes cell wall boundaries in Arabidopsis xylem vessels," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    2. Sarah Rice & Abel W. Lin & Daniel Safer & Cynthia L. Hart & Nariman Naber & Bridget O. Carragher & Shane M. Cain & Elena Pechatnikova & Elizabeth M. Wilson-Kubalek & Michael Whittaker & Edward Pate & , 1999. "A structural change in the kinesin motor protein that drives motility," Nature, Nature, vol. 402(6763), pages 778-784, December.
    3. Jaclyn P. Kerr & Patrick Robison & Guoli Shi & Alexey I. Bogush & Aaron M. Kempema & Joseph K. Hexum & Natalia Becerra & Daniel A. Harki & Stuart S. Martin & Roberto Raiteri & Benjamin L. Prosser & Ch, 2015. "Detyrosinated microtubules modulate mechanotransduction in heart and skeletal muscle," Nature Communications, Nature, vol. 6(1), pages 1-14, December.
    4. Chris Ambrose & Jun F. Allard & Eric N. Cytrynbaum & Geoffrey O. Wasteneys, 2011. "A CLASP-modulated cell edge barrier mechanism drives cell-wide cortical microtubule organization in Arabidopsis," Nature Communications, Nature, vol. 2(1), pages 1-12, September.
    5. René Schneider & Kris van’t Klooster & Kelsey L. Picard & Jasper Gucht & Taku Demura & Marcel Janson & Arun Sampathkumar & Eva E. Deinum & Tijs Ketelaar & Staffan Persson, 2021. "Long-term single-cell imaging and simulations of microtubules reveal principles behind wall patterning during proto-xylem development," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
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