United in diversity: mechanosensitive ion channels in plants

Abstract

Mechanosensitive (MS) ion channels are a common mechanism for perceiving and responding to mechanical force. This class of mechanoreceptors is capable of transducing membrane tension directly into ion flux. In plant systems, MS ion channels have been proposed to play a wide array of roles, from the perception of touch and gravity to the osmotic homeostasis of intracellular organelles. Three families of plant MS ion channels have been identified: the MscS-like (MSL), Mid1-complementing activity (MCA), and two-pore potassium (TPK) families. Channels from these families vary widely in structure and function, localize to multiple cellular compartments, and conduct chloride, calcium, and/or potassium ions. However, they are still likely to represent only a fraction of the MS ion channel diversity in plant systems.

Keywords: MCA; MSL; MscS; TPK1; mechanotransduction.

Figure 1

Models for mechanosensitive (MS) ion channel gating. (a) The lipid-disordering model. MS ion channels force the membrane to distort to establish favorable interactions with the channel (top). Lateral membrane tension (arrows) increases bilayer energy as the membrane structure is further altered. The open conformation of the channel is then favored because it reduces lipid disordering through a lower-energy interface with the membrane (bottom). The level of lipid disordering is indicated by yellow shading, and the conformational changes of the channel relative to the membrane are emphasized by dashed lines. (b) The hydrophobic mismatch model. Membrane bilayers create favorable interactions between the polar lipid heads and polar residues of an embedded protein (top). Lateral membrane tension (arrows) results in a thinner bilayer, disrupting some of these favorable interactions (middle). The open conformation of the channel, which has a shorter channel profile within the membrane, restores these interactions (bottom). The increasing hydrophobicity of regions is shown as a gradient from very hydrophilic (red) to very hydrophobic (blue).

Figure 2

Phylogenetic relationships, subcellular localizations, and topologies of MscS-like (MSL) channels. (a) The inferred phylogeny of 43 members of the MscS superfamily, presented as an unrooted radial tree. Sequences were identified by Phytozome BLAST analysis (http://www.phytozome.net) or inclusion in previous analyses (15, 43, 67, 93, 94, 101, 118, 133). The MSL region of each protein was identified by InterProScan (57) and aligned using ClustalW (114) with a gap-opening penalty of 3.0 and a gap-extension penalty of 1.8. The evolutionary history was inferred using the neighbor-joining (105) method with a JTT distance matrix (56) using MEGA6 software (113). The reliability of the tree was determined via bootstrapping (n = 1,000 replicates) (35), and branches with bootstrap values of less than 50% were collapsed. The phylogenetic origin or cluster is indicated in the colored areas. The sequences used in this analysis and their UniProt accession numbers, Arabidopsis Information Resource (TAIR) accession numbers, or Phytozome accession numbers are as follows: Escherichia coli MscS (P0C0S1), YbdG (P0AAT4); Synechocystis sp. PCC6803 bCNGa (M1ME31); Helicobacter pylori MscS (E1Q2W1); Corynebacterium glutamicum MscCG (P42531); Thermoanaerobacter tengcongensis MscS (Q8R6L9); Toxoplasma gondii (B6KM08); Plasmodium falciparum (Q8IIS3); Dictyostelium discoideum (Q54ZV3); Schizosaccharomyces pombe MSY1 (O74839), MSY2 (O14050); Chlamydomonas reinhardtii MSC1 (A3KE12), MSC2 (A8HM43), MSC3 (A8HM47); Arabidopsis thaliana MSL1 (At4g00290), MSL2 (At5g10490), MSL3 (At1g58200), MSL8 (At2g17010), MSL9 (At5g19520), MSL10 (At5g12080); Populus trichocarpa (Pt002G105900, Pt004G178900); Zea mays (GRMZM2G125494, GRMZM2G028914, GRMZM2G005013); Oryza sativa (Os02g45690, Os04g48940, Os06g10410, Os02g44770); Brachypodium distachyon (Bradi1g15920, Bradi5g19160, Bradi3g51250); Vitis vinifera (Vv00015105001, Vv00026926001, Vv00002410001); Physcomitrella patens (Pp1s79_156, Pp1s314_12, Pp1s2_4320); Carica papaya (supercontig_55.26, supercontig _22.80, supercontig _126.38, supercontig_20.126). (b)Predicted topology and subcellular localization of representative MSLs from A. thaliana. Topologies were drawn according to predictions on Aramemnon (http://aramemnon.botanik.uni-koeln.de). The regions of highest homology to E. coli MscS found in groups I, II, and III are shown in red; the group II–specific C-terminal extension is shown in green; and the group III–specific N-terminal region is shown in blue.

Figure 3

Molecularly uncharacterized mechanosensitive (MS) ion channel activities identified in plant membranes. Plasma membrane–localized (panel a) and vacuole-localized (panel b) MS ion channels identified through patch-clamp electrophysiology and activated through increased membrane tension are presented and categorized by established ion permeability. Relevant references are indicated beneath each channel. Arrows indicate the ion permeability but do not specify the direction of ion flux in or out of the cell or vacuole.