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

Authors :
Nathalie Leblanc-Fournier
Emmanuel de Langre
Jean-Marie Frachisse
Bruno Moulia
Tiffanie Girault
Marjorie Guichard
Sébastien Thomine
Daniel Tran
Jean-Marc Allain
Agroscope
Institut de Biologie Intégrative de la Cellule (I2BC)
Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)
Laboratoire de Physique et Physiologie Intégratives de l’Arbre en environnement Fluctuant (PIAF)
Université Clermont Auvergne [2017-2020] (UCA [2017-2020])-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Laboratoire d'hydrodynamique (LadHyX)
École polytechnique (X)-Centre National de la Recherche Scientifique (CNRS)
Mathematical and Mechanical Modeling with Data Interaction in Simulations for Medicine (M3DISIM)
Laboratoire de mécanique des solides (LMS)
École polytechnique (X)-Mines Paris - PSL (École nationale supérieure des mines de Paris)
Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre National de la Recherche Scientifique (CNRS)-École polytechnique (X)-Mines Paris - PSL (École nationale supérieure des mines de Paris)
Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre National de la Recherche Scientifique (CNRS)-Inria Saclay - Ile de France
Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)
ANR-09-BLAN-0245,Senzo(2009)
ANR-11-BSV7-0010,CAROLS,Canaux ioniques et espèces actives de l'oxygène dans le poil absorbant de légumineuse: rôle dans la symbiose avec Rhizobium(2011)
ANR-10-LABX-0040,SPS,Saclay Plant Sciences(2010)
Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Clermont Auvergne (UCA)
École polytechnique (X)-MINES ParisTech - École nationale supérieure des mines de Paris
Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre National de la Recherche Scientifique (CNRS)-École polytechnique (X)-MINES ParisTech - École nationale supérieure des mines de Paris
Source :
Proc Natl Acad Sci U S A, Proceedings of the National Academy of Sciences of the United States of America, Proceedings of the National Academy of Sciences of the United States of America, 2020, 118 (1), 7 p. ⟨10.1073/pnas.1919402118⟩, Proceedings of the National Academy of Sciences of the United States of America, National Academy of Sciences, 2021, 118 (1), 7 p. ⟨10.1073/pnas.1919402118⟩
Publication Year :
2020
Publisher :
National Academy of Sciences, 2020.

Abstract

International audience; 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.

Details

Language :
English
ISSN :
00278424 and 10916490
Database :
OpenAIRE
Journal :
Proc Natl Acad Sci U S A, Proceedings of the National Academy of Sciences of the United States of America, Proceedings of the National Academy of Sciences of the United States of America, 2020, 118 (1), 7 p. ⟨10.1073/pnas.1919402118⟩, Proceedings of the National Academy of Sciences of the United States of America, National Academy of Sciences, 2021, 118 (1), 7 p. ⟨10.1073/pnas.1919402118⟩
Accession number :
edsair.doi.dedup.....dec2f6ee2389015db281e16dc370b170