Petra Dietrich1, Wolfgang Moeder2, Keiko Yoshioka2,3€¦ · 23.06.2020 · In light of recent...

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TITLE: Plant Cyclic Nucleotide-Gated Channels: New Insights on their Functions and Regulation 1

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Petra Dietrich1, Wolfgang Moeder2, Keiko Yoshioka2,3 3

1. Molecular Plant Physiology, Friedrich-Alexander University Erlangen-Nuremberg, Staudtstrasse 5, 4

91058 Erlangen, Germany 5

2. Department of Cell and Systems Biology, University of Toronto, 25 Willcocks Street, Toronto, ON, M5S 6

3B2, Canada 7

3. Center for the Analysis of Genome Evolution and Function (CAGEF), University of Toronto, 25 Willcocks 8

Street, Toronto, ON, M5S 3B2, Canada 9

Orcid ID: PD 0000-0002-9209-8089; WM 0000-0003-3889-6183; KY 0000-0002-3797-4277 10

E-mail: [email protected], Fax: +1-416-978-5878, Tel: +1-416-978-3545 11

E-mail: [email protected], Fax: +49-9131-8528751, Tel: +49-9131-8525208 12

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Author for Contact: E-mail: [email protected], Fax: +1-416-978-5878, Tel: +1-416-978-3545 14

Short title: Update on CNGC Ca2+-permeable channels 15

One-sentence summary: 16

Recent advances of plant Cyclic Nucleotide-Gated Channels give new insight into their molecular functions 17

focusing on regulation, subunit assembly, and phosphorylation. 18

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Author Contributions: 20

P.D. and K.Y conceived the concept of the manuscript and P.D., W.M. and K.Y. wrote the manuscript and 21

generated Tables and Figures. 22

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Funding: 24

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This article was supported by a Discovery Grant from the Natural Science and Engineering Research Council of 26

Canada (grant no. PGPIN-2014-04114), Canadian Foundation for Innovation, and Ontario Research Fund to K.Y. 27

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Plant Physiology Preview. Published on June 23, 2020, as DOI:10.1104/pp.20.00425

Copyright 2020 by the American Society of Plant Biologists

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Introduction 29

Calcium (Ca2+) signaling is crucial for all aspects of plant physiology, including defense, abiotic stress 30

responses, and development; recent research has elucidated the role of plant cyclic nucleotide gated 31

channels (CNGCs) in Ca2+ signaling and downstream processes. CNGCs belong to the superfamily of voltage-32

gated ion channels. Like voltage-gated K+ channels, animal CNGCs, and hyperpolarization and cyclic 33

nucleotide-regulated (HCN) channels, plant CNGCs are tetrameric and have six transmembrane domains, 34

with a cytosolic N-terminal and C-terminal region per subunit (Jegla et al. 2018). The first plant CNGC 35

isoforms were identified as calmodulin (CaM)-binding proteins in 1998 (Schuurink et al., 1998; Köhler and 36

Neuhaus 1998); over the past five years, pioneering work has established CNGCs as Ca2+-permeable 37

channels involved in Ca2+ oscillations and possibly receptor-mediated signaling. 38

The spatio-temporal variation in cytosolic Ca2+ concentrations affects a wide range of cellular responses 39

(Webb et al. 1996). For example, Ca2+ flux across the plasma membrane is an early signaling step in 40

establishing symbiosis and immunity (Zipfel and Oldroyd 2017). Moreover, Ca2+ affects many 41

developmental processes: repetitive spiking or oscillations in cytosolic Ca2+ concentration entrain circadian 42

rhythms, underlie polar expansion of root hairs and pollen tubes, occur in response to the application of 43

auxin to elongating root cells, and control stomatal movements in response to CO2 and abscisic acid (Allen 44

et al. 2001; Felle 1988; Holdaway-Clarke et al. 1997; Love et al. 2004; McAinsh et al. 1995; Monshausen et 45

al. 2008). The production of Ca2+ oscillations requires positive and negative feedback regulation, and 46

theoretical modeling of Ca2+ oscillations in plants has been successfully applied to some model systems 47

(Martins et al. 2013; Liu et al., 2019). However, understanding Ca2+ dynamics on the molecular and 48

quantitative levels in plants has been hampered by lack of knowledge about the molecular nature and 49

regulation of the channels that allow Ca2+ entry. 50

In this Update, we summarize recent advances in physiological, biochemical, and electrophysiological 51

characterization of CNGCs, giving new insight into the molecular functions and regulation of plant CNGCs, 52

focusing on subunit assembly, phosphorylation, and calmodulin (CaM) binding. 53

ARE CNGCS “CYCLIC NUCLEOTIDE GATED” CHANNELS? 54

Progress in understanding the assembly, activation, and regulation of plant CNGCs has been slow. This 55

may be due in part to the pronounced differences to their animal counterparts: in contrast to early 56

assumptions that CNGCs were non-selectively permeable to cations (Talke et al. 2003), new research shows 57

that several CNGCs conduct Ca2+ but often do not allow K+ to cross. Table 1 summarizes our current 58

knowledge about the regulation by cyclic nucleotide monophosphates (cNMPs) and CaM of distinct CNGC 59

subunits expressed in heterologous expression systems, such as Xenopus oocytes and human embryonic 60

kidney (HEK) cells. 61



3

Controversial findings regarding the requirement of elevated cyclic adenosine monophosphate (cAMP) 62

or cyclic guanosine monophosphate (cGMP) levels indicate that our current assumptions about CNGC 63

gating may require major revision in the near future. As an example, Arabidopsis thaliana CNGC2 was 64

among the first cloned family members (Köhler and Neuhaus 1998). Initial electrophysiological 65

characterization in Xenopus oocytes suggested that CNGC2 is a voltage-dependent K+-permeable channel 66

activated by cAMP or cGMP(Leng et al. 1999; 2002 Table 1). In comparison, CNGC4, which together with 67

CNGC2 forms subgroup B of clade IV of Arabidopsis CNGCs (Mäser et al., 2000), was reported to encode a 68

voltage-independent cAMP- and cGMP-gated channel (Balagué et al. 2003). Recent work suggests that at 69

least in Xenopus oocytes, both channels work as a hyperpolarization-activated calcium-permeable channel 70

in a heteromeric assembly, without requirement for the elevation of cNMPs levels (Tian et al. 2019). 71

Similarly, patch-clamp recordings on plasma membranes of plant cell protoplasts have detected cNMP-72

dependent stimulation of hyperpolarization-activated Ca2+-permeable channels, and these could in some 73

cases be attributed to distinct CNGC isoforms, as in case of e.g. CNGC5 and CNGC6 in Arabidopsis guard 74

cells (Wang et al. 2013). However, depending on the expression system and experimental condition, there 75

seems to be no absolute requirement for the elevation of cNMP levels above the resting state (Table 1), 76

and cNMP affinities and binding dynamics have in most cases not been well studied. The usage of 77

genetically encoded reporters for cAMP or cGMP (Isner and Maathuis, 2013; Jiang et al., 2017) and precise 78

biochemical analysis may provide more definite answers regarding the physiological importance of cNMPs 79

to activate CNGCs in vivo. In light of recent advances towards the characterization of phosphorylation and 80

CaM binding as gating agents or modifiers, the regulation by cNMPs will have to be re-evaluated. cNMPs 81

might act only on a subset of CNGC subunits, they may act as a co-factor rather than a true trigger for 82

ligand-activation, or they may modify the voltage-dependence or affinities towards other regulators. In 83

addition, several recent reports showed that the universal calcium sensor protein CaM plays a more 84

complex and significant role in regulating CNGCs than previously thought (see below for details). Therefore, 85

despite the significant progress in recent years, the permeability, functional regulation, and nature of 86

ligands of plant CNGCs still need further studies. 87

REGULATION OF CNGC ACTIVATION AND TURNOVER BY PHOSPHORYLATION 88

In animals, phosphorylation is one way to regulate CNG and HCN channels (Kaupp and Seifert, 2002; 89

Herrmann et al., 2015). For example, the vertebrate CNGCs CNGA1 and CNGB2 function as hetero-90

tetrametric channels in rod photoreceptors and the phosphorylation status of tyrosine residues in these 91

channels controls their activity (Molokanova et al., 2003). Likewise, tyrosine phosphorylation alters the 92

gating of the HCN4 pacemaker channel (Li et al., 2008). Early pharmacological studies showed that protein 93

kinase inhibitors prevent the activity of hyperpolarization-dependent calcium channels in plant cells (Köhler 94

and Blatt 2002; Stoelzle et al., 2003), indicating that protein phosphorylation plays a critical role in stimulus-95

specific Ca2+ signaling. 96



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In recent years, regulation via direct phosphorylation by Ca2+-dependent protein kinases (CDPKs/CPKs), 97

has been documented for a number of plant ion channels, including the K+ channel KAT1, SLOW ANION 98

CHANNEL-ASSOCIATED 1 (SLAC1), and TWO-PORE CHANNEL 1 (TPC1 ) (Bender et al., 2018; Geiger et al., 99

2009; Ronzier et al., 2014, Maierhofer et al., 2014; Kintzer et al., 2016). In an extensive survey of CPK 100

substrates in Arabidopsis, Curran et al. (2011) identified CNGC6, CNGC7, CNGC9, and CNGC18 as potential 101

targets of CPK1, CPK10, or CPK34. So far, a specific CPK–CNGC interaction has only been shown for the 102

kinase domain of CPK32 and CNGC18 by yeast two-hybrid assays and Förster resonance energy transfer 103

(FRET) analysis (Table 2; Zhou et al., 2014). Co-expression of the constitutively active form of CPK32 in 104

Xenopus oocytes strongly enhanced CNGC18 channel activity, although actual phosphorylation was not 105

shown and the phosphorylation sites in CNGC18 were not identified (Zhou et al., 2014). Positive regulation 106

of CNGCs by CDPKs opens the possibility that an initial Ca2+ influx may precede activation of CNGCs by 107

CDPKs. In this scenario, CNGCs may amplify or modify a Ca2+ response initiated by a different channel or 108

from an internal calcium store, since some CDPK activation requires elevated Ca2+concentration. So far, 109

negative regulation of CNGC activity by CDPKs has not been reported but is possible. In any case, this 110

notion supports the idea that CNGCs are part of larger protein complexes that include other channels, 111

pumps, and decoders such as CDPKs, or are localized in proximity to these players. This notion is discussed 112

in detail later in this article (Figure 1) 113

Considering the plasma membrane localization of most plant CNGCs, receptor kinases or receptor-like 114

kinases (RLKs) are likely candidates for the kinases that phosphorylate CNGCs. Indeed, Ladwig et al. (2015) 115

reported that CNGC17 binds to the Arabidopsis H+-ATPases (AHA), AHA1 and AHA2, as well as to 116

BRASSINOSTEROID INSENSITIVE1-ASSOCIATED RECEPTOR KINASE 1 (BAK1). BAK1 is a leucine-rich repeat 117

RLK (LRR-RLK), which can associate with various pattern recognition receptors (PRRs) as a co-receptor, 118

forming functional receptor complexes that regulate a wide variety of physiological responses from growth 119

to immunity (Kim and Wang, 2010; Liang and Zhou 2018; Ranf 2017). The growth-regulating phytosulfokine 120

(PSK) receptor PSKR1, another LRR-RLK superfamily member, also binds to AHA1, AHA2, and BAK1, 121

suggesting that CNGC17, PSKR1, BAK1, and AHAs may form a protein nanocluster to initiate downstream 122

signals (Ladwig et al., 2015, Figure 1). In addition, these interaction data suggest that BAK1 or other LRR-123

RLKs phosphorylate plant CNGCs. 124

In 2019, three studies revealed that LRR-RLKs and related kinases phosphorylate CNGCs, and examined 125

the physiological relevance of this phosphorylation (Yu et al., 2019; Tian et al. 2019; Wang et al., 2019): 126

Tian et al. (2019) reported the relevance of CNGC phosphorylation in the recognition of 127

pathogen/microbe associated molecular patterns (PAMPs/MAMPs) in Arabidopsis. An increase of the 128

cytosolic Ca2+ concentration ([Ca2+]cyt) is essential for the oxidative burst after recognition of 129

PAMPs/MAMPs such as the bacterial elicitor peptide flagellin22 (flg22) or fungal chitin (Kadota et al.2015; 130

Seybold et al. 2014). Upon flg22 recognition by the PRR kinase FLAGELLIN SENSING 2 (FLS2), a receptor 131



5

complex consisting of FLS2, BAK1, and BOTRYTIS-INDUCED KINASE1 (BIK1) forms, leading to trans-132

phosphorylation of these kinases and release of BIK1, which activates downstream signaling (Couto and 133

Zipfel, 2016). A well-studied downstream target of BIK1 is the membrane-localized nicotinamide adenine 134

dinucleotide phosphate oxidase (NADPH) oxidase, RESPIRATORY BURST OXIDASE HOMOLOG D (RbohD), 135

which is responsible for the oxidative burst during PAMP-triggered immunity (PTI) (Kadota et al., 2015; Li et 136

al., 2014). Tian et al. (2019) reported that CNGC4, but not CNGC2, also interacts with BIK1, and is 137

phosphorylated at the C-terminal cytosolic domain upon flg22 recognition via FLS2 (Figure 1). BIK1 is a 138

cytoplasmic kinase that is a central component of PRR complexes with components such as FLS2, EF-TU 139

RECEPTOR (EFR), PERCEPTION OF THE ARABIDOPSIS DANGER SIGNAL PEPTIDES (PEPRs), and CHITIN 140

ELICITOR RECEPTOR KINASE 1 (CERK1) (Couto and Zipfel, 2016). CNGC2 and CNGC4 interact and form a 141

functional heteromeric channel, which is inhibited in the presence of CaM (Chin et al., 2013; Tian et al., 142

2019). BIK1 can activate this CNGC2-CNGC4 heteromeric channel in the presence of the inhibitory CaM, 143

possibly via phosphorylation of CNGC4, and was therefore suggested to induce CNGC2-CNGC4-mediated 144

Ca2+ influx in response to PAMP recognition. Tian et al. (2019) showed CNGC2 (also known as DEFENSE NO 145

DEATH1, DND1) and CNGC4 (also known as DND2/HYPERSENSITIVE RESPONSE-LIKE LESION MIMIC1, HLM1) 146

are positive regulators of PTI only under specific calcium concentrations (i.e. 1.5 mM [Ca2+]ext), as their null 147

mutants showed reduced PTI under this condition, but behaved like wild-type under lower calcium 148

concentrations (i.e. 0.1 mM [Ca2+]ext). They reported that sufficient [Ca2+]ext is essential to activate calcium-149

dependent PTI. However, both cngc2 and cngc4 single null mutants are hyper-sensitive to calcium and have 150

pleiotropic phenotypes (Chan et al., 2003; Yu et al., 1998; Clough et al., 2000; Wang et al., 2017). 151

Furthermore, cngc2 (dnd1) mutants experience Ca2+ stress under normal Ca2+ levels (Chan et al., 2008), 152

raising the possibility that they cannot respond normally to many triggers, including PAMPs. Therefore, 153

future studies should clarify which channels mediate the Ca2+ response under low Ca2+ supply in cngc2 154

(dnd1) mutants and whether the compromised PTI in these mutants is a result or independent of other 155

pleiotropic phenotypes. 156

In another recent study, Wang et al. (2019) examined the role of CNGC phosphorylation in rice PTI and 157

programmed cell death (PCD). The null mutants for CNGC2 (dnd1) and CNGC4 (dnd2/hlm1) show complex 158

and contradictory phenotypes such as autoimmune phenotypes with constitutive elevation of salicylic acid 159

levels and expression of pathogenesis-related (PR) genes, but reduced PCD in the hypersensitive response 160

(HR) (Yu et al., 1998; Clough et al., 2000; Moeder et al., 2011). In the absence of pathogens, Arabidopsis 161

cngc2 and cngc4 mutants also show conditional spontaneous lesions. A very similar lesion mimic phenotype 162

was observed for the barley null mutant of CNGC4, necrotic leaf spot (nec1) (Rostoks et al., 2006), and the 163

rice (Oryza sativa) mutant, cell death and susceptible 1 (cds1), which lacks a functional OsCNGC9 gene 164

(Wang et al., 2019). The rice cds1 mutant shows impaired blast fungus resistance and reduced calcium 165

influx, oxidative burst, and PTI-related gene expression, indicating that OsCNGC9 has a significant role in PTI 166

(Wang et al., 2019). Furthermore, the rice receptor-like cytoplasmic kinase (RLCK) OsRLCK185 physically 167



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interacts with and phosphorylates OsCNGC9 and this phosphorylation activates channel function (Wang et 168

al., 2019; Table 1, 2). OsRLCK185 and OsRLCK176 interact with the chitin receptor OsCERK1 (Miya et al., 169

2007). Therefore, CNGCs represent a common downstream target of phosphorylation during PTI. Since the 170

closest Arabidopsis homolog of OsCNGC9 is CNGC14, which has been associated with Ca2+ entry during 171

auxin-regulated growth (Brost et al., 2019; Dindas et al., 2018; Shih et al., 2015; Zhang et al., 2017), and not 172

CNGC2 or 4, it will be interesting to investigate the functional diversification of CNGCs in different plant 173

species. 174

In the third new study from 2019, Yu et al. (2019) used a suppressor screen to identify an Arabidopsis 175

CNGC as a key player in the mediation of cellular homeostasis , which is regulated by BAK1 and its closest 176

homologue, SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE 4 (SERK4). Like CNGC2 and CNGC4, the two 177

closely related group I channels CNGC11 and CNGC12 have been implicated in immunity and PCD (Yoshioka 178

et al., 2006, Moeder et al., 2011). Likewise, a role in immunity, wound signaling, and insect resistance has 179

been proposed for CNGC19 and CNGC20, which comprise sub-clade IV A in the CNGC family (Moeder et al, 180

2011; Meena et al., 2019). BAK1 and SERK4 are involved in a wide variety of physiological phenomena and 181

the bak1-4 serk4-1 double mutant develops severe postembryonic lethality due to hyper-activation of PCD 182

(He et al., 2007; de Oliveira et al., 2016). Yu et al. (2019) conducted a non-biased suppressor screen of cell 183

death in RNA interference-BAK1/SERK4-silenced plants and found that a knockout mutant of CNGC20 184

suppressed this cell death phenotype. Furthermore, they showed that BAK1 phosphorylates the C-terminal 185

cytosolic domain of CNGC20 (Table 2). These sites are conserved in CNGC19, which can also be 186

phosphorylated by BAK1. This breakthrough study revealed a novel mechanism of CNGC regulation in which 187

phosphorylation of the C-terminus regulates CNGC19 and CNGC20 protein stability. According to their 188

model, CNGC19 and CNGC20 form a hetero-tetrameric channel that positively regulates cell death, and 189

BAK1/SERK4 phosphorylation accelerate CNGC19/20 turnover to maintain cellular homeostasis (Figure 1). 190

These three recent studies showed that phosphorylation of CNGCs plays key roles in their regulation 191

(Table 1). One important question will be whether phosphorylation itself activates/inactivates the channel 192

or whether a conformational change will alter the accessibility or sensitivity for cNMPs or CaM. Further 193

investigation of other CNGCs may identify common patterns and will tell us whether each CNGC subunit 194

undergoes unique regulation of either activity or turnover by phosphorylation. 195

CNGC GATING BY THE CALCIUM-SENSOR PROTEIN CALMODULIN AND ITS ROLE IN SHAPING CALCIUM 196

OSCILLATIONS. 197

The partial overlap of cNMP-binding domains and the CaM binding site suggested that these signaling 198

compounds competitively regulate CNGCs (Arazi et al., 2000; Kaplan et al., 2007; Hua et al. 2003a). 199

However, a second CaM-binding domain adjacent to the cNMP-binding domain, which is formed by an 200

isoleucine-glutamine (IQ) motif and is conserved among CNGCs (Fischer et al., 2013), challenged this model. 201



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Moreover, additional CaM binding sites were mapped within the N-terminal cytosolic domain and distal of 202

the IQ-domain, and both positive and negative regulation of CNGCs by CaM was shown for CNGC12 (Figure 203

2; Chin et al. 2010; DeFalco et al., 2016). The finding that the IQ motif binds CaM in a Ca2+-independent 204

manner and is required for channel function paved the way for revisiting the gating mechanisms of CNGCs, 205

since CaM could serve as a built-in subunit that senses local changes in Ca2+ concentration upon channel 206

opening, and induces rapid, Ca2+-dependent feedback regulation (DeFalco et al., 2016; Fischer et al., 2017; 207

Demidchik et al., 2018). However, additional data is required, especially about the role of cNMPs and their 208

possible interplay with CaM, in order to gain a better understanding of the gating mechanisms of CNGCs. 209

Negative regulation by calmodulin binding 210

In Xenopus oocytes, CaM binding to the C-terminus of CNGC14 and to the CNGC2/CNGC4 complex 211

inhibits ion channel function (Tian et al., 2019; Zeb et al., 2019). Unfortunately, it is not clear which CaM 212

binding site is involved and whether this inhibition required an elevation of [Ca2+]cyt. Interestingly, in both of 213

the abovementioned studies, CaM7 functioned as a negative regulator (Figure 2) and CaM7, but not CaM2, 214

specifically inhibited currents through CNGC14 (Zeb et al., 2019). The mechanism by which CaMs exert their 215

isoform-specific regulation remains unclear, since all Arabidopsis CaM isoforms interacted with the C-216

terminus of CNGC14 and CNGC6 in yeast two-hybrid assays (Fischer et al., 2017). 217

The CaM2.1 and CaM7.1 isoforms have identical protein sequences except for one conserved K to R 218

change, while the CaM2.2 splice variant used by Zeb et al. (2019) contains 12 additional residues. CaM is 219

highly conserved across kingdoms, which poses questions about the expression levels and physiological 220

relevance of the extended splice variant described by Zeb et al. (2019). If the negative regulation of CNGCs 221

depends on Ca2+-loading of the respective CaM, this will assist in shaping the Ca2+ signature in vivo. In the 222

case of CNGC14, this will relate to Ca2+ oscillations in root hairs and auxin-dependent growth (Shih et al., 223

2015; Dindas et al., 2018; Brost et al., 2019). 224

In vivo, Ca2+-dependent binding of CaM to the N-terminal (NT) binding site of CNGC12 negatively 225

regulates its channel activity (DeFalco et al., 2016). Ectopic expression of CNGC12 with a mutated NT 226

domain, which cannot bind Ca2+-CaM, constitutively induced PCD, similar to the phenotype produced by a 227

constitutively active channel. Therefore, CaM may regulate channel activity via binding to the NT and C-228

terminal (CT) domains. As channel activity is dependent on heteromeric subunit assembly (Pan et al., 2019; 229

Tian et al., 2019), one urgent task in Ca2+ signaling research is determining the stoichiometry of natural 230

channel assemblies, including their associated CaM subunit(s). 231

Positive regulation by calmodulin binding 232

CNGC12 contains three CaM-binding sites: the NT-domain and the CT domain (which interact with Ca2+-233

CaM), and the IQ domain (which associates with apo-CaM) (DeFalco et al., 2016). A mutation in a C-234



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terminal motif that had been shown to be crucial for CaM binding (Arazi et al., 2000) resulted in a loss-of-235

function of CNGC12, indicating CaM binding to this site positively regulates CNGC function (Chin et al., 236

2010; Abdel-Hamid et al, 2010). Mutation of the core IQ sequence to DA disrupts the interaction with CaM 237

and channel function. When CNGC11/12, a chimeric channel composed of the N-terminal half of CNGC11 238

and the C-terminal half of CNGC12, is expressed in Nicotiana benthamiana leaves, PCD is induced by 239

constitutively activated Ca2+ flux (Yoshioka et al., 2006, Moeder et al., 2019). By contrast, expression of the 240

CNGC11/12DA mutant does not induce PCD (DeFalco et al., 2016). If only the Ca2+-dependent interaction of 241

CaM with the CNGC12 IQ domain was disrupted, channel function could be partially retained, suggesting 242

that the IQ domain–calcium free CaM (apo-CaM) complex supports channel function (Fischer et al., 2017). 243

This conclusion was further substantiated by heterologous expression of CNGC11 and CNGC12 in Xenopus 244

oocytes. CNGC12-mediated hyperpolarization-dependent Ca2+ currents were enhanced by about three-fold 245

upon co-expression with CaM1 or apo-CaM1, which was kept in the apo state by mutating all four Ca2+-246

binding sites (Zhang et al., 2019). In comparison, CNGC11 was inactive as a channel in Xenopus oocytes, 247

both in the presence and absence of CaM (Zhang et al., 2019). Only CaM1, which is identical to CaM4, was 248

able to activate CNGC12 in Xenopus oocytes, but CaM6 was not (Zhang et al., 2019). This again points to 249

isoform-specific CaM functions, despite the ability of CaM2 and CaM6 to bind to the C-terminus as well as 250

to the isolated IQ domain of CNGC12 in yeast (Fischer et al., 2017). The CaM1 and CaM6 protein sequences 251

(protein models CaM1.1 and CaM6.1) differ in 5 positions with conserved exchanges (E/D; K/R; T/S; I/V); 252

this led us to question how such subtle differences in protein sequence produce the observed functional 253

differences. 254

Furthermore, interaction of apo-CaM to CNGCs suggest the concept that CaM may function as a built-in 255

Ca2+ sensor of CNGCs. CaM has two lobes (C and N) with two EF-hands each connected by a flexible linker. 256

Both lobes bind Ca2+ with different affinities, which contributes to the ability of CaM to regulate many 257

target proteins (Villarroel et al., 2014). Apo-CaM can interact with the IQ domain of CNGCs via its C-lobe, 258

indicating that apo-CaM attaches to CNGCs in the resting state and plays a role as a Ca2+-sensing subunit for 259

the channel complex (Fischer et al., 2017). Indeed, apo-CaM association is required for Ca2+ sensing and for 260

channel opening, at least in some channels such as CNGC12 (DeFalco et al., 2016; Fischer et al., 2017; Zhang 261

et al., 2019) and CNGC8/CNGC18 heteromers (Figure 2; Pan et al., 2019), where the channel–CaM complex 262

may support sustained Ca2+ oscillations during pollen tube growth. As both proximal and distal regions of 263

the core IQ motif play critical roles in CaM accommodation (Fischer et al., 2017), the observation that some 264

CNGCs are activated by CaM (probably by binding of apo-CaM to their IQ domain), while others are not, 265

poses new questions about the complexity of the interaction of CaM with different CNGC subunits and 266

heteromeric CNGC complexes (Figure 2). Therefore, more quantitative and dynamic analyses of CaM 267

isoform-specific interactions with CNGCs are required to improve our understanding of any CaM-induced 268

gating mechanism. 269



9

Role in shaping Ca2+ oscillations 270

Many recent publications have shed light on the role of CNGCs as central elements of plant Ca2+ 271

oscillators. This is not unexpected because their intrinsic CaM-binding properties make CNGCs function as 272

Ca2+-feedback regulated elements (Figure 2). 273

In pollen tubes, CNGC18 is essential for guidance and tip growth (Frietsch et al., 2007; Gao et al., 2016), 274

while CNGC7 and CNGC8 have partially redundant functions in controlling pollen tube growth (Tunc-275

Ozdemir et al. 2013). In different heterologous expression systems, CNGC18 mediates hyperpolarization-276

activated calcium currents, but the regulation of channel activities appears to be complex (Table 1). In 277

HEK293T cells, addition of cAMP and cGMP activated CNGC7, CNGC8, and CNGC18 to produce inward 278

calcium currents at hyperpolarized potentials (Gao et al., 2016). In another report, CNGC18 expressed in 279

Xenopus oocytes could be activated by co-expression of a constitutively active form of the Ca2+-dependent 280

protein kinase CPK32 (Zhou et al., 2014). The authors therefore suggested that Ca2+-dependent feed-281

forward stimulation of calcium entry occurs via CPK32 during Ca2+ oscillations in growing pollen tubes (Zhou 282

et al., 2014). In later experiments, CNGC18 was highly active in Xenopus oocytes in the absence of plant 283

kinases and without addition of membrane-permeable cyclic nucleotides (Pan et al., 2019), leaving us to 284

question the impact of CNGC18 regulation by CPK32 and cyclic nucleotides in pollen tubes. 285

A recent study presented a novel mechanism for regulation by heteromeric channel assembly and CaM 286

in the absence of elevated levels of cyclic nucleotides (Table 1; Pan et al., 2019). In Xenopus oocytes, 287

CNGC18 currents were inhibited by co-expression of CNGC7 or CNGC8, and this inhibition was relieved in 288

the presence of CaM2. By contrast, CNGC7 and CNGC8 produced non-functioning homomeric channels in 289

the presence and absence of CaM2. Biochemical studies revealed that the CNGC C-termini interacted with 290

each other and with apo-CaM2 or Ca2+-CaM2. Ca2+ loading of CaM2 lowered the affinity for the CNGC8 and 291

CNGC18 C-termini from 50 nM to >800 nM, suggesting that Ca2+ induced the dissociation of CaM2 from the 292

heteromeric channel complex, which leads to channel inactivation. In this scenario, the heteromeric 293

CNGC18–CNGC8 complex would be active at low [Ca2+]cyt, when apo-CaM is associated, but a rise in [Ca2+]cyt 294

would trigger CaM release and channel closure. Pan et al. (2019) thus suggest a new model in which the 295

dissociation of Ca2+-CaM2 induces inhibition of the channel complex (Figure 2). 296

This type of Ca2+ feedback regulation perfectly meets the theoretical expectations for the situation in 297

growing pollen tubes. However, no oscillatory calcium current (or free-running membrane potential) was 298

measured in oocytes, where the ‘oscillator’ had been reconstituted. Despite the presence of high 299

extracellular Ca2+ concentrations of 30 mM, current amplitudes in the presence of CaM2 with nonfunctional 300

EF-hands (CaM21234) were only about 20% higher than those with Ca2+-sensitive CaM2. The study by Pan et 301

al. (2019) provides new and essential data for future modeling of the Ca2+ oscillator, if the suggested 302



10

mechanism can be validated in vivo. Modeling of Ca2+ oscillations could then also integrate knowledge 303

about feedback-control by membrane voltage, as well as on and off rates of CaM binding. 304

Loss of CNGC14 causes root hair defects, including swelling and branching, as well as bursting of the root 305

hair tip (Zhang et al., 2017; Brost et al., 2019), indicating its role in the regulation of cell integrity during 306

polar growth. CNGC5, CNGC6, and CNGC9 also contribute to the robustness of unidirectional cell expansion 307

and stability of cytosolic Ca2+ oscillations (Brost et al., 2019; Tan et al., 2020). Loss of CNGC14 had the 308

strongest effect by destabilizing the calcium oscillations and inducing growth defects. The typical Ca2+ 309

oscillation period of about 30 s found in wild-type root hairs was not established in the cngc14 cngc6 and 310

cngc14 cngc9 double mutants (Brost et al., 2019). However, this period was still present in cngc6 cngc9 311

double mutants and cngc9 single mutants, although with much less robustness, identifying CNGC14 as the 312

major pacemaker in vivo. Finally, under the experimental conditions used, the cngc6 cngc9 cngc14 triple 313

mutants initiated root hair bulges, which rapidly burst after transition to the rapid growth phase. In another 314

study, growth defects of the cngc5 cngc6 cngc9 triple mutant could be complemented by overexpression of 315

each of the CNGC subunits, indicating similar functions of these channels (Tan et al., 2020). Similar to the 316

results for CNGC14, heterologous expression of CNGC5, CNGC6, or CNGC9 induced hyperpolarization-317

activated Ca2+ currents in HEK293T cells, although the role of cyclic nucleotides required for channel 318

activation differs between individual studies (Table 1; Gao et al., 2016; Tan et al., 2020). In addition to 319

cytosolic Ca2+ oscillations, the participation of CNGCs in nuclear Ca2+ oscillations has also been reported 320

(Leitão et al. 2019; Charpentier et al. 2016). CNGC15 homologs from Medicago and Arabidopsis are the only 321

CNGCs so far that are localized to the nuclear envelope, where they participate in nuclear Ca2+ oscillations, 322

which are crucial for root growth and symbiosis establishment (Charpentier et al., 2016, Leitão et al., 2019). 323

CNGC HETERO-TETRAMERIZATION AND LOCALIZATION TO MEMBRANE NANODOMAINS 324

Ca2+ signals participate in many physiological responses; therefore, one important question is how 325

specific stimuli generate unique signals to maintain signaling specificity. The rates of Ca2+ entry and export, 326

Ca2+ buffering and binding to target proteins, and the respective reaction volumes determine the shape of 327

the ‘Ca2+ signature’ (Clapham, 2007; McAinsh and Pittman, 2009). Hetero-tetramerization of plant CNGCs 328

thus provides a versatile tool to generate unique patterns of Ca2+ signatures. Based on the examples 329

described above, it is reasonable to hypothesize that each subunit has a unique mode of regulation by 330

phosphorylation and CaM binding, but also a certain degree of functional redundancy. 331

The Arabidopsis CNGC family has 20 members subdivided into 5 groups (Mäser et al., 2001). Some 332

species have fewer family members, such as maize (Zea mays, 12 CNGCs) or castor bean (Ricinus communis, 333

11 CNGCs), but other species have many different channel subunits, such as soybean (Glycine max, 35 334

CNGCs) or apple (Malus domestica, 44 CNGCs), according to the presence of a family-specific sequence 335

motif (Saand et al., 2015). Hetero-tetramerization or subunit interactions have been observed or suggested 336



11

for CNGC2–CNGC4, CNGC7/CNGC8–CNGC18, CNGC19–CNGC20, CNGC6-9, CNGC6–CNGC14, and CNGC9–337

CNGC14 (Chin et al., 2013; Tian et al., 2019; Pan et al., 2019; Brost et al., 2019). Pan et al. (2019) reported 338

an intriguing inhibitory effect of CNGC7 or CNGC8 on CNGC18 heteromeric channel function, indicating that 339

some CNGC members may inhibit or modify the activity of their respective heteromeric channel complexes 340

(Table 2, Figure 2). This observation indicates that the composition of hetero-tetramers has a substantial 341

influence on channel function and regulation, thus determining their physiological function. 342

Another possible mechanism for creating unique Ca2+ signatures is the formation of protein complexes 343

at the plasma membrane acting as specific sensing modules (Figure 1). This idea is supported by the 344

observation of interactions of CNGCs with receptor kinases and other membrane-localized proteins as 345

discussed above (Ladwig et al., 2015; Yu et al., 2019, Wang et al., 2019, Meng et al., 2020; Table 2). 346

Following the membrane raft hypothesis proposed by Simons and Ikonen (1997), sub-347

compartmentalization of plasma membrane proteins in nanodomains or microdomains may produce 348

signaling hubs that give specificity in plant signaling (Keinath et al., 2010, Demir et al., 2013, Jaillais and Ott, 349

2020). For example, the FLS2 co-receptor BAK1 is also a co-receptor of the major brassinosteroid (BR) 350

receptor BRI1. Upon sensing BR, BRI1 forms an active receptor complex with BAK1, thereby initiating BR 351

signaling (Kim and Wang, 2010). Interestingly, Wang et al. (2015) showed that BRI1 localizes to membrane 352

nanodomains and that this partitioning of BRI1 is essential for proper BR signal transduction. Furthermore, 353

Bücherl et al. (2017) showed that FLS2 and BRI1 localize to distinct plasma membrane nanodomains and 354

such spatiotemporal separation of two receptor kinases could contribute to their signaling specificity in 355

immunity and growth regulation. Thus, it is plausible to hypothesize that CNGC hetero-tetrametric channels 356

are parts of sensing complexes, together with specific receptors and downstream decoder proteins, to 357

create specific downstream outputs (Figure 1). 358

CONCLUDING REMARKS 359

As discussed above, recent studies have substantially enriched the field of CNGC research (see Advances 360

Box). As expected, these new data and concepts raise further questions for deepening our understanding of 361

this channel group and its role in plant calcium signaling (see Outstanding Questions). 362

The interaction of CNGCs with receptor-like kinases and other membrane-localized proteins, as recently 363

reported for Mildew Locus O (MLO) proteins (Meng et al., 2020), would allow specific CNGCs together with 364

CaMs to be part of different nanodomains associated with their respective receptors. These membrane 365

domains may include decoder proteins such as CPKs. The exploration of how such ‘channelosomes’ 366

generate stimulus-specific Ca2+ signatures that are decoded instantly by the attached decoder proteins will 367

be an exciting future direction for CNGC research (Figure 1). Structural modeling using solved animal 368

CNGC/HCN structures has improved our understanding (Hua et al., 2003b; Baxter et al., 2008; Niu et al., 369

2019) but cannot accurately predict the structure of the important C-terminal CaM binding domains. 370



12

Therefore, resolving high-resolution structures of plant CNGCs will help our understanding of their gating 371

and regulation mechanisms. 372

The first CNGC family member was identified in 1998 in a screen for CaM binding targets in a cDNA 373

library from barley aleurone cells, and this CNGC was therefore named Hordeum vulgare Calmodulin 374

Binding Transporter 1, HvCBT1 (Schuurink et al., 1998). Around the same time, two Arabidopsis genes 375

homologous to animal CNGCs were identified and named CNGC1 and CNGC2 (Köhler and Neuhaus, 1998). 376

The CNGC nomenclature was adopted for future family members, following the suggestion of Mäser et al. 377

(2001). Indeed, within the presumed C-terminus of each channel, a cyclic nucleotide-binding domain 378

represents the most conserved sequence. Despite this clear domain classification, binding affinities of 379

cAMP or cGMP to this site have not been measured, and the exact role of these nucleotides, both for 380

channel opening and for physiological functions, is still unclear. Furthermore, there is a fierce, ongoing 381

debate about the production of cNMP in plants (Qi et al., 2010; Ashton et al., 2011). In light of recent 382

advances in understanding CNGC assembly, function, and regulation by CaM, it is time to conduct more 383

quantitative analyses by using (genetically encoded) reporters for cNMPs, as well as biochemical methods, 384

single-channel recordings, and structural approaches to assess (CaM and cNMP) ligand affinities, gating 385

behavior, and composition of membrane domains containing CNGCs. These analyses will provide us with a 386

better understanding of the role of cNMPc for CNGC regulation. 387

In this update, we summarized exciting new findings on the molecular functions of plant CNGCs and 388

discussed their significance. With this remarkable progress, we are entering a new era of research on 389

CNGCs and calcium signaling, and we anticipate that more advances in this research field will emerge in the 390

near future. 391

392

393

394

Figure Legends 395

Figure 1. Model of a CNGC-containing signal complex (nanodomain/channelosome, shown in darker grey). 396

A heterotetrametric CNGC channel is part of a sensing receptor complex containing pattern recognition 397

receptors (PRRs), their clients (e.g. BIK1, RBOHD, RLCK), various pumps (e.g. proton ATPase and Ca2+ pumps), 398

and decoders (e.g. CPKs and CaM). The formation of such a signal complex can be permanent or temporal 399

upon recognition of specific stimuli (transient signalling complex) and the combination of specific players can 400

contribute to generate precise spatiotemporal Ca2+ signals. Recruitment of CNGCs in a specific signaling 401

complex may be achieved by MLO proteins. Phosphorylation plays significant roles to activate CNGCs or 402

induce their turnover by E3 ubiquitin ligases and the 26s proteasome. V= vesicle 403

404



13

Figure 2.Three different modules of Calmodulin regulation in CNGC complexes. (A) When apo-CaM is bound 405

to the IQ domain in the presence of low Ca2+-concentration, the homo-tetrameric CNGC12 channel or the 406

CNGC8-CNGC18 hetero-complex can be gated open upon hyperpolarization to allow Ca2+ entry. (B) Elevation 407

of cytosolic Ca2+-concentration induces dissociation of Ca2+-CaM, which leads to closure of CNGC8-CNGC18. (C) 408

Alternatively, as shown for CNGC14 and CNGC2-CNGC4 hetero-complexes, binding of (Ca2+)-CaM induces 409

conformational rearrangements resulting in channel closure. Red dots and red colour indicate Ca2+ ions and 410

high Ca2+ concentration, respectively. CaM is shown with its N- and C-terminal lobes with two apo (white) or 411

Ca2+ (red) loaded EF-hands. For clarity, two C-terminal domains of CNGC subunits are shown for each complex 412

only. The conserved helical parts of the CNBD are represented by green rods, the helical IQ domain in purple. 413

The open state (A) is symbolized by a Ca2+-occupied pore and a compact arrangement of the CNBD with the 414

transmembrane part of the channel, in analogy to known structures (Li et al. 2018). In (B) and (C) the pore is 415

closed and the CNBD is separated from the membrane via the C-linker, to illustrate the closed state. 416



14

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654



ADVANCES

• Multiple proteins that interact with plant CNGCs have been discovered, including the receptor kinase BAK1, the receptor-like cytoplasmic kinases BIK1 and OsRLCK185, and the proton pump ATPases, AHA1 and AHA2. In addition, the calcium-binding proteins CaM and the calcium-dependent protein kinase CPK32 have been shown to bind plant CNGCs.

• Plant CNGCs are regulated by phosphorylation on two levels: conformational change (which regulates activity) and protein turnover. BAK1, BIK1, OsRLCK185, and CPK32 phosphorylate CNGCs.

• The universal calcium sensor protein CaM gates some plant CNGCs. CaM associates with CNGCs in Ca2+-dependent and -independent manners. Apo-CaM association with the CNGC IQ motif could function as a built-in Ca-sensing mechanism.

• Similar to animal CNGCs, some plant CNGCs form hetero-tetramers. Data suggest that multiple CNGCs act together to shape Ca2+ oscillations.



OUTSTANDING QUESTIONS

• What is the subunit composition of different native CNGC complexes? Are these combinations fixed or do they change depending on the stimulus?

• How does the subunit composition, including CaMs, of native CNGC complexes relate to the kind of Ca2+ signatures generated?

• Does a common structural rearrangement underlie the opening of CNGC channels and what does this look like?

• Are CNGCs part of membrane nanodomains that contain receptor kinases and decoder proteins to create stimulus-specific Ca2+ signatures?

• Is apo-CaM bound to IQ motifs part of most CNGC complexes? Which subunits are positively/negatively regulated by CaM?

• What are the affinities of CNGCs for cNMPs in the absence and presence of other regulators? Are only some CNGCs gated by cNMPs, do cNMPs act as co-factors, or do they modify the voltage-dependence or interaction with other regulators?



1

Table 1. Comparison of CNGCs expressed in HEK293 cells or Xenopus oocytes. Note, that in the absence of CaM2, CNGC7 and CNGC8 inhibit the current of the respective heteromeric CNGC18 complex, while in the presence of CaM2

no such inhibition occurs.

Expression in Xenopus oocytes

Expression in HEK293 cells

Subunit currents cNMPs CaM Reference currents cNMPs CaM Reference

CNGC1 K db-cAMP activates Leng et al. 2002 K and Na db-cAMP activates Hua et al. 2003b

CNGC2 K no Na db-cAMP or db-cGMP activates

Leng et al. 1999; 2002 K no Na db-cAMP activates Hua et al. 2003b; Leng et al. 2002

no not added CaM7 no effect Tian et al. 2019 K cAMP present

Ca-CaM4 inhibits Hua et al. 2003a

CNGC2 & 4 Ca not added

CaM7 inhibits Tian et al. 2019

CNGC4 K or Na cAMP or cGMP activates

Balagué et al. 2003

no not added CaM7 no effect Tian et al. 2019

CNGC7 no CaM2 no effect Pan et al. 2019 Ca

cAMP or cGMP activates Gao et al. 2016

CNGC8 no CaM2 no effect Pan et al. 2019 Ca


CNGC9 Ca cAMP or cGMP activates Gao et al. 2016




2

CNGC11 no db-cAMP no effect,

CaM1, CaM6 no effect Zhang et al. 2019

8Br-cAMP no effect

CNGC12 Ca db-cAMP no effect,

(apo)-CaM1 activates; Zhang et al. 2019

8Br-cAMP no effect CaM6 no effect

CNGC14 Ca Zhang et al. 2017

Ca

CaM2.2 no effect; CaM7 inhibits Zeb et al. 2019


CNGC18 Ca no K,

Na CaM2 no effect Pan et al. 2019 Ca


CNGC18 & 7 or 8 no/tiny db-cAMP present

(CPK32 activates) Zhou et al. 2014

no CaM2 activates Pan et al. 2019

CNGC19 Ca Yu et al. 2019

Ca no K,

Na db-cAMP activates

Meena et al. 2019


LjBRUSH no / tiny 8Br-cAMP present Chiasson et al. 2017

Ljbrush mutant Ca no K 8Br-cAMP present

Chiasson et al. 2017



3

OsCNGC9 Ca no K Wang et al. 2019

OsCNGC13 Ca Xu et al. 2017



1

Table 2. Known CNGC interactions with other proteins

Clade Isoform Interactor Position Effect Observation Technique Reference

I CNGC12

CNGC11/12

CaM

CaM1

Apo-CaM1

N-terminal CaM-BD

IQ domain

IQ domain

De-activate

Activate

Activate

Deletion causes cell death

Mutation abolishes cell

death

Transient

expression

TEVC (Xenopus)

DeFalco et al., 2016

Zhang et al., 2019


II CNGC6 CaM2,3,5,7 IQ domain neg plasma membrane Ca2+

conductance after heat

shock

Whole-cell

voltage patch

clamping of

protoplasts

Nui et al., 2019

III CNGC14 CaM7 C-terminus Neg Inhibition of Ca2+ influx TEVC (Xenopus) Zeb et al., 2014

OsCNGC9 OsRLCK185 C-terminus Positive phosphorylation

Increased [Ca2+]cyt

In vitro

phosphorylation

assay

Ca2+ imaging in

HEK cells

Wang et al., 2019

CNGC18 CNGC7/8

Apo-CaM2

Ca2+ CaM2

CPK32

MLO5/9

C-terminus

IQ domain

Negative

Positive

Negative

Activate

Inhibition of Ca2+ influx

Non Ca2+ binding CaM

activates

Release of Ca2+ CaM2

Increased Ca2+ influx

TEVC (Xenopus)

TEVC (Xenopus)

Microscale

Thermophoresis

TEVC (Xenopus)

Pan et al., 2019

Zhou et al., 2014

Meng et al., 2020



2

Increased pollen tube

width

In vivo

Pull-down, Split-

ubiquitin Y2H

MtCNGC15a,

b, c

CNGC15

MtDMI1

DMI1

N-terminus Neutral Simultaneous activation Y2H, BiFC

BiFC

Charpentier et al., 2016

Leitao et al., 2019

CNGC17 BAK1

AHA1, AHA2

nd

nd

nd

nd

Impaired phytosulfokine

response in KO

Split-ubiquitin

Y2H,

FLIM

Ladwig et al., 2015

IVa CNGC19 BAK1/SERK4

CaM2, 3, 6,

7

C-terminus

C-terminus

nd

nd

Phosphorylation leads to

turnover

coIP

Y2H, BiFC

Yu et al., 2019

Meena et al., 2019

CNGC20 BAK1/SERK4

CaM2

C-terminus

IQ domain

Negative

nd

Phosphorylation leads to

turnover

Mass

spectrometry

Y2H, BiFC

Yu et al., 2019

Fischer et al., 2013

IVb CNGC2 BIK1

CaM7

IQ domain ?

Negative

?


coIP, but no

phosphorylation

TEVC (Xenopus)

Tian et al., 2019

Tian et al., 2019



3

CNGC4 BIK1

CaM7

CNGC2

C-terminus

(and N-terminus?)

IQ domain

nd

Activate

Negative

Positive

Phosphorylation


Required for activity

patch-clamp of

protoplasts

Mass

spectrometry

TEVC (Xenopus)

TEVC (Xenopus)

Tian et al., 2019

Chin et al., 2013; Tian et al., 2019



H+

PumpCa2+

Pump

BIK1P P

P

PRR complex

CPKsP

[Ca2+ ] cyt

Turnover of CNGCs?

E3

E2

CNGCs

RBOHD

P

P

MLO

RLCK P

V

Recruitment of CNGCs?

Figure 1. Model of a CNGC-containing signal complex (nanodomain/channelosome, shown in darker grey). A heterotetrametric CNGC channel is part of a sensing receptor complex containing pattern recognition receptors (PRRs), their clients (e.g. BIK1, RBOHD, RLCK), various pumps (e.g. proton ATPase and Ca2+ pumps), and decoders (e.g. CPKs and CaM). The formation of such a signal complex can be permanent or temporal upon recognition of specific stimuli (transient signalling complex) and the combination of specific players can contribute to generate precise spatiotemporal Ca2+ signals. Recruitment of CNGCs in a specific signaling complex may be achieved by MLO proteins. Phosphorylation plays significant roles to activate CNGCs or induce their turnover by E3 ubiquitin ligases and the 26s proteasome. V= vesicle



gated open in the presence of apo-CaM! closed by dissociation of Ca2+-CaM! closed in the presence of (Ca2+?)-CaM!A! B! C!

CNGC12 CNGC8-CNGC18 complex CNGC8-CNGC18 complex CNGC14

CNGC2-CNGC4 complex

Figure 2. Three different modules of Calmodulin regulation in CNGC complexes. (A) When apo-CaM is bound to the IQ domain in the presence of low Ca2+-concentration, the homo-tetrameric CNGC12 channel or the CNGC8-CNGC18 hetero-complex can be gated open upon hyperpolarization to allow Ca2+ entry. (B) Elevation of cytosolic Ca2+-concentration induces dissociation of Ca2+-CaM, which leads to closure of CNGC8-CNGC18. (C) Alternatively, as shown for CNGC14 and CNGC2-CNGC4 hetero-complexes, binding of (Ca2+)-CaM induces conformational rearrangements resulting in channel closure. Red dots and red colour indicate Ca2+ ions and high Ca2+ concentration, respectively. CaM is shown with its N- and C-terminal lobes with two apo (white) or Ca2+ (red) loaded EF-hands. For clarity, two C-terminal domains of CNGC subunits are shown for each complex only. The conserved helical parts of the CNBD are represented by green rods, the helical IQ domain in purple. The open state (A) is symbolized by a Ca2+-occupied pore and a compact arrangement of the CNBD with the transmembrane part of the channel, in analogy to known structures (Li et al. 2018). In (B) and (C) the pore is closed and the CNBD is separated from the membrane via the C-linker, to illustrate the closed state.



Table 1. Comparison of CNGCs expressed in Xenopus oocytes or HEK293 cells

Expression in Xenopus oocytes Expression in HEK293 cellsSubunit currents cNMPs CaM Reference currents cNMPs CaM ReferenceCNGC1 K db-cAMP activates Leng et al. 2002 K and Na db-cAMP activates Hua et al. 2003b

CNGC2 K no Nadb-cAMP or db-cGMP activates

Leng et al. 1999; 2002 K no Na db-cAMP activates

Hua et al. 2003b; Leng et al. 2002

no not added CaM7 no effect Tian et al. 2019 K cAMP present Ca-CaM4 inhibits Hua et al. 2003a

CNGC2 & 4 Ca not added CaM7 inhibits Tian et al. 2019

CNGC4 K or Na cAMP or cGMP activates Balagué et al. 2003

no not added CaM7 no effect Tian et al. 2019

CNGC7 no CaM2 no effect Pan et al. 2019 CacAMP or cGMP activates Gao et al. 2016

CNGC8 no CaM2 no effect Pan et al. 2019 CacAMP or cGMP activates Gao et al. 2016

CNGC9 CacAMP or cGMP activates Gao et al. 2016


CNGC11 no db-cAMP no effect, CaM1, CaM6 no effect Zhang et al. 2019

8Br-cAMP no effect

CNGC12 Ca db-cAMP no effect, (apo)-CaM1 activates; Zhang et al. 2019

8Br-cAMP no effect CaM6 no effect

CNGC14 Ca Zhang et al. 2017

CaCaM2.2 no effect; CaM7 inhibits Zeb et al. 2019


CNGC18 Ca no K, Na CaM2 no effect Pan et al. 2019 CacAMP or cGMP activates Gao et al. 2016

CNGC18 & 7 or 8 no/tiny db-cAMP present (CPK32 activates) Zhou et al. 2014

no CaM2 activates Pan et al. 2019


Ca no K, Na db-cAMP activates Meena et al. 2019


LjBRUSH no / tiny 8Br-cAMP present Chiasson et al. 2017

Ljbrush mutant Ca no K 8Br-cAMP present Chiasson et al. 2017

OsCNGC9 Ca no K Wang et al. 2019

OsCNGC13 Ca Xu et al. 2017



Clade Isoform Interactor Position Effect Observation Technique Reference

I CNGC12

CNGC11/12

CaM

CaM1

Apo-CaM1

N-terminal CaM-BD

IQ domain

IQ domain

De-activate

Activate

Activate

Deletion causes cell death

Mutation abolishes cell death

Transient expression

TEVC (Xenopus)


Zhang et al., 2019


II CNGC6 CaM2,3,5,7 IQ domain neg plasma membrane Ca2+ conductance after heat shock

Whole-cell voltage patch clamping of protoplasts

Nui et al., 2019

III CNGC14 CaM7 C-terminus Neg Inhibition of Ca2+ influx TEVC (Xenopus) Zeb et al., 2014

OsCNGC9 OsRLCK185 C-terminus Positive phosphorylation

Increased [Ca2+]cyt

In vitro phosphorylation assay

Ca2+ imaging in HEK cells

Wang et al., 2019

CNGC18 CNGC7/8

Apo-CaM2

Ca2+ CaM2

CPK32

MLO5/9

C-terminus

IQ domain

Negative

Positive

Negative

Activate


Non Ca2+ binding CaM activates

Release of Ca2+ CaM2

Increased Ca2+ influx

Increased pollen tube width

TEVC (Xenopus)

TEVC (Xenopus)

Microscale Thermophoresis

TEVC (Xenopus)

In vivo

Pull-down, Split-ubiquitin Y2H

Pan et al., 2019

Zhou et al., 2014

Meng et al., 2020

MtCNGC15a, b, c

CNGC15

MtDMI1

DMI1

N-terminus Neutral Simultaneous activation Y2H, BiFC

BiFC

Charpentier et al., 2016

Leitao et al., 2019

CNGC17 BAK1

AHA1, AHA2

nd

nd

nd

nd

Impaired phytosulfokine response in KO Split-ubiquitin Y2H,

FLIM

Ladwig et al., 2015

IVa CNGC19 BAK1/SERK4

CaM2, 3, 6, 7

C-terminus

C-terminus

nd

nd

Phosphorylation leads to turnover coIP

Y2H, BiFC

Yu et al., 2019

Meena et al., 2019

CNGC20 BAK1/SERK4

CaM2

C-terminus

IQ domain

Negative

nd

Phosphorylation leads to turnover Mass spectrometry

Y2H, BiFC

Yu et al., 2019

Fischer et al., 2013

IVb CNGC2 BIK1

CaM7 IQ domain

?

Negative

?


coIP, but no phosphorylation

TEVC (Xenopus)

Tian et al., 2019

Tian et al., 2019

CNGC4 BIK1

CaM7

CNGC2

C-terminus

(and N-terminus?)

IQ domain

nd

Activate

Negative

Positive

Phosphorylation


Required for activity

patch-clamp of protoplasts

Mass spectrometry

TEVC (Xenopus)

TEVC (Xenopus)

Tian et al., 2019

Chin et al., 2013; Tian et al., 2019

Table 2. Known CNGC interactions with other proteins



Parsed CitationsAbdel-Hamid H, Chin K, Shahinas D, Moeder W, Yoshioka K (2010) Calmodulin binding to Arabidopsis cyclic nucleotide gated ionchannels. Plant Signal Behav 5: 1147-1149

Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, et al. (2001) A defined range of guard cell calcium oscillationparameters encodes stomatal movements. Nature 411: 1053-1057


Arazi T, Kaplan B, Sunkar R, Fromm H (2000) Cyclic-nucleotide- and Ca2+/calmodulin-regulated channels in plants: targets formanipulating heavy-metal tolerance, and possible physiological roles. Biochem Soc Trans 28: 471-475


Ashton AR (2011) Guanylyl cyclase activity in plants? Proc Natl Acad Sci U S A. 108:E96; author reply E97-8Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Balagué C, Lin B, Alcon C, Flottes G, Malmstrøm S, Köhler C, et al. (2003) HLM1, an essential signaling component in thehypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family. Plant Cell 15: 365-379


Baxter J, Moeder W, Urquhart W, Shahinas D, Chin K, Christendat D, Kang HG, Angelova M, Kato N, Yoshioka K (2008) Identification ofa functionally essential amino acid for Arabidopsis cyclic nucleotide gated ion channels using the chimeric AtCNGC11/12 gene. Plant J56: 457-469


Bender KW, Zielinski RE, Huber SC (2018) Revisiting paradigms of Ca(2+) signaling protein kinase regulation in plants. Biochem J 475:207-223


Brost C, Studtrucker T, Reimann R, Denninger P, Czekalla J, Krebs M, et al. (2019) Multiple cyclic nucleotide-gated channelscoordinate calcium oscillations and polar growth of root hairs. Plant J 99: 910-923.


Bücherl CA, Jarsch IK, Schudoma C, Segonzac C, Mbengue M, Robatzek S, MacLean D, Ott T, Zipfel C (2017) Plant immune and growthreceptors share common signalling components but localise to distinct plasma membrane nanodomains. Elife 6. e25114


Chan CWM, Schorrak LM, Smith RK, Bent AF, Sussman MR (2003) A cyclic nucleotide-gated ion channel, CNGC2, is crucial for plantdevelopment and adaptation to calcium stress. Plant Physiol. 132: 728–731


Chan CWM, Wohlbach DJ, Rodesch MJ, Sussman MR (2008) Transcriptional Changes in Response to Growth of Arabidopsis in highexternal calcium. FEBS Lett. 582:967-976


Charpentier M, Sun J, Vaz Martins T, Radhakrishnan GV, Findlay K, Soumpourou E, Thouin J, Véry AA, Sanders D, Morris RJ, OldroydGE (2016) Nuclear-localized cyclic nucleotide-gated channels mediate symbiotic calcium oscillations. Science 352: 1102-1105


Chiasson DM, Haage K, Sollweck K, Brachmann A, Dietrich P, Parniske M (2017) A Quantitative Hypermorphic CNGC Allele ConfersEctopic Calcium Flux and Impairs Cellular Development ELIfe 6 DOI: 10.7554/eLife.25012


Chin K, Moeder W, Abdel-Hamid H, Shahinas D, Gupta D, Yoshioka, K (2010) Importance of the αC-helix in the cyclic nucleotide bindingdomain for the stable channel regulation and function of cyclic nucleotide gated ion channels in Arabidopsis. J. Exp. Bot. 61: 2383-2393


Chin K, DeFalco TA, Moeder W, Yoshioka K (2013) The Arabidopsis cyclic nucleotide-gated channels, AtCNGC2 and AtCNGC4 work inthe same signaling pathway to affect pathogen defense and floral transition. Plant Physiol 163: 611-624https://plantphysiol.orgDownloaded on March 28, 2021. - Published by

Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

https://www.ncbi.nlm.nih.gov/pubmed?term=Abdel%2DHamid H%2C Chin K%2C Shahinas D%2C Moeder W%2C Yoshioka K %282010%29 Calmodulin binding to Arabidopsis cyclic nucleotide gated ion channels%2E Plant Signal Behav&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Abdel-Hamid&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=Calmodulin binding to Arabidopsis cyclic nucleotide gated ion channels&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Calmodulin binding to Arabidopsis cyclic nucleotide gated ion channels&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Abdel-Hamid&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Allen GJ%2C Chu SP%2C Harrington CL%2C Schumacher K%2C Hoffmann T%2C Tang YY%2C et al%2E %282001%29 A defined range of guard cell calcium oscillation parameters encodes stomatal movements%2E Nature&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Allen&hl=en&c2coff=1

https://scholar.google.com/scholar?as_q=A defined range of guard cell calcium oscillation parameters encodes stomatal movements&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=A defined range of guard cell calcium oscillation parameters encodes stomatal movements&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Allen&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Arazi T%2C Kaplan B%2C Sunkar R%2C Fromm H %282000%29 Cyclic%2Dnucleotide%2D and Ca2%2B%2Fcalmodulin%2Dregulated channels in plants%3A targets for manipulating heavy%2Dmetal tolerance%2C and possible physiological roles%2E Biochem Soc Trans&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Arazi&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=Cyclic-nucleotide- and Ca2+/calmodulin-regulated channels in plants: targets for manipulating heavy-metal tolerance, and possible physiological roles&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Arazi&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Ashton AR %282011%29 Guanylyl cyclase activity in plants%3F Proc Natl Acad Sci U S A%2E 108%3AE96%3B author reply E&dopt=abstract

https://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ashton&hl=en&c2coff=1

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https://scholar.google.com/scholar?as_q=Guanylyl cyclase activity in plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ashton&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

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Petra Dietrich1, Wolfgang Moeder2, Keiko Yoshioka2,3€¦ · 23.06.2020 · In light of recent...

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