Skip to main content
Log in

Polar-localised poplar K+ channel capable of controlling electrical properties of wood-forming cells

  • Rapid Communication
  • Published:
Planta Aims and scope Submit manuscript

Abstract

In previous studies, we have shown that annual expression profiles of cambial and wood tissue with respect to the Shaker K+ channel PTORK correlate with cambial activity. To follow PTORK-gene activity on the cellular level, we isolated the respective promoter regions and generated transgenic Arabidopsis plants expressing the GUS gene under the control of the PTORK promoter. Cross-sections of petioles showed PTORK-driven signals predominantly in the xylem parenchyma surrounding the vessels and in the phloem. Antibodies raised against a unique N-terminal region of PTORK in histo-immunochemical analyses recognised this K+-release channel in growth-active poplar plants only. PTORK labelling was found in differentiating xylem cells (young fibres) and mature xylem (vessel-associated cells of the ray parenchyma). Patch-clamp measurements on fibre cell protoplasts, derived from young poplar twigs, identified outward-rectifying K+ channels as the major K+ conductance of this cell type, which resembled the biophysical properties of PTORK when expressed in Xenopus oocytes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

GUS:

β-Glucuronidase

RCF:

Relative centrifugal field

SDS-PAGE:

Sodiumdodecylsulfate-polyacrylamide-gel-electrophoresis

References

  • Ache P, Becker D, Ivashikina N, Dietrich P, Roelfsema MRG, Hedrich R (2000) GORK, a delayed outward rectifier expressed in guard cells of Arabidopsis thaliana, is a K+-selective, K+-sensing ion channel. FEBS Lett 486:93–98

    Article  PubMed  CAS  Google Scholar 

  • Ache P, Becker D, Deeken R, Dreyer I, Weber H, Fromm J, Hedrich R (2001) VFK1, a Vicia faba K+ channel involved in phloem unloading. Plant J 27:571–580

    Article  PubMed  CAS  Google Scholar 

  • Arend M, Fromm J (2003) Ultrastructural changes in cambial cell derivatives during xylem differentiation in poplar. Plant Biol 5:255–264

    Article  Google Scholar 

  • Arend M, Weisenseel MH, Brummer M, Osswald W, Fromm J (2002) Seasonal changes of plasma membrane H+-ATPase and endogenous ion current during growth in poplar plants. Plant Physiol 129:1651–1663

    Article  PubMed  CAS  Google Scholar 

  • Arend M, Monshausen G, Wind C, Weisenseel H, Fromm J (2004) Effect of potassium deficiency on the plasma membrane H+-ATPase of the wood ray parenchyma in poplar. Plant Cell Environ 27:1288–1296

    Article  CAS  Google Scholar 

  • Becker D, Dreyer I, Hoth S, Reid JD, Busch H, Lehnen M, Palme K, Hedrich R (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

    Article  PubMed  CAS  Google Scholar 

  • Becker D, Hoth S, Ache P, Wenkel S, Roelfsema MRG, Meyerhoff O, Hartung W, Hedrich R (2003) Regulation of the ABA-sensitive Arabidopsis potassium channel gene GORK in response to water stress. FEBS Lett 554:119–126

    Article  PubMed  CAS  Google Scholar 

  • Carpaneto A, Geiger D, Bamberg E, Sauer N, Fromm J, Hedrich R (2005) Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under control of sucrose gradient and pmf. J Biol Chem 280: 21437–21443

    Article  PubMed  CAS  Google Scholar 

  • Chaffey N (1999) Cambium: old challenges–new opportunities. Trees 13:138–151

    Article  Google Scholar 

  • Claussen M, Lüthen H, Blatt M, Böttger M (1997) Auxin-induced growth and its linkage to potassium channels. Planta 201:227–234

    Article  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Costa A, Carpaneto A, Varotto S, Formentin E, Marin O, Barizza E, Terzi M, Gambale F, Lo Schiavo F (2004) Potassium and carrot embryogenesis: are K+ channels necessary for development? Plant Mol Biol 54:837–852

    Article  PubMed  CAS  Google Scholar 

  • Deeken R, Sanders C, Ache P, Hedrich R (2000) Developmental and light-dependent regulation of a phloem localised K+ channel of Arabidopsis thaliana. Plant J 23:285–290

    Article  PubMed  CAS  Google Scholar 

  • Deeken R, Fromm J, Koroleva O, Ache P, Langenfeld-Heyser R, Geiger D, Sauer N, May S, Hedrich R (2002) Loss of the AKT2/3 potassium channel affects sugar loading into the phloem of Arabidopsis. Planta 216:334–344

    Article  PubMed  CAS  Google Scholar 

  • Dünisch O, Bauch J (1994a) Influence of mineral elements on wood formation of old growth spruce (Picea abies L. Karst.). Holzforschung 48:5–14

    Google Scholar 

  • Dünisch O, Bauch J (1994b) Influence of soil substrate and drought on wood formation of spruce (Picea abies L. Karst.) under controlled conditions. Holzforschung 48:447–457

    Google Scholar 

  • Dünisch O, Bauch J, Müller M, Greis O (1998) Subcellular quantitative determination of K and Ca in phloem, cambium, and xylem cells of spruce (Picea abies L. Karst.) during earlywood and latewood formation. Holzforschung 52:582–588

    Google Scholar 

  • Ehrhardt T, Zimmermann S, Müller-Röber B (1997) Association of plant K+ (in) channels is mediated by conserved C-termini and does not affect subunit assembly. FEBS Lett 409:166–170

    Article  PubMed  CAS  Google Scholar 

  • Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferriere N, Thibaud J-B, Sentenac H (1998) Identification and disruption of a plant Shaker-like outward channel involved in K+ release into the xylem sap. Cell 94:647–655

    Article  PubMed  CAS  Google Scholar 

  • Giaquinta R (1980) Mechanism and control of phloem loading of sucrose. Ber Deutsch Bot Ges 93:187–201

    CAS  Google Scholar 

  • Himpkamp J (1988) Nachweis und Charakterisierung eines H+ / Glucose-Cotransportsystems in den Holzstrahlen von Populus balsamifera (Saliacae) und seine jahreszeitliche Veränderung. Dissertation, Christian Albrecht Universität

  • Höll W (2000) Distribution, fluctuation and metabolism of food reserves in the wood of trees. In: Savidge RA, Barnett JR, Napier R (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers, Oxford, pp 347–362

    Google Scholar 

  • Hsiao TC, Läuchli A (1986) Role of potassium in plant water relations. In: Tinker B, Läuchli A (eds) Advances in plant nutrition, vol 2. Praeger Scientific, New York, pp 281–312

  • Ivashikina N, Becker D, Ache P, Meyerhoff O, Felle HH, Hedrich R (2001) K+ channel profile and electrical properties of Arabidopsis root hairs. FEBS Lett 508:463–469

    Article  PubMed  CAS  Google Scholar 

  • Kuhn AJ, Schröder WH, Bauch J (1997) On the distribution and transport of mineral elements in xylem, cambium and phloem of spruce (Picea abies L. Karst.). Holzforschung 51:487–496

    CAS  Google Scholar 

  • Laemmeli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277:680–685

    Article  Google Scholar 

  • Langer K, Ache P, Geiger D, Stinzing A, Arend M, Wind C, Regan S, Fromm J, Hedrich R (2002) Poplar potassium transporters capable of controlling K+ homeostasis and K+-dependent xylogenesis. Plant J 32:997–1009

    Article  PubMed  CAS  Google Scholar 

  • Langer K, Levchenko V, Fromm J, Geiger D, Steinmeyer R, Lautner S, Ache P, Hedrich R (2004) The poplar K+ channel KPT1 is associated with K+ uptake during stomatal opening and bud development. Plant J 37:828–838

    Article  PubMed  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, San Diego, p 889

    Google Scholar 

  • Peuke AD, Jeschke WD, Hartung W (2002) Flows of elements, ions and abscisic acid in Rhicinus communis and site of nitrate reduction under potassium limitation. J Exp Bot 53:241–250

    Article  PubMed  CAS  Google Scholar 

  • Philippar K, Fuchs I, Lüthen H, Hoth S, Bauer CS, Haga K, Thiel G, Ljung K, Sandberg G, Böttger M, Becker D, Hedrich R (1999) Auxin-induced K+ channel expression represents an essential step in coleoptil growth and gravitropism. Proc Natl Acad Sci USA 96:12186–12191

    Article  PubMed  CAS  Google Scholar 

  • Philippar K, Büchsenschütz K, Abshagen M, Fuchs I, Geiger D, Lacombe B, Hedrich R (2003) The K+ channel KZM1 is capable to mediate potassium uptake into the phloem and guard cells of the C4 grass Zea mays. J Biol Chem 278:16973–16981

    Article  PubMed  CAS  Google Scholar 

  • Reintanz B, Ivashikina N, Szyroki A, Ache P, Godde M, Becker D, Palme K, Hedrich R (2002) AtKC1, a silent Arabidopsis potassium channel α-subunit modulates root hair K+ influx. Proc Natl Acad Sci USA 99:4079–4048

    Article  PubMed  CAS  Google Scholar 

  • Sauter J (2000) Photosynthate allocation to the vascular cambium: facts and problems. In: Savidge RA, Barnett JR, Napier R (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers, Oxford, pp 71–83

    Google Scholar 

  • Van Bel AJE (1990) Xylem–phloem exchange via the rays: the undervalued route of transport. J Exp Bot 41:631–644

    Article  Google Scholar 

  • Wind C, Arend M, Fromm J (2004) Potassium-dependent cambial growth in poplar. Plant Biol 6:30–37

    Article  PubMed  CAS  Google Scholar 

  • Wright JP, Fischer DB (1981) Measurement of sieve tube membrane potential. Plant Physiol 67:845–848

    Article  PubMed  CAS  Google Scholar 

  • Wullschleger SD, Jansson S, Taylor G (2002) Genomics and forest biology: Populus emerges as the perennial favorite. Plant Cell 14:2651–2655

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants of the Deutsche Forschungsgemeinschaft to the German Poplar Research Group. Thanks to D. Becker for helpful comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rainer Hedrich.

Additional information

Matthias Arend and Andrea Stinzing contributed equally to this work

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Arend, M., Stinzing, A., Wind, C. et al. Polar-localised poplar K+ channel capable of controlling electrical properties of wood-forming cells. Planta 223, 140–148 (2005). https://doi.org/10.1007/s00425-005-0122-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-005-0122-y

Keywords

Navigation