Plasma membranes are Subcompartmentalized into a plethora of coexisting and diverse microdomains in Arabidopsis and Nicotiana benthamiana

Plant Cell

Volumn 26, Issue 4, 2014, Pages 1698-1711

  Jarsch, Iris K ^a   Konrad, Sebastian S A ^a   Stratil, Thomas F ^a   Urbanus, Susan L ^a   Szymanski, Witold ^b   Braun, Pascal ^c   Braun, Karl Heinz ^a   Ott, Thomas ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84901431185     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.124446     Document Type: Article

References (54)

1. Aker, J., Hesselink, R., Engel, R., Karlova, R., Borst, J.W., Visser, A.J., and de Vries, S.C. (2007). In vivo hexamerization and characterization of the Arabidopsis AAA ATPase CDC48A complex using Forster resonance energy transfer-fluorescence lifetime imaging microscopy and fluorescence correlation spectroscopy. Plant Physiol. 145: 339-350.
2. Bhat, R.A., Miklis, M., Schmelzer, E., Schulze-Lefert, P., and Panstruga, R. (2005). Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc. Natl. Acad. Sci. USA 102: 3135-3140.
3. Binder, A., Lambert, J., Morbitzer, R., Popp, C., Ott, T., Lahaye, T., and Parniske, M. (2014). A modular plasmid assembly kit for multigene expression, gene silencing and silencing rescue in plants. PLoS ONE 9: e88218.
4. Boutté, Y., and Grebe, M. (2009). Cellular processes relying on sterol function in plants. Curr. Opin. Plant Biol. 12: 705-713.
5. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
6. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and Scheible, W.R. (2005). Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139: 5-17.
7. Demir, F., Horntrich, C., Blachutzik, J.O., Scherzer, S., Reinders, Y., Kierszniowska, S., Schulze, W.X., Harms, G.S., Hedrich, R., Geiger, D., and Kreuzer, I. (2013). Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. Proc. Natl. Acad. Sci. USA 110: 8296-8301.
8. Dinic, J., Ashrafzadeh, P., and Parmryd, I. (2013). Actin filaments attachment at the plasma membrane in live cells cause the formation of ordered lipid domains. Biochim. Biophys. Acta 1828: 1102-1111.
9. Haney, C.H., and Long, S.R. (2010). Plant flotillins are required for infection by nitrogen-fixing bacteria. Proc. Natl. Acad. Sci. USA 107: 478-483.
10. Haney, C.H., Riely, B.K., Tricoli, D.M., Cook, D.R., Ehrhardt, D.W., and Long, S.R. (2011). Symbiotic rhizobia bacteria trigger a change in localization and dynamics of the Medicago truncatula receptor kinase LYK3. Plant Cell 23: 2774-2787.
11. Harrison, S.J., Mott, E.K., Parsley, K., Aspinall, S., Gray, J.C., and Cottage, A. (2006). A rapid and robust method of identifying transformed Arabidopsis thaliana seedlings following floral dip transformation. Plant Methods 2: 19.
12. Hauck, P., Thilmony, R., and He, S.Y. (2003). A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc. Natl. Acad. Sci. USA 100: 8577-8582.
13. Henty-Ridilla, J.L., Shimono, M., Li, J., Chang, J.H., Day, B., and Staiger, C.J. (2013). The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLoS Pathog. 9: e1003290.
14. Jarsch, I.K., and Ott, T. (2011). Perspectives on remorin proteins, membrane rafts, and their role during plant-microbe interactions. Mol. Plant Microbe Interact. 24: 7-12.
15. Keinath, N.F., Kierszniowska, S., Lorek, J., Bourdais, G., Kessler, S.A., Shimosato-Asano, H., Grossniklaus, U., Schulze, W.X., Robatzek, S., and Panstruga, R. (2010). PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J. Biol. Chem. 285: 39140-39149.
16. Kierszniowska, S., Seiwert, B., and Schulze, W.X. (2009). Definition of Arabidopsis sterol-rich membrane microdomains by differential treatment with methyl-beta-cyclodextrin and quantitative proteomics. Mol. Cell. Proteomics 8: 612-623.
17. Kusumi, A., Fujiwara, T.K., Chadda, R., Xie, M., Tsunoyama, T.A., Kalay, Z., Kasai, R.S., and Suzuki, K.G. (2012). Dynamic organizing principles of the plasma membrane that regulate signal transduction: Commemorating the fortieth anniversary of Singer and Nicolson's fluid-mosaic model. Annu. Rev. Cell Dev. Biol. 28: 215-250.
18. Kusumi, A., Nakada, C., Ritchie, K., Murase, K., Suzuki, K., Murakoshi, H., Kasai, R.S., Kondo, J., and Fujiwara, T. (2005). Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: High-speed single-molecule tracking of membrane molecules. Annu. Rev. Biophys. Biomol. Struct. 34: 351-378.
19. Langhorst, M.F., Solis, G.P., Hannbeck, S., Plattner, H., and Stuermer, C.A. (2007). Linking membrane microdomains to the cytoskeleton: Regulation of the lateral mobility of reggie-1/flotillin-2 by interaction with actin. FEBS Lett. 581: 4697-4703.
20. Lefebvre, B., et al. (2010). A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc. Natl. Acad. Sci. USA 107: 2343-2348.
21. Levental, I., Grzybek, M., and Simons, K. (2010a). Greasing their way: Lipid modifications determine protein association with membrane rafts. Biochemistry 49: 6305-6316.
22. Levental, I., Lingwood, D., Grzybek, M., Coskun, U., and Simons, K. (2010b). Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proc. Natl. Acad. Sci. USA 107: 22050-22054.
23. Lherminier, J., Elmayan, T., Fromentin, J., Elaraqui, K.T., Vesa, S., Morel, J., Verrier, J.L., Cailleteau, B., Blein, J.P., and Simon-Plas, F. (2009). NADPH oxidase-mediated reactive oxygen species production: Subcellular localization and reassessment of its role in plant defense. Mol. Plant Microbe Interact. 22: 868-881.
24. Li, Q., Lau, A., Morris, T.J., Guo, L., Fordyce, C.B., and Stanley, E.F. (2004). A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: Analysis by quantitative immunocolocalization. J. Neurosci. 24: 4070-4081.
25. Li, R., Liu, P., Wan, Y., Chen, T., Wang, Q., Mettbach, U., Baluska, F., Samaj, J., Fang, X., Lucas, W.J., and Lin, J. (2012). A membrane microdomain-associated protein, Arabidopsis Flot1, is involved in a clathrin-independent endocytic pathway and is required for seedling development. Plant Cell 24: 2105-2122.
26. Lingwood, D., and Simons, K. (2010). Lipid rafts as a membrane-organizing principle. Science 327: 46-50.
27. Maekawa, T., Kusakabe, M., Shimoda, Y., Sato, S., Tabata, S., Murooka, Y., and Hayashi, M. (2008). Polyubiquitin promoter-based binary vectors for overexpression and gene silencing in Lotus japonicus. Mol. Plant Microbe Interact. 21: 375-382.
28. Malinsky, J., Opekarová, M., Grossmann, G., and Tanner, W. (2013). Membrane microdomains, rafts, and detergent-resistant membranes in plants and fungi. Annu. Rev. Plant Biol. 64: 501-529.
29. Malinsky, J., Opekarová, M., and Tanner, W. (2010). The lateral compartmentation of the yeast plasma membrane. Yeast 27: 473-478.
30. Manders, E.M., Stap, J., Brakenhoff, G.J., van Driel, R., and Aten, J.A. (1992). Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J. Cell Sci. 103: 857-862.
31. Manders, E.M., Verbeek, F.J., and Aten, J.A. (1993). Measurement of co-localization of objects in dual-colour confocal images. J. Microsc. 169: 375-382.
32. Marín, M., and Ott, T. (2012). Phosphorylation of intrinsically disordered regions in remorin proteins. Front. Plant Sci. 3: 86.
33. Marín, M., Thallmair, V., and Ott, T. (2012). The intrinsically disordered N-terminal region of AtREM1.3 remorin protein mediates protein-protein interactions. J. Biol. Chem. 287: 39982-39991.
34. Martinière, A., et al. (2012). Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc. Natl. Acad. Sci. USA 109: 12805-12810.
35. Minami, A., Fujiwara, M., Furuto, A., Fukao, Y., Yamashita, T., Kamo, M., Kawamura, Y., and Uemura, M. (2009). Alterations in detergent-resistant plasma membrane microdomains in Arabidopsis thaliana during cold acclimation. Plant Cell Physiol. 50: 341-359.
36. Müller, A., Guan, C., Gälweiler, L., Tänzler, P., Huijser, P., Marchant, A., Parry, G., Bennett, M., Wisman, E., and Palme, K. (1998). AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17: 6903-6911.
37. Raffaele, S., et al. (2009). Remorin, a Solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. Plant Cell 21: 1541-1555.
38. Raffaele, S., Mongrand, S., Gamas, P., Niebel, A., and Ott, T. (2007). Genome-wide annotation of remorins, a plant-specific protein family: Evolutionary and functional perspectives. Plant Physiol. 145: 593-600.
39. Reuff, M., Mikosch, M., and Homann, U. (2010). Trafficking, lateral mobility and segregation of the plant K channel KAT1. Plant Biol. (Stuttg.) 12 (suppl. 1): 99-104.
40. Roppolo, D., De Rybel, B., Tendon, V.D., Pfister, A., Alassimone, J., Vermeer, J.E., Yamazaki, M., Stierhof, Y.D., Beeckman, T., and Geldner, N. (2011). A novel protein family mediates Casparian strip formation in the endodermis. Nature 473: 380-383.
41. Russinova, E., Borst, J.W., Kwaaitaal, M., Caño-Delgado, A., Yin, Y., Chory, J., and de Vries, S.C. (2004). Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16: 3216-3229.
42. Shahollari, B., Peskan-Berghoefer, T., and Oelmueller, R. (2004). Receptor kinases with leucine-rich repeats are enriched in Triton X-100 insoluble plasma membrane microdomains from plants. Physiol. Plant. 122: 397-403.
43. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003). Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 13: 2498-2504.
44. Spira, F., Mueller, N.S., Beck, G., von Olshausen, P., Beig, J., and Wedlich-Söldner, R. (2012). Patchwork organization of the yeast plasma membrane into numerous coexisting domains. Nat. Cell Biol. 14: 640-648.
45. + channel at the plasma membrane. Plant Cell 18: 935-954.
46. Tanner, W., Malinsky, J., and Opekarová, M. (2011). In plant and animal cells, detergent-resistant membranes do not define functional membrane rafts. Plant Cell 23: 1191-1193.
47. Tóth, K., Stratil, T.F., Madsen, E.B., Ye, J., Popp, C., Antolín-Llovera, M., Grossmann, C., Jensen, O.N., Schüssler, A., Parniske, M., and Ott, T. (2012). Functional domain analysis of the Remorin protein LjSYMREM1 in Lotus japonicus. PLoS ONE 7: e30817.
48. Tsuda, K., Qi, Y., Nguyen, V., Bethke, G., Tsuda, Y., Glazebrook, J., and Katagiri, F. (2012). An efficient Agrobacterium-mediated transient transformation of Arabidopsis. Plant J. 69: 713-719.
49. Underwood, W., and Somerville, S.C. (2013). Perception of conserved pathogen elicitors at the plasma membrane leads to relocalization of the Arabidopsis PEN3 transporter. Proc. Natl. Acad. Sci. USA 110: 12492-12497.
50. Urbanus, S.L., and Ott, T. (2012). Plasticity of plasma membrane compartmentalization during plant immune responses. Front. Plant Sci. 3: 181.
51. van den Bogaart, G., Meyenberg, K., Risselada, H.J., Amin, H., Willig, K.I., Hubrich, B.E., Dier, M., Hell, S.W., Grubmüller, H., Diederichsen, U., and Jahn, R. (2011). Membrane protein sequestering by ionic protein-lipid interactions. Nature 479: 552-555.
52. Vermeer, J.E., Van Munster, E.B., Vischer, N.O., and Gadella, T.W., Jr.,. (2004). Probing plasma membrane microdomains in cowpea protoplasts using lipidated GFP-fusion proteins and multimode FRET microscopy. J. Microsc. 214: 190-200.
53. Zhang, Y., Immink, R., Liu, C.M., Emons, A.M., and Ketelaar, T. (2013). The Arabidopsis exocyst subunit SEC3A is essential for embryo development and accumulates in transient puncta at the plasma membrane. New Phytol. 199: 74-88.
54. Zurzolo, C., van Meer, G., and Mayor, S. (2003). The order of rafts. Conference on microdomains, lipid rafts and caveolae. EMBO Rep. 4: 1117-1121.