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

Abstract

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...

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

“…To explore this hypothesis, we assessed the AtKC1 D effect on AKT1 channel activity in X. laevis oocytes. As shown in Figure 6A, when AKT1 and AtKC1 were coexpressed in oocytes, AtKC1 inhibited AKT1-mediated inward K + currents under hyperpolarization conditions, which was consistent with previous reports (Geiger et al, 2009;Wang et al, 2010). However, compared with wild-type AtKC1, AtKC1 D exhibited stronger inhibition on AKT1 conductance (Fig.…”

“…Previous reports showed that AtKC1 inhibits AKT1 activity (Geiger et al, 2009;Wang et al, 2010). In this study, the AtKC1 D mutant showed enhanced K + uptake capacity and accumulated more K + ions under LK conditions ( Fig.…”

“…Among the inward-rectifying K + channels from the Arabidopsis Shaker family, only AKT1 and AtKC1 are abundantly expressed in root tissues (Reintanz et al, 2002). As the regulatory subunit of AKT1, AtKC1 expressed alone remains in the endoplasmic reticulum (ER), but it can be recruited to the PM to regulate AKT1 activity (Duby et al, 2008;Geiger et al, 2009;Honsbein et al, 2009;Wang et al, 2010).…”

“…atkc1 (SALK_140579) is a transfer DNA insertion mutant of AtKC1 (Fig. 1B) whose shoot phenotype was similar to that in wild-type plants in LK transfer assays (Wang et al, 2010;Fig. 3F).…”

“…In Arabidopsis, AKT1 is modulated by another Shaker a-subunit, AtKC1, which is electrically silent (Reintanz et al, 2002). By forming the AKT1/AtKC1 heteromeric K + channel, AtKC1 inhibits AKT1 conductance and negatively shifts AKT1 voltage dependence (Duby et al, 2008;Geiger et al, 2009;Wang et al, 2010). Thus, AtKC1 acts as a general modulator and negatively regulates many inward Shaker K + channels in Arabidopsis (Jeanguenin et al, 2011).…”