Receptor-Mediated Endocytosis in Plants

  • Chapter
  • First Online:
Plant Endocytosis

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

  • 226 Accesses

Abstract

Binding of ligands activates cell-surface receptors and triggers a series of signalling events. The activation of the receptors accelerates their internalisation, a process called receptor-mediated endocytosis. Thus, entire receptor--ligand complexes are internalised and processed within the cell. Recent work in a variety of cellular and developmental animal systems further supports the idea that the role of endocytosis extends beyond simply controlling the number of receptors at the cell surface. It has been shown that endocytic transport of the receptor complexes regulates signal transduction and mediates the formation of specialised signalling complexes. Signal transduction events can also modulate specific components of the endocytic machinery. Receptor internalisation in plant cells has recently been demonstrated; however, evidence for receptor-mediated endocytosis in plants is just beginning to emerge. In this review, we highlight the most recent advances in the study of receptor-mediated endocytosis in animals and compare them with what is currently known in plant systems.

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

Access this chapter

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  1. Baluška F, Hlavacka A, Šamaj J, Palme K, Robinson DG, Matoh T, McCurdy DW, Menzel D, Volkmann D (2002) F-actin-dependent endocytosis of cell wall pectins in meristematic root cells. Insights from brefeldin A-induced compartments. Plant Physiol 130:422–431

    Article  PubMed  Google Scholar 

  2. Bolte S, Talbot C, Butte Y, Catrice O, Read ND, Satian-Jeunemaitre B (2004) FM dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J Microsc 214:159–173

    Article  PubMed  MathSciNet  Google Scholar 

  3. Bonifacino JS, Traub LM (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72:395–447

    Article  PubMed  Google Scholar 

  4. Braun DM, Stone JM, Walker JC (1997) Interaction of the maize and Arabidopsis kinase interaction domain with a subset of receptor-like kinases: implications for transmembrane signalling in plants. Plant J 12:83–95

    Article  PubMed  Google Scholar 

  5. Cabrillac D, Cock MJ, Dumas C, Gaude T (2001) The S-locus receptor kinase is inhibited by thioredoxin and activated by pollen coat proteins. Nature 410:220–223

    Article  PubMed  Google Scholar 

  6. Carpenter G (2000) The EGF receptor: a nexus for trafficking and signaling. BioEssays 22:697–707

    Article  PubMed  Google Scholar 

  7. Clouse SD (2002) Brassinosteroid signal transduction: clarifying the pathway from ligand perception to gene expression. Mol Cell 10:973–982

    Article  PubMed  Google Scholar 

  8. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL (2003) Distinct endocytic pathways regulate TGF-βreceptor signalling and turnover. Nat Cell Biol 5:410–421

    Article  PubMed  Google Scholar 

  9. Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:805–809

    Google Scholar 

  10. Geldner N (2004) The plant endosomal system–-its structure and role in signal transduction and plant development. Planta 219:547–560

    Article  PubMed  Google Scholar 

  11. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM AFR-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112:219–230

    Article  PubMed  Google Scholar 

  12. Geldner N, Friml J, Stierhof Y-D, Jurgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428

    Article  PubMed  Google Scholar 

  13. Gifford ML, Dean S, Ingram GC (2003) The Arabidopsis ACR4 gene plays a role in cell layer organisation during the ovule integument and sepal margin development. Development 130:4249–4258

    Article  PubMed  Google Scholar 

  14. Gifford ML, Robertson F, Soares DC, Ingram GC (2005) ACR4 function, internalisation and turnover are dependent on the extracellular crinkly repeat domain. Plant Cell 17:1154–1166

    Article  PubMed  Google Scholar 

  15. Gómez-Gómez L, Bauer Z, Boller T (2001) Both the extracellular leucine-rich repeat domain and the kinase activity of FLS2 are required for flagellin binding and signalling in Arabidopsis. Plant Cell 13:1155–1163

    Article  PubMed  Google Scholar 

  16. Gonzáles-Gaitán M (2003) Signal dispersal and transduction through the endocytic pathway. Nat Rev Mol Cell Biol 4:213–224

    Article  PubMed  Google Scholar 

  17. Grebe M, Xu J, Möbius W, Ueda T, Nakano A, Geuze HJ, Rook MB, Scheres B (2003) Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr Biol 13:1378–1387

    Article  PubMed  Google Scholar 

  18. Gu T, Mazzurco M, Sulaman W, Matias DD, Goring DR (1998) Bindings of a novel arm repeat protein to the kinase domain of the S-locus receptor kinase. Proc Natl Acad Sci USA 97:3759–3764

    Google Scholar 

  19. Haffani YZ, Silva NF, Goring DR (2004) Receptor kinase signalling in plants. Can J Bot 82:1–15

    Article  Google Scholar 

  20. Haj FG, Verveer PJ, Squire A, Neel BG, Bastiaens PIH (2002) Imaging sites of receptor dephosphorylation by PTP1B on the surface of the endoplasmic reticulum. Science 295:1708–1711

    Article  PubMed  Google Scholar 

  21. Happel N, Höning S, Neuhaus J-M, Paris N, Robinson DG, Holstein SEH (2004) Arabidopsis μA-adaptin interacts with the tyrosine motif of the vacuolar sorting receptor VSR-PS1. Plant J 37:678–693

    Article  PubMed  Google Scholar 

  22. Holler D, Volarevic S, Dikic I (2005) Compartmentalization of growth factor receptor signalling. Curr Opin Cell Biol 17:1–5

    Article  Google Scholar 

  23. Holstein SEH (2002) Clathrin and plant endocytosis. Traffic 3:614–620

    Article  PubMed  Google Scholar 

  24. Holstein SEH (2005) Molecular dissection of the clathrin endocytosis machinery in plants (in this volume). Springer, Berlin Heidelberg New York

    Google Scholar 

  25. Horn MA, Heinstein PF, Low PS (1989) Receptor-mediated endocytosis in plant cells. Plant Cell 1:1003–1009

    Article  PubMed  Google Scholar 

  26. Jürgens G (2004) Membrane trafficking in plants. Annu Rev Cell Dev Biol 20:481–504

    Article  PubMed  Google Scholar 

  27. Katzmann DJ, Odorizzi G, Emr SD (2002) Receptor downregulation and multivesicular-body sorting. Nat Rev Mol Cell Biol 3:893–905

    Article  PubMed  Google Scholar 

  28. Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ, Fischer R, Prüfer D (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci USA 98:6511–6515

    Article  PubMed  Google Scholar 

  29. Kim M, Cho H, Kim DO-M, Lee J, Pai H-S (2003) CHRK1, a chitinase-related receptor-like kinase, interacts with NtPUB4, an armadillo repeat protein in tobacco. Biochem Biophys Acta 1651:50–59

    Google Scholar 

  30. Kinoshita T, Cano-Delgado A, Seto H, Hiranuma S, Fujioka S, Yoshida S, Chory J (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433:167–171

    Article  PubMed  Google Scholar 

  31. Kurten RC (2003) Sorting motifs in receptor trafficking. Adv Drug Del Rev 55:1405–1419

    Article  Google Scholar 

  32. Kurten RC, Eddington AD, Chowdhury P, Smith RD, Davidson AD, Shank B (2001) Self-assembly and binding of a sorting nexin to sorting endosomes. J Cell Sci 114:1743–1756

    PubMed  Google Scholar 

  33. Kwaaitaal MACJ, de Vries SC, Russinova E (2005) The Arabidopsis somatic embryogenesis receptor kinase 1 protein is present in sporophytic and gametophytic cells and undergoes endocytosis. Protoplasma 221:394–405

    Google Scholar 

  34. Levkowitz G, Waterman H, Zamir E, Kam Z, Oved S, Langdom WY, Beguinot L, Geiger B, Yarden Y (1998) C-Cbl=Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Gen Dev 12:3663–3674

    Google Scholar 

  35. Li J (2003) Brassinosteroids signal through two receptor-like kinases. Curr Opin Plant Biol 6:494–499

    Article  PubMed  Google Scholar 

  36. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–938

    Article  PubMed  Google Scholar 

  37. Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–222

    Article  PubMed  Google Scholar 

  38. Matsubayashi Y (2003) Ligand-receptor pairs in plant peptide signalling. J Cell Sci 116:3863–3870

    Article  PubMed  Google Scholar 

  39. Matsubayashi Y, Ogawa M, Morita A, Sakagami Y (2002) An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296:1470–1472

    Article  PubMed  Google Scholar 

  40. Meckel T, Hurst AC, Thiel G, Homann U (2004) Endocytosis 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

    Article  PubMed  Google Scholar 

  41. Merino-Trigo A, Kerr MC, Houghton F, Linberg A, Mitchell C, Teasdale RD, Gleeson P (2004) Sortin nexin 5 is localized to a subdomain of the early endosomes and is recruited to the plasma membrane following EGF stimulation. J Cell Biol 117:6413–6424

    Google Scholar 

  42. Miaczynska M, Christoforidis S, Giner A, Shevchenko A, Uttenweiler-Joseph S, Habermann B, Wilm M, Patron RG, Zerial M (2004) APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116:445–456

    Article  PubMed  Google Scholar 

  43. Miaczynska M, Pelkmans L, Zerial M (2004) Not just a sink: endosomes in control of signal transduction. Curr Opin Cell Biol 16:400–406

    Article  PubMed  Google Scholar 

  44. Murphy AS, Bandyopadhyay A, Holstein SE, Peer WA (2005) Endocytotic cycling of PM proteins. Annu Rev Plant Biol 56:221–251

    Article  PubMed  Google Scholar 

  45. Nam KH, Li J (2002) BRI1=BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110:203–212

    Article  PubMed  Google Scholar 

  46. Park A, Cho SK, Yun U, ** M, Lee S, Sachetto-Martins G, Park OK (2001) Interaction of the Arabidopsis receptor protein kinase Wak1 with glycine-rich protein AtGRP-3. J Biol Chem 276:26688–26693

    Article  PubMed  Google Scholar 

  47. Robinson MS, Bonifacino JS (2001) Adaptor-related proteins. Curr Opin Cell Biol 13:444–453

    Article  PubMed  Google Scholar 

  48. Russinova E, Borst J-W, Kwaitaal M, Caño-Delgado A, Yin Y, Chory J, de Vries SC (2004) Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16:3216–3229

    Article  PubMed  Google Scholar 

  49. Šamaj J (2005) Methods and molecular tools to study endocytosis in plants–-an overview (in this volume). Springer, Berlin Heidelberg New York

    Google Scholar 

  50. Šamaj J, Baluška F, Voigt B, Schlicht M, Volkmann D, Menzel D (2004) Endocytosis, actin cytoskeleton and signaling. Plant Physiol 135:1150–1161

    Article  PubMed  Google Scholar 

  51. Scheer JM, Ryan CA Jr (2002) The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proc Natl Acad Sci USA 99:9585–9590

    Article  PubMed  Google Scholar 

  52. Shah K, Gadella TWJ, van Erp H, Hecht V, de Vries SC (2001) Subcellular localization and dimerization of the A. thaliana somatic embryogenesis receptor kinase 1 protein. J Mol Biol 309:641–655

    Article  PubMed  Google Scholar 

  53. Shah K, Russinova E, Gadella TWJ Jr, Willemse J, de Vries SC (2002) The Arabidopsis kinase-associated protein phosphatase controls internalization of the somatic embryogenesis receptor kinase 1. Genes Dev 16:1707–1720

    Article  PubMed  Google Scholar 

  54. Shiu S-H, Bleecker AB (2003) Expansion of the receptor-like kinase=Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–543

    Article  PubMed  Google Scholar 

  55. Sorkin A, McClure M, Huang F, Carter R (2000) Interaction of EGF receptor and grb2 in living cells visualized by fluorescence resonance energy transfer (FRET) microscopy. Curr Biol 10:1395–1398

    Article  PubMed  Google Scholar 

  56. Sorkin A, Von Zastrow M (2002) Signal transduction and endocytosis: close encounters of many kinds. Nat Rev Mol Cell Biol 3:600–614

    Article  PubMed  Google Scholar 

  57. Stone JM, Trotochaud AE, Walker JC, Clark SE (1998) Control of meristem development by CLAVATA1 receptor kinase and kinase-associated protein phosphatase interactions. Plant Physiol 117:1217–1225

    Article  PubMed  Google Scholar 

  58. Stone SL, Anderson EM, Mullen R, Goring DR (2003) ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15:885–898

    Article  PubMed  Google Scholar 

  59. Takayama S, Shimosato H, Shiba H, Funato M, Che F-S, Watanabe M, Iwano M, Isogal A (2001) Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature 413:534–538

    Article  PubMed  Google Scholar 

  60. Teis D, Huber LA (2003) The odd couple: signal transduction and endocytosis. Cell Mol Life Sci 60:2020–2033

    Article  PubMed  Google Scholar 

  61. Tichtinsky G, Vanoosthuyse V, Cock MJ, Gaude T (2003) Making inroads into plant receptor kinase signalling pathways. Trends Plant Sci 8:231–237

    Article  PubMed  Google Scholar 

  62. Trotochaud AE, Hao T, Wu G, Yang Z, Clark SE (1999) The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell 11:393–406

    Article  PubMed  Google Scholar 

  63. Ueda T, Yamaguchi M, Uchimiya H, Nakano A (2001) Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana. EMBO J 20:4730–4741

    Article  PubMed  Google Scholar 

  64. Ueda T, Uemura T, Sato MH, Nakano A (2004) Functional differentiation of endosomes in Arabidopsis cells. Plant J 40:783–789

    Article  PubMed  Google Scholar 

  65. Vanoosthuyse V, Tichtinsky G, Dumas C, Gaude T, Cock MJ (2003) Interaction of calmodulin, a sorting nexin and kinase-associated protein phosphatase with the Brassica oleracea S locus receptor kinase. Plant Physiol 133:919–929

    Article  PubMed  Google Scholar 

  66. Wang Z-Y, Seto H, Fujioka S, Yoshida S, Chory J (2001) BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410:380–383

    Article  PubMed  Google Scholar 

  67. Williams RW, Wilson JM, Meyerowitz EM (1997) A possible role for kinase-associated protein phosphatase in the Arabidopsis CLAVATA1 signaling pathway. Proc Natl Acad Sci USA 94:10467–10472

    Article  PubMed  Google Scholar 

  68. Xu J, Scheres B (2005) Dissection of Arabidopsis ADP-Ribosylation Factor 1 function in epidermal cell polarity. Plant Cell 17:525–536

    Article  PubMed  Google Scholar 

  69. Yin Y, Wang Z-Y, Mora-Garcia S, Li J, Yoshida S, Asami T, Chory J (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109:181–191

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sacco de Vries .

Editor information

Jozef Šamaj František Baluška Diedrik Menzel

Rights and permissions

Reprints and permissions

About this chapter

Cite this chapter

Russinova, E., de Vries, S. Receptor-Mediated Endocytosis in Plants. In: Šamaj, J., Baluška, F., Menzel, D. (eds) Plant Endocytosis. Plant Cell Monographs, vol 1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_007

Download citation

Publish with us

Policies and ethics

Navigation