Dual lipid modification of Arabidopsis Gγ-subunits is required for efficient plasma membrane targeting

Plant Physiology

Volumn 143, Issue 3, 2007, Pages 1119-1131

  Zeng, Qin ^a   Wang, Xuejun ^a   Running, Mark P ^a  

^a DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; LIPIDS; PROTEINS;

ARABIDOPSIS; EUKARYOTIC CELLS; LIPID MODIFICATION;

PLANTS (BOTANY);

LIPIDS; MEMBRANES; PLANTS; PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA; MAMMALIA;

EID: 34250619111     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.106.093583     Document Type: Article

References (91)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen HM, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
2. Bonetta D, Bayliss P, Sun S, Sage T, McCourt P (2000) Farnesylation is involved in meristem organization in Arabidopsis. Planta 211: 182-190
3. Booden MA, Baker TL, Solski PA, Der CJ, Punke SG, Buss JE (1999) A non-farnesylated Ha-Ras protein can be palmitoylated and trigger potent differentiation and transformation. J Biol Chem 274: 1423-1431
4. Bracha K, Lavy M, Yalovsky S (2002) The Arabidopsis AtSTE24 is a CAAX protease with broad substrate specificity. J Biol Chem 277: 29856-29864
5. Cabrera-Vera TM, Vanhauwe J, Thomas TO, Medkova M, Preininger A, Mazzoni MR, Hamm HE (2003) Insights into G protein structure, function, and regulation. Endocr Rev 24: 765-781
6. 12-oleic acid desaturases. J Biol Chem 279: 12495-12502
7. 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: 1416-1429
8. Casey PJ (1995) Protein lipidation in cell signaling. Science 268: 221-225
9. Chen J-G, Gao Y, Jones AM (2006) Differential roles of Arabidopsis heterotrimeric G-protein subunits in modulating cell division in roots. Plant Physiol 141: 887-897
10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
11. Coursol S, Fan LM, Le Stunff H, Spiegel S, Gilroy S, Assmann SM (2003) Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature 423: 651-654
12. Crowell DN, Kennedy M (2001) Identification and functional expression in yeast of a prenylcysteine alpha-carboxyl methyltransferase gene from Arabidopsis thaliana. Plant Mol Biol 45: 469-476
13. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462-469
14. 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: 1239-1241
15. Dietrich A, Schee A, Illenberger D, Kloog Y, Henis Y, Gierschik P (2003) Studies on G-protein alpha.betagamma heterotrimer formation reveal a putative S-prenyl-binding site in the alpha subunit. Biochem J 376: 449-456
16. Dixit R, Cyr R, Gilroy S (2006) Using intrinsically fluorescent proteins for plant cell imaging. Plant J 45: 599-615
17. Dong X, Mitchell DA, Lobo S, Zhao L, Bartels DJ, Deschenes RJ (2003) Palmitoylation and plasma membrane localization of Ras2p by a non-classical trafficking pathway in Saccharomyces cerevisiae. Mol Cell Biol 23: 6574-6584
18. Downes BP, Saracco SA, Lee SS, Crowell DN, Vierstra RD (2006) MUBs, a family of ubiquitin-fold proteins that are plasma membrane-anchored by prenylation. J Biol Chem 281: 27145-27157
19. αi to these domains requires palmitoyltransferase activity. J Biol Chem 276: 43300-43304
20. Dunphy JT, Schroeder H, Leventis R, Greentree WK, Knudsen JK, Silvius JR, Linder ME (2000) Differential effects of acyl-CoA binding protein on enzymatic and non-enzymatic thioacylation of protein and peptide substrates. Biochim Biophys Acta 1485: 185-198
21. Dykema P, Sipes P, Marie A, Biermann B, Crowell D, Randall S (1999) A new class of proteins capable of binding transition metals. Plant Mol Biol 41: 139-150
22. Falquet L, Pagni M, Bucher P, Hulo N, Sigrist CJA, Hofmann K, Bairoch A (2002) The PROSITE database, its status in 2002. Nucleic Acids Res 30: 235-238
23. Fan LM, Zhao Z, Assmann SM (2004) Guard cells: a dynamic signaling model. Curr Opin Plant Biol 7: 537-546
24. Galichet A, Gruissem W (2006) Developmentally controlled farnesylation modulates AtNAP1;1 function in cell proliferation and cell expansion during Arabidopsis leaf development. Plant Physiol 142: 1412-1426
25. Galy V, Mattaj IW, Askjaer P (2003) Caenorhabditis elegans nucleoporins Nup93 and Nup205 determine the limit of nuclear pore complex size exclusion in vivo. Mol Biol Cell 14: 5104-5115
26. Gietz RD, Woods RA (2002) Transformation of yeast by the LiAc/SS carrier DNA/PEG method. Methods Enzymol 350: 87-96
27. Hancock J, Cadwallader K, Marshall C (1991) Methylation and proteolysis are essential for efficient membrane binding of prenylated p21K-ras(B). EMBO J 10: 641-646
28. Hancock JF, Magee AI, Childs JE, Marshall CJ (1989) All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57: 1167-1177
29. Hancock JF, Paterson H, Marshall CJ (1990) A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell 63: 133-139
30. He B, Chen P, Chen S, Vancura K, Michaelis S, Powers S (1991) RAM2, an essential gene of yeast, and RAM1 encode the two polypeptide components of the farnesyltransferase that prenylates a-factor and Ras proteins. Proc Natl Acad Sci USA 88: 11373-11377
31. Hemsley PA, Kemp AC, Grierson CS (2005) The TIP GROWTH DEFECTIVE1 S-acyl transferase regulates plant cell growth in Arabidopsis. Plant Cell 17: 2554-2563
32. Hirschman JE, Jenness DD (1999) Dual lipid modification of the yeast Gγ subunit Ste18p determines membrane localization of Gβγ. Mol Cell Biol 19: 7705-7711
33. James GL, Goldstein JL, Brown MS (1995) Polylysine and CVIM sequences of K-RasB dictate specificity of prenylation and confer resistance to benzodiazepine peptidomimetic in vitro. J Biol Chem 270: 6221-6226
34. Johnson CD, Chary SN, Chernoff EN, Zeng Q, Running MP, Crowell DN (2005) Protein geranylgeranyltransferase I is involved in specific aspects of abscisic acid and auxin signaling in Arabidopsis. Plant Physiol 139: 722-733
35. Jones AM (2002) G-protein-coupled signaling in Arabidopsis. Curr Opin Plant Biol 5: 402-407
36. Jones AM, Assmann SM (2004) Plants: the latest model system for G-protein research. EMBO Rep 5: 572-578
37. Kato C, Mizutani T, Tamaki H, Kumagai H, Kamiya T, Hirobe A, Fujisawa Y, Kato H, Iwasaki Y (2004) Characterization of heterotrimeric G protein complexes in rice plasma membrane. Plant J 38: 320-331
38. Lane K, Beese L (2006) Thematic review series: lipid posttranslational modifications. Structural biology of protein farnesyltransferase and geranylgeranyltransferase type I. J Lipid Res 47: 681-699
39. Lavy M, Bracha-Drori K, Sternberg H, Yalovsky S (2002) A cell-specific, prenylation-independent mechanism regulates targeting of type II RACs. Plant Cell 14: 2431-2450
40. Lavy M, Yalovsky S (2006) Association of Arabidopsis type-II ROPs with the plasma membrane requires a conserved C-terminal sequence motif and a proximal polybasic domain. Plant J 46: 934-947
41. Lease KA, Wen J, Li J, Doke JT, Liscum E, Walker JC (2001) A mutant Arabidopsis heterotrimeric G-protein β-subunit affects leaf, flower, and fruit development. Plant Cell 13: 2631-2641
42. Lobo S, Greentree WK, Linder ME, Deschenes RJ (2002) Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J Biol Chem 277: 41268-41273
43. Ma H, Yanofsky M, Meyerowitz E (1990) Molecular cloning and characterization of GPA1, a G protein α subunit gene from Arabidopsis thaliana. Proc Natl Acad Sci USA 87: 3821-3825
44. Magee AI, Seabra MC (2003) Are prenyl groups on proteins sticky fingers or greasy handles? Biochem J 376: e3-e4
45. Magee T, Marshall C (1999) New insights into the interaction of Ras with the plasma membrane. Cell 98: 9-12
46. Manahan CL, Patnana M, Blumer KJ, Linder ME (2000) Dual lipid modification motifs in Galpha and Ggamma subunits are required for full activity of the pheromone response pathway in Saccharomyces cerevisiae. Mol Biol Cell 11: 957-968
47. Mason MG, Botella JR (2000) Completing the heterotrimer: isolation and characterization of an Arabidopsis thaliana G protein gamma-subunit cDNA. Proc Natl Acad Sci USA 97: 14784-14788
48. Mason MG, Botella JR (2001) Isolation of a novel G-protein γ-subunit from Arabidopsis thaliana and its interaction with Gβ. Biochim Biophys Acta 1520: 147-153
49. Maurer-Stroh S, Eisenhaber F (2005) Refinement and prediction of protein prenylation motifs. Genome Biol 6: r55
50. Michaelson D, Ahearn I, Bergo M, Young S, Philips M (2002) Membrane trafficking of heterotrimeric G proteins via the endoplasmic reticulum and Golgi. Mol Biol Cell 13: 3294-3302
51. Michaelson D, Silletti J, Murphy G, D'Eustachio P, Rush M, Philips MR (2001) Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J Cell Biol 152: 111-126
52. Milligan G, Parenti M, Magee AI (1995) The dynamic role of palmitoylation in signal transduction. Trends Biochem Sci 20: 181-186
53. Mishra G, Zhang W, Deng F, Zhao J, Wang X (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312: 264-266
54. Mitchell DA, Vasudevan A, Linder ME, Deschenes RJ (2006) Protein palmitoylation by a family of DHHC protein S-acyltransferases. J Lipid Res 47: 1118-1127
55. Narasimha Chary S, Bultema RL, Packard CE, Crowell DN (2002) Prenylcysteine alpha-carboxyl methyltransferase expression and function in Arabidopsis thaliana. Plant J 32: 735-747
56. Nebenfuhr A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM, Meehl JB, Staehelin LA (1999) Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol 121: 1127-1141
57. Pandey S, Chen J-G, Jones AM, Assmann SM (2006) G-protein complex mutants are hypersensitive to abscisic acid regulation of germination and postgermination development. Plant Physiol 141: 243-256
58. Perfus-Barbeoch L, Jones AM, Assmann SM (2004) Plant heterotrimeric G protein function: insights from Arabidopsis and rice mutants. Curr Opin Plant Biol 7: 719-731
59. Preuss ML, Serna J, Falbel TG, Bednarek SY, Nielsen E (2004) The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 16: 1589-1603
60. Pronin AN, Gautam N (1993) Proper processing of a G protein γ subunit depends on complex formation with a β subunit. FEBS Lett 328: 89-93
61. Randall SK, Marshall MS, Crowell DN (1993) Protein isoprenylation in suspension-cultured tobacco cells. Plant Cell 5: 433-442
62. Resh MD (2006a) Palmitoylation of ligands, receptors, and intracellular signaling molecules. Sci. STKE 2006: re14
63. Resh MD (2006b) Use of analogs and inhibitors to study the functional significance of protein palmitoylation. Methods 40: 191-197
64. 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: 775-784
65. Rodriguez-Concepcion M, Yalovsky S, Zik M, Fromm H, Gruissem W (1999) The prenylation status of a novel plant calmodulin directs plasma membrane or nuclear localization of the protein. EMBO J 18: 1996-2007
66. Roth AF, Feng Y, Chen L, Davis NG (2002) The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase. J Cell Biol 159: 23-28
67. Roth AF, Wan J, Bailey AO, Sun B, Kuchar JA, Green WN, Phinney BS, Yates JR III, Davis NG (2006) Global analysis of protein palmitoylation in yeast. Cell 125: 1003-1013
68. Running MP, Fletcher JC, Meyerowitz EM (1998) The WIGGUM gene is required for proper regulation of floral meristem size in Arabidopsis. Development 125: 2545-2553
69. Running MP, Lavy M, Sternberg H, Galichet A, Gruissem W, Hake S, Or N, Yalovsky S (2004) Enlarged meristems and delayed growth in plp mutants result from lack of CaaX prenyltransferases. Proc Natl Acad Sci USA 101: 7815-7820
70. Seabra M, Goldstein J, Sudhof T, Brown M (1992) Rab geranylgeranyl transferase: a multisubunit enzyme that prenylates GTP-binding proteins terminating in Cys-X-Cys or Cys-Cys. J Biol Chem 267: 14497-14503
71. Slessareva JE, Routt SM, Temple B, Bankaitis VA, Dohlman HG (2006) Activation of the phosphatidylinositol 3-kinase Vps34 by a G protein a subunit at the endosome. Cell 126: 191-203
72. Suharsono U, Fujisawa Y, Kawasaki T, Iwasaki Y, Satoh H, Shimamoto K (2002) The heterotrimeric G protein alpha subunit acts upstream of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci USA 99: 13307-13312
73. Takida S, Wedegaertner PB (2003) Heterotrimer formation, together with isoprenylation, is required for plasma membrane targeting of Gbeta gamma. J Biol Chem 278: 17284-17290
74. Trusov Y, Rookes JE, Chakravorty D, Armour D, Schenk PM, Botella JR (2006) Heterotrimeric G proteins facilitate Arabidopsis resistance to necrotrophic pathogens and are involved in jasmonate signaling. Plant Physiol 140: 210-220
75. Ueguchi-Tanaka M, Fujisawa Y, Kobayashi M, Ashikari M, Iwasaki Y, Kitano H, Matsuoka M (2000) Rice dwarf mutant d1, which is defective in the alpha subunit of the heterotrimeric G protein, affects gibberellin signal transduction. Proc Natl Acad Sci USA 97: 11638-11643
76. Ullah H, Chen JG, Temple B, Boyes DC, Alonso JM, Davis KR, Ecker JR, Jones AM (2003) The β-subunit of the Arabidopsis G protein negatively regulates auxin-induced cell division and affects multiple developmental processes. Plant Cell 15: 393-409
77. Ullah H, Chen JG, Wang S, Jones AM (2002) Role of a heterotrimeric G protein in regulation of Arabidopsis seed germination. Plant Physiol 129: 897-907
78. Ullah H, Chen JG, Young JC, Im KH, Sussman MR, Jones AM (2001) Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science 292: 2066-2069
79. Veit B (2004) The human SNARE protein Ykt6 mediates its own palmitoylation at C-terminal cysteine residues. Biochem J 384: 233-237
80. Veit B, Dietrich LEP, Ungermann C (2003) Biochemical characterization of the vacuolar palmitoyl acyltransferase. FEBS Lett 540: 101-105
81. Veit M (2000) Palmitoylation of the 25-kDa synaptosomal protein (SNAP-25) in vitro occurs in the absence of an enzyme, but is stimulated by binding to syntaxin. Biochem J 345: 145-151
82. Wang XQ, Ullah H, Jones AM, Assmann SM (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292: 2022-2023
83. Warpeha KM, Lateef SS, Lapik Y, Anderson M, Lee B-S, Kaufman LS (2006) G-protein-coupled receptor 1, G-protein Ga-subunit 1, and prephenate dehydratase 1 are required for blue light-induced production of phenylalanine in etiolated Arabidopsis. Plant Physiol 140: 844-855
84. Wedegaertner PB, Wilson PT, Bourne HR (1995) Lipid modifications of trimeric G proteins. J Biol Chem 270: 503-506
85. Yalovsky S, Kulukian A, Rodriguez-Concepcion M, Young CA, Gruissem W (2000a) Functional requirement of plant farnesyltransferase during development in Arabidopsis. Plant Cell 12: 1267-1278
86. Yalovsky S, Rodriguez-Concepcion M, Bracha K, Toledo-Ortiz G, Gruissem W (2000b) Prenylation of the floral transcription factor APETALA1 modulates its function. Plant Cell 12: 1257-1266
87. Yalovsky S, Trueblood CE, Callan KL, Narita JO, Jenkins SM, Rine J, Gruissem W (1997) Plant farnesyltransferase can restore yeast Ras signaling and mating. Mol Cell Biol 17: 1986-1994
88. Yang YD, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr Biol 16: 1123-1127
89. Zhang FL, Casey PJ (1996) Protein prenylation: molecular mechanisms and functional consequences. Annu Rev Biochem 65: 241-269
90. Zhang FL, Moomaw JF, Casey PJ (1994) Properties and kinetic mechanism of recombinant mammalian protein geranylgeranyltransferase type I. J Biol Chem 269: 23465-23470
91. Ziegelhoffer EC, Medrano LJ, Meyerowitz EM (2000) Cloning of the Arabidopsis WIGGUM gene identifies a role for farnesylation in meristem development. Proc Natl Acad Sci USA 97: 7633-7638