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Plant potassium channels are in general dual affinity uptake systems

Centro de Bioinformática y Simulación Molecular, Facultad de Ingeniería, Universidad de Talca, Talca, Chile

Special Issue: BIOPHYSICS OF ION TRANSPORT IN PLANTS

In plant science, we are currently at the dawn of an era, in which mathematical modeling and computational simulations will influence and boost tremendously the gain of new knowledge. However, for many plant scientists mathematical modeling is still rather dubious and is often negligently considered as an oversimplification of the real situation. The goal of this article is to provide a toolbox that allows first steps in the modeling of transport phenomena in plants. The provided framework is applied in the simulation of K+ uptake by cells via K+ channels. Historically, K+ uptake systems are divided into “high affinity” (e.g. H+-coupled K+ transporters) and “low affinity” (K+ channels) transporters. The computational cell biology studies presented here refute this separation. They show that K+ channels are in general uptake systems with “low” and “high affinity” components. The analyses clarify that constraints in wet-lab experiments usually mask the “high affinity” component. Consequently, the channels were widely assigned a “low affinity” component, only. The results presented here unmask the absurdity of the concept of “high- and low-affinity” transporters.
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Keywords ion channels; computational cell biology; transport; membrane; mathematical modeling

Citation: Ingo Dreyer. Plant potassium channels are in general dual affinity uptake systems. AIMS Biophysics, 2017, 4(1): 90-106. doi: 10.3934/biophy.2017.1.90

References

  • 1. G. Volkov A, B. Shtessel Y (2016) Propagation of electrotonic potentials in plants: Experimental study and mathematical modeling. AIMS Biophys 3: 358–379.    
  • 2. Hedrich R, Salvador-Recatalà V, Dreyer I (2016) Electrical wiring and long-distance plant communication. Trends Plant Sci 21: 376–387.    
  • 3. Jane Beilby M, Al Khazaaly S (2016) Re-modeling Chara action potential: I. from Thiel model of Ca2+ transient to action potential form. AIMS Biophys 3: 431–449.
  • 4. Hills A, Chen ZH, Amtmann A, et al. (2012) OnGuard, a computational platform for quantitative kinetic modeling of guard cell physiology. Plant Physiol 159: 1026–1042.    
  • 5. Blatt MR, Wang Y, Leonhardt N, et al. (2014) Exploring emergent properties in cellular homeostasis using OnGuard to model K+ and other ion transport in guard cells. J Plant Physiol 171: 770–778.    
  • 6. Gajdanowicz P, Michard E, Sandmann M, et al. (2011) Potassium (K+) gradients serve as a mobile energy source in plant vascular tissues. Proc Natl Acad Sci USA 108: 864–869.    
  • 7. Foster KJ, Miklavcic SJ (2015) Toward a biophysical understanding of the salt stress response of individual plant cells. J Theor Biol 385: 130–142.    
  • 8. Schott S, Valdebenito B, Bustos D, et al. (2016) Cooperation through Competition-Dynamics and Microeconomics of a Minimal Nutrient Trade System in Arbuscular Mycorrhizal Symbiosis. Front Plant Sci 7: 912.
  • 9. Epstein E, Rains DW, Elzam OE (1963) Resolution of dual mechanisms of potassium absorption by barley roots. Proc Natl Acad Sci USA 49: 684–692.    
  • 10. Hille B (2001) Ion channels of excitable membranes, 3rd Ed., Sunderland, MA: Sinauer.
  • 11. Gajdanowicz P, Garcia-Mata C, Gonzalez W, et al. (2009) Distinct roles of the last transmembrane domain in controlling Arabidopsis K+ channel activity. New Phytol 182: 380–391.    
  • 12. Riedelsberger J, Sharma T, Gonzalez W, et al. (2010) Distributed structures underlie gating differences between the K in channel KAT1 and the Kout channel SKOR. Mol Plant 3: 236–245.    
  • 13. Garcia-Mata C, Wang J, Gajdanowicz P, et al. (2010) A minimal cysteine motif required to activate the SKOR K+ channel of arabidopsis by the reactive oxygen species H2O2. J Biol Chem 285: 29286–29294.    
  • 14. González W, Riedelsberger J, Morales-Navarro SE, et al. (2012) The pH sensor of the plant K+-uptake channel KAT1 is built from a sensory cloud rather than from single key amino acids. Biochem J 442: 57–63.    
  • 15. Lefoulon C, Karnik R, Honsbein A, et al. (2014) Voltage-sensor transitions of the inward-rectifying K+ channel kat1 indicate a latching mechanism biased by hydration within the voltage sensor. Plant Physiol 166: 960–975.    
  • 16. Hedrich R, Bregante M, Dreyer I, et al. (1995) The voltage-dependent potassium-uptake channel of corn coleoptiles has permeation properties different from other K+ channels. Planta 197: 193–199.
  • 17. Hedrich R, Moran O, Conti F, et al. (1995) Inward rectifier potassium channels in plants differ from their animal counterparts in response to voltage and channel modulators. Eur Biophys J 24: 107–115.
  • 18. Becker D, Dreyer I, Hoth S, et al. (1996) Changes in voltage activation, Cs+ sensitivity, and ion permeability in H5 mutants of the plant K+ channel KAT1. Proc Natl Acad Sci USA 93: 8123–8128.    
  • 19. Dreyer I, Antunes S, Hoshi T, et al. (1997) Plant K+ channel α-subunits assemble indiscriminately. Biophys J 72: 2143–2150.    
  • 20. Dietrich P, Dreyer I, Wiesner P, et al. (1998) Cation sensitivity and kinetics of guard-cell potassium channels differ among species. Planta 205: 277–287.    
  • 21. Dreyer I, Becker D, Bregante M, et al. (1998) Single mutations strongly alter the K+-selective pore of the K(in) channel KAT1. FEBS Lett 430: 370–376.    
  • 22. Brüggemann L, Dietrich P, Dreyer I, et al. (1999) Pronounced differences between the native K+ channels and KAT1 and KST1 alpha-subunit homomers of guard cells. Planta 207: 370–376.    
  • 23. Dreyer I, Michard E, Lacombe B, et al. (2001) A plant Shaker-like K+ channel switches between two distinct gating modes resulting in either inward-rectifying or "leak" current. FEBS Lett 505: 233–239.    
  • 24. Michard E, Lacombe B, Porée F, et al. (2005) A unique voltage sensor sensitizes the potassium channel AKT2 to phosphoregulation. J Gen Physiol 126: 605–617.    
  • 25. Michard E, Dreyer I, Lacombe B, et al. (2005) Inward rectification of the AKT2 channel abolished by voltage-dependent phosphorylation. Plant J 44: 783–797.    
  • 26. Xicluna J, Lacombe B, Dreyer I, et al. (2007) Increased functional diversity of plant K+ channels by preferential heteromerization of the Shaker-like subunits AKT2 and KAT2. J Biol Chem 282: 486–494.    
  • 27. Geiger D, Becker D, Vosloh D, et al. (2009) Heteromeric AtKC1.AKT1 channels in Arabidopsis roots facilitate growth under K+-limiting conditions. J Biol Chem 284: 21288–21295.
  • 28. Held K, Pascaud F, Eckert C, et al. (2011) Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex. Cell Res 21: 1116–1130.    
  • 29. Garriga M, Raddatz N, Véry AA, et al. (2017) Cloning and functional characterization of HKT1 and AKT1 genes of Fragaria spp.-Relationship to plant response to salt stress. J Plant Physiol 210: 9–17.
  • 30. Dreyer I, Müller-Röber B, Köhler B (2004) Voltage gated ion channels, Blatt MR, Annual Plant Reviews, Membrane Transport in Plants, Oxford: Blackwell Publishing, 150–192.
  • 31. Eyring H (1935) The activated complex in chemical reactions. J Chem Phys 3: 107.    
  • 32. Dreyer I, Blatt MR (2009) What makes a gate? The ins and outs of Kv-like K+ channels in plants. Trends Plant Sci 14: 383–390.
  • 33. Sharma T, Dreyer I, Riedelsberger J (2013) The role of K(+) channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana. Front Plant Sci 4: 224.
  • 34. Sharma T, Dreyer I, Kochian L, et al. (2016) The ALMT family of organic acid transporters in plants and their involvement in detoxification and nutrient security. Front Plant Sci 7: 1488.
  • 35. Loew LM, Schaff JC (2001) The Virtual Cell: a software environment for computational cell biology. Trends Biotechnol 19: 401–406.    
  • 36. Brüggemann L, Dietrich P, Becker D, et al. (1999) Channel-mediated high-affinity K+ uptake into guard cells from Arabidopsis. Proc Natl Acad Sci USA 96: 3298–3302.    

 

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