Cullin-containing E3 ubiquitin ligases in plant development

Current Opinion in Plant Biology

Volumn 7, Issue 6, 2004, Pages 677-686

  Schwechheimer, Claus ^a   Villalobos, Luz Irina A Calderón ^a  

^a Centre for Plant Molecular Biology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CARRIER PROTEIN; CELL CYCLE PROTEIN; CONSTITUTIVE PHOTOMORPHOGENIC 1 PROTEIN, ARABIDOPSIS; CULLIN; DET1 PROTEIN, ARABIDOPSIS; EIN3 PROTEIN, ARABIDOPSIS; ETHYLENE; ETHYLENE DERIVATIVE; GAI PROTEIN, ARABIDOPSIS; GIBBERELLIC ACID; GIBBERELLIN; HY5 PROTEIN, ARABIDOPSIS; HYH PROTEIN, ARABIDOPSIS; NUCLEAR PROTEIN; RGA PROTEIN, PLANT; TRANSCRIPTION FACTOR; UBIQUITIN PROTEIN LIGASE; VEGETABLE PROTEIN;

ARABIDOPSIS; CHEMICAL STRUCTURE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; REVIEW; SIGNAL TRANSDUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CULLIN PROTEINS; ETHYLENES; GIBBERELLINS; MODELS, MOLECULAR; NUCLEAR PROTEINS; PLANT PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES;

ARABIDOPSIS; EUKARYOTA;

EID: 6044254445     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2004.09.009     Document Type: Review

References (102)

1. A. Hershko, and A. Chiechanover The ubiquitin system Annu Rev Biochem 67 1998 425 479
2. W. Baumeister, J. Walz, F. Zühl, and E. Seemüller The proteasome: paradigm of a self-compartmentalizing protease Cell 92 1998 367 380
3. R.J. Deshaies SCF and Cullin/RING H2-based ubiquitin ligases Annu Rev Cell Dev Biol 15 1999 435 467
4. W.-Y. Kim, R. Geng, and D.E. Somers Circadian phase-specific degradation of the F-box protein ZTL is mediated by the proteasome Proc Natl Acad Sci USA 100 2003 4933 4938 This is the first report of a plant F-box protein that is itself subject to proteolysis.
5. A.G. von Arnim, and X.-W. Deng Light inactivation of Arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning Cell 79 1994 1035 1045
6. Y. Yoshida, T. Chiba, F. Tokunaga, H. Kawasaki, K. Iwai, T. Suzuki, Y. Ito, K. Matsuoka, M. Yoshida, and K. Tanaka E3 ubiquitin ligase that recognizes sugar chains Nature 418 2002 438 442
7. Chung KKK, B. Thomas, X. Li, O. Pletnikova, J.C. Troncoso, L. Marsh, V.L. Dawson, and T.M. Dawson S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function Science 304 2004 1328 1331
8. 2-regulated prolyl hydroxylation Science 292 2001 468 472
9. C.S. Hardtke, K. Gohda, M.T. Osterlund, T. Oyama, K. Okada, and X.W. Deng HY5 stability and activity in Arabidopsis is regulated by phosphorylation in its COP1 binding domain EMBO J 19 2000 4997 5006
10. Wilkinson KD, Hochstrasser M: The deubiquitinating enzymes. In Ubiquitin and the Biology of the Cell. Edited by Peters J-M, Harris JR, Finley D. New York: Plenum Press; 1998:99-126.
11. M. Hochstrasser Biochemistry. All in the ubiquitin family Science 289 2000 563 564
12. T. Hori, F. Osaka, T. Chiba, C. Miyamoto, K. Okabayashi, N. Shimbara, S. Kato, and K. Tanaka Covalent modification of all members of human cullin family proteins by NEDD8 Oncogene 18 1999 6829 6834
13. Cand1, an inhibitor of CUL1-SKP1 binding and SCF ligases Mol Cell 10 2002 1511 1518
14. J. Zheng, X. Yang, J.M. Harrell, S. Ryzhikov, E.-H. Shim, K. Lykke-Andersen, N. Wei, H. Sun, R. Kobayashi, and H. Zhang CAND1 binds to unneddylated CUL1 and regulates the formation of SCF ubiquitin E3 ligase complex Mol Cell 10 2002 1519 1526
15. K.-W. Min, J.-W. Hwang, J.-S. Lee, Y. Park, T.-A. Tamura, and J.-B. Yoon TIP120A associates with cullins and modulates ubiquitin ligase activity J Biol Chem 278 2003 15905 15910 A description of the CAND protein as a regulator of E3 complex assembly.
16. S. Lyapina, G. Cope, A. Shevchenko, G. Serino, C. Zhou, D.A. Wolf, N. Wei, A. Shevchenko, and R.J. Deshaies COP9 signalosome promotes cleavage of NEDD8-CUL1 conjugates Science 292 2001 1382 1385
17. TIR1 in mediating auxin response Science 292 2001 1379 1382
18. G.A. Cope, Suh GSB, L. Aravind, S.E. Schwarz, S.L. Zipursky, E.V. Koonin, and R.J. Deshaies Role for predicted metalloprotease motif of JAB1/Csn5 in cleavage of NEDD8 from CUL1 Science 298 2002 608 611
19. M.H. Glickman, D.M. Rubin, O. Coux, I. Wefes, G. Pfeifer, Z. Cjeka, W. Baumeister, V.A. Fried, and D. Finley A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3 Cell 94 1998 615 623
20. C. Schwechheimer, and X.-W. Deng COP9 signalosome revisited: a novel mediator of protein degradation Trends Cell Biol 11 2001 420 426
21. N. Wei, and X.W. Deng The COP9 signalosome Annu Rev Cell Dev Biol 19 2003 261 286
22. N. Wei, D.A. Chamovitz, and X.-W. Deng Arabidopsis COP9 is a component of a novel signaling complex mediating light control of development Cell 78 1994 117 124
23. R. Groisman, J. Polanowska, I. Kuraoka, J.-I. Sawada, M. Siaijo, K. Tanaka, and Y. Nakatani The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage Cell 113 2003 357 367 This report describes, for the first time, an E3 enzyme that contains CULLIN4 and its association with the COP9 signalosome.
24. D.A. Wolf, C. Zhou, and S. Wee The COP9 signalosome: an assembly and maintenance platform for cullin ubiquitin ligases? Nat Cell Biol 5 2003 1029 1033
25. Z. Peng, Y. Shen, S. Feng, X. Wang, B.N. Chittetei, R.D. Vierstra, and X.W. Deng Evidence for a physical association of the COP9 signalosome, the proteasome, and specific SCF E3 ligases in vivo Curr Biol 13 2003 R504 R505
26. J. Smalle, and R. Vierstra The ubiquitin 26S proteasome proteolytic pathway Annu Rev Plant Physiol Plant Mol Biol 55 2004 555 590 A comprehensive review of the plant ubiquitin-proteasome system.
27. A. Bachmair, M. Novatchkova, T. Potuschak, and F. Eisenhaber Ubiquitylation in plants: a post-genomic look at a post-translational modification Trends Plant Sci 6 2001 463 470
28. Kosarev P, Mayer KFX, Hardtke CS: Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome. Genome Biol 2002, 3:0016.0011-0016.0012.
29. J.M. Gagne, B.P. Downes, S.H. Shiu, A.M. Durski, and R.D. Vierstra The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis Proc Natl Acad Sci USA 99 2002 11519 11524
30. D.E. Richards, K.E. King, T. Ait-ali, and N.P. Harberd How gibberellin regulates plant growth and development: a molecular genetic analysis of gibberellin signaling Annu Rev Plant Physiol Plant Mol Biol 52 2001 67 88
31. A.L. Silverstone, P.Y.A. Mak, E.C. Martinez, and T.-p. Sun The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana Genetics 146 1997 1087 1099
32. H. Yu, T. Ito, Y. Zhao, J. Peng, P. Kumar, and E.M. Meyerowitz Floral homeotic genes are targets of gibberellin signaling in flower development Proc Natl Acad Sci USA 101 2004 7827 7832
33. K.E. King, T. Moritz, and N.P. Harberd Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA Genetics 159 2001 767 776
34. A. Dill, and Sun T.-P. Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana Genetics 159 2001 777 785
35. S. Lee, H. Cheng, K.E. King, W. Wang, Y. He, A. Hussain, J. Lo, N.P. Harberd, and J. Peng Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition Genes Dev 16 2002 646 658
36. J. Peng, P. Carol, D.E. Richards, K.E. King, R.J. Cowling, G.P. Murphy, and N.P. Harberd The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses Genes Dev 11 1997 3194 3205
37. J. Peng, D.E. Richards, N.M. Hartley, G.P. Murphy, K.M. Devos, J.E. Flintham, J. Beales, L. Fish, A.J. Worland, and F. Pelica "Green revolution" genes encode mutant gibberellin response modulators Nature 400 1999 256 261
38. A. Dill, H.-S. Jung, and T.-p. Sun The DELLA motif is essential for gibberellin-induced degradation of RGA Proc Natl Acad Sci USA 98 2001 14162 14167
39. A.L. Silverstone, H.-S. Jung, A. Dill, H. Kawaide, Y. Kamiya, and T.-P. Sun Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis Plant Cell 13 2001 1555 1565
40. ••].
41. ••] describe the gain-of-function SLY1 allele gar2-1, a mutant with increased RGA and GAI turnover.
42. C.M. Steber, S.E. Cooney, and P. McCourt Isolation of the GA-response mutant sly1 as a suppressor of ABI1-1 in Arabidopsis thaliana Genetics 149 1998 509 521
43. K.M. McGinnis, S.G. Thomas, J.D. Soule, L.C. Strader, J.M. Zale, T.-P. Sun, and C.M. Steber The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase Plant Cell 15 2003 1120 1130
44. A. Sasaki, H. Itoh, K. Gomi, M. Ueguchi-Tanaka, K. Ishiyama, M. Kobayashi, D.-H. Jeong, G. An, H. Kitano, and M. Ashikari Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant Science 299 2003 1896 1898 The first report of the SLY1 ortholog from rice. The authors provide the first evidence that phosphorylation might precede DELLA protein degradation.
45. K. Gomi, A. Sasaki, H. Itoh, M. Ueguchi-Tanaka, M. Ashikari, H. Kitano, and M. Matsuoka GID2, an F-box subunit of the SCF E3 complex, specifically interacts with phosphorylated SLR1 protein and regulates the gibberellin-dependent degradation of SLR1 in rice Plant J 37 2004 626 634
46. R.N. Wilson, and C.R. Somerville Phenotypic suppression of the gibberellin-insensitive mutant (gai) of Arabidopsis Plant Physiol 108 1995 495 502
47. H. Guo, and J.R. Ecker The ethylene signaling pathway: new insights Curr Opin Plant Biol 7 2004 40 49
48. R. Solano, A. Stepanova, Q. Chao, and J.R. Ecker Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1 Genes Dev 12 1998 3703 3714
49. Q. Chao, M. Rothenberg, R. Solano, G. Roman, W. Terzaghi, and J.R. Ecker Activation of the ethylene gas response pathway in Arabidopsis by the nuclear proteins ETHYLENE-INSENSITIVE3 and related genes Cell 89 1997 1133 1144
50. S. Yanagisawa, S.-D. Yoo, and J. Sheen Differential regulation of EIN3 stability by glucose and ethylene signalling in plants Nature 425 2003 521 525 First evidence of EIN3 degradation by the 26S proteasome.
51. ••].
52. ••].
53. ••] describe the independent isolation of EBF1 and EBF2 as cognate E3 ubiquitin ligases of EIN3.
54. J.P. Vogel, K.E. Woeste, A. Theologis, and J.J. Kieber Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively Proc Natl Acad Sci USA 95 1998 4766 4771
55. H.S. Chae, F. Faure, and J.J. Keiber The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein Plant Cell 15 2003 545 559
56. K.L-.C. Wang, H. Yoshida, C. Lurin, and J.R. Ecker Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein Nature 428 2004 945 950 First report of an E3 enzyme that contains CULLIN3 from Arabidopsis.
57. L. Xu, Y. Wei, J. Reboul, P. Vaglio, T.-H. Shin, M. Vidal, S.J. Elledge, and J.W. Harper BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing Cul-3 Nature 425 2003 316 321
58. P. Spanu, D.G. Grosskopf, G. Felix, and T. Boller The apparent turnover of 1-aminocyclopropane-1-carboxylate synthase in tomato cells is regulated by protein phosphorylation and dephosphorylation Plant Physiol 106 1994 529 535
59. M. Tatsuki, and H. Mori Phosphorylation of tomato 1-aminocyclopropane-1- carboxylic acid synthase, Le-ACS2, at the C-terminal region J Biol Chem 276 2001 28051 28057
60. T. Oyama, Y. Shimura, and K. Okada The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl Genes Dev 11 1997 2983 2995
61. S. Chattopadhyay, L.-H. Ang, P. Puente, X.-W. Deng, and N. Wei Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression Plant Cell 10 1998 673 683
62. L.-H. Ang, S. Chattopadhyay, N. Wei, T. Oyama, K. Okada, A. Batschauer, and X.-W. Deng Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development Mol Cell 1 1998 213 222
63. M. Holm, L. Ma, L.-J. Qu, and X.W. Deng Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis Genes Dev 16 2002 1247 1259
64. M.T. Osterlund, C.S. Hardtke, N. Wei, and X.W. Deng Targeted destabilization of HY5 during light-regulated development of Arabidopsis Nature 405 2000 462 466
65. Y. Saijo, J.A. Sullivan, H. Wang, J.-Y. Yang, Y. Shen, V. Rubia, L. Ma, U. Hoecker, and X.W. Deng The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity Genes Dev 17 2003 2642 2647
66. A. Pepper, T. Delaney, T. Wahsburn, D. Poole, and J. Chory DET1, a negative regulator of light-mediated development and gene expression in Arabidopsis, encodes a novel nuclear-localized protein Cell 78 1994 109 116
67. D.F. Schroeder, M. Gahrtz, B.B. Maxwell, R.K. Cook, J.M. Kan, J.M. Alonso, J.R. Ecker, and J. Chory De-etiolated 1 and Damaged DNA Binding Protein 1 interact to regulate Arabidopsis photomorphogenesis Curr Biol 12 2002 1462 1472
68. ••].
69. ••] together helped to identify the novel CULLIN4-containing DCX-complexes. These complexes regulate the degradation of c-JUN and p53 in humans, and possibly the degradation of HY5, HYH, LAF1 and phyA in plants.
70. H.S. Seo, J.-Y. Yang, M. Ishikawa, C. Bolle, M.L. Ballesteros, and N.-H. Chua LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1 Nature 423 2003 995 999
71. H.S. Seo, E. Watanabe, S. Tokutomi, A. Nagatani, and N.-H. Chua Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling Genes Dev 18 2004 617 622
72. U. Hoecker, J.M. Tepperman, and P.H. Quail SPA1, a WD-repeat protein specific to phytochrome A signal transduction Science 284 1999 496 499
73. U. Hoecker, and P. Quail The phytochrome A-specific signaling intermediate SPA1 interacts directly with COP1, a constitutive repressor of light signaling in Arabidopsis J Biol Chem 276 2001 38173 38178
74. S.F. Kwok, J.M. Staub, and X.-W. Deng Characterization of two subunits of Arabidopsis 19S proteasome regulatory complex and its possible interaction with the COP9 complex J Mol Biol 285 1999 85 95
75. T. Potuschak, S. Stary, P. Schlögelhofer, F. Becker, V. Nehjinskaia, and A. Bachmair PRT1 of Arabidopsis thaliana encodes a component of the plant N-end rule pathway Proc Natl Acad Sci USA 95 1998 7904 7908
76. L. Lopez-Molina, S. Mongrand, N. Kinoshita, and N.-H. Chua AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation Genes Dev 17 2003 410 418
77. M. Ruegger, E. Dewey, W.M. Gray, L. Hobbie, J. Turner, and M. Estelle The TIR protein of Arabidopsis function in auxin response and is related to human SKP2 and yeast Grr1p Genes Dev 12 1998 198 207
78. W.M. Gray, J.C. del Pozo, L. Walker, L. Hobbie, E. Risseeuw, T. Banks, W.L. Crosby, M. Yang, and M. Estelle Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana Genes Dev 13 1999 1678 1687
79. TIR1-dependent degradation of AUX/IAA proteins Nature 414 2001 271 276
80. Q. Xie, H.-S. Guo, G. Dallman, S. Fang, A.M. Weissman, and N.-H. Chua SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals Nature 419 2002 167 170
81. T. Sieberer, G.J. Seifert, M.-T. Hauser, P. Grisafi, G.R. Fink, and C. Luschnig Post-transcriptional control of the Arabidopsis auxin efflux carrier EIR1 requires AXR1 Curr Biol 10 2000 1595 1598
82. J.-X. He, J.M. Gendron, Y. Yang, J. Li, and Z.-Y. Wang The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis Proc Natl Acad Sci USA 99 2002 10185 10190
83. J.C. del Pozo, M.B. Boniotti, and C. Gutierrez Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCF(AtSKP2) pathway in response to light Plant Cell 14 2002 3057 3071
84. P. Genschik, M.C. Criqui, Y. Parmentier, A. Derevier, and J. Fleck Cell cycle-dependent proteolysis in plants: identification of the destruction box pathway and metaphase arrest produced by the proteasome inhibitor MG132 Plant Cell 10 1998 2063 2075
85. M.M. Castellano, J.C. del Pozo, E. Ramirez-Parra, S. Brown, and C. Gutierrez Expression and stability of Arabidopsis CDC6 are associated with endoreduplication Plant Cell 13 2001 2671 2686
86. Y. Zhou, G. Li, F. Brandizzi, L.C. Fowke, and H. Wang The plant cyclin-dependent kinase inhibitor ICK1 has distinct function domains for in vivo inhibition, protein instability and nuclear localization Plant J 35 2003 476 489
87. F. Valverde, A. Mouradov, W. Soppe, D. Ravenscroft, A. Samach, and G. Coupland Photoreceptor regulation of CONSTANS protein in photoperiodic flowering Science 303 2004 1003 1006
88. D.E. Somers, T.F. Schultz, M. Milnamow, and S.A. Kay ZEITLUPE encodes a novel clock-associate PAS protein from Arabidopsis Cell 101 2000 319 329
89. D.C. Nelson, J. Lasswell, L.E. Rogg, M.A. Cohen, and B. Bartel FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis Cell 101 2000 331 340
90. P. Mas, W.-Y. Kim, D.E. Somers, and S.A. Kay Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana Nature 426 2003 567 570
91. J. Yan, J. Wang, Q. Li, J.R. Hwang, C. Patterson, and H. Zhang AtCHIP, a U-box containing E3 ubiquitin ligase, plays a critical role in temperature stress tolerance in Arabidopsis Plant Physiol 132 2003 861 869
92. X. Wang, S. Feng, N. Nakayama, W.L. Crosby, V.F. Irish, X.W. Deng, and N. Wei The COP9 signalosome interacts with SCF UFO and participates in Arabidopsis flower development Plant Cell 15 2003 1071 1082
93. J.Z. Levin, and E.M. Meyerowitz UFO: an Arabidopsis gene involved in both floral meristem and floral organ development Plant Cell 7 1995 529 548
94. D.-X. Xie, B.F. Feys, S. James, M. Nieto-Rostro, and J.G. Turner COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility Science 280 1998 1091 1094
95. H.S. Kim, and T.P. Delaney Arabidopsis SON1 is an F-box protein that regulates a novel induced defense response independent of both salicylic acid and systemic acquired resistance Plant Cell 14 2002 1469 1482
96. M. Dieterle, Y.-C. Zhou, E. Schäfer, M. Funk, and T. Kretsch EID1, an F-box protein involved in phytochrome A-specific light signaling Genes Dev 15 2001 939 944
97. F.G. Harmon, and S.A. Kay The F box protein AFR is a positive regulator of phytochrome A-mediated light signaling Curr Biol 13 2003 2091 2096
98. P. Stirnberg, K. van de Sande, and H.M.O. Leyser MAX1 and MAX2 control shoot lateral branching in Arabidopsis Development 129 2002 1131 1141
99. H.R. Woo, K.M. Chung, J.-H. Park, S.A. Oh, T. Ahn, S.H. Hong, S.K. Jang, and H.G. Nam ORE9, an F-box protein that regulates leaf senescence in Arabidopsis Plant Cell 13 2001 1779 1790
100. A. El Refy, D. Perazza, L. Zekraoui, J.G. Valay, N. Bechtold, S. Brown, M. Hülskamp, M. Herzog, and J.M. Bonneville The Arabidopsis KAKTUS gene encodes a HECT protein and controls the number of endoreduplication cycles Mol Genet Genomics 270 2003 403 414
101. B.P. Downes, R.M. Stupar, D.J. Gingerich, and R.D. Vierstra The HECT ubiquitin-protein ligase (UPL) family in Arabidopsis: UPL3 has a specific role in trichome development Plant J 35 2003 729 742
102. A. Hannoufa, V. Negruk, G. Eisner, and B. Lemieux The CER3 gene of Arabidopsis thaliana is expressed in leaves, stems, roots, flowers and apical meristems Plant J 10 1996 459 467