ROS and Plant Membrane Rafts

  • Françoise Simon-Plas
  • Sébastien MongrEmail author
Part of the Signaling and Communication in Plants book series (SIGCOMM)


Although excess reactive oxygen species (ROS) are toxic, physiological concentrations of ROS may function as signaling molecules to mediate various responses. However, given that ROS are diffusible and short-lived, localizing the ROS signal at a precise subcellular location is essential for stimulation of specific redox signaling. In animals, recent studies have indicated lipid microdomain platforms or lipid rafts may be importantly implicated in redox signaling of a variety of cells in response to agonists or stimuli (for a review, see Li and Gulbins 2007). The plant plasma membrane (PM) is in charge of sensing the various environmental modifications faced by the plant cell and triggering the appropriate physiological responses. It thus exemplifies this requirement for an extremely fine-tuning of ROS production in plants, which has been evidenced as a mediator in many different biotic or abiotic stresses leading to significantly different responses. The spatial compartmentalization of ROS-producing enzymes in specialized domains of the plant PM could be one key element of such a regulation.


Reactive Oxygen Species Reactive Oxygen Species Production NADPH Oxidase Lipid Raft Cytochrome B561 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L, Kalde M, Wanner G, Peck SC, Edwards H, Ramonell K (2004) The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol Biol Cell 15:5118–5129PubMedCrossRefGoogle Scholar
  2. Bagnat M, Keranen S, Shevchenko A, Simons, K (2000) Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc Natl Acad Sci USA 97:3254–3259PubMedCrossRefGoogle Scholar
  3. Beck J, Mathieu D, Loudet C, Buchoux S, Dufourc E (2007) Plant sterols in “rafts”: a better way to regulate membrane thermal shocks, FASEB J 21:1714–1723PubMedCrossRefGoogle Scholar
  4. Berczi A, Horvath G (2003) Lipid rafts in the plant plasma membrane? Acta Biol Szeged 47:7–10Google Scholar
  5. Berczi A, Luthje S, Asard H (2001) b-Type cytochromes in plasma membranes of Phaseolus vulgaris hypocotyls, Arabidopsis thaliana leaves, and Zea mays roots. Protoplasma 217:50–55PubMedCrossRefGoogle Scholar
  6. Berczi A, Su D, Asard H (2007) An Arabidopsis cytochrome b561 with trans-membrane ferrireductase capability. FEBS Lett 581:1505–8PubMedCrossRefGoogle Scholar
  7. Bestwick CS, Brown IR, Bennett MH, Mansfield JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 9:209–221PubMedCrossRefGoogle Scholar
  8. Bhat RA, Miklis M, Schmelzer E, Schulze-Lefert P, Panstruga R (2005) Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc Natl Acad Sci USA 102:3135–3140PubMedCrossRefGoogle Scholar
  9. Bhat RA, Panstruga R (2005) Lipid rafts in plants. Planta 223:5–19PubMedCrossRefGoogle Scholar
  10. Boka K, Orban N, Kristof Z (2007) Dynamics and localization of H2O2 production in elicited plant cells. Protoplasma 230:89–97PubMedCrossRefGoogle Scholar
  11. 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 137:104–116PubMedCrossRefGoogle Scholar
  12. Briggs RT, Dratch DB, Karnovsky ML, Karnovsky MJ (1975) Localization of NADH oxidase on the surface of human polymorphonuclear leukocytes by a new cytochemical method. J Cell Biol 67:566–596PubMedCrossRefGoogle Scholar
  13. Brown DA, Rose JK (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:533–544PubMedCrossRefGoogle Scholar
  14. Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, Derbyshire P, Drea S, Zarsky V, Dolan L (2005) A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438:1013–1016PubMedCrossRefGoogle Scholar
  15. Chamberlain LH, Burgoyne RD, Gould GW (2001) SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis. Proc Natl Acad Sci USA 98:5619–5624PubMedCrossRefGoogle Scholar
  16. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Huckelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–977PubMedCrossRefGoogle Scholar
  17. Dykstra ML, Cherukuri A, Pierce SK (2001) Floating the raft hypothesis for immune receptors: access to rafts controls receptor signaling and trafficking. Traffic 2:160–166PubMedCrossRefGoogle Scholar
  18. Dufourc E (2008) The role of phytosterols in plant adaptation to temperature, Plant Signal Behav 3:133–134PubMedCrossRefGoogle Scholar
  19. Field KA, Holowka D, Baird B (1997) Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains. J Biol Chem 272:4276–4280PubMedCrossRefGoogle Scholar
  20. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446PubMedCrossRefGoogle Scholar
  21. Frassanito MC, Piccoli C, Capozzi V, Boffoli D, Tabilio A, Capitanio N (2008) Topological organization of NADPH-oxidase in haematopoietic stem cell membrane: preliminary study by fluorescence near-field optical microscopy. J Microsc 229:517–524PubMedCrossRefGoogle Scholar
  22. Furt F, Lefebvre B, Cullimore J, Bessoule JJ, Mongrand S (2007) Plant lipid rafts fluctuat nec mergitur. Plant Signal Behav 2:1011–1013CrossRefGoogle Scholar
  23. Galbiati F, Razani B, Lisanti MP (2001) Emerging themes in lipid rafts and caveolae. Cell 106:403–411PubMedCrossRefGoogle Scholar
  24. Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230PubMedCrossRefGoogle Scholar
  25. Gekara NO, Weiss S (2004) Lipid rafts clustering and signalling by listeriolysin O. Biochem Soc Trans 32:712–714PubMedCrossRefGoogle Scholar
  26. Glebov OO, Nichols BJ (2004) Distribution of lipid raft markers in live cells. Biochem Soc Trans 32:673–675PubMedCrossRefGoogle Scholar
  27. Grossmann G, Opekarova M, Novakova L, Stolz J, Tanner, W (2006) Lipid raft-based membrane compartmentation of a plant transport protein expressed in Saccharomyces cerevisiae. Eukaryot Cell 5:945–953PubMedCrossRefGoogle Scholar
  28. Hilenski LL, Clempus RE, Quinn MT, Lambeth JD, Griendling KK (2004) Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 24:677–683PubMedCrossRefGoogle Scholar
  29. Ikonen E (2001) Roles of lipid rafts in membrane transport. Curr Opin Cell Biol 13(4):470–477PubMedCrossRefGoogle Scholar
  30. Jacobson K, Mouritsen OG, Anderson RG (2007) Lipid rafts: at a crossroad between cell biology and physics. Nat Cell Biol 9:7–14PubMedCrossRefGoogle Scholar
  31. Katagiri YU, Kiyokawa N, Fujimoto J (2001) A role for lipid rafts in immune cell signaling. Microbiol Immunol 45:1–8PubMedGoogle Scholar
  32. Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua, NH (1999) Rac homologues and compartmentalized phosphatidylinositol 4,5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145:317–330PubMedCrossRefGoogle Scholar
  33. Kubler E, Dohlman HG, Lisanti MP (1996) Identification of Triton X-100 insoluble membrane domains in the yeast Saccharomyces cerevisiae. Lipid requirements for targeting of heterotrimeric G-protein subunits. J Biol Chem 271:32975–32980PubMedCrossRefGoogle Scholar
  34. Lefebvre B, Furt F, Hartmann MA, Michaelson LV, Carde JP, Sargueil-Boiron F, Rossignol M, Napier JA, Cullimore J, Bessoule JJ, Mongrand S (2007) Characterization of lipid rafts from Medicago truncatula root plasma membranes: a proteomic study reveals the presence of a raft-associated redox system. Plant Physiol 144:402–418PubMedCrossRefGoogle Scholar
  35. Lherminier J, Elmayan T, Fromentin J, Tantaoui Elaraquia K, Vesa S, Morel J, Verrier JL, Cailleteau B, Blein JP, Simon-Plas F (2009) NADPH oxidase mediated Ros production: subcellular localization and reassesment of its role in plant defense. MPMI in pressGoogle Scholar
  36. Li PL, Gulbins E (2007) Lipid rafts and redox signaling. Antioxid. Redox Signal 9:1411–1415PubMedCrossRefGoogle Scholar
  37. Lu Y, Cederbaum A (2007) The mode of cisplatin-induced cell death in CYP2E1-overexpressing HepG2 cells: modulation by ERK, ROS, glutathione, and thioredoxin. Free Radic Biol Med 43:1061–1075PubMedCrossRefGoogle Scholar
  38. Malinska K, Malinsky J, Opekarova M, Tanner W (2003) Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol Biol Cell 14:4427–4436PubMedCrossRefGoogle Scholar
  39. Malinska K, Malinsky J, Opekarova M, Tanner W (2004) Distribution of Can1p into stable domains reflects lateral protein segregation within the plasma membrane of living S. cerevisiae cells. J Cell Sci 117:6031–6041PubMedCrossRefGoogle Scholar
  40. Mika A, Minibayeva F, Beckett R, Lüthje S (2004) Possible functions of extracellular peroxidases in stress-induced generation and detoxification of active oxygen species. Phytochem Rev 3:173–193CrossRefGoogle Scholar
  41. Miura H, Bosnjak JJ, Ning G, Saito T, Miura M, Gutterman DD (2003) Role for hydrogen peroxide in flow-induced dilation of human coronary arterioles. Circ Res 92:e31–40PubMedCrossRefGoogle Scholar
  42. 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 characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. J Biol Chem 279:36277–36286CrossRefGoogle Scholar
  43. Morel J, Claverol S, Mongrand S, Furt F, Fromentin J, Bessoule JJ, Blein JP, Simon-Plas F (2006) Proteomics of plant detergent resistant membranes. Mol Cell Proteomics 5:1396–1411PubMedCrossRefGoogle Scholar
  44. Niemela PS, Ollila S, Hyvonen MT, Karttunen M, Vattulainen I (2007) Assessing the nature of lipid raft membranes. PLoS Comput Biol 3(2):e34PubMedCrossRefGoogle Scholar
  45. Nanasato Y, Akashi K, Yokota A (2005) Co-expression of cytochrome b561 and ascorbate oxidase in leaves of wild watermelon under drought and high light conditions. Plant Cell Physiol 46:1515–1524PubMedCrossRefGoogle Scholar
  46. Pauly N, Pucciariello C, Mandon K, Innocenti G, Jamet A, Baudouin E, Hérouart D, Frendo P, Puppo A (2006) Reactive oxygen and nitrogen species and glutathione: key players in the legume-Rhizobium symbiosis. J Exp Bot 57:1769–1776PubMedCrossRefGoogle Scholar
  47. Pellinen R, Palva T, Kangasjarvi J (1999) Short communication: subcellular localization of ozone-induced hydrogen peroxide production in birch (Betula pendula) leaf cells. Plant J 20:349–356PubMedCrossRefGoogle Scholar
  48. Pike LJ (2006) Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J Lipid Res 47:1597–1598PubMedCrossRefGoogle Scholar
  49. Powel L (2006) From the archive; Lipid raft idea is floated. J Cell Biol 172:166–167CrossRefGoogle Scholar
  50. Ponting CP (2001) Domain homologues of dopamine beta-hydroxylase and ferric reductase: roles for iron metabolism Hum Mol Genet 10:1853–1858PubMedCrossRefGoogle Scholar
  51. Prior IA, Muncke C, Parton RG, Hancock JF (2003) Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J Cell Biol 160:165–170PubMedCrossRefGoogle Scholar
  52. Rietveld A, Simons K (1998) The differential miscibility of lipids as the basis for the formation of functional membrane rafts. Biochim Biophys Acta 1376:467–479PubMedGoogle Scholar
  53. Roper K Corbeil D, Huttner WB (2000) Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat Cell Biol 2:582–592CrossRefGoogle Scholar
  54. Roche Y, Gerbeau-Pissot P, Buhot B, Thomas D, Bonneau L, Gresti J, Mongrand S, Perrier-Cornet JM, Simon-Plas F (2008) Role of phytosterols in the structuration of plant plasma membrane. FASEB J 22:3980–3991PubMedCrossRefGoogle Scholar
  55. Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290PubMedCrossRefGoogle Scholar
  56. Shahollari B, Peskan-Bergho T, Oelmuller R (2004) Receptor kinases with leucine-rich repeats insoluble plasma membrane microdomains Physiol. Plantarum 122:397–403CrossRefGoogle Scholar
  57. Simon-Plas F, Elmayan T, Blein JP (2002) The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. Plant J 31:137–147PubMedCrossRefGoogle Scholar
  58. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569–572PubMedCrossRefGoogle Scholar
  59. Simons K, van Meer G (1988) Lipid sorting in epithelial cells. Biochemistry 27(17): 6197–6202PubMedCrossRefGoogle Scholar
  60. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31–39PubMedCrossRefGoogle Scholar
  61. Soares FA, Shaughnessy SG, MaClarkey WR, Orr FW (1994) Quantification and morphologic demonstration of reactive oxygen species produced by Walker-256 Tumor-Cells In-Vitro and during metastasis in-vivo. Lab Invest 71:480–489PubMedGoogle Scholar
  62. Stauffer TP, Meyer T (1997) Compartmentalized IgE receptor-mediated signal transduction in living cells. J Cell Biol 139:1447–1454PubMedCrossRefGoogle Scholar
  63. Sutter JU, Campanoni P, Tyrrell M, Blatt MR (2006) Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K+ channel at the plasma membrane. Plant Cell 18:935–954PubMedCrossRefGoogle Scholar
  64. Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–2653PubMedCrossRefGoogle Scholar
  65. Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241–1244PubMedCrossRefGoogle Scholar
  66. Tanimura N, Nagafuku M, Minaki Y, Umeda Y, Hayashi F, Sakakura J, Kato A, Liddicoat DR, Ogata M, Hamaoka T, Kosugi A (2003) Dynamic changes in the mobility of LAT in aggregated lipid rafts upon T cell activation. J Cell Biol 160:125–135PubMedCrossRefGoogle Scholar
  67. Triantafilou M, Manukyan M, Mackie A, Morath S, Hartung T, Heine H, Triantafilou K (2004) Lipoteichoic acid and toll-like receptor 2 internalization and targeting to the Golgi are lipid raft-dependent. J Biol Chem 279:40882–40889PubMedCrossRefGoogle Scholar
  68. Vilhardt F, van Deurs B (2004) The phagocyte NADPH oxidase depends on cholesterol-enriched membrane microdomains for assembly. EMBO J 23:739–748PubMedCrossRefGoogle Scholar
  69. Warren JS, Kunkel RG, Simon RH, Johnson KJ, Ward PA (1989) Ultrastructural cytochemical analysis of oxygen radical-mediated immunoglobulin A immume complex induced lung injury in the rat. Lab Invest 60:651–658PubMedGoogle Scholar
  70. Yamazaki D, Yoshida S, Asami T, Kuchitsu K (2003) Visualization of abscisic acid-perception sites on the plasma membrane of stomatal guard cells. Plant J 35:129–139PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  1. 1.Laboratoire de Biogenèse MembranaireUMR 5200 CNRS-Université de BordeauxBordeauxFrance

Personalised recommendations