MscS-like Mechanosensitive Channels in Plants and Microbes

Abstract

The challenge of osmotic stress is something all living organisms must face as a result of environmental dynamics. Over the past three decades, innovative research and cooperation across disciplines has irrefutably established that cells utilize mechanically gated ion channels to release osmolytes and prevent cell lysis during hypoosmotic stress. Early electrophysiological analysis of the inner membrane of Escherichia coli identified the presence of three distinct mechanosensitive activities. The subsequent discoveries of the genes responsible for two of these activities, the mechanosensitive channels of large (MscL) and small (MscS) conductance, led to the identification of two diverse families of mechanosensitive channels. The latter of these two families, the MscS family, is made up of members from bacteria, archaea, fungi, and plants. Genetic and electrophysiological analysis of these family members has provided insight into how organisms use mechanosensitive channels for osmotic regulation in response to changing environmental and developmental circumstances. Furthermore, solving the crystal structure of E. coli MscS and several homologs in several conformational states has contributed to the understanding of the gating mechanisms of these channels. Here we summarize our current knowledge of MscS homologs from all three domains of life, and address their structure, proposed physiological functions, electrophysiological behaviors, and topological diversity.

Arabidopsis MSL10 Has a Regulated Cell Death Signaling Activity That Is Separable from Its Mechanosensitive Ion Channel Activity

“…As a result, we and others have previously speculated that the topological and domain diversity associated with MscS homologs indicates a multiplicity of functions and regulatory mechanisms and further proposed that MscS homologs might serve as membrane tension sensors with outputs independent of ion flux Wilson et al, 2013;Cox et al, 2014). Here, we present a structural and functional analysis of Arabidopsis MSL10 that supports these ideas.…”

“…Homologs of MscS are found in nearly all bacterial species (Pivetti et al, 2003;Lai et al, 2013;Martinac et al, 2013), protozoa (Prole and Taylor, 2013), archaea (Palmieri et al, 2009), some fungi (Nakayama et al, 2012), and all plant genomes so far analyzed (Wilson et al, 2013) but have not been identified in animals. The region of sequence similarity between MscS and other members of the MscS superfamily is restricted to a relatively small portion of the protein that includes the pore-lining helix of MscS and ;100 amino acids of the upper cytoplasmic domain (Kloda and Martinac, 2002;Pivetti et al, 2003;Balleza and Gómez-Lagunas, 2009;Haswell et al, 2011).…”

“…E. coli MscS is among the smallest members of its eponymous family of proteins, and deletion studies indicate that it contains little nonessential protein sequence (Miller et al, 2003b;Schumann et al, 2004). However, other MscS family members show substantial variation in size and topology, containing anywhere from 3 to 12 TM helices ) and a variety of domains not found in MscS, such as large cytoplasmic loops, N-or C-terminal extensions, extracellular domains, and ion or cyclic nucleotide binding motifs (Li et al, 2002(Li et al, , 2007Haswell et al, 2011;Malcolm and Maurer, 2012;Nakayama et al, 2012;Wilson et al, 2013).…”

Rapid hyperosmotic-induced Ca 2+ responses in Arabidopsis thaliana exhibit sensory potentiation and involvement of plastidial KEA transporters

“…No significant effects were observed in the higher-order mechanosensitive Ca 2+ channel root Mid1-complementing activity mca1;mca2 (AT4G35920, AT2G17780) double mutant (34,35) or the plasma membrane-targeted members of the mechano-sensitive channel of small conductance (MscS)-like family msl4,5,6,9,10 (AT1G53470, AT3G14810, AT1G78610, AT5G19520, AT5G12080) quintuple mutant ( Fig. S4) (36). Additionally, it has been shown previously that the tpc1 (AT4G03560) mutants in the vacuolar Ca 2+ -activated Ca 2+ -permeable SV channel do not affect the rapid osmotically induced increase in Ca 2+ but rather impair the ensuing root-to-shoot Ca 2+ wave (12).…”

Biophysical and Structural Studies of Escherichia coli Mechanosensitive Channel of Large Conductance in Lipid Bilayers

“…Although MscS is a non-specific channel, other members of this family are ligand-specific and some of them are hypothesised not to be channel proteins at all, which explains the plurality of MscS-like proteins in a species (Gibson et al, 2015;Wilson et al, 2013).…”