Mechanisms of cytosolic calcium elevation in plants: the role of ion channels, calcium extrusion systems and NADPH oxidase-mediated 'ROS-Ca2+ Hub'

Abstract

Elevation in the cytosolic free calcium is crucial for plant growth, development and adaptation. Calcium influx into plant cells is mediated by Ca2+ depolarisation-activated, hyperpolarisation-activated and voltage-independent Ca2+-permeable channels (DACCs, HACCs and VICCs respectively). These channels are encoded by the following gene families: (1) cyclic nucleotide-gated channels (CNGCs), (2) ionotropic glutamate receptors (GLRs), (3) annexins, (4) ‘mechanosensitive channels of small (MscS) conductance’-like channels (MSLs), (5) ‘mid1-complementing activity’ channels (MCAs), Piezo channels, and hyperosmolality-induced [Ca2+]cyt. channel 1 (OSCA1). Also, a ‘tandem-pore channel1’ (TPC1) catalyses Ca2+ efflux from the vacuole in response to the plasma membrane-mediated Ca2+ elevation. Recent experimental data demonstrated that Arabidopsis thaliana (L.) Heynh. CNGCs 2, 5–10, 14, 16 and 18, GLRs 1.2, 3.3, 3.4, 3.6 and 3.7, TPC1, ANNEXIN1, MSL9 and MSL10,MCA1 and MCA2, OSCA1, and some their homologues counterparts in other species, are responsible for Ca2+ currents and/or cytosolic Ca2+ elevation. Extrusion of Ca2+ from the cytosol is mediated by Ca2+-ATPases and Ca2+/H+ exchangers which were recently examined at the level of high resolution crystal structure. Calcium-activated NADPH oxidases and reactive oxygen species (ROS)-activated Ca2+ conductances form a self-amplifying ‘ROS-Ca2+hub’, enhancing and transducing Ca2+ and redox signals. The ROS-Ca2+ hub contributes to physiological reactions controlled by ROS and Ca2+, demonstrating synergism and unity of Ca2+ and ROS signalling mechanisms.

Calcium transport across plant membranes: mechanisms and functions

“…Their transmembrane topology and structural highlights are summarized in Fig. and Table and were recently comprehensively discussed by Demidchik & Shabala (). The heterologous expression studies (Table ) and in vivo electrophysiological tests (Table ) demonstrated that some of these genes do indeed encode Ca 2+ ‐permeable channels.…”

“…Membrane topology of Ca 2+ ‐permeable channel subunits (adapted from Demidchik & Shabala, , with modifications). NT and CT , N‐ and C‐terminal calmodulin‐binding sites (CaMBS), respectively; IQ , ‘isoleucine‐glutamine’ domain, which functions as calmodulin‐binding site; CNBD , cyclic nucleotide‐binding domain; P, pore domain; EF , EF ‐hand motif, which binds Ca 2+ ; ATD , amino terminal domain; LBD , ligand‐binding domain; OSCA 1 transmembrane domain (grey colour) could be a cleavable signal peptide.…”

“…This supports the self‐amplification mechanism, which increases the duration of both Ca 2+ and ROS signals and amplifies an initially weak signal into a dramatic O 2 •– ‐Ca 2+ increase (Demidchik et al ., , ). Hypothetically, this ‘ROS‐Ca 2+ hub’ can be stimulated by the CDF of CNGCs and phosphorylation of both the channels and NADPH oxidase (Demidchik & Shabala, ). Down‐regulation of the ROS‐Ca 2+ hub may involve the CDI of CNGCs (Ben‐Johny et al ., ; DeFalco et al ., ), induction of Ca 2+ ‐ATPase through Ca 2+ ‐CaM binding to CaMBS1 and CaMBS2 (Tidow et al ., ), suppression of Rac/Rop GTPases (Baxter‐Burrell et al ., ) and CDPK‐catalysed phosphorylation of ion channels (Zhou et al ., ) or BIK1‐catalysed phosphorylation of NADPH oxidase (Kadota et al ., ).…”

“…, referred to as a Ca 2+ signal. This signal is essential for decoding internal and external stimuli, transducing them into physiological and gene expression responses (Dodd et al ., ; Hedrich, ; Swarbreck et al ., ; Edel et al ., ; Demidchik & Shabala, ).…”

“…, referred to as a Ca 2+ signal. This signal is essential for decoding internal and external stimuli, transducing them into physiological and gene expression responses (Dodd et al, 2010;Hedrich, 2012;Swarbreck et al, 2013;Edel et al, 2017;Demidchik & Shabala, 2018). The chemical activity of Ca 2+ in the cytosol is maintained by living cells with amazing accuracy.…”