Cellular transduction of mechanical oscillations in plants by the plasma-membrane mechanosensitive channel MSL10

Proc Natl Acad Sci U S A. 2021 Jan 5;118(1):e1919402118. doi: 10.1073/pnas.1919402118.

Abstract

Plants spend most of their life oscillating around 1-3 Hz due to the effect of the wind. Therefore, stems and foliage experience repetitive mechanical stresses through these passive movements. However, the mechanism of the cellular perception and transduction of such recurring mechanical signals remains an open question. Multimeric protein complexes forming mechanosensitive (MS) channels embedded in the membrane provide an efficient system to rapidly convert mechanical tension into an electrical signal. So far, studies have mostly focused on nonoscillatory stretching of these channels. Here, we show that the plasma-membrane MS channel MscS-LIKE 10 (MSL10) from the model plant Arabidopsis thaliana responds to pulsed membrane stretching with rapid activation and relaxation kinetics in the range of 1 s. Under sinusoidal membrane stretching MSL10 presents a greater activity than under static stimulation. We observed this amplification mostly in the range of 0.3-3 Hz. Above these frequencies the channel activity is very close to that under static conditions. With a localization in aerial organs naturally submitted to wind-driven oscillations, our results suggest that the MS channel MSL10, and by extension MS channels sharing similar properties, represents a molecular component allowing the perception of oscillatory mechanical stimulations by plants.

Keywords: frequency; mechanosensitive channel; mechanotransduction; oscillation; wind.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / metabolism
  • Arabidopsis Proteins / metabolism*
  • Arabidopsis Proteins / physiology
  • Cell Membrane / metabolism*
  • Cell Membrane / physiology
  • Ion Channels / metabolism
  • Ion Transport
  • Mechanoreceptors / metabolism
  • Mechanotransduction, Cellular / physiology*
  • Membrane Proteins / metabolism*
  • Membrane Proteins / physiology
  • Plants, Genetically Modified / metabolism
  • Signal Transduction

Substances

  • Arabidopsis Proteins
  • Ion Channels
  • MSL10 protein, Arabidopsis
  • Membrane Proteins