Higher plant myosin XI moves processively on actin with 35 nm steps at high velocity

Motoki Tominaga, Hiroaki Kojima, Etsuo Yokota, Hidefumi Orii, Rinna Nakamori, Eisaku Katayama, Michael Anson, Teruo Shimmen, Kazuhiro Oiwa

Research output: Contribution to journalArticle

136 Citations (Scopus)

Abstract

High velocity cytoplasmic streaming is found in various plant cells from algae to angiosperms. We characterized mechanical and enzymatic properties of a higher plant myosin purified from tobacco bright yellow-2 cells, responsible for cytoplasmic streaming, having a 175 kDa heavy chain and calmodulin light chains. Sequence analysis shows it to be a class XI myosin and a dimer with six IQ motifs in the light chain-binding domains of each heavy chain. Electron microscopy confirmed these predictions. We measured its ATPase characteristics, in vitro motility and, using optical trap nanometry, forces and movement developed by individual myosin XI molecules. Single myosin XI molecules move processively along actin with 35 nm steps at 7 μm/s, the fastest known processive motion. Processivity was confirmed by actin landing rate assays. Mean maximal force was ∼0.5 pN, smaller than for myosin IIs. Dwell time analysis of beads carrying single myosin XI molecules fitted the ATPase kinetics, with ADP release being rate limiting. These results indicate that myosin XI is highly specialized for generation of fast processive movement with concomitantly low forces.

Original languageEnglish
Pages (from-to)1263-1272
Number of pages10
JournalEMBO Journal
Volume22
Issue number6
DOIs
Publication statusPublished - 2003 Mar 17
Externally publishedYes

Fingerprint

Myosins
Actins
Cytoplasmic Streaming
Molecules
Adenosine Triphosphatases
Optical Tweezers
Light
Angiosperms
Tobacco
Plant Cells
Calmodulin
Algae
Landing
Dimers
Adenosine Diphosphate
Electron microscopy
Sequence Analysis
Assays
Electron Microscopy
Kinetics

Keywords

  • In vitro motility
  • Myosin XI
  • Optical trap
  • Processivity
  • Single molecule

ASJC Scopus subject areas

  • Genetics
  • Cell Biology

Cite this

Tominaga, M., Kojima, H., Yokota, E., Orii, H., Nakamori, R., Katayama, E., ... Oiwa, K. (2003). Higher plant myosin XI moves processively on actin with 35 nm steps at high velocity. EMBO Journal, 22(6), 1263-1272. https://doi.org/10.1093/emboj/cdg130

Higher plant myosin XI moves processively on actin with 35 nm steps at high velocity. / Tominaga, Motoki; Kojima, Hiroaki; Yokota, Etsuo; Orii, Hidefumi; Nakamori, Rinna; Katayama, Eisaku; Anson, Michael; Shimmen, Teruo; Oiwa, Kazuhiro.

In: EMBO Journal, Vol. 22, No. 6, 17.03.2003, p. 1263-1272.

Research output: Contribution to journalArticle

Tominaga, M, Kojima, H, Yokota, E, Orii, H, Nakamori, R, Katayama, E, Anson, M, Shimmen, T & Oiwa, K 2003, 'Higher plant myosin XI moves processively on actin with 35 nm steps at high velocity', EMBO Journal, vol. 22, no. 6, pp. 1263-1272. https://doi.org/10.1093/emboj/cdg130
Tominaga, Motoki ; Kojima, Hiroaki ; Yokota, Etsuo ; Orii, Hidefumi ; Nakamori, Rinna ; Katayama, Eisaku ; Anson, Michael ; Shimmen, Teruo ; Oiwa, Kazuhiro. / Higher plant myosin XI moves processively on actin with 35 nm steps at high velocity. In: EMBO Journal. 2003 ; Vol. 22, No. 6. pp. 1263-1272.
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