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K2P channels in plants and animals

  • Wendy GonzálezEmail author
  • Braulio Valdebenito
  • Julio Caballero
  • Gonzalo Riadi
  • Janin Riedelsberger
  • Gonzalo Martínez
  • David Ramírez
  • Leandro Zúñiga
  • Francisco V. Sepúlveda
  • Ingo Dreyer
  • Michael Janta
  • Dirk BeckerEmail author
Invited Review

Abstract

Two-pore domain potassium (K2P) channels are membrane proteins widely identified in mammals, plants, and other organisms. A functional channel is a dimer with each subunit comprising two pore-forming loops and four transmembrane domains. The genome of the model plant Arabidopsis thaliana harbors five genes coding for K2P channels. Homologs of Arabidopsis K2P channels have been found in all higher plants sequenced so far. As with the K2P channels in mammals, plant K2P channels are targets of external and internal stimuli, which fine-tune the electrical properties of the membrane for specialized transport and/or signaling tasks. Plant K2P channels are modulated by signaling molecules such as intracellular H+ and calcium and physical factors like temperature and pressure. In this review, we ask the following: What are the similarities and differences between K2P channels in plants and animals in terms of their physiology? What is the nature of the last common ancestor (LCA) of these two groups of proteins? To answer these questions, we present physiological, structural, and phylogenetic evidence that discards the hypothesis proposing that the duplication and fusion that gave rise to the K2P channels occurred in a prokaryote LCA. Conversely, we argue that the K2P LCA was most likely a eukaryote organism. Consideration of plant and animal K2P channels in the same study is novel and likely to stimulate further exchange of ideas between students of these fields.

Keywords

K2P channels Plants Animals 

Notes

Acknowledgments

This work was supported by the Comisión Nacional Científica y Tecnológica from Chile (grants DAAD-Conicyt-2012 to WG, JC, MJ, and DB; Fondecyt #1140624 to WG and BV; ACT1104 to WG and JR; Fondef Idea CA13I10223 to WG and LZ; and Fondecyt #11110217 to LZ. The Centro de Estudios Científicos (CECs) is funded by the Centres of Excellence Base Financing Programme of CONICYT). Funding of DB and MJ by the DFG Research Training Group (Graduiertenkolleg) GRK 1342 is greatly acknowledged. We thank Tracey Ann Cuin for the critical reading of and helpful comments on the manuscript and Javier Sánchez-Contreras for managing the bibliography.

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

424_2014_1638_MOESM1_ESM.pdf (66 kb)
Online Resource 1 Pairwise global alignments of hK2Ps and AtTPKs. The alignments were generated using the EMBOSS implementation of the Needleman-Wunsh global alignment algorithm of Rice et al. [64]. The sequence identity is shown above the diagonal and the sequence similarity can be observed under the diagonal. For hK2Ps, the systematic (HUGO) name is indicated first, followed by the conventional name. The sequence identities and similarities between hK2Ps and AtTPKs are highlighted in boxes. (PDF 66 kb)
424_2014_1638_MOESM2_ESM.pdf (792 kb)
Online Resource 2 Transmembrane segments predictions for the NgKC and K2P channels selected for this study. The transmembrane segment prediction, done at the InterPro website by the TMhelix server, shows TM segments in all channels aligned with the two-pore domain potassium channel domain (IPR013099) annotated in InterPro (blue boxes). An additional TM domain is predicted for hK2Ps (except TASK-1) and NgKC, which could be a mistake of the TMhelix server (blue arrow). For the TOK1 channel, another four transmembrane domain prediction appears (red box), which corresponds to the four TM extra segments of the 2*2TM. For hK2Ps, the systematic (HUGO) name is indicated first, followed by the conventional name. (PDF 792 kb)
424_2014_1638_MOESM3_ESM.pdf (1.1 mb)
Online Resource 3 MSA of hK2Ps, NgKC, AtTPKs. The alignment was performed with Kalign [45] and colored by conservation in a ramp from white (not conserved) to dark blue (highly conserved). The secondary structure of the recently crystalized K2P channel TRAAK is indicated above the sequences and labeled with PD1 and PD2, signifying pore domain 1 and 2, respectively [14]. K+ selectivity filters are shown as green lines. Helices in pore domain 1 are colored blue and helices in pore domain 2, orange. The arrows colors are for the same positions in the aligment as in Fig. 2 and the hydrophobic positions of the PD2 inner helix found in TWIK-1 [7] are also with red arrows here. (PDF 1090 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Wendy González
    • 1
    Email author
  • Braulio Valdebenito
    • 1
  • Julio Caballero
    • 1
  • Gonzalo Riadi
    • 1
  • Janin Riedelsberger
    • 1
  • Gonzalo Martínez
    • 1
  • David Ramírez
    • 1
  • Leandro Zúñiga
    • 2
  • Francisco V. Sepúlveda
    • 3
  • Ingo Dreyer
    • 4
  • Michael Janta
    • 5
  • Dirk Becker
    • 5
    Email author
  1. 1.Centro de Bioinformática y Simulación Molecular (CBSM)Universidad de TalcaTalcaChile
  2. 2.Centro de Investigaciones Médicas (CIM), Escuela de MedicinaUniversidad de TalcaTalcaChile
  3. 3.Centro de Estudios Científicos (CECs)ValdiviaChile
  4. 4.Centro de Biotecnología y Genómica de PlantasUniversidad Politécnica de MadridMadridSpain
  5. 5.Plant Molecular Biology and BiophysicsUniversity of WuerzburgWuerzburgGermany

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