Distinct roles of the last transmembrane domain in controlling <i>Arabidopsis </i>K<sup>+</sup> channel activity

Gajdanowicz, Paweł; Garcı́a-Mata, Carlos; González, Wendy; Morales-Navarro, Samuel; Sharma, Tripti; González‐Nilo, Fernando; Gutowicz, Jan; Mueller‐Roeber, Bernd; Blatt, Michael R.; Drèyer, Ingo

doi:10.1111/j.1469-8137.2008.02749.x

Cited by 38 publications

(45 citation statements)

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“…The amino acid residue Gly 315 in AtKC1 is highly conserved in S6 region of the Arabidopsis Shaker family ( Figure 1C). A recent report showed that mutation of this amino acid residue in KAT1 (G286I) led to the shift of activation threshold to more negative voltage when compared with wild-type KAT1 [27]. Thus, the Gly residue in S6 region may be very important for the gating of K + channels.…”

Section: Atkc1 Regulates Akt1 Activitymentioning

confidence: 99%

Potassium channel α-subunit AtKC1 negatively regulates AKT1-mediated K+ uptake in Arabidopsis roots under low-K+ stress

Wang

et al. 2010

Cell Res

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Potassium transporters play crucial roles in K + uptake and translocation in plants. However, so far little is known about the regulatory mechanism of potassium transporters. Here, we show that a Shaker-like potassium channel AtKC1, encoded by the AtLKT1 gene cloned from the Arabidopsis thaliana low-K + (LK)-tolerant mutant Atlkt1, significantly regulates AKT1-mediated K + uptake under LK conditions. Under LK conditions, the Atkc1 mutants maintained their root growth, whereas wild-type plants stopped their root growth. Lesion of AtKC1 significantly enhanced the tolerance of the Atkc1 mutants to LK stress and markedly increased K + uptake and K + accumulation in the Atkc1-mutant roots under LK conditions. Electrophysiological results showed that AtKC1 inhibited the AKT1-mediated inward K + currents and negatively shifted the voltage dependence of AKT1 channels. These results demonstrate that the 'silent' K + channel α-subunit AtKC1 negatively regulates the AKT1-mediated K + uptake in Arabidopsis roots and consequently alters the ratio of root-to-shoot under LK stress conditions. Keywords: Arabidopsis; potassium channel; low-K + stress; AKT1; AtKC1 Cell Research (2010) IntroductionPotassium is an essential mineral element for plant growth and development, and it plays essential roles in many important physiological and biochemical processes in living plant cells, such as regulation of enzyme activation, electrical neutralization, osmoregulation, control of membrane potential, co-transport of sugars, and so on [1,2]. Plant growth and development need millimolar K + in the soil or growth medium, but typical K + concentration at the interface of roots and soils is within micromolar range [3]. Thus, plants often encounter low-K + (LK) stress under natural conditions. Although different plants or different genotypes of a plant species show varied K + utilization efficiency [4], most plants show K + -deficient symptom under LK stress, typically leaf chlorosis and subsequent inhibition of plant growth and development [5].Absorption of K + by plant cells and K + translocation between different tissues and organs in plants are mediated by plant K + transporters and channels [2,6,7]. Over the past decade, a large number of genes encoding plant K + transporters and channels, particularly for Arabidopsis, have been characterized [6][7][8]. These K + transporters vary in K + affinity, kinetics, transcriptional modulation, regulatory mechanism, etc [2,[6][7][8], and they compose a complex system for plant K + uptake and translocation. Among these K + transporters and channels, members of the Shaker K + channel family are well characterized for their potential functions and are probably the most important for K + uptake and transport in Arabidopsis [8] Recent reports showed that channel heterotetramerization is a key regulatory mechanism for K + channels, which was found not only in animals [14][15][16] but also in plants [17,18]. Different kinds of potassium channel subunits may assemble together to form functional heteromer...

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Section: Atkc1 Regulates Akt1 Activitymentioning

confidence: 99%

Potassium channel α-subunit AtKC1 negatively regulates AKT1-mediated K+ uptake in Arabidopsis roots under low-K+ stress

Wang

et al. 2010

Cell Res

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“…Currents were recorded after filtering at 1 kHz and analyzed as described previously (17,20). Xenopus oocytes were prepared, injected with cRNA, and currents were recorded as described previously (17,18). Data are reported as mean Ϯ S.E.…”

Section: Methodsmentioning

confidence: 99%

“…Molecular Biology-Site mutations were generated in wildtype SKOR and the C-terminal deletion mutant SKOR-⌬K746 as described previously (17,18), and mutants and wild-type SKOR were subcloned into the bicistronic expression vector pCIG2, which contains an internal ribosome entry site and an enhanced green fluorescent protein cassette. All clones were verified by sequencing.…”

Section: Methodsmentioning

confidence: 99%

A Minimal Cysteine Motif Required to Activate the SKOR K+ Channel of Arabidopsis by the Reactive Oxygen Species H2O2*

Garcı́a-Mata

Wang

Gajdanowicz

et al. 2010

Journal of Biological Chemistry

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122

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Reactive oxygen species (ROS) are essential for development and stress signaling in plants. They Reactive oxygen species (ROS) 3 are major signals in virtually every aspect of eukaryotic cell biology (1, 2). In animals, they are important regulators of cell division and muscle contraction among others (3), and in plants they are essential for development (4) and stress signaling, including drought (5, 6) and defense against pathogens (7). Within proteins, ROS target a small subset of amino acids, notably cysteine (Cys) residues, chemically modifying these amino acids and thereby altering protein structure and function (8). Nonetheless, the targeted residues and associated motifs are often poorly defined, the effects wide ranging and protein-specific, thus confounding molecular analyses. Indeed, among the few well documented examples, ROS modifications in mammalian ryanodine-receptor and BK channels have different consequences depending on the positions of the residues targeted (3, 9).For development and signaling in plants, the activities of membrane ion channels are essential, often including their regulation by ROS. For example, ROS affect non-selective cation channels during Fucus development (10); they regulate Ca 2ϩ channels and Ca 2ϩ -based signaling (5) as well as voltage-sensitive K ϩ channels of guard cells (11) that are important for stomatal movement; they contribute in responses to drought and pathogen defense (12); and they have been implicated in targeting K ϩ efflux during programmed cell death (13). However, until now virtually nothing has been known of the molecular targets for ROS in plants, nor has a site of action been identified with an ion channel protein.SKOR is one of two K ϩ channels found in Arabidopsis thaliana that rectify strongly outward, thereby mediating K ϩ efflux from the cell. It is expressed within the xylem parenchyma of the root where it facilitates K ϩ loading into the xylem (14), thereby contributing directly to K ϩ homeostasis and indirectly, through charge balance, to the transport of other solutes throughout the plant (12,15). Like other members of the Kvlike channel superfamily (16), the functional channel assembles from four monomers with each SKOR monomer incorporating six transmembrane ␣-helices. The first four ␣-helices form a positively charged voltage-sensor complex or "paddle" that moves within the membrane in response to voltage and couples this movement to the channel gate. The fifth and sixth ␣-helices line the aqueous pore through the membrane and assemble in a diaphragm or "gate" at the inner membrane surface, which opens/closes to regulate ion flux through the channel. Here we report that K ϩ current through the heterologously expressed SKOR is modulated by H 2 O 2 , thereby identifying the K ϩ channel as a potential target for ROS, and we show that a single Cys within the voltage sensor complex is essential for its ROS sen-

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“…Mutagenesis analyses have supported that mutations in crucial regions could significantly alter the transport properties and/or activities of ion channels and transporters. Several studies in Arabidopsis have revealed that different site-specific mutants in the S6 domain cause the different gating properties and K + dependence of Shaker K + channels (Johansson et al, 2006;Gajdanowicz et al, 2009). Such mutations or variations endow channels or transporters with plasticity and diversity in ion transport properties and/or activities, which may be utilized in plant nutrient use efficiency improvement (Wang and Wu, 2015).…”

Section: Variations Endow Channels or Transporters With Plasticity Anmentioning

confidence: 99%

AtKC1 and CIPK23 Synergistically Modulate AKT1-Mediated Low-Potassium Stress Responses in Arabidopsis

et al. 2016

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In Arabidopsis (Arabidopsis thaliana), the Shaker K + channel AKT1 conducts K + uptake in root cells, and its activity is regulated by CBL1/9-CIPK23 complexes as well as by the AtKC1 channel subunit. CIPK23 and AtKC1 are both involved in the AKT1-mediated low-K + (LK) response; however, the relationship between them remains unclear. In this study, we screened suppressors of low-K + sensitive [lks1 (cipk23)] and isolated the suppressor of lks1 (sls1) mutant, which suppressed the leaf chlorosis phenotype of lks1 under LK conditions. Map-based cloning revealed a point mutation in AtKC1 of sls1 that led to an amino acid substitution (G322D) in the S6 region of AtKC1. The G322D substitution generated a gain-of-function mutation, AtKC1 D , that enhanced K + uptake capacity and LK tolerance in Arabidopsis. Structural prediction suggested that glycine-322 is highly conserved in K + channels and may function as the gating hinge of plant Shaker K + channels. Electrophysiological analyses revealed that, compared with wild-type AtKC1, AtKC1 D showed enhanced inhibition of AKT1 activity and strongly reduced K + leakage through AKT1 under LK conditions. In addition, phenotype analysis revealed distinct phenotypes of lks1 and atkc1 mutants in different LK assays, but the lks1 atkc1 double mutant always showed a LK-sensitive phenotype similar to that of akt1. This study revealed a link between CIPK-mediated activation and AtKC1-mediated modification in AKT1 regulation. CIPK23 and AtKC1 exhibit distinct effects; however, they act synergistically and balance K + uptake/leakage to modulate AKT1-mediated LK responses in Arabidopsis.

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Distinct roles of the last transmembrane domain in controlling Arabidopsis K⁺ channel activity

Cited by 38 publications

References 31 publications

Potassium channel α-subunit AtKC1 negatively regulates AKT1-mediated K+ uptake in Arabidopsis roots under low-K+ stress

Potassium channel α-subunit AtKC1 negatively regulates AKT1-mediated K+ uptake in Arabidopsis roots under low-K+ stress

A Minimal Cysteine Motif Required to Activate the SKOR K+ Channel of Arabidopsis by the Reactive Oxygen Species H2O2*

AtKC1 and CIPK23 Synergistically Modulate AKT1-Mediated Low-Potassium Stress Responses in Arabidopsis

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Distinct roles of the last transmembrane domain in controlling Arabidopsis K+ channel activity

Cited by 38 publications

References 31 publications

Potassium channel α-subunit AtKC1 negatively regulates AKT1-mediated K+ uptake in Arabidopsis roots under low-K+ stress

Potassium channel α-subunit AtKC1 negatively regulates AKT1-mediated K+ uptake in Arabidopsis roots under low-K+ stress

A Minimal Cysteine Motif Required to Activate the SKOR K+ Channel of Arabidopsis by the Reactive Oxygen Species H2O2*

AtKC1 and CIPK23 Synergistically Modulate AKT1-Mediated Low-Potassium Stress Responses in Arabidopsis

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Distinct roles of the last transmembrane domain in controlling Arabidopsis K⁺ channel activity