The ubiquitin 26S proteasome proteolytic pathway

Annual Review of Plant Biology

Volumn 55, Issue , 2004, Pages 555-590

  Smalle, Jan ^a   Vierstra, Richard D ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Arabidopsis; Cell regulation; Polypeptide tags; Proteolysis

Indexed keywords

ATP DEPENDENT 26S PROTEASE; PROTEASOME; UBIQUITIN;

CIRCADIAN RHYTHM; ENZYMOLOGY; GENOME; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; PLANT; RADIATION EXPOSURE; REVIEW;

CIRCADIAN RHYTHM; GENOME, PLANT; LIGHT; PLANTS; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITIN;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 3242665372     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.55.031903.141801     Document Type: Review

References (190)

1. Alvarez-Fernandez J, De Luca V. 1994. Ubiquitin-mediated degradation of tryptophan decarboxylase from Catharanthus roseus. Phytochemistry 36:1123-28
2. Austin MJ, Muskett P, Kahn K, Feys BJ, Jones JD, Parker JE. 2002. Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295:2077-80
3. Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu K, Schulze-Lefert P. 2002. The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295:2073-76
4. Azevedo C, Santos-Rosa MJ, Shirasu K. 2001. The U-Box protein family in plants. Trends Plant Sci. 6:354-58
5. Bach I, Ostendorff HP. 2003. Orchestrating nuclear functions: ubiquitin sets the rhythm. Trends Biochem. Sci. 28:189-95
6. Bachmair A, Becker F, Schell J. 1993. Use of a reporter transgene to generate Arabidopsis mutants in ubiquitin-dependent proteolysis. Proc. Natl. Acad. Sci. USA 90:418-21
7. Bachmair A, Novatchkova M, Potuschak T, Eisenhaber F. 2001. Ubiquitylation in plants: a post-genomic look at a post-translational modification. Trends Plant Sci. 6:463-70
8. Bates PW, Vierstra RD. 1999. UPL1 and 2, two 405 kDa ubiquitin-protein ligases from Arabidopsis thaliana related to the HECT-domain protein family. Plant J. 20:183-95
9. Becker F, Buschfeld E, Schell J, Bachmair A. 1993. Altered response to viral infection by tobacco plants perturbed in the ubiquitin system. Plant J. 3:875-81
10. Blilou I, Frugier F, Folmer S, Serralbo O, Willemsen V, et al. 2002. The Arabidopsis HOBBIT gene encodes a CDC27 homolog that links the plant cell cycle to progression of cell differentiation. Genes Dev. 16:2566-75
11. Boyes DC, Nam J, Dangl JL. 1998. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proc. Natl. Acad. Sci. USA 95:15849-54
12. Callis J, Carpenter T, Sun CW, Vierstra RD. 1995. Structure and evolution of genes encoding polyubiquitin and ubiquitin-like proteins in Arabidopsis thaliana ecotype Columbia. Genetics 139:921-39
13. Callis J, Raasch JA, Vierstra RD. 1990. Ubiquitin extension proteins of Arabidopsis thaliana. Structure, localization, and expression of their promoters in transgenic tobacco. J. Biol. Chem. 265:12486-93
14. Capron A, Okresz L, Genschik P. 2003. First glance at the plant APC/C, a highly conserved ubiquitin-protein ligase. Trends Plant Sci. 8:83-89
15. Capron A, Serralbo O, Fulop K, Fruigier F, Parmentier Y, et al. 2003. The Arabidopsis APC/C: molecular and genetic characterization of the APC2 subunit. Plant Cell. 15:2370-82
16. Castellano MM, del Pozo JC, Ramirez-Parra E, Brown S, Gutierrez C. 2001. Expression and stability of Arabidopsis CDC6 are associated with endoreplication. Plant Cell 13:2671-86
17. Cebolla A, Vinardell JM, Kiss E, Olah B, Roudier F, et al. 1999. The mitotic inhibitor CCS52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J. 18:4476-84
18. Chae HS, Faure F, Kieber JJ. 2003. The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 15:545-59
19. Chen L, Madura K. 2002. Rad23 promotes the targeting of proteolytic substrates to the proteasome. Mol. Cell. Biol. 22:4902-13
20. Christensen AH, Quail PH. 1996. Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyle-donous plants. Transgenic Res. 5:213-18
21. Clough RC, Jordan-Beebe ET, Lohman KN, Marita JM, Walker JM, et al. 1999. Sequences within both the N- and C-terminal domains of phytochrome A are required for Pfr ubiquitination and degradation. Plant J. 17:155-67
22. Clough RC, Vierstra RD. 1997. Phytochrome degradation. Plant Cell Environ. 20:713-21
23. Cope GA, Suh GSB, Aravind L, Schwarz SE, Zipursky SL, et al. 2002. Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cull. Science 298:608-11
24. Criqui MC, Engler JD, Camasses A, Capron A, Parmentier Y, et al. 2002. Molecular characterization of plant ubiquitin-conjugating enzymes belonging to the UBCP4/E2-C/UBCx/ UBCH10 gene family. Plant Physiol. 130:1230-40
25. Dahan J, Etienne P, Petitot AS, Houot V, Blein JP, Suty L. 2001. Cryptogein affects expression of alpha3, alpha6 and betal 20S proteasome subunit s encoding genes in tobacco. J. Exp. Bot. 52:1947-48
26. del Pozo JC, Boniotti MB, Gutierrez C. 2002. Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCF(AtSKP2) pathway in response to light. Plant Cell 14:3057-71
27. del Pozo JC, Dharmasiri S, Hellmann H, Walker L, Gray WM, Estelle M. 2002. AXR1-ECR1-dependent conjugation of RUB1 to the Arabidopsis cullin AtCUL1 is required for auxin response. Plant Cell 14:421-33
28. DeMartino GN, Slaughter CA. 1999. The proteasome, a novel protease regulated by multiple mechanisms. J. Biol. Chem. 274:22123-26
29. Deshaies RJ. 1999. SCF and Cullin/Ring H2-based ubiquitin ligases. Annu. Rev. Cell. Dev. Biol. 15:435-67
30. Devoto A, Nieto-Rostro M, Xie DX, Ellis C, Harmston R, et al. 2002. COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. Plant J. 32:457-66
31. Dewitte W, Murray JAH. 2003. The plant cell cycle. Annu. Rev. Plant Biol. 54:235-64
32. Dharmasiri N, Dharmasiri S, Jones AM, Estelle M. 2003. Auxin action in a cell-free system. Curr. Biol. 13:1418-22
33. Dharmasiri S, Dharmasiri N, Hellmann H, Estelle M. 2003. The RUB/Nedd8 conjugation pathway is required for early development in Arabidopsis. EMBO J. 22:1762-70
34. Dickman MB, Park YK, Oltersdorf T, Li W, Clemente T, French R. 2001. Abrogation of disease development in plants expressing animal anti-apoptotic genes. Proc. Natl. Acad. Sci. USA 98:6957-62
35. Dieterle M, Zhou YC, Schafer E, Funk M, Kretsch T. 2001. EID1, an F-Box protein involved in phytochrome A-specific light signaling. Genes Dev. 15:939-44
36. Ditzel M, Wilson R, Tenev T, Zachariou A, Paul A, et al. 2003. Degradation of DIAP1 by the N-end rule pathway is essential for regulating apoptosis. Nat. Cell Biol. 5:467-73
37. Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD. 2002. The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J. Biol. Chem. 277:33105-14
38. Doelling JH, Yan N, Kurepa J, Walker J, Vierstra RD. 2001. The ubiquitin-specific protease UBP14 is essential for early embryo development in Arabidopsis thaliana. Plant J. 27:393-405
39. Downes BP, Stupar RM, Gingerich DJ, Vierstra RD. 2003. The HECT ubiquitin-protein ligase (UPL) family in Arabidopsis: UPL3 has a specific role in trichome development. Plant J. 35:729-42
40. Dunand-Sauthier I, Walker C, Wilkinson C, Gordon C, Crane R, et al. 2002. Sum1, a component of the fission yeast eIF3 translation initiation complex, is rapidly relocalized during environmental stress and interacts with components of the 26S proteasome. Mol. Biol. Cell 13:1626-40
41. Elsasser S, Gali RR, Schwickart M, Larsen CN, Leggett DS, et al. 2002. Proteasome subunit Rpn1 binds ubiquitin-like protein domains. Nat. Cell Biol. 4:725-30
42. Farras R, Ferrando A, Jasik J, Kleinow T, Okresz L, et al. 2001. SKP1-SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase. EMBO J. 20:2742-56
43. Feng S, Ma L, Wang X, Xie D, Dinesh-Kumar SP, et al. 2003. The COP9 signalosome interacts physically with SCFCOI1 and modulates jasmonate responses. Plant Cell 15:1083-94
44. Fu H, Doelling JH, Arendt CS, Hochstrasser M, Vierstra RD. 1998. Molecular organization of the 20S proteasome gene family from Arabidopsis thaliana. Genetics 149:677-92
45. Fu H, Doelling JH, Rubin DM, Vierstra RD. 1999. Structural and functional analysis of the six regulatory particle AAA-ATPase subunits from the Arabidopsis 26S proteasome. Plant J. 18:529-39
46. Fu H, Reis N, Lee Y, Glickman MH, Vierstra RD. 2001. Subunit interaction maps for the regulatory particle of the 26S proteasome and the COP9 signalosome. EMBO J. 20:7096-107
47. Fu H, Sadis S, Rubin DM, Glickman M, van Nocker S, et al. 1998. Multiubiquitin chain binding and protein degradation are mediated by distinct domains within the 26S proteasome subunit Mcbl. J. Biol. Chem. 273:1970-81
48. Fu XD, Harberd NP. 2003. Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740-43
49. Fu XD, Richards DE, Ait-Ali T, Hynes LW, Ougham H, et al. 2002. Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14:3191-200
50. Gagne JM, Downes BP, Shiu S-H, Durski AM, Vierstra RD. 2002. The F-Box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc. Natl. Acad. Sci. USA 99:11519-24
51. Gagne JM, Smalle J, Gingrich D, Walker JM, Yoo S, et al. 2004. The Arabidopsis F-box proteins EBF1 and EBF2 form SCF E3s that repress ethylene action and promote growth by directing EIN3 degradation. Proc. Natl. Acad. Sci. In press
52. Genschik P, Criqui MC, Parmentier Y, Derevier A, Fleck J. 1998. Cell cycle-dependent proteolysis in plants. Identification of the destruction box pathway and metaphase arrest produced by the proteasome inhibitor MG132. Plant Cell 10:2063-76
53. Girod PA, Carpenter TB, van Mocker S, Sullivan ML, Vierstra RD. 1993. Homologs of the essential ubiquitin conjugating enzymes UBC1, 4, and 5 in yeast are encoded by a multigene family in Arabidopsis thaliana. Plant J. 3:545-52
54. Girod PA, Fu H, Zryd JP, Vierstra RD. 1999. Multiubiquitin chain binding subunit MCB1 (RPN10) of the 26S proteasome is essential for developmental progression in Physcomitrella patens. Plant Cell 11:1457-71
55. Glickman MH, Rubin DM, Coux O, Wefes I, Pfeifer G, et al. 1998. A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94:615-23
56. Gray WM, Hellmann H, Dharmasiri S, Estelle M. 2002. Role of the Arabidopsis RING-H2 Protein RBX1 in RUB Modification and SCF Function. Plant Cell 14:2137-44
57. TIR1-dependent degradation of AUX/IAA proteins. Nature 414:271-76
58. TIR-mediated auxin response. Plant Cell 15:1310-19
59. Groisman R, Polanowska J, Kuraoka I, Sawada J, Saijo M, et al. 2003. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113:357-67
60. Groll M, Bajorek M, Kohler A, Moroder L, Rubin DM, et al. 2000. A gated channel into the proteasome core particle. Nat. Struct. Biol. 7:1062-67
61. Groll M, Ditzel L, Lowe J, Stock D, Bochtler M, et al. 1997. Structure of 20S proteasome from yeast at 2.4 A resolution. Nature 386:463-71
62. Guo H, Ecker JR. 2003. Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115:667-77
63. Hamilton KS, Ellison MJ, Barber KR, Williams RS, Huzil JT, et al. 2001. Structure of a conjugating enzyme-ubiquitin thiolester intermediate reveals a novel role for the ubiquitin tail. Structure 9:897-904
64. Hannoufa A, Negruk V, Eisner G, Lemieux B. 1996. The CER3 gene of Arabidopsis thaliana is expressed in leaves, stems, roots, flowers and apical meristems. Plant J. 10:459-67
65. Hardtke CS, Okamoto H, Stoop-Myer C, Deng XW. 2002. Biochemical evidence for ubiquitin ligase activity of the Arabidopsis COP1 interacting protein 8 (CIP8). Plant J. 30:385-94
66. Harmon FG, Kay SA. 2003. The F box protein AFR is a positive regulator of phytochrome A-mediated light signaling. Curr Biol. 13:2091-96
67. Harper JW, Burton JL, Solomon MJ. 2002. The anaphase-promoting complex: it's not just for mitosis any more. Genes Dev. 16:2179-206
68. Hartmann-Petersen R, Seeger M, Gordon C. 2003. Transferring substrates to the 26S proteasome. Trends Biochem. Sci. 28:26-31
69. Hatfield PM, Gosink MM, Carpenter TB, Vierstra RD. 1997. The ubiquitin-activating enzyme (E1) gene family in Arabidopsis thaliana. Plant J. 11:213-26
70. Hazelwood D, Zaitlin W. 1990. Ubiquitinated conjugates are found in preparations of several plant viruses. Virology 177:352-56
71. He JX, Gendron JM, Yang YL, Li JM, Wang ZY. 2002. The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc. Natl. Acad. Sci. USA 99:10185-90
72. Hellmann H, Estelle M. 2002. Plant development: regulation by protein degradation. Science 297:793-97
73. Hershko A, Ciechanover A. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-79
74. Hicke L. 2001. Protein regulation by monoubiquitin. Nat. Rev. Mol. Cell Biol. 2:195-201
75. Hermann K, Falquet L. 2001. A ubiquitin-interacting motif conserved in components of the proteasomal and lysosomal protein degradation systems. Trends Biochem. Sci. 26:347-50
76. Holm M, Ma LG, Qu LJ, Deng XW. 2002. Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev. 16:1247-59
77. Hondred D, Walker JM, Mathews DE, Vierstra RD. 1999. Use of ubiquitin fusions to augment protein expression in transgenic plants. Plant Physiol. 119:713-23
78. Hoppe T, Matuschewski K, Rape M, Schlenker S, Ulrich HD, Jentsch S. 2000. Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102:577-86
79. Huffaker RC, Peterson LW. 1974. Protein turnover in plants and possible means of its regulation. Annu. Rev. Plant Physiol. 25:363-92
80. Imaizumi T, Tran HG, Swartz TE, Briggs WR, Kay SA. 2003. FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426:302-6
81. Jentsch S, Pyrowolakis G. 2000. Ubiquitin and its kin: how close are the family ties? Trends Cell Biol. 10:335-42
82. Kepinski S, Leyser O. 2002. Ubiquitination and auxin signaling: a degrading story. Plant Cell 14 (Suppl):S81-95
83. Kim HS, Delaney TP. 2002. 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 14:1469-82
84. Kim M, Ann JW, Jin UH, Choi D, Pack KH, Pai HS. 2003. Activation of the programmed cell death pathway by inhibition of proteasome function in plants. J. Biol. Chem. 278:19406-15
85. Kim WY, Geng RS, Somers DE. 2003. Circadian phase-specific degradation of the F-box protein ZTL is mediated by the proteasome. Proc. Natl. Acad. Sci. USA 100:4933-38
86. Kitagawa K, Skowyra D, Elledge SJ, Harper JW, Hieter P. 1999. SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex. Mol. Cell 4:21-33
87. Kopito RR. 2000. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10:524-30
88. Kosarev P, Mayer KF, Hardtke CS. 2002. Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome. Genome Biol. 3:1-12
89. Kostova Z, Wolf DH. 2003. For whom the bell tolls: protein quality control of the endoplasmic reticulum and the ubiquitin-proteasome connection. EMBO J. 22:2309-17
90. Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, et al. 2003. The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and -2 conjugates is increased by stress. J. Biol. Chem. 278:6862-72
91. Kwok SF, Staub JM, Deng XW. 1999. Characterization of two subunits of Arabidopsis 19S proteasome regulatory complex and its possible interaction with the COP9 complex. J. Mol. Biol. 285:85-95
92. Lam YA, Lawson TG, Velayutham M, Zweier JL, Pickart CM. 2002. A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal. Nature 416:763-67
93. Lam YA, Xu W, DeMartino GN, Cohen RE. 1997. Editing of ubiquitin conjugates by an isopeptidase in the 26S proteasome. Nature 385:737-40
94. Lechner E, Xie DX, Grava S, Pigaglio E, Planchais S, et al. 2002. The At RBX1 protein is part of plant SCF complexes, and its down-regulation causes severe growth and developmental defects. J. Biol. Chem. 277:50069-80
95. Lee HJ, Xiong LM, Gong ZZ, Ishitani M, Stevenson B, Zhu JK. 2001. The Arabidopsis HOSI gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning. Genes Dev. 15:912-24
96. Lee SS, Cho HS, Yoon GM, Ahn JW, Kim HH, Pai HS. 2003. Interaction of NtCDPK1 calcium-dependent protein kinase with NtRpn3 regulatory subunit of the 26S proteasome in Nicotiana tabacum. Plant J. 33:825-40
97. Leggett DS, Hanna J, Borodovsky A, Crosas B, Schmidt M, et al. 2002. Multiple associated proteins regulate proteasome structure and function. Mol. Cell 10:495-507
98. Liu JD, Furukawa M, Matsumoto T, Xiong Y. 2002. NEDD8 modification of CUL1 dissociates p120(CAND1), an inhibitor of CUL1-SKP1 binding and SCF ligases. Mol. Cell 10:1511-18
99. Lopez-Molina L, Mongrand S, Chua NH. 2001. A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc. Natl. Acad. Sci. USA 98:4782-87
100. Lopez-Molina L, Mongrand S, Kinoshita N, Chua NH. 2003. AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes Dev. 17:410-18
101. Mas P, Kim WY, Somers DE, Kay SA. 2003. Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426:567-70
102. Matile PH. 1982. Protein degradation. In Encyclopedia of Plant Physiology, New Series, ed. D Coulter, B Partier, 14a:168-94. Berlin: Springer-Verlag
103. McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, et al. 2003. The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15:1120-30
104. Melchior F. 2000. SUMO-nonclassical ubiquitin. Annu. Rev. Cell Dev. Biol. 16:591-626
105. Melchior F, Hengst L. 2000. Mdm2-SUMO1: is bigger better? Nat. Cell Biol. 2:161-63
106. Min JH, Yang H, Ivan M, Gertler F, Kaelin WG Jr, Pavletich NP. 2002. Structure of an HIF-1alpha-pVHL complex: hydroxyproline recognition in signaling. Science 296:1886-89
107. Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B. 2000. FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101:331-40
108. Newbigin E, Vierstra RD. 2003. Plant reproduction: Sex and self-denial. Nature 423:229-30
109. Ohi MD, Vander Kooi CW, Rosenberg JA, Chazin WJ, Gould KL. 2003. Structural insights into the U-Box, a domain associated with multiubiquitination. Nat. Struct. Biol. 10:250-55
110. CDC4 ubiquitin ligase. Cell 112:243-56
111. Osterlund MT, Hardtke CS, Wei N, Deng XW. 2000. Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405:462-66
112. Peart JR, Lu R, Sadanandom A, Malcuit I, Moffett P, et al. 2002. Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc. Natl. Acad. Sci. USA 99:10865-69
113. Peng J, Schwartz D, Elias JE, Thoreen CC, Cheng D, et al. 2003. A proteomics approach to understanding protein ubiquitination. Nat. Biotech. 21:921-26
114. Peng ZH, Shen YP, Feng SH, Wang XP, Chitteti BN, et al. 2003. Evidence for a physical association of the COP9 signalosome, the proteasome, and specific SCF E3 ligases in vivo. Curr. Biol. 12:504-5
115. Pickart CM. 2001. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70:503-33
116. Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, et al. 2003. EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115:679-89
117. Potuschak T, Stary S, Schlogelhofer P, Becker F, Nejinskaia V, Bachmair A. 1998. PRT1 of Arabidopsis thaliana encodes a component of the plant N-end rule pathway. Proc. Natl. Acad. Sci. USA 95:7904-8
118. Ramos JA, Zenser N, Leyser O, Callis J. 2001. Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain II and is proteasome dependent. Plant Cell 13:2349-60
119. Rao-Naik C, delaCruz W, Laplaza JM, Tan S, Callis J, Fisher AJ. 1998. The RUB family of ubiquitin-like proteins. Crystal structure of Arabidopsis RUB1 and expression of multiple RUBs in Arabidopsis. J. Biol. Chem. 273:34976-82
120. Reichel C, Beachy RN. 2000. Degradation of tobacco mosaic virus movement protein by the 26S proteasome. J. Virol. 74:3330-37
121. Risseeuw EP, Daskalchuk TE, Banks TW, Liu E, Cotelesage J, et al. 2003. Protein interaction analysis of SCF ubiquitin E3 ligase subunits from Arabidopsis. Plant J. 34:753-67
122. Rivett AJ, Bose S, Brooks P, Broadfoot KI. 2001. Regulation of proteasome complexes by gamma-interferon and phosphorylation. Biochimie 83:363-66
123. 116a. Saijo Y, Sullivan JA, Wang H, Yang J, Shen Y, et al. 2003. The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev. 17:2642-47
124. Samach A, Klenz JE, Kohalmi SE, Risseeuw E, Haughn GW, Crosby WL. 1999. The UNUSUAL FLORAL ORGANS gene of Arabidopsis thaliana is an F-Box protein required for normal patterning and growth in the floral meristem. Plant J. 20:433-45
125. Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, et al. 2003. Accumulation of phosphorylated repressor for gibberellin signaling in an F-Box mutant. Science 299:1896-98
126. Schrammeijer B, Risseeuw E, Pansegrau W, Regensburg-Tuink TJG, Crosby WL, Hooykaas PJJ. 2001. Interaction of the virulence protein VurF of Agrobacterium tumefaciens with plant homologs of the yeast SKP1 protein. Curr. Biol. 11:258-62
127. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR. 2000. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404:770-74
128. 120a. Schultz TF, Kiyosue T, Yanovsky M, Wada M, Kay SA. 2001. A role for LKP2 in the circadian clock of Arabidopsis. Plant Cell 13:2659-70
129. Schultz TF, Quatrano RS. 1997. Characterization and expression of a rice RAD23 gene. Plant Mol. Biol. 34:557-62
130. TIRI in mediating auxin response. Science 292:1379-82
131. Schwechheimer C, Serino G, Deng XW. 2002. Multiple ubiquitin ligase-mediated processes require COP9 signalosome and AXR1 function. Plant Cell 14:2553-63
132. Semple CAM, RIKEN GER Group, GSL Members. 2003. The comparative proteomics of ubiquitination in mouse. Genome Res. 13:1389-94
133. Seo HS, Yang JY, Ishikawa M, Bolle C, Ballesteros ML, Chua NH. 2003. LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 423:995-99
134. Serino G, Deng XW. 2003. The COP9 signalsome: regulating plant development through control of proteolysis. Annu. Rev. Plant Biol. 54:165-82
135. Shalitin D, Yang HY, Mockler TC, Maymon M, Guo HW, et al. 2002. Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation. Nature 417:763-67
136. Shen WH, Parmentier Y, Hellmann H, Lechner E, Dong A, et al. 2002. Null mutation of AtCUL1 causes arrest in early embryogenesis in Arabidopsis. Mol. Biol. Cell. 13:1916-28
137. Shibahara T, Kawasaki H, Hirano H. 2002. Identification of the 19S regulatory particle subunits from the rice 26S proteasome. Eur. J. Biochem. 269:1474-83
138. Sieberer T, Seifen GJ, Hauser MT, Grisafi P, Fink GR, Luschnig C. 2000. Post-transcriptional control of the Arabidopsis auxin efflux carrier EIR1 requires AXR1. Curr. Biol. 10:1595-98
139. Smalle J, Kurepa J, Yang P, Babiychuk E, Kushnir S, et al. 2002. Cytokinin growth responses in Arabidopsis involve the 26S proteasome subunit RPN12a. Plant Cell 14:17-32
140. Smalle J, Kurepa J, Yang P, Emborg TJ, Babyichuk E, et al. 2003. The pleiotropic role of the 26S proteasome subunit RPN10 in Arabidopsis thaliana growth and development supports a substrate-specific function in abscisic acid signaling. Plant Cell 15:965-80
141. Somers DE, Schultz TF, Milnamow M, Kay SA. 2000. ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 101:319-29
142. Stimberg P, van de Sande K, Leyser HM. 2002. MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129:1131-41
143. Stone SL, Anderson EM, Mullen RT, Goring DR. 2003. ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15:885-98
144. Sun CW, Griffen S, Callis J. 1997. A Model for the evolution of polyubiquitin genes from the study of Arabidopsis thaliana ecotypes. Plant Mol. Biol. 34:745-58
145. Suzuki G, Yanagawa Y, Kwok SF, Matsui M, Deng XW. 2002. Arabidopsis COP10 is a ubiquitin-conjugating enzyme variant that acts together with COP1 and the COP9 signalosome in repressing photomorphogenesis. Genes Dev. 16:554-59
146. Takai R, Matsuda N, Nakano A, Hasegawa K, Akimoto C, et al. 2002. EL5, a rice N-acetylchitooligosaccharide elicitor-responsive RING-H2 finger protein, is a ubiquitin ligase which functions in vitro in cooperation with an elicitor-responsive ubiquitin-conjugating enzyme, Os UBC5b. Plant J. 30:447-55
147. Tang GQ, Hardin SC, Dewey R, Huber SC. 2003. A novel C-terminal proteolytic processing of cytosolic pyruvate kinase, its phosphorylation and degradation by the proteasome in developing soybean seeds. Plant J. 34:77-93
148. Thomma B, Eggermont K, Penninckx I, Mauch-Mani B, Vogelsang R, et al. 1998. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. USA 95:15107-11
149. Tzafrir I, McElver JA, Liu CM, Yang LJ, Wu JQ, et al. 2002. Diversity of TITAN functions in Arabidopsis seed development. Plant Physiol. 128:38-51
150. Unno M, Mizushima T, Morimoto Y, Tomisugi Y, Tanaka K, et al. 2002. The structure of the mammalian 20S proteasome at 2.75 angstrom resolution. Structure 10:609-18
151. Ushijima K, Sassa H, Dandekar AM, Gradziel TM, Tao R, Hirano H. 2003. Structural and transcriptional analysis of the self-incompatibility locus of almond: identification of a pollen-expressed F-Box gene with haplotype-specific polymorphism. Plant Cell 15:771-81
152. Ustrell V, Hoffman L, Pratt G, Rechsteiner M. 2002. PA200, a nuclear proteasome activator involved in DNA repair. EMBO J. 21:3516-25
153. VanDemark AP, Hofmann RM, Tsui C, Pickart CM, Wolberger C. 2001. Molecular insights into polyubiquitin chain assembly: crystal structure of the MMS2/UBC13 heterodimer. Cell 105:711-20
154. van Nocker S, Vierstra RD. 1993. Multiubiquitin chains linked through lysine 48 are abundant in vivo and are competent intermediates in the ubiquitin proteolytic pathway. J. Biol. Chem. 268:24766-73
155. Varshavsky A. 2003. The N-end rule and regulation of apoptosis. Nat. Cell Biol. 5:373-76
156. Verdecia MA, Joazeiro CAP, Wells NJ, Ferrer JL, Bowman ME, et al. 2003. Conformational flexibility underlies ubiquitin ligation mediated by the WWP1 HECT domain E3 ligase. Mol. Cell 11:249-59
157. Verma R, Aravind L, Oania R, McDonald WH, Yates JR 3rd, et al. 2002. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298:611-15
158. Verma R, Chen S, Feldman R, Schieltz D, Yates J, et al. 2000. Proteasomal proteomics: Identification of nucleotide-sensitive proteasome-interacting proteins by mass spectrometric analysis of affinity-purified proteasomes. Mol. Biol. Cell 11:3425-39
159. Verma R, Deshaies RJ. 2000. A proteasome howdunit: the case of the missing signal. Cell 101:341-44
160. Vierstra RD. 1993. Protein degradation in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44:385-410
161. Vierstra RD. 1996. Proteolysis in plants: mechanisms and functions. Plant Mol. Biol. 32:275-302
162. Vierstra RD. 2003. The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci. 8:135-42
163. Vierstra RD, Callis J. 1999. Polypeptide tags, ubiquitous modifiers for plant protein regulation. Plant Mol. Biol. 41:435-42
164. Vinardell JM, Fedorova E, Cebolla A, Kevei Z, Horvath G, et al. 2003. Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules. Plant Cell 15:2093-105
165. Voges D, Zwickl P, Baumeister W. 1999. The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68:1015-68
166. von Arnim AG, Chamovitz DA. 2003. Protein homeostasis: A degrading role for Int6/eIF3e. Curr. Biol. 13:323-25
167. Weissman AM. 2001. Themes and variations on ubiquitylation. Nat. Rev. Mol. Cell Biol. 2:169-78
168. Wilkinson M, Silva ED, Zachgo S, Saedler H, Schwarz-Sommer Z. 2000. CHORIPETALA and DESPENTEADO: general regulators during plant development and potential floral targets of FIMBRIATA-mediated degradation. Development 127:3725-34
169. Wing SS. 2003. Deubiquitinating enzymes - the importance of driving in reverse along the ubiquitin-proteasome pathway. Int. J. Biochem. Cell Biol. 35:590-605
170. Woffenden BJ, Freeman TB, Beers EP. 1998. Proteasome inhibitors prevent tracheary element differentiation in Zinnia mesophyll cell cultures. Plant Physiol. 118:419-30
171. Woo HR, Chung KM, Park JH, Oh SA, Ahn T, et al. 2001. ORE9, an F-Box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13:1779-90
172. Worley CK, Ling R, Callis J. 1998. Engineering in vivo instability of firefly luciferase and Escherichia coli β-glucuronidase in higher plants using recognition elements from the ubiquitin pathway. Plant Mol. Biol. 37:337-47
173. Wu G, Xu GZ, Schulman BA, Jeffrey PD, Harper JW, Pavletich NP. 2003. Structure of a β-TrCP1-Skp1-β-catenin complex: destruction motif binding and lysine specificity of the SCF β-TrCP1 ubiquitin ligase. Mol. Cell 11:1445-56
174. Xie Q, Guo HS, Dallman G, Fang SY, Weissman AM, Chua NH. 2002. SINAT5 promotes ubiquitin-related degradation of NACl to attenuate auxin signals. Nature 419:167-70
175. Xie Y, Varshavsky A. 2000. Physical association of ubiquitin ligases and the 26S proteasome. Proc. Natl. Acad. Sci. USA 97:2497-502
176. Xie Y, Varshavsky A. 2001. RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: A negative feedback circuit. Proc. Natl. Acad. Sci. USA 98:3056-61
177. COII ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14:1919-35
178. Xu L, Wei Y, Reboul J, Vaglio P, Shin T-H, et al. 2003. BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 425:316-21
179. Van J, Wang J, Li Q, Hwang J-R, Patterson C, Zhang H. 2003. AtCHIP, a U-Box-containing E3 ubiquitin ligase, plays a critical role in temperature stress tolerance in Arabidopsis. Plant Physiol. 132:1-9
180. Yan N, Doelling JH, Falbel TG, Durski AM, Vierstra RD. 2000. The ubiquitin-specific protease family from Arabidopsis. AtUBP1 and 2 are required for the resistance to the amino acid analog canavanine. Plant Physiol. 124:1828-43
181. Yanagawa Y, Hasezawa S, Kumagai F, Oka M, Fujimuro M, et al. 2002. Cell-cycle dependent dynamic change of 26S proteasome distribution in tobacco B Y-2 cells. Plant Cell Physiol. 43:604-13
182. Yanagisawa S, Yoo S-D, Sheen J. 2003. Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425:521-25
183. Yang M, Hu Y, Lodhi M, McCombie WR, Ma H. 1999. The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation. Proc. Natl. Acad. Sci. USA 96:11416-21
184. Yang P, Fu H, Walker J, Papa CM, Smalle J, et al. 2004. Purification of the Arabidopsis 26S proteasome: biochemical and molecular analyses revealed the presence of multiple isoforms. J. Biol. Chem. 279:6401-13
185. Yoshida S, Ito M, Callis J, Nishida I, Watanabe A. 2002. A delayed leaf senescence mutant is defective in arginyl-tRNA: protein arginyltransferase, a component of the N-End Rule pathway in Arabidopsis. Plant J. 32:129-37
186. Zenser N, Ellsmore A, Leasure C, Callis J. 2001. Auxin modulates the degradation rate of Aux/IAA proteins. Proc. Natl. Acad. Sci. USA 98:11795-1800
187. Zhao DZ, Yu QL, Chen M, Ma H. 2001. The ASK1 gene regulates B function gene expression in cooperation with UFO and LEAFY in Arabidopsis. Development 128:2735-46
188. Zhao YD, Dai XH, Blackwell HE, Schreiber SL, Chory J. 2003. SIR1, an upstream component in auxin signaling identified by chemical genetics. Science 301:1107-10
189. Zheng N, Schulman BA, Song L, Miller JJ, Jeffrey PD, et al. 2002. Structure of the Cull-Rbx1-Skp1-F Box Skp2 SCF ubiquitin ligase complex. Nature 416:703-9
190. Zheng N, Wang P, Jeffrey PD, Pavletich NP. 2000. Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases. Cell 102:533-39