The Potassium Channel KAT1 Is Activated by Plant and Animal 14-3-3 Proteins

Sottocornola, B.; Visconti, Sabina; Orsi, Sara A.; Gazzarrini, Sabrina; Giacometti, Sonia; Olivari, C.; Camoni, Lorenzo; Aducci, Patrizia; Marra, Mauro; Abenavoli, Alessandra; Thiel, Gerhard; Moroni, Anna

doi:10.1074/jbc.m603361200

Cited by 63 publications

(51 citation statements)

References 40 publications

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“…It is well established that animal 14-3-3 proteins activate KAT1 conductance in two ways: by increasing the current density (i.e., the number of active channels in the plasma membrane) and by increasing the channel open probability at a given voltage. As a result of 14-3-3 binding, the channel maximal current increases and the half activation potential, the voltage value at which 50% of the channels are open (V 1/2 ), shifts positive of ;10 mV (Sottocornola et al, 2006(Sottocornola et al, , 2008. All mutants generated voltage-dependent, slowly activating, inward rectifying K + currents, typical of the wild-type KAT1 channel ( Figure 1B).…”

Section: -3-3 Binding To Kat1 Is Regulated By S676 Phosphorylationmentioning

confidence: 99%

“…Currently it is not known how the activity of the KAT1 channel is integrated in this scenario. Some indirect evidence for a regulatory modulation of KAT1 by the 14-3-3 proteins can be anticipated from data, which show that activity and trafficking of the channel are promoted by an overexpression of 14-3-3 proteins (Sottocornola et al, 2006(Sottocornola et al, , 2008. So far, direct binding of 14-3-3 proteins to the KAT1 channel has not been demonstrated.…”

Section: Introductionmentioning

confidence: 98%

“…When measured in excised inside-out patches, the KAT1 current undergoes a phenomenon referred to as rundown (Tang and Hoshi, 1999;Sottocornola et al, 2006). In this process, the voltage dependency of KAT1 is progressively shifted toward very negative voltages (>50 mV of left shift in the activation curve).…”

Section: A Molecular Explanation For Kat1 Channel Rundownmentioning

confidence: 99%

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Fusicoccin Activates KAT1 Channels by Stabilizing their Interaction with 14-3-3- Proteins

et al. 2017

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Plants acquire potassium (K + ) ions for cell growth and movement via regulated diffusion through K + channels. Here, we present crystallographic and functional data showing that the K + inward rectifier KAT1 (K + Arabidopsis thaliana 1) channel is regulated by 14-3-3 proteins and further modulated by the phytotoxin fusicoccin, in analogy to the H + -ATPase. We identified a 14-3-3 mode III binding site at the very C terminus of KAT1 and cocrystallized it with tobacco (Nicotiana tabacum) 14-3-3 proteins to describe the protein complex at atomic detail. Validation of this interaction by electrophysiology shows that 14-3-3 binding augments KAT1 conductance by increasing the maximal current and by positively shifting the voltage dependency of gating. Fusicoccin potentiates the 14-3-3 effect on KAT1 activity by stabilizing their interaction. Crystal structure of the ternary complex reveals a noncanonical binding site for the toxin that adopts a novel conformation. The structural insights underscore the adaptability of fusicoccin, predicting more potential targets than so far anticipated. The data further advocate a common mechanism of regulation of the proton pump and a potassium channel, two essential elements in K + uptake in plant cells.

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Section: -3-3 Binding To Kat1 Is Regulated By S676 Phosphorylationmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 98%

Section: A Molecular Explanation For Kat1 Channel Rundownmentioning

confidence: 99%

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Fusicoccin Activates KAT1 Channels by Stabilizing their Interaction with 14-3-3- Proteins

et al. 2017

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“…Previous studies have shown that posttranslational regulation is an important mechanism for regulation of K + channel activities in plant cells [13,[38][39][40]. One of the examples is the regulation of AKT1 activity by a protein kinase AtCIPK23.…”

Section: A Complex K + Uptake Regulatory Pathway In Arabidopsis In Rementioning

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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“…14-3-3 proteins are a family of evolutionary conserved dimeric proteins that accomplish a wide range of regulatory roles in eukaryotes (Fu et al, 2000). In plants, in addition to the plasma membrane transport through the regulation of the H þ -ATPase activity, 14-3-3s are involved in the control of gene expression, in the cellular trafficking, in the control of the activities of diverse enzymes of metabolism, in the hormone signaling, and in general in the coordination of different signal transduction pathways (Aducci et al, 2002;Sottocornola et al, 2006;Camoni et al, 2011;Schoonheim et al, 2009;Denison et al, 2011). Lots of evidence suggest also a role of 14-3-3s in the plant response to stress conditions (G€ okirmak et al, 2010): environmental and biotic stresses can affect the expression levels of 14-3-3 genes (Chevalier et al, 2009) and also a large number of stresserelated proteins have been identified as 14-3-3 clients (Chang et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Cold stress affects H + -ATPase and phospholipase D activity in Arabidopsis

Muzi

Camoni

Visconti

et al. 2016

Plant Physiology and Biochemistry

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a b s t r a c tLow temperature is an environmental stress that greatly influences plant performance and distribution. Plants exposed to cold stress exhibit modifications of plasma membrane physical properties that can affect their functionality. Here it is reported the effect of low temperature exposure of Arabidopsis plants on the activity of phospholipase D and H þ -ATPase, the master enzyme located at the plasma membrane.The H þ -ATPase activity was differently affected, depending on the length of cold stress imposed. In particular, an exposure to 4 C for 6 h determined the strong inhibition of the H þ -ATPase activity, that correlates with a reduced association with the regulatory 14-3-3 proteins. A longer exposure first caused the full recovery of the enzymatic activity followed by a significant activation, in accordance with both the increased association with 14-3-3 proteins and induction of H þ -ATPase gene transcription. Different time lengths of cold stress treatment were also shown to strongly stimulate the phospholipase D activity and affect the phosphatidic acid levels of the plasma membranes. Our results suggest a functional correlation between the activity of phospholipase D and H þ -ATPase mediated by phosphatidic acid release during the cold stress response.

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The Potassium Channel KAT1 Is Activated by Plant and Animal 14-3-3 Proteins

Cited by 63 publications

References 40 publications

Fusicoccin Activates KAT1 Channels by Stabilizing their Interaction with 14-3-3- Proteins

Fusicoccin Activates KAT1 Channels by Stabilizing their Interaction with 14-3-3- Proteins

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

Cold stress affects H + -ATPase and phospholipase D activity in Arabidopsis

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