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Posttranslational Modifications of Plasma Membrane Proteins and Their Implications for Plant Growth and Development

  • Christian LuschnigEmail author
  • Georg J. SeifertEmail author
Chapter
Part of the Plant Cell Monographs book series (CELLMONO, volume 19)

Abstract

Posttranslational modifications of plasma membrane (PM) proteins are essential for a variety of processes that take place at the interface between cells and their environment. A plethora of PM protein modifications have been identified, several of which have been characterized for their role in the regulation of PM-protein fate. In this chapter, we will focus on a number of selected protein modifications that have been shown to affect protein targeting. Both reversible and irreversible covalent protein modifications appear to affect distinct steps in protein trafficking, and regulate protein association with hydrophobic environments, thereby defining the impact of those proteins on a large variety of plant growth responses.

Keywords

Pollen Tube Root Hair Lipid Modification Elongate Pollen Tube Cellulose Deposition 
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.

References

  1. Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J, Moulinier-Anzola JC, Sieberer T, Friml J, Luschnig C (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8:249–256PubMedCrossRefGoogle Scholar
  2. Albrecht V, Ritz O, Linder S, Harter K, Kudla J (2001) The NAF domain defines a novel protein–protein interaction module conserved in Ca2+-regulated kinases. EMBO J 20:1051–1063PubMedCrossRefGoogle Scholar
  3. Albrecht V, Weinl S, Blazevic D, D’angelo C, Batistic O, Kolukisaoglu U, Bock R, Schulz B, Harter K, Kudla J (2003) The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J 36:457–470PubMedCrossRefGoogle Scholar
  4. Apodaca G, Mostov K (1993) Transcytosis of placental alkaline phosphatase-polymeric immunoglobulin receptor fusion proteins is regulated by mutations of Ser664. J Biol Chem 268:23712–23719PubMedGoogle Scholar
  5. Babu P, Deschenes R, Robinson L (2004) Akr1p-dependent palmitoylation of Yck2p yeast casein kinase 1 is necessary and sufficient for plasma membrane targeting. J Biol Chem 279:27138–27147PubMedCrossRefGoogle Scholar
  6. Baskin TI (2001) On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215:150–171PubMedCrossRefGoogle Scholar
  7. Batistic O, Sorek N, Schultke S, Yalovsky S, Kudla J (2008) Dual fatty acyl modification determines the localization and plasma membrane targeting of CBL/CIPK Ca2+ signaling complexes in Arabidopsis. Plant Cell 20:1346–1362PubMedCrossRefGoogle Scholar
  8. Benjamins R, Ampudia C, Hooykaas P, Offringa R (2003) PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol 132:1623–1630PubMedCrossRefGoogle Scholar
  9. Benjamins R, Malenica N, Luschnig C (2005) Regulating the regulator: the control of auxin transport. Bioessays 27:1246–1255PubMedCrossRefGoogle Scholar
  10. Benting JH, Rietveld AG, Simons K (1999) N-Glycans mediate the apical sorting of a GPI-anchored, raft-associated protein in Madin-Darby canine kidney cells. J Cell Biol 146:313–320PubMedCrossRefGoogle Scholar
  11. Bhatnagar R, Gordon J (1997) Understanding covalent modifications of proteins by lipids: where cell biology and biophysics mingle. Trends Cell Biol 7:14–20PubMedCrossRefGoogle Scholar
  12. Boisson B, Giglione C, Meinnel T (2003) Unexpected protein families including cell defense components feature in the N-myristoylome of a higher eukaryote. J Biol Chem 278:43418–43429PubMedCrossRefGoogle Scholar
  13. Bonetta D, Bayliss P, Sun S, Sage T, Mccourt P (2000) Farnesylation is involved in meristem organization in Arabidopsis. Planta 211:182–190PubMedCrossRefGoogle Scholar
  14. Borner GH, Sherrier DJ, Stevens TJ, Arkin IT, Dupree P (2002) Prediction of glycosylphosphatidylinositol-anchored proteins in arabidopsis. A genomic analysis. Plant Physiol 129:486–499PubMedCrossRefGoogle Scholar
  15. Borner GH, Lilley KS, Stevens TJ, Dupree P (2003) Identification of glycosylphosphatidylinositol-anchored proteins in arabidopsis. A proteomic and genomic analysis. Plant Physiol 132:568–577PubMedCrossRefGoogle Scholar
  16. Bracha K, Lavy M, Yalovsky S (2002) The Arabidopsis AtSTE24 is a CAAX protease with broad substrate specificity. J Biol Chem 277:29856–29864PubMedCrossRefGoogle Scholar
  17. Brady SM, Song S, Dhugga KS, Rafalski JA, Benfey PN (2007) Combining expression and comparative evolutionary analysis. The COBRA gene family. Plant Physiol 143:172–187PubMedCrossRefGoogle Scholar
  18. Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295PubMedCrossRefGoogle Scholar
  19. Cadinanos J, Schmidt W, Fueyo A, Varela I, Lopez-Otin C, Freije J (2003a) Identification, functional expression and enzymic analysis of two distinct CaaX proteases from Caenorhabditis elegans. Biochem J 370:1047–1054PubMedCrossRefGoogle Scholar
  20. Cadinanos J, Varela I, Mandel D, Schmidt W, Diaz-Perales A, Lopez-Otin C, Freije J (2003b) AtFACE-2, a functional prenylated protein protease from Arabidopsis thaliana related to mammalian Ras-converting enzymes. J Biol Chem 278:42091–42097PubMedCrossRefGoogle Scholar
  21. Caldelari D, Sternberg H, Rodriguez-Concepcion M, Gruissem W, Yalovsky S (2001) Efficient prenylation by a plant geranylgeranyltransferase-I requires a functional CaaL box motif and a proximal polybasic domain. Plant Physiol 126:1416–1429PubMedCrossRefGoogle Scholar
  22. Camp L, Hofmann S (1993) Purification and properties of a palmitoyl-protein thioesterase that cleaves palmitate from H-Ras. J Biol Chem 268:22566–22574PubMedGoogle Scholar
  23. Casanova J, Breitfeld P, Ross S, Mostov K (1990) Phosphorylation of the polymeric immunoglobulin receptor required for its efficient transcytosis. Science 248:742–745PubMedCrossRefGoogle Scholar
  24. Coppinger P, Repetti PP, Day B, Dahlbeck D, Mehlert A, Staskawicz BJ (2004) Overexpression of the plasma membrane-localized NDR1 protein results in enhanced bacterial disease resistance in Arabidopsis thaliana. Plant J 40:225–237PubMedCrossRefGoogle Scholar
  25. Crowell D, Sen S, Randall S (1998) Prenylcysteine alpha-carboxyl methyltransferase in suspension-cultured tobacco cells. Plant Physiol 118:115–123PubMedCrossRefGoogle Scholar
  26. Cunnac S, Wilson A, Nuwer J, Kirik A, Baranage G, Mudgett M (2007) A conserved carboxylesterase is a SUPPRESSOR OF AVRBST-ELICITED RESISTANCE in Arabidopsis. Plant Cell 19:688–705PubMedCrossRefGoogle Scholar
  27. Cutler S, Ghassemian M, Bonetta D, Cooney S, Mccourt P (1996) A protein farnesyl transferase involved in abscisic acid signal transduction in Arabidopsis. Science 273:1239–1241PubMedCrossRefGoogle Scholar
  28. Day B, Dahlbeck D, Staskawicz BJ (2006) NDR1 interaction with RIN4 mediates the differential activation of multiple disease resistance pathways in Arabidopsis. Plant Cell 18:2782–2791PubMedCrossRefGoogle Scholar
  29. Duncan J, Gilman A (1998) A cytoplasmic acyl-protein thioesterase that removes palmitate from G protein alpha subunits and p21(RAS). J Biol Chem 273:15830–15837PubMedCrossRefGoogle Scholar
  30. Eisenhaber B, Wildpaner M, Schultz CJ, Borner GH, Dupree P, Eisenhaber F (2003) Glycosylphosphatidylinositol lipid anchoring of plant proteins. Sensitive prediction from sequence- and genome-wide studies for arabidopsis and rice. Plant Physiol 133:1691–1701PubMedCrossRefGoogle Scholar
  31. Elortza F, Nuhse TS, Foster LJ, Stensballe A, Peck SC, Jensen ON (2003) Proteomic analysis of glycosylphosphatidylinositol-anchored membrane proteins. Mol Cell Proteomics 2:1261–1270PubMedCrossRefGoogle Scholar
  32. Elortza F, Mohammed S, Bunkenborg J, Foster LJ, Nuhse TS, Brodbeck U, Peck SC, Jensen ON (2006) Modification-specific proteomics of plasma membrane proteins: identification and characterization of glycosylphosphatidylinositol-anchored proteins released upon phospholipase D treatment. J Proteome Res 5:935–943PubMedCrossRefGoogle Scholar
  33. Friml J, Benkova E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jürgens G, Palme K (2002) AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108:661–673PubMedCrossRefGoogle Scholar
  34. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153PubMedCrossRefGoogle Scholar
  35. Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk P, Ljung K, Sandberg G, Hooykaas P, Palme K, Offringa R (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306:862–865PubMedCrossRefGoogle Scholar
  36. Galichet A, Gruissem W (2003) Protein farnesylation in plants – conserved mechanisms but different targets. Curr Opin Plant Biol 6:530–535PubMedCrossRefGoogle Scholar
  37. Galvan-Ampudia CS, Offringa R (2007) Plant evolution: AGC kinases tell the auxin tale. Trends Plant Sci 12:541–547PubMedCrossRefGoogle Scholar
  38. Gälweiler L, Guan C, Müller 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
  39. Gillmor CS, Lukowitz W, Brininstool G, Sedbrook JC, Hamann T, Poindexter P, Somerville C (2005) Glycosylphosphatidylinositol-anchored proteins are required for cell wall synthesis and morphogenesis in arabidopsis. Plant Cell 17:1128–1140PubMedCrossRefGoogle Scholar
  40. Goritschnig S, Weihmann T, Zhang Y, Fobert P, Mccourt P, Li X (2008) A novel role for protein farnesylation in plant innate immunity. Plant Physiol 148:348–357PubMedCrossRefGoogle Scholar
  41. Haglund K, Dikic I (2005) Ubiquitylation and cell signaling. EMBO J 24:3353–3359PubMedCrossRefGoogle Scholar
  42. Hauser MT, Morikami A, Benfey PN (1995) Conditional root expansion mutants of Arabidopsis. Development 121:1237–1252PubMedGoogle Scholar
  43. Hemsley P, Grierson C (2008) Multiple roles for protein palmitoylation in plants. Trends Plant Sci 13:295–302PubMedCrossRefGoogle Scholar
  44. Hemsley P, Kemp A, Grierson C (2005) The TIP GROWTH DEFECTIVE1 S-acyl transferase regulates plant cell growth in Arabidopsis. Plant Cell 17:2554–2563PubMedCrossRefGoogle Scholar
  45. Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19:141–172PubMedCrossRefGoogle Scholar
  46. Hicke L, Zanolari B, Riezman H (1998) Cytoplasmic tail phosphorylation of the alpha-factor receptor is required for its ubiquitination and internalization. J Cell Biol 141:349–358PubMedCrossRefGoogle Scholar
  47. Hochholdinger F, Wen TJ, Zimmermann R, Chimot-Marolle P, da Costa e Silva O, Bruce W, Lamkey KR, Wienand U, Schnable PS (2008) The maize (Zea mays L.) roothairless 3 gene encodes a putative GPI-anchored, monocot-specific, COBRA-like protein that significantly affects grain yield. Plant J 54:888–898PubMedCrossRefGoogle Scholar
  48. Ishitani M, Liu J, Halfter U, Kim C, Shi W, Zhu J (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12:1667–1678PubMedGoogle Scholar
  49. Jacobson K, Mouritsen OG, Anderson RG (2007) Lipid rafts: at a crossroad between cell biology and physics. Nat Cell Biol 9:7–14PubMedCrossRefGoogle Scholar
  50. Johnson C, Chary S, Chernoff E, Zeng Q, Running M, Crowell D (2005) Protein geranylgeranyltransferase I is involved in specific aspects of abscisic acid and auxin signaling in Arabidopsis. Plant Physiol 139:722–733PubMedCrossRefGoogle Scholar
  51. Jones MA, Raymond MJ, Smirnoff N (2006) Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in arabidopsis. Plant J 45:83–100PubMedCrossRefGoogle Scholar
  52. Jürgens G, Geldner N (2007) The high road and the low road: trafficking choices in plants. Cell 130:977–979PubMedCrossRefGoogle Scholar
  53. Kim B, Waadt R, Cheong Y, Pandey G, Dominguez-Solis JR, Schultke S, Lee S, Kudla J, Luan S (2007) The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J 52:473–484PubMedCrossRefGoogle Scholar
  54. Kleine-Vehn J, Friml J (2008) Polar targeting and endocytic recycling in auxin-dependent plant development. Annu Rev Cell Dev Biol 24:447–473PubMedCrossRefGoogle Scholar
  55. Kolukisaoglu U, Weinl S, Blazevic D, Batistic O, Kudla J (2004) Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. Plant Physiol 134:43–58PubMedCrossRefGoogle Scholar
  56. Lalanne E, Honys D, Johnson A, Borner GH, Lilley KS, Dupree P, Grossniklaus U, Twell D (2004) SETH1 and SETH2, two components of the glycosylphosphatidylinositol anchor biosynthetic pathway, are required for pollen germination and tube growth in arabidopsis. Plant Cell 16:229–240PubMedCrossRefGoogle Scholar
  57. Lamport DTA, Kieliszewski MJ, Showalter AM (2006) Salt stress upregulates periplasmic arabinogalactan proteins: using salt stress to analyse AGP function. New Phytol 169:479–492PubMedCrossRefGoogle Scholar
  58. Lemichez E, Wu Y, Sanchez J, Mettouchi A, Mathur J, Chua N (2001) Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes Dev 15:1808–1816PubMedCrossRefGoogle Scholar
  59. Loraine A, Yalovsky S, Fabry S, Gruissem W (1996) Tomato Rab1A homologs as molecular tools for studying Rab geranylgeranyl transferase in plant cells. Plant Physiol 110:1337–1347PubMedCrossRefGoogle Scholar
  60. Magee T, Seabra M (2005) Fatty acylation and prenylation of proteins: what’s hot in fat. Curr Opin Cell Biol 17:190–196PubMedCrossRefGoogle Scholar
  61. Maurer-Stroh S, Eisenhaber B, Eisenhaber F (2002a) N-terminal N-myristoylation of proteins: refinement of the sequence motif and its taxon-specific differences. J Mol Biol 317:523–540PubMedCrossRefGoogle Scholar
  62. Maurer-Stroh S, Eisenhaber B, Eisenhaber F (2002b) N-terminal N-myristoylation of proteins: prediction of substrate proteins from amino acid sequence. J Mol Biol 317:541–557PubMedCrossRefGoogle Scholar
  63. Maurer-Stroh S, Washietl S, Eisenhaber F (2003) Protein prenyltransferases. Genome Biol 4:212PubMedCrossRefGoogle Scholar
  64. Maurer-Stroh S, Koranda M, Benetka W, Schneider G, Sirota F, Eisenhaber F (2007) Towards complete sets of farnesylated and geranylgeranylated proteins. PLoS Comput Biol 3:e66PubMedCrossRefGoogle Scholar
  65. McCabe PF, Valentine TA, Forsberg LS, Pennell RI (1997) Soluble signals from cells identified at the cell wall establish a developmental pathway in carrot. Plant Cell 9:2225–2241PubMedGoogle Scholar
  66. Michniewicz M, Zago M, Abas L, Weijers D, Schweighofer A, Meskiene I, Heisler M, Ohno C, Zhang J, Huang F, Schwab R, Weigel D, Meyerowitz E, Luschnig C, Offringa R, Friml J (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130:1044–1056PubMedCrossRefGoogle Scholar
  67. Molendijk A, Bischoff F, Rajendrakumar C, Friml J, Braun M, Gilroy S, Palme K (2001) Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J 20:2779–2788PubMedCrossRefGoogle Scholar
  68. Motose H, Sugiyama M, Fukuda H (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature 429:873–878PubMedCrossRefGoogle Scholar
  69. Müller A, Guan C, Galweiler L, Tanzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 17:6903–6911PubMedCrossRefGoogle Scholar
  70. Murphy AS, Hoogner KR, Peer WA, Taiz L (2002) Identification, purification, and molecular cloning of N-1-naphthylphthalmic acid-binding plasma membrane-associated aminopeptidases from Arabidopsis. Plant Physiol 128:935–950PubMedCrossRefGoogle Scholar
  71. Nguema-Ona E, Bannigan A, Chevalier L, Baskin TI, Driouich A (2007) Disruption of arabinogalactan proteins disorganizes cortical microtubules in the root of Arabidopsis thaliana. Plant J 52:240–251PubMedCrossRefGoogle Scholar
  72. Nothnagel EA (1997) Proteoglycans and related components in plant cells. Int Rev Cytol 174:195–291PubMedCrossRefGoogle Scholar
  73. Orlean P, Menon AK (2007) Thematic review series: lipid posttranslational modifications. GPI anchoring of protein in yeast and mammalian cells, or: how we learned to stop worrying and love glycophospholipids. J Lipid Res 48:993–1011PubMedCrossRefGoogle Scholar
  74. Oxley D, Bacic A (1999) Structure of the glycosylphosphatidylinositol anchor of an arabinogalactan protein from Pyrus communis suspension-cultured cells. Proc Natl Acad Sci USA 96:14246–14251PubMedCrossRefGoogle Scholar
  75. Paladino S, Sarnataro D, Pillich R, Tivodar S, Nitsch L, Zurzolo C (2004) Protein oligomerization modulates raft partitioning and apical sorting of GPI-anchored proteins. J Cell Biol 167:699–709PubMedCrossRefGoogle Scholar
  76. Paulick MG, Bertozzi CR (2008) The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins. Biochemistry 17:17Google Scholar
  77. Pei Z, Ghassemian M, Kwak C, Mccourt P, Schroeder J (1998) Role of farnesyltransferase in ABA regulation of guard cell anion channels and plant water loss. Science 282:287–290PubMedCrossRefGoogle Scholar
  78. Petrasek J, Mravec J, Bouchard R, Blakeslee J, Abas M, Seifertova D, Wisniewska J, Tadele Z, Kubes M, Covanova M, Dhonukshe P, Skupa P, Benkova E, Perry L, Krecek P, Lee O, Fink G, Geisler M, Murphy A, Luschnig C, Zazimalova E, Friml J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–918PubMedCrossRefGoogle Scholar
  79. Pierre M, Traverso J, Boisson B, Domenichini S, Bouchez D, Giglione C, Meinnel T (2007) N-myristoylation regulates the SnRK1 pathway in Arabidopsis. Plant Cell 19:2804–2821PubMedCrossRefGoogle Scholar
  80. Polge C, Thomas M (2007) SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control. Trends Plant Sci 12:20–28PubMedCrossRefGoogle Scholar
  81. Potter BA, Hughey RP, Weisz OA (2006) Role of N- and O-glycans in polarized biosynthetic sorting. Am J Physiol Cell Physiol 290:C1–C10PubMedCrossRefGoogle Scholar
  82. Qi Q, Rajala R, Anderson W, Jiang C, Rozwadowski K, Selvaraj G, Sharma R, Datla R (2000) Molecular cloning, genomic organization, and biochemical characterization of myristoyl-CoA:protein N-myristoyltransferase from Arabidopsis thaliana. J Biol Chem 275:9673–9683PubMedCrossRefGoogle Scholar
  83. Qian D, Zhou D, Ju R, Cramer C, Yang Z (1996) Protein farnesyltransferase in plants: molecular characterization and involvement in cell cycle control. Plant Cell 8:2381–2394PubMedGoogle Scholar
  84. Randall S, Marshall M, Crowell D (1993) Protein isoprenylation in suspension-cultured tobacco cells. Plant Cell 5:433–442PubMedGoogle Scholar
  85. Resh M (1999) Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim Biophys Acta 1451:1–16PubMedCrossRefGoogle Scholar
  86. Rocks O, Peyker A, Kahms M, Verveer P, Koerner C, Lumbierres M, Kuhlmann J, Waldmann H, Wittinghofer A, Bastiaens P (2005) An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 307:1746–1752PubMedCrossRefGoogle Scholar
  87. Rodriguez-Concepcion M, Toledo-Ortiz G, Yalovsky S, Caldelari D, Gruissem W (2000) Carboxyl-methylation of prenylated calmodulin CaM53 is required for efficient plasma membrane targeting of the protein. Plant J 24:775–784PubMedCrossRefGoogle Scholar
  88. Roskoski RJ (2003) Protein prenylation: a pivotal posttranslational process. Biochem Biophys Res Commun 303:1–7PubMedCrossRefGoogle Scholar
  89. Roth A, Feng Y, Chen L, Davis N (2002) The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase. J Cell Biol 159:23–28PubMedCrossRefGoogle Scholar
  90. Roudier F, Schindelman G, DeSalle R, Benfey PN (2002) The COBRA family of putative GPI-anchored proteins in Arabidopsis. A new fellowship in expansion. Plant Physiol 130:538–548PubMedCrossRefGoogle Scholar
  91. Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GH, Schindelman G, Song S, Baskin TI, Dupree P, Wasteneys GO, Benfey PN (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17:1749–1763PubMedCrossRefGoogle Scholar
  92. Running M, Lavy M, Sternberg H, Galichet A, Gruissem W, Hake S, Ori N, Yalovsky S (2004) Enlarged meristems and delayed growth in plp mutants result from lack of CaaX prenyltransferases. Proc Natl Acad Sci USA 101:7815–7820PubMedCrossRefGoogle Scholar
  93. Sardar HS, Yang J, Showalter AM (2006) Molecular interactions of arabinogalactan proteins with cortical microtubules and F-actin in Bright Yellow-2 tobacco cultured cells. Plant Physiol 142:1469–1479PubMedCrossRefGoogle Scholar
  94. Sauer M, Balla J, Luschnig C, Wisniewska J, Reinohl V, Friml J, Benkova E (2006) Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 20:2902–2911PubMedCrossRefGoogle Scholar
  95. Schafer W, Trueblood C, Yang C, Mayer M, Rosenberg S, Poulter C, Kim S, Rine J (1990) Enzymatic coupling of cholesterol intermediates to a mating pheromone precursor and to the ras protein. Science 249:1133–1139PubMedCrossRefGoogle Scholar
  96. Schiefelbein J, Galway M, Masucci J, Ford S (1993) Pollen tube and root-hair tip growth is disrupted in a mutant of Arabidopsis thaliana. Plant Physiol 103:979–985PubMedCrossRefGoogle Scholar
  97. Schindelman G, Morikami A, Jung J, Baskin TI, Carpita NC, Derbyshire P, McCann MC, Benfey PN (2001) COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev 15:1115–1127PubMedCrossRefGoogle Scholar
  98. Schuck S, Simons K (2004) Polarized sorting in epithelial cells: raft clustering and the biogenesis of the apical membrane. J Cell Sci 117:5955–5964PubMedCrossRefGoogle Scholar
  99. Schultz CJ, Gilson P, Oxley D, Youl JJ, Bacic A (1998) GPI-anchors an arabinogalactan-proteins: implications for signalling in plants. Trends Plant Sci 3:426–431CrossRefGoogle Scholar
  100. Schultz CJ, Rumsewicz MP, Johnson KL, Jones BJ, Gaspar YM, Bacic A (2002) Using genomic resources to guide research directions. The arabinogalactan protein gene family as a test case. Plant Physiol 129:1448–1463PubMedCrossRefGoogle Scholar
  101. Sedbrook JC, Carroll KL, Hung KF, Masson PH, Somerville CR (2002) The Arabidopsis SKU5 gene encodes an extracellular glycosyl phosphatidylinositol-anchored glycoprotein involved in directional root growth. Plant Cell 14:1635–1648PubMedCrossRefGoogle Scholar
  102. Seifert GJ, Roberts K (2007) The biology of arabinogalactan-proteins. Annu Rev Plant Biol 58:137–161PubMedCrossRefGoogle Scholar
  103. Shahinian S, Silvius J (1995) Doubly-lipid-modified protein sequence motifs exhibit long-lived anchorage to lipid bilayer membranes. Biochemistry 34:3813–3822PubMedCrossRefGoogle Scholar
  104. Shahollari B, Peskan-Berghofer T, Oelmuller R (2004) Receptor kinases with leucine-rich repeats are enriched in Triton X-100 insoluble plasma membrane microdomains from plants. Physiol Plant 122:397–403CrossRefGoogle Scholar
  105. Shenoy S, Mcdonald P, Kohout T, Lefkowitz R (2001) Regulation of receptor fate by ubiquitination of activated beta 2-adrenergic receptor and beta-arrestin. Science 294:1307–1313PubMedCrossRefGoogle Scholar
  106. Shi H, Kim Y, Guo Y, Stevenson B, Zhu JK (2003) The arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell 15:19–32PubMedCrossRefGoogle Scholar
  107. Showalter AM (2001) Arabinogalactan-proteins: structure, expression and function. Cell Mol Life Sci 58:1399–1417PubMedCrossRefGoogle Scholar
  108. Sorek N, Poraty L, Sternberg H, Bar E, Lewinsohn E, Yalovsky S (2007) Activation status-coupled transient S acylation determines membrane partitioning of a plant Rho-related GTPase. Mol Cell Biol 27:2144–2154PubMedCrossRefGoogle Scholar
  109. Sun B, Chen L, Cao W, Roth A, Davis N (2004) The yeast casein kinase Yck3p is palmitoylated, then sorted to the vacuolar membrane with AP-3-dependent recognition of a YXXPhi adaptin sorting signal. Mol Biol Cell 15:1397–1406PubMedCrossRefGoogle Scholar
  110. Svetek J, Yadav MP, Nothnagel EA (1999) Presence of a glycosylphosphatidylinositol lipid anchor on rose arabinogalactan proteins. J Biol Chem 274:14724–14733PubMedCrossRefGoogle Scholar
  111. Tam A, Schmidt W, Michaelis S (2001) The multispanning membrane protein Ste24p catalyzes CAAX proteolysis and NH2-terminal processing of the yeast a-factor precursor. J Biol Chem 276:46798–46806PubMedCrossRefGoogle Scholar
  112. Tanimura N, Saitoh S, Kawano S, Kosugi A, Miyake K (2006) Palmitoylation of LAT contributes to its subcellular localization and stability. Biochem Biophys Res Commun 341:1177–1183PubMedCrossRefGoogle Scholar
  113. Thompson GJ, Okuyama H (2000) Lipid-linked proteins of plants. Prog Lipid Res 39:19–39PubMedCrossRefGoogle Scholar
  114. Titapiwatanakun B, Blakeslee JJ, Bandyopadhyay A, Yang H, Mravec J, Sauer M, Cheng Y, Adamec J, Nagashima A, Geisler M, Sakai T, Friml J, Peer WA, Murphy AS (2009) ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. Plant J 57:27–44PubMedCrossRefGoogle Scholar
  115. Vieten A, Sauer M, Brewer P, Friml J (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci 12:160–168PubMedCrossRefGoogle Scholar
  116. Vogel JP, Raab TK, Schiff C, Somerville SC (2002) PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in arabidopsis. Plant Cell 14:2095–2106PubMedCrossRefGoogle Scholar
  117. Wasteneys GO, Fujita M (2006) Establishing and maintaining axial growth: wall mechanical properties and the cytoskeleton. J Plant Res 119:5–10PubMedCrossRefGoogle Scholar
  118. Wilcox C, Hu J, Olson E (1987) Acylation of proteins with myristic acid occurs cotranslationally. Science 238:1275–1278PubMedCrossRefGoogle Scholar
  119. Wisniewska J, Xu J, Seifertova D, Brewer P, Ruzicka K, Blilou I, Rouquie D, Benkova E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883PubMedCrossRefGoogle Scholar
  120. Yalovsky S, Loraine A, Gruissem W (1996) Specific prenylation of tomato rab proteins by geranylgeranyl type-II transferase requires a conserved cysteine-cysteine motif. Plant Physiol 110:1349–1359PubMedGoogle Scholar
  121. Yalovsky S, Rodriguez-Concepcion M, Bracha K, Toledo-Ortiz G, Gruissem W (2000) Prenylation of the floral transcription factor APETALA1 modulates its function. Plant Cell 12:1257–1266PubMedGoogle Scholar
  122. Yang Z, Cramer C, Watson J (1993) Protein farnesyltransferase in plants. Molecular cloning and expression of a homolog of the beta subunit from the garden pea. Plant Physiol 101:667–674PubMedCrossRefGoogle Scholar
  123. Zegzouti H, Anthony R, Jahchan N, Bogre L, Christensen S (2006) Phosphorylation and activation of PINOID by the phospholipid signaling kinase 3-phosphoinositide-dependent protein kinase 1 (PDK1) in Arabidopsis. Proc Natl Acad Sci USA 103:6404–6409PubMedCrossRefGoogle Scholar
  124. Zhu J, Bressan R, Hasegawa P (1993) Isoprenylation of the plant molecular chaperone ANJ1 facilitates membrane association and function at high temperature. Proc Natl Acad Sci USA 90:8557–8561PubMedCrossRefGoogle Scholar
  125. Ziegelhoffer E, Medrano L, Meyerowitz E (2000) Cloning of the Arabidopsis WIGGUM gene identifies a role for farnesylation in meristem development. Proc Natl Acad Sci USA 97:7633–7638PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.Department of Applied Genetics and Cell BiologyUniversity of Natural Resources and Life Sciences (BOKU)ViennaAustria
  2. 2.Department of Applied Genetics and Cell BiologyUniversity of Natural Resources and Life Sciences (BOKU)A-1190 ViennaAustria

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