The bare necessities of plant K+ channel regulation

Abstract

Potassium (K+) channels serve a wide range of functions in plants from mineral nutrition and osmotic balance to turgor generation for cell expansion and guard cell aperture control. Plant K+ channels are members of the superfamily of voltage-dependent K+ channels, or Kv channels, that include the Shaker channels first identified in fruit flies (Drosophila melanogaster). Kv channels have been studied in depth over the past half-century and are the best-known of the voltage-dependent channels in plants. Like the Kv channels of animals, the plant Kv channels are regulated over timescales of milliseconds by conformational mechanisms that are commonly referred to as gating. Many aspects of gating are now well established, but these channels still hold some secrets, especially when it comes to the control of gating. How this control is achieved is especially important, as it holds substantial prospects for solutions to plant breeding with improved growth and water use efficiencies. Resolution of the structure for the KAT1 K+ channel, the first channel from plants to be crystallized, shows that many previous assumptions about how the channels function need now to be revisited. Here, I strip the plant Kv channels bare to understand how they work, how they are gated by voltage and, in some cases, by K+ itself, and how the gating of these channels can be regulated by the binding with other protein partners. Each of these features of plant Kv channels has important implications for plant physiology.

A charged existence: A century of transmembrane ion transport in plants

“…Similar characteristics show up in the few grass stomata that have been characterized ( Fairley-Grenot and Assmann 1992 ; Buchsenschutz et al 2005 ). Furthermore, we have a good understanding of the mechanics of their gating with voltage and its dependence on the conformation of the so-called voltage sensor domain ( Hoshi 1995 ; Blatt and Gradmann 1997 ; Marten and Hoshi 1997 ; Zei and Aldrich 1998 ; Eisenach et al 2014 ; Lefoulon et al 2018 ; Lefoulon 2021 ). This understanding is supported by the crystal structures ( Table 1 ) for KAT1 ( Clark et al 2020 ), the related AKT1 channel ( Dickinson et al 2022 ; Lu et al 2022 ) and the SKOR channel ( Li et al 2023 ) that is near sequence-identical with GORK.…”

“…For the interested reader, I recommend several excellent reviews that cover transport integration, voltage-dependent gating of channels and channel structure, and signaling in guard cells ( Lawson and Blatt 2014 ; Maurel et al 2015 ; Assmann and Jegla 2016 ; Jezek and Blatt 2017 ; Jegla et al 2018 ; Lefoulon 2021 ; Blatt et al 2022 ), Ca 2+ signaling ( Hetherington and Brownlee 2004 ; McAinsh and Pittman 2009 ; Roelfsema and Hedrich 2010 ), action potentials, transport, and signaling in Characean algae ( Thiel et al 1997 ; Shepherd et al 2002 ; Beilby and Al Khazaaly 2016 , 2017 ; Beilby et al 2022 ), the Venus flytrap ( Dionaea muscipula ) ( Sibaoka 1969 ; Hedrich et al 2016 ), pollen and root hairs ( Campanoni and Blatt 2007 ; Zonia and Munnik 2007 ), and systemic signaling in pathogenesis and herbivory ( Choi et al 2016 ; Johns et al 2021 ; Klejchova et al 2021 ). Readers interested in the conceptual approaches and methods of membrane transport research will find much detail in treatments of the all-important kinetics of transport and its interpretation [see Sanders (1990) and several useful chapters in Membrane Transport in Plants ( Blatt 2004 )], the practical guides Microelectrode Techniques ( Standen et al 1987 ) and Microelectrode Methods for Intracellular Recording and Electrophoresis ( Purves 1981 ), as well as the textbooks Ion Channels of Excitable Membranes ( Hille 2001 ) and Cellular Biophysics ( Weiss 1996 ).…”

Nanomaterial-induced modulation of hormonal pathways enhances plant cell growth

“…K serves as an important osmotic substance to regulate cell expansion. 42 Consequently, the acidification could activate the expansins, leading to cell wall loosening. 14 In accordance, the expression of EXP encoding the expansins was up-regulated at 2 and 12 h in the presence of nMnFe 2 O 4 , while a delayed (after 24 h) up-regulation of EXP was observed for N-CD exposure (Fig.…”

Structural and Functional Insights into the Role of Guard Cell Ion Channels in Abiotic Stress-Induced Stomatal Closure

“…Positively charged amino acids (lysine or arginine) are present at the fourth TM segment, which controls the shaker channel gating by voltage; the changes in TM electrical potential cause this segment to move within the membrane, resulting in conformational changes in the channel and consequently leading to the opening or closure of the channel pore. Shaker channels have a rather large C-terminus that contains multiple domains comprising a cyclic-nucleotide binding site in addition to an ankyrin repeat domain responsible for interaction with regulatory proteins, and an acidic (KHA) C-terminal end [11,[57][58][59][60][61].…”