Skip to main content

Organization and dynamics of functional plant membrane microdomains

Cellular and Molecular Life Sciences volume 77, pages 275–287 (2020)Cite this article

Abstract

Plasma membranes are heterogeneous and laterally compartmentalized into distinct microdomains. These membrane microdomains consist of special lipids and proteins and are thought to act as signaling platforms. In plants, membrane microdomains have been detected by super-resolution microscopy, and there is evidence that they play roles in several biological processes. Here, we review current knowledge about the lipid and protein components of membrane microdomains. Furthermore, we summarize the dynamics of membrane microdomains in response to different stimuli. We also explore the biological functions associated with membrane microdomains as signal integration hubs. Finally, we outline challenges and questions for further studies.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  1. Lichtenberg D, Goni FM, Heerklotz H (2005) Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem Sci 30:430–436

    CAS  PubMed  Google Scholar 

  2. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720–731

    CAS  PubMed  Google Scholar 

  3. Yu J, Fischman DA, Steck TL (1973) Selective solubilization of proteins and phospholipids from red blood cell membranes by nonionic detergents. J Supramol Struct 1:233–248

    CAS  PubMed  Google Scholar 

  4. Varma R, Mayor S (1998) GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394:798–801

    CAS  PubMed  Google Scholar 

  5. Pralle A, Keller P, Florin EL, Simons K, Horber JK (2000) Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J Cell Biol 148:997–1008

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Friedrichson T, Kurzchalia TV (1998) Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature 394:802–805

    CAS  PubMed  Google Scholar 

  7. Simons K, van Meer G (1988) Lipid sorting in epithelial cells. Biochemistry 27:6197–6202

    CAS  PubMed  Google Scholar 

  8. Simons K, Vaz WLC (2004) Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 33:269–295

    CAS  PubMed  Google Scholar 

  9. Jacobson K, Mouritsen OG, Anderson RGW (2007) Lipid rafts: at a crossroad between cell biology and physics. Nat Cell Biol 9:7–14

    CAS  PubMed  Google Scholar 

  10. Malinsky J, Opekarova M, Tanner W (2010) The lateral compartmentation of the yeast plasma membrane. Yeast 27:473–478

    CAS  PubMed  Google Scholar 

  11. Mongrand S, Stanislas T, Bayer EMF, Lherminier J, Simon-Plas F (2010) Membrane rafts in plant cells. Trends Plant Sci 15:656–663

    CAS  PubMed  Google Scholar 

  12. Simons K, Gerl MJ (2010) Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Bio 11:688–699

    CAS  Google Scholar 

  13. Sezgin E, Levental I, Mayor S, Eggeling C (2017) The mystery of membrane organization: composition, regulation and roles of lipid rafts. Nat Rev Mol Cell Bio 18:361–374

    CAS  Google Scholar 

  14. Brown DA, Rose JK (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:533–544

    CAS  PubMed  Google Scholar 

  15. Shogomori H, Brown DA (2003) Use of detergents to study membrane rafts: the good, the bad, and the ugly. Biol Chem 384:1259–1263

    CAS  PubMed  Google Scholar 

  16. Malinsky J, Opekarova M, Grossmann G, Tanner W (2013) Membrane microdomains, rafts, and detergent-resistant membranes in plants and fungi. Annu Rev Plant Bio 64:501–529

    CAS  Google Scholar 

  17. Sezgin E, Schwille P (2012) Model membrane platforms to study protein-membrane interactions. Mol Membr Biol 29:144–154

    CAS  PubMed  Google Scholar 

  18. Day CA, Kenworthy AK (2009) Tracking microdomain dynamics in cell membranes. Biochim Biophys Acta 1788:245–253

    CAS  PubMed  Google Scholar 

  19. Lagerholm BC, Weinreb GE, Jacobson K, Thompson NL (2005) Detecting microdomains in intact cell membranes. Annu Rev Phys Chem 56:309–336

    CAS  PubMed  Google Scholar 

  20. Yang K, Cheng H, Gross RW, Han X (2009) Automated lipid identification and quantification by multidimensional mass spectrometry-based shotgun lipidomics. Anal Chem 81:4356–4368

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Herzog R, Schwudke D, Schuhmann K, Sampaio JL, Bornstein SR, Schroeder M, Shevchenko A (2011) A novel informatics concept for high-throughput shotgun lipidomics based on the molecular fragmentation query language. Genome Biol 12:R8

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Haimi P, Uphoff A, Hermansson M, Somerharju P (2006) Software tools for analysis of mass spectrometric lipidome data. Anal Chem 78:8324–8331

    CAS  PubMed  Google Scholar 

  23. 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

    CAS  PubMed  Google Scholar 

  24. Laloi M, Perret AM, Chatre L, Melser S, Cantrel C, Vaultier MN, Zachowski A, Bathany K, Schmitter JM, Vallet M et al (2007) Insights into the role of specific lipids in the formation and delivery of lipid microdomains to the plasma membrane of plant cells. Plant Physiol 143:461–472

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Cacas JL, Furt F, Le Guedard M, Schmitter JM, Bure C, Gerbeau-Pissot P, Moreau P, Bessoule JJ, Simon-Plas F, Mongrand S (2012) Lipids of plant membrane rafts. Prog Lipid Res 51:272–299

    CAS  PubMed  Google Scholar 

  26. Guo DA, Venkatramesh M, Nes WD (1995) Developmental regulation of sterol biosynthesis in Zea mays. Lipids 30:203–219

    CAS  PubMed  Google Scholar 

  27. Travis RL, Berkowitz RL (1980) Characterization of soybean plasma membrane during development: free sterol composition and concanavalin a binding studies. Plant Physiol 65:871–879

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Norberg P, Liljenberg C (1991) Lipids of plasma membranes prepared from oat root cells: effects of induced water-deficit tolerance. Plant Physiol 96:1136–1141

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Grandmougin A, Bouvier-Nave P, Ullmann P, Benveniste P, Hartmann MA (1989) Cyclopropyl sterol and phospholipid composition of membrane fractions from maize roots treated with fenpropimorph. Plant Physiol 90:591–597

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Pata MO, Hannun YA, Ng CKY (2010) Plant sphingolipids: decoding the enigma of the Sphinx. New Phytol 185:611–630

    CAS  PubMed  Google Scholar 

  31. Cacas JL, Bure C, Furt F, Maalouf JP, Badoc A, Cluzet S, Schmitter JM, Antajan E, Mongrand S (2013) Biochemical survey of the polar head of plant glycosylinositolphosphoceramides unravels broad diversity. Phytochemistry 96:191–200

    CAS  PubMed  Google Scholar 

  32. Sperling P, Heinz E (2003) Plant sphingolipids: structural diversity, biosynthesis, first genes and functions. Bba-Mol Cell Biol L 1632:1–15

    CAS  Google Scholar 

  33. Cacas JL, Bure C, Grosjean K, Gerbeau-Pissot P, Lherminier J, Rombouts Y, Maes E, Bossard C, Gronnier J, Furt F et al (2016) Revisiting plant plasma membrane lipids in tobacco: a focus on sphingolipids. Plant Physiol 170:367–384

    CAS  PubMed  Google Scholar 

  34. Furt F, Konig S, Bessoule JJ, Sargueil F, Zallot R, Stanislas T, Noirot E, Lherminier J, Simon-Plas F, Heilmann I et al (2010) Polyphosphoinositides are enriched in plant membrane rafts and form microdomains in the plasma membrane. Plant Physiol 152:2173–2187

    CAS  PubMed  PubMed Central  Google Scholar 

  35. van Meer G, Stelzer EH, Wijnaendts-van-Resandt RW, Simons K (1987) Sorting of sphingolipids in epithelial (Madin-Darby canine kidney) cells. J Cell Biol 105:1623–1635

    PubMed  Google Scholar 

  36. Lentz BR, Burgess SW (1989) A dimerization model for the concentration dependent photophysical properties of diphenylhexatriene and its phospholipid derivatives. DPHpPC and DPHpPA. Biophys J 56:723–733

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Kusube M, Tamai N, Matsuki H, Kaneshina S (2005) Pressure-induced phase transitions of lipid bilayers observed by fluorescent probes Prodan and Laurdan. Biophys Chem 117:199–206

    CAS  PubMed  Google Scholar 

  38. Jin L, Millard AC, Wuskell JP, Dong X, Wu D, Clark HA, Loew LM (2006) Characterization and application of a new optical probe for membrane lipid domains. Biophys J 90:2563–2575

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Beknke O, Tranum-Jensen J, van Deurs B (1984) Filipin as a cholesterol probe. I. Morphology of filipin-cholesterol interaction in lipid model systems. Eur J Cell Biol 35:189–199

    CAS  PubMed  Google Scholar 

  40. Singh RD, Liu Y, Wheatley CL, Holicky EL, Makino A, Marks DL, Kobayashi T, Subramaniam G, Bittman R, Pagano RE (2006) Caveolar endocytosis and microdomain association of a glycosphingolipid analog is dependent on its sphingosine stereochemistry. J Biol Chem 281:30660–30668

    CAS  PubMed  Google Scholar 

  41. Le Guyader L, Le Roux C, Mazeres S, Gaspard-Iloughmane H, Gornitzka H, Millot C, Mingotaud C, Lopez A (2007) Changes of the membrane lipid organization characterized by means of a new cholesterol-pyrene probe. Biophys J 93:4462–4473

    PubMed  PubMed Central  Google Scholar 

  42. Konigshofer H, Tromballa HW, Loppert HG (2008) Early events in signalling high-temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production. Plant Cell Environ 31:1771–1780

    CAS  PubMed  Google Scholar 

  43. Liu P, Li RL, Zhang L, Wang QL, Niehaus K, Baluska F, Samaj J, Lin JX (2009) Lipid microdomain polarization is required for NADPH oxidase-dependent ROS signaling in Picea meyeri pollen tube tip growth. Plant J 60:303–313

    CAS  PubMed  Google Scholar 

  44. Zhao X, Li R, Lu C, Baluska F, Wan Y (2015) Di-4-ANEPPDHQ, a fluorescent probe for the visualisation of membrane microdomains in living Arabidopsis thaliana cells. Plant Physiol Biochem 87:53–60

    CAS  PubMed  Google Scholar 

  45. Li R, Liu P, Wan Y, Chen T, Wang Q, Mettbach U, Baluska F, Samaj J, Fang X, Lucas WJ et al (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

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Stauffer TP, Ahn S, Meyer T (1998) Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells. Curr Biol 8:343–346

    CAS  PubMed  Google Scholar 

  47. Varnai P, Balla T (1998) Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J Cell Biol 143:501–510

    CAS  PubMed  PubMed Central  Google Scholar 

  48. van Leeuwen W, Vermeer JE, Gadella Jr TW, Munnik T. (2007) Visualization of phosphatidylinositol 4,5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings. Plant J 52:1014–1026

  49. Demir F, Horntrich C, Blachutzik JO, Scherzer S, Reinders Y, Kierszniowska S, Schulze WX, Harms GS, Hedrich R, Geiger D et al (2013) Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. Proc Natl Acad Sci USA 110:8296–8301

    CAS  PubMed  Google Scholar 

  50. Hao H, Fan L, Chen T, Li R, Li X, He Q, Botella MA, Lin J (2014) Clathrin and membrane microdomains cooperatively regulate rbohd dynamics and activity in Arabidopsis. Plant Cell 26:1729–1745

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Li X, Wang X, Yang Y, Li R, He Q, Fang X, Luu DT, Maurel C, Lin J (2011) Single-molecule analysis of PIP2;1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation. Plant Cell 23:3780–3797

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Keinath NF, Kierszniowska S, Lorek J, Bourdais G, Kessler SA, Shimosato-Asano H, Grossniklaus U, Schulze WX, Robatzek S, 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

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Takahashi A, Kawasaki T, Wong HL, Suharsono U, Hirano H, Shimamoto K (2003) Hyperphosphorylation of a mitochondrial protein, prohibitin, is induced by calyculin A in a rice lesion-mimic mutant cdr1. Plant Physiol 132:1861–1869

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Ahn CS, Lee JH, Reum Hwang A, Kim WT, Pai HS (2006) Prohibitin is involved in mitochondrial biogenesis in plants. Plant J 46:658–667

    CAS  PubMed  Google Scholar 

  55. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Winzer T, Bairl A, Linder M, Linder D, Werner D, Muller P (1999) A novel 53-kDa nodulin of the symbiosome membrane of soybean nodules, controlled by Bradyrhizobium japonicum. Mol Plant Microbe Interact 12:218–226

    CAS  PubMed  Google Scholar 

  57. Saalbach G, Erik P, Wienkoop S (2002) Characterisation by proteomics of peribacteroid space and peribacteroid membrane preparations from pea (Pisum sativum) symbiosomes. Proteomics 2:325–337

    CAS  PubMed  Google Scholar 

  58. Nadimpalli R, Yalpani N, Johal GS, Simmons CR (2000) Prohibitins, stomatins, and plant disease response genes compose a protein superfamily that controls cell proliferation, ion channel regulation, and death. J Biol Chem 275:29579–29586

    CAS  PubMed  Google Scholar 

  59. Rostoks N, Schmierer D, Kudrna D, Kleinhofs A (2003) Barley putative hypersensitive induced reaction genes: genetic mapping, sequence analyses and differential expression in disease lesion mimic mutants. Theor Appl Genet 107:1094–1101

    CAS  PubMed  Google Scholar 

  60. Raffaele S, Mongrand S, Gamas P, Niebel A, Ott T (2007) Genome-wide annotation of remorins, a plant-specific protein family: evolutionary and functional perspectives. Plant Physiol 145:593–600

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Konrad SS, Ott T (2015) Molecular principles of membrane microdomain targeting in plants. Trends Plant Sci 20:351–361

    CAS  PubMed  Google Scholar 

  62. Wang L, Xue Y, Xing J, Song K, Lin J (2018) Exploring the spatiotemporal organization of membrane proteins in living plant cells. Annu Rev Plant Biol 69:525–551

    CAS  PubMed  Google Scholar 

  63. Yu M, Liu H, Dong Z, Xiao J, Su B, Fan L, Komis G, Samaj J, Lin J, Li R (2017) The dynamics and endocytosis of Flot1 protein in response to flg22 in Arabidopsis. J Plant Physiol 215:73–84

    CAS  PubMed  Google Scholar 

  64. Jarsch IK, Konrad SS, Stratil TF, Urbanus SL, Szymanski W, Braun P, Braun KH, Ott T (2014) Plasma membranes are subcompartmentalized into a plethora of coexisting and diverse microdomains in Arabidopsis and Nicotiana benthamiana. Plant Cell 26:1698–1711

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Hodzic A, Rappolt M, Amenitsch H, Laggner P, Pabst G (2008) Differential modulation of membrane structure and fluctuations by plant sterols and cholesterol. Biophys J 94:3935–3944

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Garcia-Saez AJ, Schwille P (2010) Stability of lipid domains. FEBS Lett 584:1653–1658

    CAS  PubMed  Google Scholar 

  67. Gui J, Zheng S, Liu C, Shen J, Li J, Li L (2016) OsREM4.1 Interacts with OsSERK1 to coordinate the Interlinking between abscisic acid and brassinosteroid signaling in rice. Dev Cell 38:201–213

    CAS  PubMed  Google Scholar 

  68. Konrad SS, Popp C, Stratil TF, Jarsch IK, Thallmair V, Folgmann J, Marin M, Ott T (2014) S-acylation anchors remorin proteins to the plasma membrane but does not primarily determine their localization in membrane microdomains. New Phytol 203:758–769

    CAS  PubMed  Google Scholar 

  69. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46–50

    CAS  PubMed  Google Scholar 

  70. Gronnier J, Crowet JM, Habenstein B, Nasir MN, Bayle V, Hosy E, Platre MP, Gouguet P, Raffaele S, Martinez D et al (2017) Structural basis for plant plasma membrane protein dynamics and organization into functional nanodomains. Elife 6:e26404

    PubMed  PubMed Central  Google Scholar 

  71. Ernst AM, Contreras FX, Brugger B, Wieland F (2010) Determinants of specificity at the protein-lipid interface in membranes. FEBS Lett 584:1713–1720

    CAS  PubMed  Google Scholar 

  72. Szymanski WG, Zauber H, Erban A, Gorka M, Wu XN, Schulze WX (2015) Cytoskeletal components define protein location to membrane microdomains. Mol Cell Proteomics 14:2493–2509

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Lv X, Jing Y, Xiao J, Zhang Y, Zhu Y, Julian R, Lin J (2017) Membrane microdomains and the cytoskeleton constrain AtHIR1 dynamics and facilitate the formation of an AtHIR1-associated immune complex. Plant J 90:3–16

    CAS  PubMed  Google Scholar 

  74. Owen DM, Williamson D, Rentero C, Gaus K (2009) Quantitative microscopy: protein dynamics and membrane organisation. Traffic 10:962–971

    CAS  PubMed  Google Scholar 

  75. Wang L, Li H, Lv X, Chen T, Li R, Xue Y, Jiang J, Jin B, Baluska F, Samaj J et al (2015) Spatiotemporal dynamics of the BRI1 receptor and its regulation by membrane microdomains in living Arabidopsis cells. Mol Plant 8:1334–1349

    CAS  PubMed  Google Scholar 

  76. Haney CH, Long SR (2010) Plant Flotillins are required for infection by nitrogen-fixing bacteria. Proc Natl Acad Sci USA 107:478–483

    CAS  PubMed  Google Scholar 

  77. Cui Y, Li X, Yu M, Li R, Fan L, Zhu Y, Lin J (2018) Sterols regulate endocytic pathways during flg22-induced defense responses in Arabidopsis. Development 145(19):dev165688

    PubMed  Google Scholar 

  78. Bucherl CA, Jarsch IK, Schudoma C, Segonzac C, Mbengue M, Robatzek S, MacLean D, Ott T, Zipfel C (2017) Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains. Elife 6:e25114

    PubMed  PubMed Central  Google Scholar 

  79. Perraki A, Gronnier J, Gouguet P, Boudsocq M, Deroubaix AF, Simon V, German-Retana S, Legrand A, Habenstein B, Zipfel C et al (2018) REM1.3’s phospho-status defines its plasma membrane nanodomain organization and activity in restricting PVX cell-to-cell movement. PLoS Pathog 14:e1007378

    PubMed  PubMed Central  Google Scholar 

  80. Qi Y, Tsuda K, le Nguyen V, Wang X, Lin J, Murphy AS, Glazebrook J, Thordal-Christensen H, Katagiri F (2011) Physical association of Arabidopsis hypersensitive induced reaction proteins (HIRs) with the immune receptor RPS2. J Biol Chem 286:31297–31307

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Ishikawa T, Aki T, Yanagisawa S, Uchimiya H, Kawai-Yamada M (2015) Overexpression of BAX INHIBITOR-1 links plasma membrane microdomain proteins to stress. Plant Physiol 169:1333–1343

    PubMed  PubMed Central  Google Scholar 

  82. Xue Y, Xing J, Wan Y, Lv X, Fan L, Zhang Y, Song K, Wang L, Wang X, Deng X et al (2018) Arabidopsis blue light receptor phototropin 1 undergoes blue light-induced activation in membrane microdomains. Mol Plant 11:846–859

    CAS  PubMed  Google Scholar 

  83. Baral A, Irani NG, Fujimoto M, Nakano A, Mayor S, Mathew MK (2015) Salt-induced remodeling of spatially restricted clathrin-independent endocytic pathways in Arabidopsis root. Plant Cell 27:1297–1315

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Claus LAN, Savatin DV, Russinova E (2018) The crossroads of receptor-mediated signaling and endocytosis in plants. J Integr Plant Biol 60:827–840

    PubMed  Google Scholar 

  85. Mbengue M, Bourdais G, Gervasi F, Beck M, Zhou J, Spallek T, Bartels S, Boller T, Ueda T, Kuhn H et al (2016) Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases. Proc Natl Acad Sci USA 113:11034–11039

    CAS  PubMed  Google Scholar 

  86. Yoshinari A, Hosokawa T, Amano T, Beier MP, Kunieda T, Shimada T, Hara-Nishimura I, Naito S, Takano J (2019) Polar localization of the borate exporter BOR1 requires AP2-Dependent endocytosis. Plant Physiol 179:1569–1580

    CAS  PubMed  Google Scholar 

  87. Kroumanova K, Kocourkova D, Danek M, Lamparova L, Pospichalova R, Malinska K, Krckova Z, Burketova L, Valentova O, Martinec J et al (2019) Characterisation of Arabidopsis Flotillins in response to stresses. Biol Plant 63:144–152

    Google Scholar 

  88. Wang Q, Zhao Y, Luo W, Li R, He Q, Fang X, Michele RD, Ast C, von Wiren N, Lin J (2013) Single-particle analysis reveals shutoff control of the Arabidopsis ammonium transporter AMT1;3 by clustering and internalization. Proc Natl Acad Sci USA 110:13204–13209

    CAS  PubMed  Google Scholar 

  89. Slupianek A, Kasprowicz-Maluski A, Myskow E, Turzanska M, Sokolowska K (2019) Endocytosis acts as transport pathway in wood. New Phytol 222:1846–1861

    CAS  PubMed  Google Scholar 

  90. Li X, Luu DT, Maurel C, Lin J (2013) Probing plasma membrane dynamics at the single-molecule level. Trends Plant Sci 18:617–624

    CAS  PubMed  Google Scholar 

  91. Viola A, Gupta N (2007) Tether and trap: regulation of membrane-raft dynamics by actin-binding proteins. Nat Rev Immunol 7:889–896

    CAS  PubMed  Google Scholar 

  92. Szymanski DB, Cosgrove DJ (2009) Dynamic coordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Curr Biol 19:R800–R811

    CAS  PubMed  Google Scholar 

  93. McKenna JF, Tolmie AF, Runions J (2014) Across the great divide: the plant cell surface continuum. Curr Opin Plant Biol 22:132–140

    CAS  PubMed  Google Scholar 

  94. Martiniere A, Lavagi I, Nageswaran G, Rolfe DJ, Maneta-Peyret L, Luu DT, Botchway SW, Webb SE, Mongrand S, Maurel C et al (2012) Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc Natl Acad Sci USA 109:12805–12810

    CAS  PubMed  Google Scholar 

  95. Sorci-Thomas MG, Thomas MJ (2016) Microdomains, inflammation, and atherosclerosis. Circ Res 118:679–691

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Goldfinger LE, Michael JV (2017) Regulation of Ras signaling and function by plasma membrane microdomains. Biosci Trends 11:23–40

    CAS  PubMed  Google Scholar 

  97. Takahashi D, Kawamura Y, Uemura M (2013) Detergent-resistant plasma membrane proteome to elucidate microdomain functions in plant cells. Front Plant Sci 4:27

    PubMed  PubMed Central  Google Scholar 

  98. Willemsen V, Friml J, Grebe M, van den Toorn A, Palme K, Scheres B (2003) Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function. Plant Cell 15:612–625

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Men S, Boutte Y, Ikeda Y, Li X, Palme K, Stierhof YD, Hartmann MA, Moritz T, Grebe M (2008) Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat Cell Biol 10:237–244

    CAS  PubMed  Google Scholar 

  100. Grison MS, Brocard L, Fouillen L, Nicolas W, Wewer V, Dormann P, Nacir H, Benitez-Alfonso Y, Claverol S, Germain V et al (2015) Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Plant Cell 27:1228–1250

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Zavaliev R, Dong X, Epel BL (2016) Glycosylphosphatidylinositol (GPI) modification serves as a primary plasmodesmal sorting signal. Plant Physiol 172:1061–1073

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Raffaele S, Bayer E, Lafarge D, Cluzet S, German Retana S, Boubekeur T, Leborgne-Castel N, Carde JP, Lherminier J, Noirot E et al (2009) Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. Plant Cell 21:1541–1555

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Li S, Su X, Zhang B, Huang Q, Hu Z, Lu M (2013) Molecular cloning and functional analysis of the Populus deltoides remorin gene PdREM. Tree Physiol 33:1111–1121

    CAS  PubMed  Google Scholar 

  104. Gui J, Liu C, Shen J, Li L (2014) Grain setting defect1, encoding a remorin protein, affects the grain setting in rice through regulating plasmodesmatal conductance. Plant Physiol 166:1463–1478

    PubMed  PubMed Central  Google Scholar 

  105. Colebatch G, Desbrosses G, Ott T, Krusell L, Montanari O, Kloska S, Kopka J, Udvardi MK (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J 39:487–512

    PubMed  Google Scholar 

  106. El Yahyaoui F, Kuster H, Ben Amor B, Hohnjec N, Puhler A, Becker A, Gouzy J, Vernie T, Gough C, Niebel A et al (2004) Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiol 136:3159–3176

    PubMed  PubMed Central  Google Scholar 

  107. Coaker GL, Willard B, Kinter M, Stockinger EJ, Francis DM (2004) Proteomic analysis of resistance mediated by Rcm 2.0 and Rcm 5.1, two loci controlling resistance to bacterial canker of tomato. Mol Plant Microbe Interact 17:1019–1028

    CAS  PubMed  Google Scholar 

  108. Lefebvre B, Timmers T, Mbengue M, Moreau S, Herve C, Toth K, Bittencourt-Silvestre J, Klaus D, Deslandes L, Godiard L et al (2010) A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc Natl Acad Sci USA 107:2343–2348

    CAS  PubMed  Google Scholar 

  109. Toth K, Stratil TF, Madsen EB, Ye J, Popp C, Antolin-Llovera M, Grossmann C, Jensen ON, Schussler A, Parniske M et al (2012) Functional domain analysis of the Remorin protein LjSYMREM1 in Lotus japonicus. PLoS One 7:e30817

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Jamann TM, Luo X, Morales L, Kolkman JM, Chung CL, Nelson RJ (2016) A remorin gene is implicated in quantitative disease resistance in maize. Theor Appl Genet 129:591–602

    CAS  PubMed  Google Scholar 

  111. Son S, Oh CJ, An CS (2014) Arabidopsis thaliana remorins interact with SnRK1 and play a role in susceptibility to beet curly top virus and beet severe curly top virus. Plant Pathol J 30:269–278

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ, Coaker G (2009) RIN4 functions with plasma membrane H+ -ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol 7:e1000139

    PubMed  PubMed Central  Google Scholar 

  113. Jung HW, Lim CW, Lee SC, Choi HW, Hwang CH, Hwang BK (2008) Distinct roles of the pepper hypersensitive induced reaction protein gene CaHIR1 in disease and osmotic stress, as determined by comparative transcriptome and proteome analyses. Planta 227:409–425

    CAS  PubMed  Google Scholar 

  114. Duan Y, Guo J, Shi X, Guan X, Liu F, Bai P, Huang L, Kang Z (2013) Wheat hypersensitive-induced reaction genes TaHIR1 and TaHIR3 are involved in response to stripe rust fungus infection and abiotic stresses. Plant Cell Rep 32:273–283

    CAS  PubMed  Google Scholar 

  115. Jung HW, Hwang BK (2007) The leucine-rich repeat (LRR) protein, CaLRR1, interacts with the hypersensitive induced reaction (HIR) protein, CaHIR1, and suppresses cell death induced by the CaHIR1 protein. Mol Plant Pathol 8:503–514

    CAS  PubMed  Google Scholar 

  116. Zhou L, Cheung MY, Zhang Q, Lei CL, Zhang SH, Sun SS, Lam HM (2009) A novel simple extracellular leucine-rich repeat (eLRR) domain protein from rice (OsLRR1) enters the endosomal pathway and interacts with the hypersensitive-induced reaction protein 1 (OsHIR1). Plant Cell Environ 32:1804–1820

    CAS  PubMed  Google Scholar 

  117. Checker VG, Khurana P (2013) Molecular and functional characterization of mulberry EST encoding remorin (MiREM) involved in abiotic stress. Plant Cell Rep 32:1729–1741

    CAS  PubMed  Google Scholar 

  118. Yue J, Li C, Liu Y, Yu J (2014) A remorin gene SiREM6, the target gene of SiARDP, from foxtail millet (Setaria italica) promotes high salt tolerance in transgenic Arabidopsis. PLoS One 9:e100772

    PubMed  PubMed Central  Google Scholar 

  119. Cui Y, Zhang X, Yu M, Zhu Y, Xing J, Lin J (2019) Techniques for detecting protein-protein interactions in living cells: principles, limitations, and recent progress. Sci China Life Sci 62:619–632

    PubMed  Google Scholar 

Download references

Acknowledgements

We thank lab members for helpful discussions and critical reading of the paper. This work was supported by the State ‘13.5’ Key Research Program of China (No. 2016YFD0600102), the National Natural Science Foundation of China (31530084, 31761133009, 31670182, 31401149), and the Fundamental Research Funds for the Central Universities (2019ZY29, 2017ZY10) and the Program of Introducing Talents of Discipline to Universities (111 project, B13007).

Author information

Author notes

  1. Meng Yu and Yaning Cui contributed equally to this work.

Affiliations

  1. Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing, 100083, China

    Meng Yu, Ruili Li & Jinxing Lin

  2. College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China

    Meng Yu, Yaning Cui, Xi Zhang, Ruili Li & Jinxing Lin

Authors
  1. Meng Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yaning Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ruili Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinxing Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ruili Li or Jinxing Lin.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yu, M., Cui, Y., Zhang, X. et al. Organization and dynamics of functional plant membrane microdomains. Cell. Mol. Life Sci. 77, 275–287 (2020). https://doi.org/10.1007/s00018-019-03270-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-019-03270-7

Keywords

  • Microdomain marker proteins
  • Lipid
  • Assembly
  • Motion
  • Stress