Skip to main content
SpringerLink
Log in

Dynamin-Related Proteins in Plant Endocytosis

  • Chapter
  • First Online:
Book cover Plant Endocytosis

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 1))

Abstract

Over the past decade, it has become evident that multiple endocytic pathways operate in eukaryotic cells, and several of these are dependent on dynamins and dynamin-related proteins (DRPs). Many members of the DRP superfamily possess the ability to self-assemble into long spiral polymers that wrap around lipid bilayers and thus facilitate tubulation and vesicle pinching from the plasma membrane and other membrane compartments, a process that is fundamental for endocytosis. Here, we discuss the roles of dynamins and DRPs in plants. DRPs have been shown to be present at different subcellular locations in plant cells including the cell plate, plasma membrane, Golgi apparatus, vesicles, mitochondria, chloroplasts, and peroxisomes. Arabidopsis contains 16 DRP members that are grouped into six functional subfamilies (DRP1--6) on the basis of their phylogeny and the presence of functional motifs. Members of the DRP1 subfamily are closest to soybean phragmoplastin and mediate membrane tubulation at the cell plate. The DRP2 subfamily members represent the bona fide plant dynamins characterized by the presence of a pleckstrin homology (PH) domain in the middle of the molecule and a proline-rich (PR) motif near the C-terminus ; they are involved in membrane recycling at the cell plate and the trans-Golgi region. The DRP3 subfamily does not contain PH or PR motifs; their function has been implicated in the division of mitochondria and peroxisomes, whereas the DRP5 subfamily in Arabidopsis is likely to play a role in plastid division. A DRP5 ortholog from the red alga Cyanidioschyzon has recently been shown to be a component of the chloroplast outer division-ring on the cytoplasmic face of the plastid double membrane. Finally, the DRP4 subfamily contains orthologs of the animal antiviral Mx proteins, but their function has not yet been established, and the role of DRP6 is entirely unknown so far. It is obvious that plant cells employ unique DRP subfamilies to carry out the mechanochemical work required for membrane deformation and segregation in various membranous compartments. However, to understand the function of DRPs in further detail, much is yet to be learned about the proteins that apparently interact with them to regulate their activity and specify their functions.

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

Access this chapter

Log in via an institution

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arimura S, Aida GP, Fujimoto M, Nakazono M, Tsutsumi N (2004) Arabidopsis dynamin-like protein 2a (ADL2a), like ADL2b, is involved in plant mitochondrial division. Plant Cell Physiol 45:236–242

    Article  Google Scholar 

  2. Arimura S, Tsutsumi N (2002) A dynamin-like protein (ADL2b), rather than FtsZ, is involved in Arabidopsis mitochondrial division. Proc Natl Acad Sci USA 99:5727–5731

    Article  PubMed  Google Scholar 

  3. Assaad FF, Huet Y, Mayer U, Jurgens G (2001) The cytokinesis gene KEULE encodes a Sec1 protein that binds the syntaxin KNOLLE. J Cell Biol 152:531–543

    Article  PubMed  Google Scholar 

  4. Battey NH, James NC, Greenland AJ, Brownlee C (1999) Exocytosis and endocytosis. Plant Cell 11:643–659

    Article  PubMed  Google Scholar 

  5. Bednarek SY, Falbel TG (2002) Membrane trafficking during plant cytokinesis. Traffic 3:621–629

    Article  PubMed  Google Scholar 

  6. Blackbourn HD, Jackson AP (1996) Plant clathrin heavy chain: sequence analysis and restricted localisation in growing pollen tubes. J Cell Sci 109:777–786

    PubMed  Google Scholar 

  7. Borner GH, Sherrier DJ, Weimar T, Michaelson LV, Hawkins ND, Macaskill A, Napier JA, Beale MH, Lilley KS, Dupree P (2005) Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol 137:104–116

    Article  PubMed  Google Scholar 

  8. Cousin MA, Robinson PJ (2000) Ca2+influx inhibits dynamin and arrests synaptic vesicle endocytosis at the active zone. J Neurosci 20:949–957

    PubMed  Google Scholar 

  9. Dombrowski JE, Raikhel NV (1995) Isolation of a cDNA encoding a novel GTP-binding protein of Arabidopsis thaliana. Plant Mol Biol 28:1121–1126

    Article  PubMed  Google Scholar 

  10. Damke H, Baba T, Warnock DE, Schmid SL (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127:915–934

    Article  PubMed  Google Scholar 

  11. Dong X, Hong Z, Sivaramakrishnan M, Verma DPS (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and pollen viability in Arabidopsis. Plant J 42:315–328

    Article  PubMed  Google Scholar 

  12. Elias M, Drdova E, Ziak D, Bavlnka B, Hala M, Cvrckova F, Soukupova H, Zarsky V (2003) The exocyst complex in plants. Cell Biol Int 27:199–201

    Google Scholar 

  13. Emons AM, Traas JA (1986) Coated pits and coated vesicles on the plasma membrane of plant cells. Eur J Cell Biol 41:57–64

    Google Scholar 

  14. Gao H, Kadirjan-Kalbach D, Froehlich JE, Osteryoung KW (2003) ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc Natl Acad Sci USA 100:4328–4333

    Article  PubMed  Google Scholar 

  15. Geisler-Lee J, Hong Z, Verma DPS (2002) Overexpression of the cell plate-associated dynamin-like GTPase, phragmoplastin, results in the accumulation of callose at the cell plate and arrest of plant growth. Plant Sci 163:33–42

    Article  Google Scholar 

  16. Grigliatti TA, Hall L, Rosenbluth R, Suzuki DT (1973) Temperature-sensitive mutations in Drosophila melanogaster. XIV: A selection of immobile adults. Mol Gen Genet 120:107–114

    Article  PubMed  Google Scholar 

  17. Gu X, Verma DPS (1996) Phragmoplastin, a dynamin-like protein associated with cell plate formation in plants. EMBO J 15:695–704

    PubMed  Google Scholar 

  18. Gu X, Verma DPS (1997) Dynamics of phragmoplastin in living cells during cell plate formation and uncoupling of cell elongation from the plane of cell division. Plant Cell 9:157–169

    Article  PubMed  Google Scholar 

  19. Heese M, Gansel X, Sticher L, Wick P, Grebe M, Granier F, Jurgens G (2001) Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis. J Cell Biol 155:239–249

    Article  PubMed  Google Scholar 

  20. Henley JR, Krueger EW, Oswald BJ, McNiven MA (1998) Dynamin-mediated internalization of caveolae. J Cell Biol 141:85–99

    Article  PubMed  Google Scholar 

  21. Hepler PK, Callaham DA (1987) Free calcium increases during anaphase in stamen hair cells of Tradescantia. J Cell Biol 105:2137–2143

    Article  PubMed  Google Scholar 

  22. Hinshaw JE (2000) Dynamin and its role in membrane fission. Annu Rev Cell Dev Biol 16:483–519

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  24. Hong Z, Bednarek S, Blumwald E, Hwang I, Jurgens G, Menzel D, Osteryoung K, Raikhel N, Shinozaki K, Tsutsumi N, Verma DPS (2003) A unified nomenclature for Arabidopsis dynamin-related large GTPases based on homology and possible functions. Plant Mol Biol 53:261–265

    Article  PubMed  Google Scholar 

  25. Hong Z, Delauney AJ, Verma DPS (2001) A cell plate-specific callose synthase and its interaction with phragmoplastin and UDP-glucose transferase. Plant Cell 13:755–768

    Article  PubMed  Google Scholar 

  26. Hong Z, Geisler-Lee J, Zhang Z, Verma DPS (2003) Phragmoplastin dynamics: multiple forms, microtubule association, and their roles in cell plate formation in plants. Plant Mol Biol 53:297–312

    Article  PubMed  Google Scholar 

  27. Hong Z, Zhang Z, Olson J, Verma DPS (2001) A novel UDP-glucose transferase interacts with callose synthase and phragmoplastin at the forming cell plate. Plant Cell 13:769–779

    Article  PubMed  Google Scholar 

  28. Hsu SC, TerBush D, Abraham M, Guo W (2004) The exocyst complex in polarized exocytosis. Int Rev Cytol 233:243–265

    PubMed  Google Scholar 

  29. Iversen TG, Skretting G, van Deurs B, Sandvig K (2003) Clathrin-coated pits with long, dynamin-wrapped necks upon expression of a clathrin antisense RNA. Proc Natl Acad Sci USA 100:5175–5180

    Article  PubMed  Google Scholar 

  30. Jin JB, Kim YA, Kim SJ, Lee SH, Kim DH, Cheong GW, Hwang I (2001) A new dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis. Plant Cell 13:1511–1526

    Article  PubMed  Google Scholar 

  31. Johannes L, Lamaze C (2002) Clathrin-dependent or not: is it still the question? Traffic 3:443–451

    Article  PubMed  Google Scholar 

  32. Jones SM, Howell KE, Henley JR, Cao H, McNiven MA (1998) Role of dynamin in the formation of transport vesicles from the trans-Golgi network. Science 279:573–577

    Article  PubMed  Google Scholar 

  33. Jurgens G, Geldner N (2002) Protein secretion in plants: from the trans-Golgi network to the outer space. Traffic 3:605–613

    Article  PubMed  Google Scholar 

  34. Kang B, Busse JS, Dickey C, Rancour DM, Bednarek SY (2001) The Arabidopsis cell plate-associated dynamin-like protein, ADL1Ap, is required for multiple stages of plant growth and development. Plant Physiol 126:47–68

    Article  PubMed  Google Scholar 

  35. Kang BH, Busse JS, Bednarek SY (2003) Members of the Arabidopsis dynamin-like gene family, ADL1, are essential for plant cytokinesis and polarized cell growth. Plant Cell 15:899–913

    Article  PubMed  Google Scholar 

  36. Kang BH, Rancour DM, Bednarek SY (2003) The dynamin-like protein ADL1C is essential for plasma membrane maintenance during pollen maturation. Plant J 35:1–15

    Article  PubMed  Google Scholar 

  37. Kang SG, Jing JB, Hai PL, Kyeong P, Hyun JJ, Jeong L, Hwang I (1998) Molecular cloning of an Arabidopsis cDNA encoding a dynamin-like protein that is localized to plastids. Plant Mol Biol 38:437–447

    Article  PubMed  Google Scholar 

  38. Kim YW, Park DS, Park SC, Kim SH, Cheong GW, Hwang I (2001) Arabidopsis dynamin-like 2 that binds specifically to phosphatidylinositol 4-phosphate assembles into a high molecular weight complex in vivo and in vitro. Plant Physiol 127:1243–1255

    Article  PubMed  Google Scholar 

  39. Koenig JH, Ikeda K (1989) Disappearance and re-formation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J Neurosci 9:3844–3860

    PubMed  Google Scholar 

  40. Lai MM, Hong JJ, Ruggiero AM, Burnett PE, Slepnev VI, De Camilli P, Snyder SH (1999) The calcineurin-dynamin 1 complex as a calcium sensor for synaptic vesicle endocytosis. J Biol Chem 274:25963–25966

    Article  PubMed  Google Scholar 

  41. Lam BC, Sage TL, Bianchi F, Blumwald E (2002) Regulation of ADL6 activity by its associated molecular network. Plant J 31:565–576

    Article  PubMed  Google Scholar 

  42. Lamaze C, Dujeancourt A, Baba T, Lo CG, Benmerah A, Dautry-Varsat A (2001) Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol Cell 7:661–671

    Article  PubMed  Google Scholar 

  43. Lauber MH, Waizenegger I, Steinmann T, Schwarz H, Mayer U, Hwang I, Lukowitz W,Jurgens G (1997) The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J Cell Biol 139:1485–1493

    Article  PubMed  Google Scholar 

  44. Lee SH, Jin JB, Song J, Min MK, Park DS, Kim YW, Hwang I (2002) The intermolecular interaction between the PH domain and the C-terminal domain of Arabidopsis dynamin-like 6 determines lipid binding specificity. J Biol Chem 277:31842–31849

    Article  PubMed  Google Scholar 

  45. Logan DC, Scott I, Tobin AK (2004) ADL2a, like ADL2b, is involved in the control of higher plant mitochondrial morphology. J Exp Bot 55:783–785

    Article  PubMed  Google Scholar 

  46. Lukowitz W, Mayer U, Jurgens G (1996) Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84:61–71

    Article  PubMed  Google Scholar 

  47. Mano S, Nakamori C, Kondo M, Hayashi M, Nishimura M (2004) An Arabidopsis dynamin-related protein, DRP3A, controls both peroxisomal and mitochondrial division. Plant J 38:487–498

    Article  PubMed  Google Scholar 

  48. Marks B, Stowell MH, Vallis Y, Mills IG, Gibson A, Hopkins CR, McMahon HT (2001) GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410:231–235

    Article  PubMed  Google Scholar 

  49. McNiven MA (1998) Dynamin: a molecular motor with pinchase action. Cell 94:151–154

    Article  PubMed  Google Scholar 

  50. Mikami K, Iuchi S, Yamaguchi-Shinozaki K, Shinozaki K (2000) A novel Arabidopsis thaliana dynamin-like protein containing the pleckstrin homology domain. J Exp Bot 51:317–318

    Article  PubMed  Google Scholar 

  51. Miyagishima SY, Nishida K, Mori T, Matsuzaki M, Higashiyama T, Kuroiwa H, Kuroiwa T (2003) A plant-specific dynamin-related protein forms a ring at the chloroplast division site. Plant Cell 15:655–665

    Article  PubMed  Google Scholar 

  52. Mongrand S, Morel J, Laroche J, Claverol S, Carde JP, Hartmann MA, Bonneu M, Simon-Plas F, Lessire R, Bessoule JJ (2004) Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. J Biol Chem 279:36277–36286

    Article  PubMed  Google Scholar 

  53. Nishida K, Takahara M, Miyagishima SY, Kuroiwa H, Matsuzaki M, Kuroiwa T (2003) Dynamic recruitment of dynamin for final mitochondrial severance in a primitive red alga. Proc Natl Acad Sci USA 100:2146–2151

    Article  PubMed  Google Scholar 

  54. Obar RA, Collins CA, Hammarback JA, Shpetner HS, Vallee RB (1990) Molecular cloning of the microtubule-associated mechanochemical enzyme dynamin reveals homology with a new family of GTP-binding proteins. Nature 347:256–261

    Article  PubMed  Google Scholar 

  55. Oh P, McIntosh DP, Schnitzer JE (1998) Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J Cell Biol 141:101–114

    Article  PubMed  Google Scholar 

  56. Otegui MS, Staehelin LS (2004) Electron tomographic analysis of post-meiotic cytokinesis during pollen development in Arabidopsis thaliana. Planta 218:501–515

    Article  PubMed  Google Scholar 

  57. Otegui MS, Mastronarde DN, Kang B, Bednarek SY, Staehelin LA (2001) Three-dimensional analysis of cellularization visualized by high-resolution electron tomography. Plant Cell 13:2033–2051

    Article  PubMed  Google Scholar 

  58. Park JM, Cho JH, Kang SG, Jang HJ, Pih KT, Piao HL, Cho MJ, Hwang I (1998) A dynamin-like protein in Arabidopsis thaliana is involved in biogenesis of thylakoid membranes. EMBO J 17:859–867

    Article  PubMed  Google Scholar 

  59. Peskan T, Westermann M, Oelmuller R (2000) Identification of low-density Triton X-100-insoluble plasma membrane microdomains in higher plants. Eur J Biochem 267:6989–6995

    Article  PubMed  Google Scholar 

  60. Praefcke GJ, McMahon HT (2004) The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 5:133–147

    Article  PubMed  Google Scholar 

  61. Roth TF, Porter KR (1964) Yolk protein uptake in the oocyte of the mosquito Aedes aegypti. L. J Cell Biol 20:313–332

    Article  PubMed  Google Scholar 

  62. Samuels AL, Giddings TH, Staehelin LA (1995) Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 130:1345–1357

    Article  PubMed  Google Scholar 

  63. Schmid SL, McNiven MA, De Camilli P (1998) Dynamin and its partners: a progress report. Curr Opin Cell Biol 10:504–512

    Article  PubMed  Google Scholar 

  64. Segui-Simarro JM, Austin JR II, White EA, Staehelin LA (2004) Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16:836–856

    Article  PubMed  Google Scholar 

  65. Sever S (2002) Dynamin and endocytosis. Curr Opin Cell Biol 14:463–467

    Article  PubMed  Google Scholar 

  66. Slepnev VI, Ochoa GC, Butler MH, Grabs D, De Camilli P (1998) Role of phosphorylation in regulation of the assembly of endocytic coat complexes. Science 281:821–824

    Article  PubMed  Google Scholar 

  67. Surpin M, Raikhel N (2004) Traffic jams affect plant development and signal transduction. Nat Rev Mol Cell Biol 5:1000–1009

    Google Scholar 

  68. Stowell MH (1999) Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nat Cell Biol 1:27–32

    Article  PubMed  Google Scholar 

  69. Sweitzer SM, Hinshaw JE (1998) Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93:1021–1029

    Article  PubMed  Google Scholar 

  70. Takei K, McPherson PS, Schimid S, De Camilli P (1995) Tubular membrane invaginations coated by dynamin rings are induced by GTP-γ-S in nerve terminals. Nature 374:186–190

    Article  PubMed  Google Scholar 

  71. Takei K, Mundigl O, Daniell L, De Camilli P (1996) The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J Cell Biol 133:1237–1250

    Article  PubMed  Google Scholar 

  72. Takei K, Haucke V, Slepnev V, Farsad K, Salazar M, Chen H, De Camilli P (1998) Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell 94:131–141

    Article  PubMed  Google Scholar 

  73. TerBush DR, Maurice T, Roth D, Novick P (1996) The exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J 15:6483–6494

    PubMed  Google Scholar 

  74. Tomizawa K, Sunada S, Lu YF, Oda Y, Kinuta M, Ohshima T, Saito T, Wei FY, Matsushita M, Li ST, Tsutsui K, Hisanaga S, Mikoshiba K, Takei K, Matsui H (2003) Cophosphorylation of amphiphysin I and dynamin I by Cdk5 regulates clathrin-mediated endocytosis of synaptic vesicles. J Cell Biol 163:813–824

    Article  PubMed  Google Scholar 

  75. van der Bliek AM, Meyerowitz EM (1991) Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351:411–414

    Article  PubMed  Google Scholar 

  76. Verma DPS (2001) Cytokinesis and building of the cell plate in plants. Annu Rev Plant Physiol Plant Mol Biol 52:751–784

    Article  PubMed  Google Scholar 

  77. Verma DPS, Hong Z (2001) Plant callose synthase complexes. Plant Mol Biol 47:693–701

    Article  PubMed  Google Scholar 

  78. Verma DPS, Hong Z (2005) The ins and outs in membrane dynamics: tubulation and vesiculation. Trends Plant Sci 10:159–165

    Article  PubMed  Google Scholar 

  79. Volker A, Stierhof YD, Jurgens G (2001) Cell cycle-independent expression of the Arabidopsis cytokinesis-specific syntaxin KNOLLE results in mistargeting to the plasma membrane and is not sufficient for cytokinesis. J Cell Sci 114:3001–3012

    PubMed  Google Scholar 

  80. Wolniak SM, Hepler PK, Jackson WT (1980) Detection of membrane-calcium distribution during mitosis in Haemanthus endosperm with chlortetracycline. J Cell Biol 87:23–32

    Article  PubMed  Google Scholar 

  81. Wyrzykowska J, Fleming A (2003) Cell division pattern influences gene expression in the shoot apical meristem. Proc Natl Acad Sci USA 100:5561–5566

    Article  PubMed  Google Scholar 

  82. Zhang Z, Hong Z, Verma DPS (2000) Phragmoplastin polymerizes into spiral coiled structures via intermolecular interaction of two self-assembly domains. J Biol Chem 275:8779–8784

    Article  PubMed  Google Scholar 

  83. Zheng H, Bednarek SY, Sanderfoot AA, Alonso J, Ecker JR, Raikhel NV (2002) NPSN11 is a cell plate-associated SNARE protein that interacts with the syntaxin KNOLLE. Plant Physiol 129:530–539

    Article  PubMed  Google Scholar 

  84. Yoon Y, Pitts KR, McNiven MA (2001) Mammalian dynamin-like protein DLP1 tubulates membranes. Mol Biol Cell 12:2894–2905

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Genetics and Plant Biotechnology Center, The Ohio State University, 43210, Columbus, OH, USA

    D. P. S. Verma

  2. Plant Biotechnology Center, The Ohio State University, 240 Rightmire Hall, 1060 Carmack Road, 43210, Columbus, OH, USA

    D. P. S. Verma

  3. Department of Microbiology, Molecular Biology, and Biochemistry, University of Idaho, 83844, Moscow, ID, USA

    Z. Hong

  4. Institut für Zelluläre und Molekulare Botanik (IZMB), Abteilung Zellbiologie der Pflanzen, Rheinische Friedrich-Wilhelms-Universität, Kirschallee 1, 53115, Bonn, Germany

    D. Menzel

Authors
  1. D. P. S. Verma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Z. Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Menzel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. P. S. Verma .

Editor information

Jozef Šamaj František Baluška Diedrik Menzel

Rights and permissions

Reprints and permissions

About this chapter

Cite this chapter

Verma, D.P.S., Hong, Z., Menzel, D. Dynamin-Related Proteins in Plant Endocytosis. In: Šamaj, J., Baluška, F., Menzel, D. (eds) Plant Endocytosis. Plant Cell Monographs, vol 1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_013

Download citation

Publish with us

Policies and ethics

Search

Navigation