Skip to main content
Springer Nature Link
Log in

Guard cells undergo constitutive and pressure-driven membrane turnover

  • Published:
Protoplasma Aims and scope Submit manuscript

Summary.

During stomatal movement, guard cells undergo large and reversible changes in cell volume and consequently surface area. These alterations in surface area require addition and removal of plasma membrane material. How this is achieved is largely unknown. Here we summarize recent studies of membrane turnover in guard cells using electrophysiology and fluorescent imaging techniques. The results implicate that membrane turnover in guard cells and most likely in plant cells in general is sensitive to changes in membrane tension. We suggest that this provides a mechanism for the adaptation of surface area of guard cells to osmotically driven changes in cell volume. In addition, guard cells also exhibit constitutive membrane turnover. Constitutive and pressure-driven membrane turnover were found to be associated with addition and removal of K+ channels. This implies that some of the exo- and endocytic vesicles carry K+ channels. Together the results demonstrate that exo- and endocytosis is an essential process in guard cell functioning.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • M Barth SEH Holstein (2004) ArticleTitleIdentification and functional characterization of Arabidopsis AP180, a binding partner of plant αC-adaptin. J Cell Sci 117 2051–2062 Occurrence Handle10.1242/jcs.01062 Occurrence Handle1:CAS:528:DC%2BD2cXksVyrsrs%3D Occurrence Handle15054111

    Article  CAS  PubMed  Google Scholar 

  • I Bick G Thiel U Homann (2001) ArticleTitleCytochalasin D attenuates the desensitisation of pressure-stimulated vesicle fusion in guard cell protoplasts. Eur J Cell Biol 80 521–526 Occurrence Handle10.1078/0171-9335-00189 Occurrence Handle1:CAS:528:DC%2BD3MXns1KitLs%3D Occurrence Handle11561903

    Article  CAS  PubMed  Google Scholar 

  • S Bolte C Talbot Y Boutte O Catrice ND Read B Satiat-Jeunemaitre (2004a) ArticleTitleFM dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J Microsc 214 159–173 Occurrence Handle10.1111/j.0022-2720.2004.01348.x Occurrence Handle1:CAS:528:DC%2BD2cXksFOlt7Y%3D

    Article  CAS  Google Scholar 

  • – Brown S, Satiat-Jeunemaitre B (2004b) The N-myristoylated Rab-GTPase m-Rabmc is involved in post-Golgi trafficking events to the lytic vacuole in plant cells. J Cell Sci 117: 943–954

    Google Scholar 

  • F Brandizzi N Frangne S Marc-Martin C Hawes JM Neuhaus N Paris (2002) ArticleTitleThe destination for single-pass membrane proteins is influenced markedly by the length of the hydrophobic domain. Plant Cell 14 1077–1092 Occurrence Handle1:CAS:528:DC%2BD38XksVGqtr0%3D Occurrence Handle12034898

    CAS  PubMed  Google Scholar 

  • Claessens MMAE (2003) Size regulation and stability of charged lipid vesicles. PhD thesis, Wageningen University, Wageningen, The Netherlands

  • W Diekmann R Hedrich K Raschke DG Robinson (1993) ArticleTitleOsmocytosis and vacuolar fragmentation in guard cell protoplasts: their relevance to osmotically-induced volume changes in gurad cells. J Exp Bot 44 1569–1577

    Google Scholar 

  • E Farge PF Devaux (1992) ArticleTitleShape changes of giant liposomes induced by an asymmetric transmembrane distribution of phospholipids. Biophys J 61 347–357 Occurrence Handle1:CAS:528:DyaK38XhsVKnsbk%3D Occurrence Handle1547324

    CAS  PubMed  Google Scholar 

  • – Ojcius DM, Subtil A, Dautry-Varsat A (1999) Enhancement of endocytosis due to aminophospholipid transport across the plasma membrane of living cells. Am J Physiol 276: 725–733

    Google Scholar 

  • MGJ Ford IG Mills BJ Peter Y Vallis GJK Praefcke PR Evans HAT McMahon (2002) ArticleTitleCurvature of clathrin-coated pits driven by epsin. Nature 419 361–366 Occurrence Handle10.1038/nature01020 Occurrence Handle1:CAS:528:DC%2BD38XntlGgsLc%3D Occurrence Handle12353027

    Article  CAS  PubMed  Google Scholar 

  • D Gradmann DG Robinson (1989) ArticleTitleDoes turgor prevent endocytosis in plant cells? Plant Cell Environ 12 151–154

    Google Scholar 

  • M Hao FR Maxfield (2000) ArticleTitleCharacterization of rapid membrane internalization and recycling. J Biol Chem 275 15279–15286 Occurrence Handle10.1074/jbc.275.20.15279 Occurrence Handle1:CAS:528:DC%2BD3cXjsFamsro%3D Occurrence Handle10809763

    Article  CAS  PubMed  Google Scholar 

  • SEH Holstein (2002) ArticleTitleClathrin and plant endocytosis. Traffic 3 614–620 Occurrence Handle10.1034/j.1600-0854.2002.30903.x Occurrence Handle1:CAS:528:DC%2BD38XmslSrsrk%3D Occurrence Handle12191013

    Article  CAS  PubMed  Google Scholar 

  • U Homann (1998) ArticleTitleFusion and fission of plasma-membrane material accommodates for osmotically induced changes in the surface area of guard cell protoplasts. Planta 206 329–333 Occurrence Handle10.1007/s004250050408 Occurrence Handle1:CAS:528:DyaK1cXltlKhs7g%3D

    Article  CAS  Google Scholar 

  • – Thiel G (1999) Unitary exocytotic and endocytotic events in guard-cell protoplasts during osmotically driven volume changes. FEBS Lett 460: 495–499

    Google Scholar 

  • – – (2002) The number of K+ channels in the plasma membrane of guard cell protoplasts changes in parallel with the surface area. Proc Natl Acad Sci USA 99: 10215–10220

  • AC Hurst T Meckel S Tayefeh G Thiel U Homann (2004) ArticleTitleTrafficking of the plant potassium inward rectifier KAT1 in guard cell protoplasts of Vicia faba. Plant J 37 391–397 Occurrence Handle10.1046/j.1365-313X.2003.01972.x Occurrence Handle1:CAS:528:DC%2BD2cXhvFejtrw%3D Occurrence Handle14731259

    Article  CAS  PubMed  Google Scholar 

  • U Kubitscheck U Homann G Thiel (2000) ArticleTitleOsmotic evoked shrinking of guard cell protoplasts causes retrieval of plasma membrane into the cytoplasm. Planta 210 423–431 Occurrence Handle1:CAS:528:DC%2BD3cXhtVKisbo%3D Occurrence Handle10750900

    CAS  PubMed  Google Scholar 

  • D Lambrechts JI Schroeder JP Verbelen (1992) ArticleTitleThe influence of osmolarity on the surface properties of the plasma membrane of isolated guard cell protoplasts from Vicia faba L. Plant Physiol (Life Sci Adv) 11 25–32

    Google Scholar 

  • T Meckel AC Hurst G Thiel U Homann (2004) ArticleTitleEndocytosis against high turgor: intact guard cells of Vicia faba constitutively endocytose fluorescently labelled plasma membrane and GFP-tagged K-channel KAT1. Plant J 39 182–193 Occurrence Handle10.1111/j.1365-313X.2004.02119.x Occurrence Handle1:CAS:528:DC%2BD2cXntFGrt78%3D Occurrence Handle15225284

    Article  CAS  PubMed  Google Scholar 

  • CE Morris U Homann (2001) ArticleTitleCell surface area regulation and membrane tension. J Membr Biol 179 79–102 Occurrence Handle1:CAS:528:DC%2BD3MXjvFGhu7w%3D Occurrence Handle11220366

    CAS  PubMed  Google Scholar 

  • SA Mousavi L Malerod T Berg R Kjeken (2004) ArticleTitleClathrin-dependent endocytosis. Biochem J 377 1–16 Occurrence Handle10.1042/BJ20031000 Occurrence Handle1:CAS:528:DC%2BD2cXis1Sqtw%3D%3D Occurrence Handle14505490

    Article  CAS  PubMed  Google Scholar 

  • S Mukherjee TT Soe FR Maxfield (1999) ArticleTitleEndocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails. J Cell Biol 44 1271–1284

    Google Scholar 

  • R Nossal (2001) ArticleTitleEnergetics of clathrin basket assembly. Traffic 2 138–147 Occurrence Handle10.1034/j.1600-0854.2001.020208.x Occurrence Handle1:STN:280:DC%2BD3MvotlCgsA%3D%3D Occurrence Handle11247304

    Article  CAS  PubMed  Google Scholar 

  • KJ Oparka DAM Prior N Harris (1990) ArticleTitleOsmotic induction of fluid-phase endocytosis in onion epidermal cells. Planta 180 555–561

    Google Scholar 

  • T Pomorski JCM Holthuis A Herrmann G van Meer (2004) ArticleTitleTracking down lipid flippases and their biological functions. J Cell Sci 117 805–813 Occurrence Handle10.1242/jcs.01055 Occurrence Handle1:CAS:528:DC%2BD2cXis1akt7Y%3D Occurrence Handle14963021

    Article  CAS  PubMed  Google Scholar 

  • JL Ramsay KL Koster (2002) ArticleTitleA comparison of anhydrous fixation methods for the observation of pea embryonic axes (Pisum sativum L. cv. Alaska). Seed Sci Res 12 83–90

    Google Scholar 

  • Raschke K (1979) Movements of stomata. In: Haupt W, Feinleb ME (eds) Physiology of movements. Springer, Berlin, pp 382–441 (Pirson A, Zimmermann MH [eds] Encyclopedia of plant physiology, vol 7)

  • C Rauch E Farge (2000) ArticleTitleEndocytosis switch controlled by transmembrane osmotic pressure and phospholipid number asymmetry. Biophys J 78 3036–3047 Occurrence Handle1:CAS:528:DC%2BD3cXjvFOgsr0%3D Occurrence Handle10827982

    CAS  PubMed  Google Scholar 

  • D Raucher MP Sheetz (1999) ArticleTitleCharacteristics of a membrane reservoir buffering membrane tension. Biophys J 77 1992–2002 Occurrence Handle1:CAS:528:DyaK1MXmtl2msb0%3D Occurrence Handle10512819

    CAS  PubMed  Google Scholar 

  • Robinson DG, Hedrich R, Herkt B, Diekmann W, Robert-Nicoud M (1991) Endocytosis in plants: problems and perspectives. In: Courtoy PJ (ed) Endocytosis. Springer, Berlin, pp 459–466 (NATO ASI series, series H, vol 62)

  • JC Shope DB DeWald KA Mott (2003) ArticleTitleChanges in surface area of intact guard cells are correlated with membrane internalization. Plant Physiol 133 1314–1321 Occurrence Handle10.1104/pp.103.027698 Occurrence Handle1:CAS:528:DC%2BD3sXptFGitbo%3D Occurrence Handle14551331

    Article  CAS  PubMed  Google Scholar 

  • RV Stahelin F Long BJ Peter D Murray P De Camilli HT McMahon W Cho (2003) ArticleTitleContrasting membrane interaction mechanisms of AP180 N-terminal homology (ANTH) and epsin N-terminal homology (ENTH) domains. J Biol Chem 278 28993–28999 Occurrence Handle1:CAS:528:DC%2BD3sXlsl2msL4%3D Occurrence Handle12740367

    CAS  PubMed  Google Scholar 

  • Steponkus PL (1991) Behaviour of the plasma membrane during osmotic excursions. In: Hawes CR, Coleman JOD, Evans DE (eds) Endocytosis, exocytosis and vesicle traffic in plants. Cambridge University Press, Cambridge, pp 103–128

  • M Wartenberg J Hamann I Pratsch E Donath (1992) ArticleTitleOsmotically induced fluid-phase uptake of fluorescent markers by protoplasts of Chenopodium album. Protoplasma 166 61–66 Occurrence Handle10.1007/BF01320144

    Article  Google Scholar 

  • MA Williams M Fukuda (1990) ArticleTitleAccumulation of membrane glycoproteins in lysosomes requires a tyrosine residue at a particular position in the cytoplasmic tail. J Cell Biol 111 955–966 Occurrence Handle10.1083/jcb.111.3.955 Occurrence Handle1:CAS:528:DyaK3cXls1Oms7w%3D Occurrence Handle2391371

    Article  CAS  PubMed  Google Scholar 

  • J Wolfe PL Steponkus (1983) ArticleTitleMechanical properties of the plasma membrane of isolated plant protoplasts. Plant Physiol 71 276–285 Occurrence Handle10.1104/pp.71.2.276 Occurrence Handle16662817

    Article  PubMed  Google Scholar 

  • KM Wright KJ Oparka (1989) ArticleTitleUptake of Lucifer Yellow CH into plant cell protoplasts: a quantitative assessment of fluid-phase endocytosis. Planta 179 257–264 Occurrence Handle10.1007/BF00393697 Occurrence Handle1:CAS:528:DyaL1MXlvFSktLo%3D

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Botany, Darmstadt University of Technology, Darmstadt

    T. Meckel, A. C. Hurst, G. Thiel & U. Homann

Authors
  1. T. Meckel
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. A. C. Hurst
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. G. Thiel
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. U. Homann
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to U. Homann.

Additional information

Correspondence and reprints: Institute of Botany, Darmstadt University of Technology, Schnittspahnstrasse 3, 64287 Darmstadt, Federal Republic of Germany.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meckel, T., Hurst, A., Thiel, G. et al. Guard cells undergo constitutive and pressure-driven membrane turnover. Protoplasma 226, 23–29 (2005). https://doi.org/10.1007/s00709-005-0106-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-005-0106-6