Two MscS Homologs Provide Mechanosensitive Channel Activities in the Arabidopsis Root

In bacterial and animal systems, mechanosensitive (MS) ion channels are thought to mediate the perception of pressure, touch, and sound [1Kung C. A possible unifying principle for mechanosensation.Nature. 2005; 436: 647-654Crossref PubMed Scopus (504) Google Scholar, 2Vogel V. Sheetz M. Local force and geometry sensing regulate cell functions.Nat. Rev. Mol. Cell Biol. 2006; 7: 265-275Crossref PubMed Scopus (1778) Google Scholar, 3Hamill O.P. Martinac B. Molecular basis of mechanotransduction in living cells.Physiol. Rev. 2001; 81: 685-740Crossref PubMed Scopus (921) Google Scholar]. Although plants respond to a wide variety of mechanical stimuli, and although many mechanosensitive channel activities have been characterized in plant membranes by the patch-clamp method, the molecular nature of mechanoperception in plant systems has remained elusive [4Haswell E.S. MscS-Like Proteins in Plants.in: Hamill O.P. Mechanosensitive Ion Channels, Part A. Volume 58. Academic Press, San Diego, CA2007Crossref Scopus (57) Google Scholar]. Likely candidates are relatives of MscS (Mechanosensitive channel of small conductance), a well-characterized MS channel that serves to protect E. coli from osmotic shock [5Levina N. Totemeyer S. Stokes N.R. Louis P. Jones M.A. Booth I.R. Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: Identification of genes required for MscS activity.EMBO J. 1999; 18: 1730-1737Crossref PubMed Scopus (551) Google Scholar]. Ten MscS-Like (MSL) proteins are found in the genome of the model flowering plant Arabidopsis thaliana [4Haswell E.S. MscS-Like Proteins in Plants.in: Hamill O.P. Mechanosensitive Ion Channels, Part A. Volume 58. Academic Press, San Diego, CA2007Crossref Scopus (57) Google Scholar, 6Pivetti C.D. Yen M.R. Miller S. Busch W. Tseng Y.H. Booth I.R. Saier Jr., M.H. Two families of mechanosensitive channel proteins.Microbiol. Mol. Biol. Rev. 2003; 67: 66-85Crossref PubMed Scopus (179) Google Scholar, 7Kloda A. Martinac B. Common evolutionary origins of mechanosensitive ion channels in Archaea, Bacteria and cell-walled Eukarya.Archaea. 2002; 1: 35-44Crossref PubMed Scopus (62) Google Scholar]. MSL2 and MSL3, along with MSC1, a MscS family member from green algae, are implicated in the control of organelle morphology [8Nakayama Y. Fujiu K. Sokabe M. Yoshimura K. Molecular and electrophysiological characterization of a mechanosensitive channel expressed in the chloroplasts of Chlamydomonas.Proc. Natl. Acad. Sci. USA. 2007; 104: 5883-5888Crossref PubMed Scopus (72) Google Scholar, 9Haswell E.S. Meyerowitz E.M. MscS-like proteins control plastid size and shape in Arabidopsis thaliana.Curr. Biol. 2006; 16: 1-11Abstract Full Text Full Text PDF PubMed Scopus (230) Google Scholar]. Here, we characterize MSL9 and MSL10, two MSL proteins found in the plasma membrane of root cells. We use a combined genetic and electrophysiological approach to show that MSL9 and MSL10, along with three other members of the MSL family, are required for MS channel activities detected in protoplasts derived from root cells. This is the first molecular identification and characterization of MS channels in plant membranes.