Commandeering Channel Voltage Sensors for Secretion, Cell Turgor, and Volume Control

Abstract

Control of cell volume and osmolarity is central to cellular homeostasis in all eukaryotes. It lies at the heart of the century-old problem of how plants regulate turgor, mineral and water transport. Plants use strongly electrogenic H+-ATPases, and the substantial membrane voltages they foster, to drive solute accumulation and generate turgor pressure for cell expansion. Vesicle traffic adds membrane surface and contributes to wall remodelling as the cell grows. Although a balance between vesicle traffic and ion transport is essential for cell turgor and volume control, the mechanisms coordinating these processes have remained obscure. Recent discoveries have now uncovered interactions between conserved subsets of soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) proteins that drive the final steps in secretory vesicle traffic and ion channels that mediate in inorganic solute uptake. These findings establish the core of molecular links, previously unanticipated, that coordinate cellular homeostasis and cell expansion.

Gating control and K+ uptake by the KAT1 K+ channel leaveraged through membrane anchoring of the trafficking protein SYP121

“…Previous work showed that the SYP121 interacts with KAT1 and the closely related KC1 channel subunits in vitro (Honsbein et al, ; Honsbein et al, ), and binding with KC1 in roots was essential for channel mediated K + uptake in vivo and growth (Honsbein et al, ). These and additional studies isolated the binding motifs to the N‐terminal F 9 xRF motif of SYP121 and the RYxxWE motif immediately preceding the first transmembrane α‐helices of the K + channels (Grefen et al, ; Grefen, Chen, et al, ; Karnik et al, ). Although SNARE‐channel binding promotes vesicle traffic as well as channel‐mediated K + influx, how these two, physiologically distinct processes might be temporally coordinated has remained obscure.…”

“…Although we note some quantitative differences, the overall effect of SYP121 on the macroscopic KAT1 current is qualitatively similar. Like the KC1 channel, SYP121 action also depended on the conserved RYxxWE motif at the cytosolic face of the VSD (Grefen et al, ; Karnik et al, ), and mutation of Trp 62 in KAT1 was sufficient to eliminate the effects of SYP121 on KAT1 gating (Figure a). Heterologous function of the KC1‐AKT1 assembly requires CBL‐dependent kinase expression in oocytes (Honsbein et al, ).…”

“…A major action of the Qa-SNARE protein SYP121 is on the activity of K + channels already situated in the plasma membrane and independent of K + channel traffic (Karnik et al, 2017). Previous work showed that the SYP121 interacts with KAT1 and the closely related KC1 channel subunits in vitro (Honsbein et al, 2009;Honsbein et al, 2011), and binding with KC1 in roots was essential for channel mediated K + uptake in vivo and growth (Honsbein et al, 2009).…”

“…KAT1 and KC1, a close channel homolog, also bind directly and selectively with the plasma membrane protein SYP121 through a conserved RYxxWE motif located at the cytosolic surface of the VSD (Grefen et al, 2015;Honsbein, Blatt, & Grefen, 2011). SYP121 is one of two so-called Qa-SNAREs (Soluble NSF Attachment protein REceptor) proteins that facilitate accelerated vesicle traffic at the plasma membrane of Arabidopsis (Karnik et al, 2017). In general, SNAREs from target and vesicle membranes drive vesicle fusion and membrane intercalation by assembling in ternary complexes of cognate partner Qa-, Qb-, Qc-and R-SNAREs, designations defined by the respective residues at the core of the SNARE complex (Lipka, Kwon, & Panstruga, 2007).…”

VAMP721 Conformations Unmask an Extended Motif for K+ Channel Binding and Gating Control

“…SYP121 also binds with the K + channels KC1 and KAT1, altering channel gating to promote K + uptake and conferring a voltage dependence to secretory traffic for growth (Honsbein et al, 2009Grefen et al, 2010Grefen et al, , 2015. Binding with SYP121 has been shown to promote vesicle traffic with osmotic solute uptake, including that of K + , effectively coordinating the two processes and maintaining turgor as the cell expands (Karnik et al, 2017).…”