Plant E3 ligases: Flexible enzymes in a sessile world

Molecular Plant

Volumn 6, Issue 5, 2013, Pages 1388-1404

  Chen, Liyuan ^a   Hellmann, Hanjo ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

E3 ligases; plant development; plant physiology; ubiquitin proteasome pathway

Indexed keywords

ANIMALIA;

UBIQUITIN PROTEIN LIGASE;

BIOLOGICAL MODEL; CLASSIFICATION; E3 LIGASES; ENZYMOLOGY; METABOLISM; PLANT; PLANT DEVELOPMENT; PLANT PHYSIOLOGY; REVIEW; UBIQUITIN PROTEASOME PATHWAY;

E3 LIGASES; PLANT DEVELOPMENT; PLANT PHYSIOLOGY; UBIQUITIN PROTEASOME PATHWAY;

MODELS, BIOLOGICAL; PLANTS; UBIQUITIN-PROTEIN LIGASES;

EID: 84885037043     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sst005     Document Type: Review

References (217)

1. Adenot, X., et al. (2006). DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr. Biol. 16, 927-932.
2. Al Khateeb, W.M., and Schroeder, D.F. (2009). Overexpression of Arabidopsis damaged DNA binding protein 1A (DDB1A) enhances UV tolerance. Plant Mol. Biol. 70, 371-383.
3. Amador, V., Monte, E., Garcia-Martinez, J.L., and Prat, S. (2001). Gibberellins signal nuclear import of PHOR1, a photoperiodresponsive protein with homology to Drosophila armadillo. Cell. 106, 343-354.
4. An, F., et al. (2010). Ethylene-induced stabilization of ETHYLENE INSENSITIVE3 and EIN3-LIKE1 is mediated by proteasomal degradation of EIN3 binding F-box 1 and 2 that requires EIN2 in Arabidopsis. Plant Cell. 22, 2384-2401.
5. Andrade, M.A., and Bork, P. (1995). HEAT repeats in the Huntington's disease protein. Nat. Genet. 11, 115-116.
6. Ariizumi, T., and Steber, C.M. (2007). Seed germination of GA-insensitive sleepy1 mutants does not require RGL2 protein disappearance in Arabidopsis. Plant Cell. 19, 791-804.
7. Ariizumi, T., Lawrence, P.K., and Steber, C.M. (2011). The role of two F-box proteins, SLEEPY1 and SNEEZY, in Arabidopsis gibberellin signaling. Plant Physiol. 155, 765-775.
8. Ariizumi, T., Murase, K., Sun, T.P., and Steber, C.M. (2008). Proteolysis-independent downregulation of DELLA repression in Arabidopsis by the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1. Plant Cell. 20, 2447-2459.
9. Azevedo, C., Santos-Rosa, M.J., and Shirasu, K. (2001). The U-box protein family in plants. Trends Plant Sci. 6, 354-358.
10. Bae, H., Kim, S.K., Cho, S.K., Kang, B.G., and Kim, W.T. (2011). Overexpression of OsRDCP1, a rice RING domain-containing E3 ubiquitin ligase, increased tolerance to drought stress in rice (Oryza sativa L.). Plant Sci. 180, 775-782.
11. Barford, D. (2011). Structural insights into anaphase-promoting complex function and mechanism. Philos. Trans. R Soc. Lond. B Biol. Sci. 366, 3605-3624.
12. Bates, P.W., and Vierstra, R.D. (1999). UPL1 and 2, two 405 kDa ubiquitin-protein ligases from Arabidopsis thaliana related to the HECT-domain protein family. Plant J. 20, 183-195.
13. Bergler, J., and Hoth, S. (2011). Plant U-box armadillo repeat proteins AtPUB18 and AtPUB19 are involved in salt inhibition of germination in Arabidopsis. Plant Biol. (Stuttg.). 13, 725-730.
14. Bernhardt, A., et al. (2006). CUL4 associates with DDB1 and DET1 and its downregulation affects diverse aspects of development in Arabidopsis thaliana. Plant J. 47, 591-603.
15. Bernhardt, A., Mooney, S., and Hellmann, H. (2010). Arabidopsis DDB1a and DDB1b are critical for embryo development. Planta. 232, 555-566.
16. Biedermann, S., and Hellmann, H. (2010). The DDB1a interacting proteins ATCSA-1 and DDB2 are critical factors for UV-B tolerance and genomic integrity in Arabidopsis thaliana. Plant J. 62, 404-415.
17. Biedermann, S., and Hellmann, H. (2011). WD40 and CUL4-based E3 ligases: lubricating all aspects of life. Trends Plant Sci. 16, 38-46.
18. Biedermann, S., Mooney, S., and Hellmann, H. (2011). Recognition and repair pathways of damaged DNA in higher plants. In Selected Topics in DNA Repair, Chen, C.C., ed. (New York: InTech Publishing).
19. Binder, B.M., Walker, J.M., Gagne, J.M., Emborg, T.J., Hemmann, G., Bleecker, A.B., and Vierstra, R.D. (2007). The Arabidopsis EIN3 binding F-box proteins EBF1 and EBF2 have distinct but overlapping roles in ethylene signaling. Plant Cell. 19, 509-523.
20. Bjerkan, K.N., Jung-Romeo, S., Jurgens, G., Genschik, P., and Grini, P.E. (2012). Arabidopsis WD repeat domain55 Interacts with DNA damaged binding protein1 and is required for apical patterning in the embryo. Plant Cell. 24, 1013-1033.
21. Blilou, I., Frugier, F., Folmer, S., Serralbo, O., Willemsen, V., Wolkenfelt, H., Eloy, N.B., Ferreira, P.C., Weisbeek, P., and Scheres, B. (2002). The Arabidopsis HOBBIT gene encodes a CDC27 homolog that links the plant cell cycle to progression of cell differentiation. Genes Dev. 16, 2566-2575.
22. Boh, B.K., Ng, M.Y., Leck, Y.C., Shaw, B., Long, J., Sun, G.W., Gan, Y.H., Searle, M.S., Layfield, R., Hagen, T. (2011). Inhibition of cullin RING ligases by cycle inhibiting factor: evidence for interference with Nedd8-induced conformational control J. Mol. Biol. 413, 430-437.
23. Borden, K.L. (2000). RING domains: master builders of molecular scaffolds? J. Mol. Biol. 295, 1103-1112.
24. Cai, Y., Zhuang, X., Wang, J., Wang, H., Lam, S.K., Gao, C., Wang, X., and Jiang, L. (2012). Vacuolar degradation of two integral plasma membrane proteins, AtLRR84A and OsSCAMP1, is cargo ubiquitination-independent and prevacuolar compartmentmediated in plant cells. Traffic. 13, 1023-1040.
25. Calderon-Villalobos, L.I., Tan, X., Zheng, N., and Estelle, M. (2010). Auxin perception-structural insights. Cold Spring Harb. Perspect. Biol. 2, a005546.
26. Calderon Villalobos, L.I., et al. (2012). A combinatorial TIR1/AFBAux/ IAA co-receptor system for differential sensing of auxin. Nat. Chem. Biol. 8, 477-485.
27. Callis, J., and Vierstra, R.D. (2000). Protein degradation in signaling. Curr. Opin. Plant Biol. 3, 381-386.
28. Callis, J., Carpenter, T., Sun, C.W., and Vierstra, R.D. (1995). Structure and evolution of genes encoding polyubiquitin and ubiquitin-like proteins in Arabidopsis thaliana ecotype Columbia. Genetics. 139, 921-939.
29. Capron, A., Okresz, L., and Genschik, P. (2003). First glance at the plant APC/C, a highly conserved ubiquitin-protein ligase. Trends Plant Sci. 8, 83-89.
30. Carter, R.S., Pennington, K.N., Arrate, P., Oltz, E.M., and Ballard, D.W. (2005). Site-specific monoubiquitination of IkappaB kinase IKKbeta regulates its phosphorylation and persistent activation. J. Biol. Chem. 280, 43272-43279.
31. Castells, E., Molinier, J., Benvenuto, G., Bourbousse, C., Zabulon, G., Zalc, A., Cazzaniga, S., Genschik, P., Barneche, F., and Bowler, C. (2011). The conserved factor DE-ETIOLATED 1 cooperates with CUL4-DDB1DDB2 to maintain genome integrity upon UV stress. EMBO J. 30, 1162-1172.
32. Chastagner, P., Israel, A., and Brou, C. (2006). Itch/AIP4 mediates Deltex degradation through the formation of K29-linked polyubiquitin chains. EMBO Rep. 7, 1147-1153.
33. Chen, G., Zhang, B., Liu, L., Li, Q., Zhang, Y., Xie, Q., and Xue, Y. (2012). Identification of a ubiquitin-binding structure in the S-locus F-box protein controlling S-RNase-based self-incompatibility. J. Genet. Genomics. 39, 93-102.
34. Chen, H., et al. (2010). Arabidopsis CULLIN4-damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1- SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time. Plant Cell. 22, 108-123.
35. Cheng, M.C., Hsieh, E.J., Chen, J.H., Chen, H.Y., and Lin, T.P. (2012). Arabidopsis RGLG2, functioning as a RING E3 ligase, interacts with AtERF53 and negatively regulates the plant drought stress response. Plant Physiol. 158, 363-375.
36. Cheng, Y., Qin, G., Dai, X., and Zhao, Y. (2007). NPY1, a BTB-NPH3- like protein, plays a critical role in auxin-regulated organogenesis in Arabidopsis. Proc. Natl Acad. Sci. U S A. 104, 18825-18829.
37. Chini, A., et al. (2007). The JAZ family of repressors is the missing link in jasmonate signalling. Nature. 448, 666-671.
38. Cho, S.K., Ryu, M.Y., Seo, D.H., Kang, B.G., and Kim, W.T. (2011). The Arabidopsis RING E3 ubiquitin ligase AtAIRP2 plays combinatory roles with AtAIRP1 in abscisic acid-mediated drought stress responses. Plant Physiol. 157, 2240-2257.
39. Christians, M.J., Gingerich, D.J., Hansen, M., Binder, B.M., Kieber, J.J., and Vierstra, R.D. (2009). The BTB ubiquitin ligases ETO1, EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels. Plant J. 57, 332-345.
40. Christie, J.M. (2007). Phototropin blue-light receptors. Annu. Rev. Plant Biol. 58, 21-45.
41. Chuang, H.W., Zhang, W., and Gray, W.M. (2004). Arabidopsis ETA2, an apparent ortholog of the human cullin-interacting protein CAND1, is required for auxin responses mediated by the SCF(TIR1) ubiquitin ligase. Plant Cell. 16, 1883-1897.
42. Cope, G.A., and Deshaies, R.J. (2003). COP9 signalosome: a multifunctional regulator of SCF and other cullin-based ubiquitin ligases. Cell. 114, 663-671.
43. Craig, K.L., and Tyers, M. (1999). The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. Prog. Biophys. Mol. Biol. 72, 299-328.
44. del Pozo, J.C., and Estelle, M. (1999). The Arabidopsis cullin AtCUL1 is modified by the ubiquitin-related protein RUB1. Proc. Natl Acad. Sci. U S A. 96, 15342-15347.
45. del Pozo, J.C., Boniotti, M.B., and Gutierrez, C. (2002a). Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin- SCF(AtSKP2) pathway in response to light. Plant Cell. 14, 3057-3071.
46. del Pozo, J.C., Dharmasiri, S., Hellmann, H., Walker, L., Gray, W.M., and Estelle, M. (2002b). AXR1-ECR1-dependent conjugation of RUB1 to the Arabidopsis Cullin AtCUL1 is required for auxin response. Plant Cell. 14, 421-433.
47. Devoto, A., Nieto-Rostro, M., Xie, D., Ellis, C., Harmston, R., Patrick, E., Davis, J., Sherratt, L., Coleman, M., and Turner, J.G. (2002). COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. Plant J. 32, 457-466.
48. Dharmasiri, N., Dharmasiri, S., and Estelle, M. (2005a). The F-box protein TIR1 is an auxin receptor. Nature. 435, 441-445.
49. Dharmasiri, N., Dharmasiri, S., Weijers, D., Lechner, E., Yamada, M., Hobbie, L., Ehrismann, J.S., Jürgens, G., and Estelle, M. (2005b). Plant development is regulated by a family of auxin receptor F box proteins. Dev. Cell. 9, 109-119.
50. Dharmasiri, N., Dharmasiri, S., Weijers, D.,Karunarathna, N., Jurgens, G.,and Estelle, M. (2007). AXL and AXR1 have redundant functions in RUB conjugation and growth and development in Arabidopsis. Plant J. 52, 114-123.
51. Dharmasiri, S., Dharmasiri, N., Hellmann, H., and Estelle, M. (2003). The RUB/Nedd8 conjugation pathway is required for early development in Arabidopsis. EMBO J. 22, 1762-1770.
52. Dieterle, M., Thomann, A., Renou, J.P., Parmentier, Y., Cognat, V., Lemonnier, G., Muller, R., Shen, W. H., Kretsch, T., and Genschik, P. (2005). Molecular and functional characterization of Arabidopsis Cullin 3A. Plant J. 41, 386-399.
53. Dill, A., Thomas, S.G., Hu, J., Steber, C.M., and Sun, T.P. (2004). The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell. 16, 1392-1405.
54. Dohmann, E.M., Kuhnle, C., and Schwechheimer, C. (2005). Loss of the CONSTITUTIVE PHOTOMORPHOGENIC9 signalosome subunit 5 is sufficient to cause the cop/det/fus mutant phenotype in Arabidopsis. Plant Cell. 17, 1967-1978.
55. Downes, B.P., Stupar, R.M., Gingerich, D.J., and Vierstra, R.D. (2003). The HECT ubiquitin-protein ligase (UPL) family in Arabidopsis: UPL3 has a specific role in trichome development. Plant J. 35, 729-742.
56. Duda, D.M., Scott, D.C., Calabrese, M.F., Zimmerman, E.S., Zheng, N., and Schulman, B.A. (2011). Structural regulation of cullin-RING ubiquitin ligase complexes. Curr. Opin. Struct. Biol. 21, 257-264.
57. Dumbliauskas, E., et al. (2011). The Arabidopsis CUL4-DDB1 complex interacts with MSI1 and is required to maintain MEDEA parental imprinting. EMBO J. 30, 731-743.
58. El Refy, A., Perazza, D., Zekraoui, L., Valay, J. G., Bechtold, N., Brown, S., Hulskamp, M.,Herzog, M., and Bonneville, J.M. (2003). The Arabidopsis KAKTUS gene encodes a HECT protein and controls the number of endoreduplication cycles. Mol. Genet. Genomics. 270, 403-414.
59. Eloy, N.B., et al. (2012). SAMBA, a plant-specific anaphase-promoting complex/cyclosome regulator is involved in early development and A-type cyclin stabilization. Proc. Natl Acad. Sci U S A. 109, 13853-13858.
60. Feng, S., Shen, Y., Sullivan, J.A., Rubio, V., Xiong, Y., Sun, T.P., and Deng, X.W. (2004). Arabidopsis CAND1, an unmodified CUL1- interacting protein, is involved in multiple developmental pathways controlled by ubiquitin/proteasome-mediated protein degradation. Plant Cell. 16, 1870-1882.
61. Freemont, P.S., Hanson, I.M., and Trowsdale, J. (1991). A novel cysteine-rich sequence motif. Cell. 64, 483-484.
62. Fu, Z.Q., et al. (2012). NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature. 486, 228-232.
63. Fukudome, A., Kanaya, A., Egami, M., Nakazawa Y., Hiraguri, A., Moriyama, H., and Fukuhara, T. (2011). Specific requirement of DRB4, a dsRNA-binding protein, for the in vitro dsRNA-cleaving activity of Arabidopsis Dicer-like 4. RNA. 17, 750-760.
64. Furutani, M., Sakamoto, N., Yoshida, S., Kajiwara, T., Robert, H.S., Friml, J., and Tasaka, M. (2011). Polar-localized NPH3-like proteins regulate polarity and endocytosis of PIN-FORMED auxin efflux carriers. Development. 138, 2069-2078.
65. Gagne, J.M., Downes, B.P., Shiu, S.H., Durski, A.M., and Vierstra, R.D. (2002). The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc. Natl Acad. Sci. U S A. 99, 11519-11524.
66. Gagne J.M., Smalle J., Gingerich D.J., Walker J.M., Yoo S.D., Yanagisawa S., and Vierstra R.D. (2004). Arabidopsis EIN3- binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proc. Natl Acad. Sci. U S A. 101, 6803-6808.
67. Gao, T., Smalle J., Gingerich D.J., Walker J.M., Yoo S.D., Yanagisawa S., and Vierstra R.D. (2011). OsSDIR1 overexpression greatly improves drought tolerance in transgenic rice. Plant Mol. Biol. 76, 145-156.
68. Gilkerson, J., Hu, J., Brown, J., Jones , A., Sun, T.P., and Callis, J. (2009). Isolation and characterization of cul1-7, a recessive allele of CULLIN1 that disrupts SCF function at the C terminus of CUL1 in Arabidopsis thaliana. Genetics. 181, 945-963.
69. Gingerich, D.J., Gagne, J.M., Salter, D.W., Hellmann, H., Estelle, M., Ma, L., and Vierstra, R.D. (2005). Cullins 3a and 3b assemble with members of the broad complex/tramtrack/bric-a-brac (BTB) protein family to form essential ubiquitin-protein ligases (E3s) in Arabidopsis. J. Biol. Chem. 280, 18810-18821.
70. Gingerich, D.J., Hanada, K., Shiu, S.H., and Vierstra, R.D. (2007). Large-scale, lineage-specific expansion of a bric-a-brac/ tramtrack/broad complex ubiquitin-ligase gene family in rice. Plant Cell. 19, 2329-2348.
71. Glotzer, M., Murray, A.W., and Kirschner, M.W. (1991). Cyclin is degraded by the ubiquitin pathway. Nature. 349, 132-138.
72. Gomi, K., et al. (2004). 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, 626-634.
73. Gray, W.M., Hellmann, H., Dharmasiri, S., and Estelle, M. (2002). Role of the Arabidopsis RING-H2 protein RBX1 in RUB modification and SCF function. Plant Cell. 14, 2137-2144.
74. Greenham, K., Santner, A., Castillejo, C., Mooney, S., Sairanen, I., Ljung, K., and Estelle, M. (2011). The AFB4 auxin receptor is a negative regulator of auxin signaling in seedlings. Curr. Biol. 21, 520-525.
75. Griffiths, J., et al. (2006). Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell. 18, 3399-3414.
76. Guerra, D., Mastrangelo, A.M.,Lopez-Torrejon, G.,Marzin, S., Schweizer, P., Stanca, A.M.,del Pozo, J.C., Cattivelli, L., and Mazzucotelli, E. (2012). Identification of a protein network interacting with TdRF1, a wheat RING ubiquitin ligase with a protective role against cellular dehydration. Plant Physiol. 158, 777-789.
77. Guo, H., and Ecker, J.R. (2003). Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell. 115, 667-677.
78. Gusmaroli, G., Figueroa, P., Serino, G., and Deng, X.W. (2007). Role of the MPN subunits in COP9 signalosome assembly and activity, and their regulatory interaction with Arabidopsis Cullin3- based E3 ligases. Plant Cell. 19, 564-581.
79. Han, L., Mason, M., Risseeuw, E.P., Crosby, W.L., and Somers, D.E. (2004). Formation of an SCF(ZTL) complex is required for proper regulation of circadian timing. Plant J. 40, 291-301.
80. Harmon, F., Imaizumi, T., and Gray, W.M. (2008). CUL1 regulates TOC1 protein stability in the Arabidopsis circadian clock. Plant J. 55, 568-579.
81. Harmon, F.G., and Kay, S.A. (2003). The F box protein AFR is a positive regulator of phytochrome A-mediated light signaling. Curr. Biol. 13, 2091-2096.
82. Hatakeyama, S., Yada, M., Matsumoto, M., Ishida, N., and Nakayama, K.I. (2001). U box proteins as a new family of ubiquitin- protein ligases. J. Biol. Chem. 276, 33111-33120.
83. Hatzfeld, M. (1999). The armadillo family of structural proteins. Int. Rev. Cytol. 186, 179-224.
84. Hayward, A., Stirnberg, P., Beveridge, C., and Leyser, O. (2009). Interactions between auxin and strigolactone in shoot branching control. Plant Physiol. 151, 400-412.
85. Hellmann, H., and Estelle, M. (2002). Plant development: regulation by protein degradation. Science. 297, 793-797.
86. Helmstaedt, K., Schwier, E.U., Christmann, M., Nahlik, K., Westermann, M., Harting, R., Grond, S., Busch, S., and Braus, G.H. (2011). Recruitment of the inhibitor Cand1 to the cullin substrate adaptor site mediates interaction to the neddylation site. Mol. Biol. Cell. 22, 153-164.
87. Herve, C., Lefebvre, B., and Cullimore, J. (2011). How many E3 ubiquitin ligase are involved in the regulation of nodulation? Plant Signal. Behav. 6, 660-664.
88. Himmelbach, A., Hoffmann, T., Leube, M., Hohener, B., and Grill, E. (2002). Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. EMBO J. 21, 3029-3038.
89. Ho, M.S., Tsai, P.I., and Chien, C.T. (2006). F-box proteins: the key to protein degradation. J. Biomed. Sci. 13, 181-191.
90. Holm, M., Ma, L.G., Qu, L.J., and Deng, X.W. (2002). Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev. 16, 1247-1259.
91. Hong, J.K., Choi, H.W., Hwang, I.S., and Hwang, B.K. (2007). Role of a novel pathogen-induced pepper C3-H-C4 type RING-finger protein gene, CaRFPI, in disease susceptibility and osmotic stress tolerance. Plant Mol. Biol. 63, 571-588.
92. Hong, M.J., Kim, D.Y., Kang, S.Y., Kim, D.S., Kim, J.B., and Seo, Y.W. (2012). Wheat F-box protein recruits proteins and regulates their abundance during wheat spike development. Mol. Biol. Rep 39, 9681-9696.
93. Hotton, S.K., and Callis, J. (2008). Regulation of cullin RING ligases. Annu. Rev. Plant Biol. 59, 467-489.
94. Hotton, S.K., Eigenheer, R.A., Castro, M.F., Bostick, M., and Callis, J. (2011). AXR1-ECR1 and AXL1-ECR1 heterodimeric RUBactivating enzymes diverge in function in Arabidopsis thaliana. Plant Mol. Biol. 75, 515-526.
95. Hu, Y., Dong, Q., and Yu, D. (2012). Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci. 185-186, 288-297.
96. Hua, Z., and Kao, T.H. (2006). Identification and characterization of components of a putative petunia S-locus F-box-containing E3 ligase complex involved in S-RNase-based self-incompatibility. Plant Cell. 18, 2531-2553.
97. Hua, Z., and Vierstra, R.D. (2011). The cullin-RING ubiquitin-protein ligases. Annu. Rev. Plant Biol. 62, 299-334.
98. Huibregtse, J.M., Scheffner, M., Beaudenon, S., and Howley, P.M. (1995). A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl Acad. Sci. U S A. 92, 5249.
99. Hur, Y.J., Yi, Y.B., Lee, J.H., Chung , Y.S., Jung, H.W., Yun, D.J., Kim, K.M., Park, D.S., and Kim, D.H. (2012). Molecular cloning and characterization of OsUPS, a U-box containing E3 ligase gene that respond to phosphate starvation in rice (Oryza sativa). Mol. Biol. Rep. 39, 5883-5888.
100. Ikeda, F., and Dikic, I. (2008). Atypical ubiquitin chains: new molecular signals. 'Protein Modifications: Beyond the Usual Suspects' review series. EMBO Rep. 9, 536-542.
101. Imaizumi, T., Schultz, T.F., Harmon, F.G., Ho, L.A., and Kay, S.A. (2005). FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science. 309, 293-297.
102. Jin, J., Cardozo, T., Lovering, R.C., Elledge, S.J., Pagano, M., and Harper, J.W. (2004). Systematic analysis and nomenclature of mammalian F-box proteins. Genes Dev. 18, 2573-2580.
103. Katsir, L., Chung, H.S., Koo, A.J., and Howe, G.A. (2008). Jasmonate signaling: a conserved mechanism of hormone sensing. Curr. Opin. Plant Biol. 11, 428-435.
104. Katzmann, D.J., Sarkar, S., Chu, T., Audhya, A., and Emr, S.D. (2004). Multivesicular body sorting: ubiquitin ligase Rsp5 is required for the modification and sorting of carboxypeptidase S. Mol. Biol. Cell. 15, 468-480.
105. Kendrick, M.D., and Chang, C. (2008). Ethylene signaling: new levels of complexity and regulation. Curr. Opin. Plant Biol. 11, 479-485.
106. Kepinski, S., and Leyser, O. (2005). The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature. 435, 446-451.
107. Kim, H.J., Oh, S.A., Brownfield, L., Hong, S.H., Ryu, H., Hwang, I., Twell, D., and Nam, H.G., (2008). Control of plant germline proliferation by SCF(FBL17) degradation of cell cycle inhibitors. Nature. 455, 1134-1137.
108. Kim, S.J., Ryu, M.Y., and Kim, W.T. (2012). Suppression of Arabidopsis RING-DUF1117 E3 ubiquitin ligases, AtRDUF1 and AtRDUF2, reduces tolerance to ABA-mediated drought stress. Biochem. Biophys. Res. Commun. 420, 141-147.
109. Kitashiba, H., Liu, P., Nishio, T., Nasrallah, J.B., and Nasrallah, M.E. (2011). Functional test of Brassica self-incompatibility modifiers in Arabidopsis thaliana. Proc. Natl Acad. Sci. U S A. 108, 18173-18178.
110. Koegl, M., Hoppe, T., Schlenker, S., Ulrich, H.D., Mayer, T.U., and Jentsch, S.A (1999). A novel ubiquitination factor, E4, is involved in multiubiquitin chain assembly. Cell. 96, 635-644.
111. Kohler, C., Hennig, L., Bouveret, R., Gheyselinck, J., Grossniklaus, U., and Gruissem, W. (2003). Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J. 22, 4804-4814.
112. Kraft, E., Stone, S.L., Ma, L., Su, N., Gao, Y., Lau, O.S., Deng, X.W., and Callis, J. (2005). Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiol. 139, 1597-1611.
113. Lau, O.S., and Deng, X.W. (2012). The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci 17, 584-593.
114. Lechner, E., Leonhardt, N., Eisler, H., Parmentier, Y., Alioua, M., Jacquet, H.,Leung, J.,and Genschik, P. (2011). MATH/BTB CRL3 receptors target the homeodomain-leucine zipper ATHB6 to modulate abscisic acid signaling. Dev. Cell. 21, 1116-1128.
115. Lee, H.K., Cho, S.K., Son, O., Xu, Z., Hwang, I., and Kim, W.T. (2009). Drought stress-induced Rma1H1, a RING membraneanchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell. 21, 622-641.
116. Lee, J.H., Terzaghi, W., Gusmaroli, G., Charron, J.B., Yoon, H.J., Chen, H., He, Y.J., Xiong, Y., and Deng, X.W. (2008). Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell. 20, 152-167.
117. Leverson, J.D., Joazeiro, C.A., Page, A.M., Huang, H., Hieter, P., and Hunter, T. (2000). The APC11 RING-H2 finger mediates E2-dependent ubiquitination. Mol. Biol. Cell. 11, 2315-2325.
118. Li, W., Dai, L., and Wang, G.L. (2012). PUB13, a U-box/ARM E3 ligase, regulates plant defense, cell death, and flowering time. Plant Signal Behav. 7, 239-250.
119. Li, X., et al. (2003). Control of tillering in rice. Nature. 422, 618-621.
120. Lima Mde, F., et al. (2010). Genomic evolution and complexity of the Anaphase-promoting Complex (APC) in land plants. BMC Plant Biol. 10, 254.
121. Lin, H., et al. (2009). DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell. 21, 1512-1525.
122. Liu, L., Zhang, Y.,Tang, S., Zhao, Q., Zhang, Z., Dong, L., Guo, H., and Xie, Q. (2010). An efficient system to detect protein ubiquitination by agroinfiltration in Nicotiana benthamiana. Plant J. 61, 893-903.
123. Liu, Y.C., Wu, Y.R., Huang, X.H., Sun, J., and Xie, Q. (2011). AtPUB19, a U-box E3 ubiquitin ligase, negatively regulates abscisic acid and drought responses in Arabidopsis thaliana. Mol. Plant. 4, 938-946.
124. Luna, E., Bruce, T.J., Roberts, M.R., Flors, V., and Ton, J. (2012). Next-generation systemic acquired resistance. Plant Physiol. 158, 844-853.
125. Luo, J., Shen, G., Yan, J., He, C., and Zhang, H. (2006). AtCHIP functions as an E3 ubiquitin ligase of protein phosphatase 2A subunits and alters plant response to abscisic acid treatment. Plant J. 46, 649-657.
126. Lupas, A., Baumeister, W., and Hofmann, K. (1997). A repetitive sequence in subunits of the 26S proteasome and 20S cyclosome (anaphase-promoting complex). Trends Biochem. Sci. 22, 195-196.
127. Lyzenga, W.J., Booth, J.K., and Stone, S.L. (2012). The Arabidopsis RING-type E3 ligase XBAT32 mediates the proteasomal degradation of the ethylene biosynthetic enzyme, 1-aminocyclopropane- 1-carboxylate synthase 7. Plant J. 71, 23-34.
128. Marrocco, K., Zhou, Y., Bury, E., Dieterle, M., Funk, M., Genschik, P., Krenz, M., Stolpe, T., and Kretsch, T. (2006). Functional analysis of EID1, an F-box protein involved in phytochrome A-dependent light signal transduction. Plant J. 45, 423-438.
129. Marrocco, K., Criqui, M.C., Zervudacki, J., Schott, G., Eisler, H., Parnet, A., Dunoyer, P., and Genschik, P., (2012). APC/C-mediated degradation of dsRNA-binding protein 4 (DRB4) involved in RNA silencing. PLoS One. 7, e35173.
130. Mashiguchi, K., Sasaki, E., Shimada, Y., Nagae, M., Ueno, K., Nakano, T.,Yoneyama, K., Suzuki, Y., and Asami, T. (2009). Feedback-regulation of strigolactone biosynthetic genes and strigolactone-regulated genes in Arabidopsis. Biosci. Biotechnol. Biochem. 73, 2460-2465.
131. Mbengue, M., et al. (2010). The Medicago truncatula E3 ubiquitin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation. Plant Cell. 22, 3474-3488.
132. McGinnis, K.M., Thomas, S.G., Soule, J.D., Strader, L.C., Zale, J.M., Sun, T.P., and Steber, C.M. (2003). The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell. 15, 1120-1130.
133. Meng, X., Hua, Z., Sun, P., and Kao, T.H. (2011). The amino terminal F-box domain of Petunia inflata S-locus F-box protein is involved in the S-RNase-based self-incompatibility mechanism. AoB Plants. 2011, plr016.
134. Miao, Y., and Zentgraf, U. (2010). A HECT E3 ubiquitin ligase negatively regulates Arabidopsis leaf senescence through degradation of the transcription factor WRKY53. Plant J. 63, 179-188.
135. Mizoi, J., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2012). AP2/ ERF family transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta. 1819, 86-96.
136. Molinier, J., Lechner, E., Dumbliauskas, E., and Genschik, P. (2008). Regulation and role of Arabidopsis CUL4-DDB1A-DDB2 in maintaining genome integrity upon UV stress. PLoS Genet. 4, e1000093.
137. Murray, A. (1995). Cyclin ubiquitination: the destructive end of mitosis. Cell. 81, 149-152.
138. Nakamura, M., Toyota, M., Tasaka, M., and Morita, M.T. (2011). An Arabidopsis E3 ligase, SHOOT GRAVITROPISM9, modulates the interaction between statoliths and F-actin in gravity sensing. Plant Cell. 23, 1830-1848.
139. Nakazawa, Y., Hiraguri, A., Moriyama, H., and Fukuhara, T. (2007). The dsRNA-binding protein DRB4 interacts with the Dicer-like protein DCL4 in vivo and functions in the trans-acting siRNA pathway. Plant Mol. Biol. 63, 777-785.
140. Ning, Y., et al. (2011). The SINA E3 ligase OsDIS1 negatively regulates drought response in rice. Plant Physiol. Behav. 157, 242-255.
141. Ning, Y., Xie, Q., and Wang, G.L. (2011). OsDIS1-mediated stress response pathway in rice. Plant Signal. Behav. 6, 1684-1686.
142. Ohi, M.D., Vander Kooi, C.W., Rosenberg, J.A., Chazin, W.J., and Gould, K.L. (2003). Structural insights into the U-box, a domain associated with multi-ubiquitination. Nat. Struct. Biol. 10, 250-255.
143. Osterlund, M.T., Hardtke, C.S., Wei, N., and Deng, X.W. (2000). Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature. 405, 462-466.
144. Pan, J., Fujioka, S., Peng, J., Chen, J., Li, G., and Chen, R. (2009). The E3 ubiquitin ligase SCFTIR1/AFB and membrane sterols play key roles in auxin regulation of endocytosis, recycling, and plasma membrane accumulation of the auxin efflux transporter PIN2 in Arabidopsis thaliana. Plant Cell. 21, 568-580.
145. Park, G.G., Park, J.J., Yoon, J., Yu, S.N., and An, G. (2010). A RING finger E3 ligase gene, Oryza sativa Delayed Seed Germination 1 (OsDSG1), controls seed germination and stress responses in rice. Plant Mol. Biol. 74, 467-478.
146. Parry, G., Calderon-Villalobos, L.I., Prigge, M., Peret, B., Dharmasiri, S., Itoh, H., Lechner, E., Gray, W.M., Bennett, M., and Estelle, M. (2009). Complex regulation of the TIR1/AFB family of auxin receptors. Proc. Natl Acad. Sci. U S A. 106, 22540-22545.
147. Pavri, R., Zhu, B.,Li, G., Trojer, P., Mandal, , S., Shilatifard, A., and Reinberg, D. (2006). Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell. 125, 703-717.
148. Pazhouhandeh, M., Molinier, J., Berr, A., and Genschik, P. (2011). MSI4/FVE interacts with CUL4-DDB1 and a PRC2-like complex to control epigenetic regulation of flowering time in Arabidopsis. Proc. Natl Acad. Sci. U S A. 108, 3430-3435.
149. Perazza, D., Herzog, M., Hulskamp, M., Brown, S., Dorne, A.M., and Bonneville, J.M. (1999). Trichome cell growth in Arabidopsis thaliana can be derepressed by mutations in at least five genes. Genetics. 152, 461-476.
150. Pfleger, C.M., and Kirschner, M.W. (2000). The KEN box: an APC recognition signal distinct from the D box targeted by Cdh1. Genes Dev. 14, 655-665.
151. Pilot, G., Stransky, H., Bushey, D.F., Pratelli, R., Ludewig, U., Wingate, V.P., and Frommer, W.B. (2004). Overexpression of GLUTAMINE DUMPER1 leads to hypersecretion of glutamine from Hydathodes of Arabidopsis leaves. Plant Cell. 16, 1827-1840.
152. Pintard, L., et al. (2003). The BTB protein MEL-26 is a substratespecific adaptor of the CUL-3 ubiquitin-ligase. Nature. 425, 311-316.
153. Potuschak, T., Lechner, E.,Parmentier, Y., Yanagisawa,, S., Grava, S., Koncz, C., and Genschik, P. (2003). EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell. 115, 679-689.
154. Pratelli, R., Guerra, D.D., Yu, S., Wogulis, M., Kraft, E.,Frommer, W.B., Callis, J., and Pilot, G. (2012). The ubiquitin E3 ligase LOSS OF GDU2 is required for GLUTAMINE DUMPER1-induced amino acid secretion in Arabidopsis. Plant Physiol. 158, 1628-1642.
155. Puig, J., Pauluzzi, G., Guiderdoni, E., and Gantet, P. (2012). Regulation of shoot and root development through mutual signaling. Mol. Plant. 5, 974-983.
156. Qiao, H., Chang, K.N., Yazaki, J., and Ecker, J.R. (2009). Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis. Genes Dev. 23, 512-521.
157. Raab, S., Drechsel, G., Zarepou, M., Hartung, W., Koshiba, T., Bittner, F., and Hoth, S. (2009). Identification of a novel E3 ubiquitin ligase that is required for suppression of premature senescence in Arabidopsis. Plant J. 59, 39-51.
158. Rasmussen, A., et al. (2012). Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol. 158, 1976-1987.
159. Roberts, D., Pedmale, U.V., Morrow, J., Sachdev, S., Lechner, E., Tang, X., Zheng, N., Hannink, M., Genschik, P., and Liscum, E. (2011). Modulation of phototropic responsiveness in Arabidopsis through ubiquitination of phototropin 1 by the CUL3-RING E3 ubiquitin ligase CRL3(NPH3). Plant Cell. 23, 3627-3640.
160. Robson, F., Okamoto, H., Patrick, E., Harris, S.R., Wasternack, C., Brearley, C., and Turner, J.G. (2010). Jasmonate and phytochrome A signaling in Arabidopsis wound and shade responses are integrated through JAZ1 stability. Plant Cell. 22, 1143-1160.
161. Ruggeri, Z.M., and Ware, J. (1993). von Willebrand factor. FASEB J. 7, 308-316.
162. Rushton, D.L., et al. (2012). WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnol. J. 10, 2-11.
163. Sakai, T., Mochizuki, S., Haga, K., Uehara, Y., Suzuki, A., Harada, A., Wada, T., Ishiguro, S., and Okada, K. (2012). The wavy growth 3 E3 ligase family controls the gravitropic response in Arabidopsis roots. Plant J. 70, 303-314.
164. Salt, J.N., Yoshioka, K., Moeder, W., and Goring, D.R. (2011). Altered germination and subcellular localization patterns for PUB44/SAUL1 in response to stress and phytohormone treatments. PLoS One. 6, e21321.
165. Samuel, M.A., Mudgil, Y., Salt, J.N., Delmas, F., Ramachandran, S., Chilelli, A., and Goring, D.R. (2008). Interactions between the S-domain receptor kinases and AtPUB-ARM E3 ubiquitin ligases suggest a conserved signaling pathway in Arabidopsis. Plant Physiol. 147, 2084-2095.
166. Sawa, M., Nusinow, D.A., Kay, S.A., and Imaizumi, T. (2007). FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science. 318, 261-265.
167. Scheffner, M., Nuber, U., and Huibregtse, J.M. (1995). Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature. 373, 81-83.
168. Schmidt, M.W., McQuary, P.R., Wee, S., Hofmann, K., and Wolf, D.A. (2009). F-box-directed CRL complex assembly and regulation by the CSN and CAND1. Mol. Cell. 35, 586-597.
169. Schroeder, D.F., Gahrtz, M.,Maxwell, B.B., Cook, R.K., Kan, J.M., Alonso, J.M., Ecker, J.R., and Chory, J. (2002). De-etiolated 1 and damaged DNA binding protein 1 interact to regulate Arabidopsis photomorphogenesis. Curr. Biol. 12, 1462-1472.
170. Schulman, B.A. (2011). Twists and turns in ubiquitin-like protein conjugation cascades. Protein Sci. 20, 1941-1954.
171. Schulman, B.A., Carrano, A.C., Jeffrey, P.D., Bowen, Z., Kinnucan, E.R., Finnin, M.S., Elledge, S.J., Harper, J.W., Pagano, M., and Pavletich, N.P. (2000). Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex. Nature. 408, 381-386.
172. Schwarz, S.E., Rosa, J.L., and Scheffner, M. (1998). Characterization of human hect domain family members and their interaction with UbcH5 and UbcH7. J. Biol. Chem. 273, 12148-12154.
173. Seo, D.H., Ryu, M.Y., Jammes, F., Hwang, J.H., Turek, M., Kang, B.G., Kwak, J.M., and Kim, W.T. (2012a). Roles of four Arabidopsis U-box E3 ubiquitin ligases in negative regulation of ABA-mediated drought stress responses. Plant Physiol 160, 556-568.
174. Seo, Y.S., Choi, J.Y., Kim, S.J., Kim, E.Y., Shin, J.S., and Kim, W.T. (2012b). Constitutive expression of CaRma1H1, a hot pepper ER-localized RING E3 ubiquitin ligase, increases tolerance to drought and salt stresses in transgenic tomato plants. Plant Cell Rep 31, 1659-1665.
175. Serino, G., Su, H., Peng, Z., Tsuge,, T., Wei, N., Gu, H., and Deng, X.W. (2003). Characterization of the last subunit of the Arabidopsis COP9 signalosome: implications for the overall structure and origin of the complex. Plant Cell. 15, 719-731.
176. Sheard, L.B., et al. (2010). Jasmonate perception by inositolphosphate- potentiated COI1-JAZ co-receptor. Nature. 468, 400-405.
177. Shen, G., Adam, Z., and Zhang, H. (2007a). The E3 ligase AtCHIP ubiquitylates FtsH1, a component of the chloroplast FtsH protease, and affects protein degradation in chloroplasts. Plant J. 52, 309-321.
178. Shen, G., Yan, J., Pasapula, V., Luo, , J., He, C., Clarke, A.K., and Zhang, H. (2007b). The chloroplast protease subunit ClpP4 is a substrate of the E3 ligase AtCHIP and plays an important role in chloroplast function. Plant J. 49, 228-237.
179. Shen, H., Luong, P., and Huq, E. (2007c). The F-box protein MAX2 functions as a positive regulator of photomorphogenesis in Arabidopsis. Plant Physiol. 145, 1471-1483.
180. Song, Y.H., Smith, R.W., To, B.J., Millar, A.J., and Imaizumi, T. (2012). FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science. 336, 1045-1049.
181. Spoel, S.H., Mou, Z., Tada, Y., Spivey, N.W., Genschik, P., and Dong, X. (2009). Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell. 137, 860-872.
182. Stirnberg, P., Furner, I.J., and Ottoline Leyser, H.M. (2007). MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J. 50, 80-94.
183. Stogios, P.J., Downs, G.S., Jauhal, J.J., Nandra, S.K., and Prive, G.G. (2005). Sequence and structural analysis of BTB domain proteins. Genome Biol. 6, R82.
184. Stone, S.L., Anderson, E.M., Mullen, R.T., and Goring, D.R. (2003). ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell. 15, 885-898.
185. Stone, S.L., Hauksdottir, H., Troy, A., Herschleb, J., Kraft, E., and Callis, J. (2005). Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol. 137, 13-30.
186. Stuttmann, J., Parker, J.E., and Noel, L.D. (2009). COP9 signalosome- and 26S proteasome-dependent regulation of SCFTIR1 accumulation in Arabidopsis. J. Biol. Chem. 284, 7920-7930.
187. Tan, X., Calderon-Villalobos L.I., Sharon M., Zheng C., Robinson C.V., Estelle M., and Zheng N. (2007). Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature. 446, 640-645.
188. Tanaka, Y., Tanaka, N.,Saeki, Y., Tanaka, K., Murakami, M., Hirano,, T., Ishii, N., and Sugamura, K. (2008). c-Cbl-dependent monoubiquitination and lysosomal degradation of gp130. Mol. Cell. Biol. 28, 4805-4818.
189. Tang, Z., Li, B., Bharadwaj, R., Zhu, H., Ozkan, E., Hakala, K., Deisenhofer, J., and Yu, H. (2001). APC2 Cullin protein and APC11 RING protein comprise the minimal ubiquitin ligase module of the anaphase-promoting complex. Mol. Biol. Cell. 12, 3839-3851.
190. Thines, B., Katsir, L., Melotto, M., Niu, Y., Mandaokar, A., Liu, G., Nomura, K., He, S.Y., Howe, G.A., and Browse, J. (2007). JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature. 448, 661-665.
191. Thomann, A., Lechner, E., Hansen, M., Dumbliauskas, E., Parmentier, Y., Kieber, J., Scheres, B., and Genschik, P. (2009). Arabidopsis CULLIN3 genes regulate primary root growth and patterning by ethylene-dependent and -independent mechanisms. PLoS Genet. 5, e1000328.
192. Vogel, J.T., et al. (2010). SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J. 61, 300-311.
193. Wager, A., and Browse, J. (2012). Social network: JAZ protein interactions expand our knowledge of jasmonate signaling. Front Plant Sci. 3, 41.
194. Wang, Y., Hou, Y., Gu, H., Kang, RD., Chen, Z., Liu, J.,and Qu, J. (2012). The Arabidopsis APC4 subunit of the anaphase-promoting complex/cyclosome (APC/C) is critical for both female gametogenesis and embryogenesis. Plant J. 69, 227-240.
195. Weber, H., and Hellmann, H. (2009). Arabidopsis thaliana BTB/ POZ-MATH proteins interact with members of the ERF/AP2 transcription factor family. FEBS J. 276, 6624-6635.
196. Weber, H., Bernhardt, A., Dieterle, M., Hano, P., Mutlu, A., Estelle, M., Genschik, P., and Hellmann, H. (2005). Arabidopsis AtCUL3a and AtCUL3b form complexes with members of the BTB/POZ-MATH protein family. Plant Physiol. 137, 83-93.
197. Wee, S., Geyer, R.K., Toda, T., and Wolf, D.A. (2005). CSN facilitates cullin-RING ubiquitin ligase function by counteracting autocatalytic adapter instability. Nat. Cell. Biol. 7, 387-391.
198. Wiborg, J., O'Shea, C., and Skriver, K. (2008). Biochemical function of typical and variant Arabidopsis thaliana U-box E3 ubiquitin- protein ligases. Biochem. J. 413, 447-457.
199. Willemsen, V., Wolkenfelt, H., de Vrieze, G., Weisbeek, P., and Scheres, B. (1998). The HOBBIT gene is required for formation of the root meristem in the Arabidopsis embryo. Development. 125, 521-531.
200. Woo, H.R., Chung, K.M., Park, J.H., Oh, S.A., Ahn, T., Hong, S.H., Jang, S.K., and Nam, H.G. (2001). ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell. 13, 1779-1790.
201. Xia, Z., Liu, Q., Wu, J., and Ding, J. (2012). ZmRFP1, the putative ortholog of SDIR1, encodes a RING-H2 E3 ubiquitin ligase and responds to drought stress in an ABA-dependent manner in maize. Gene. 495, 146-153.
202. Xu, C., Wang, Y., Yu, Y., Duan, J., Liao, Z., Xiong, G., Meng, X., Liu, G., Qian, Q., and Li, J. (2012). Degradation of MONOCULM 1 by APC/C(TAD1) regulates rice tillering. Nat. Commun. 3, 750.
203. Yan, J., Wang, J., Li, Q., Hwang, J.R., Patterson, C., and Zhang, H. (2003). AtCHIP, a U-box-containing E3 ubiquitin ligase, plays a critical role in temperature stress tolerance in Arabidopsis. Plant Physiol. 132, 861-869.
204. Yan, J., et al. (2009). The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell. 21, 2220-2236.
205. Yang, J., et al. (2005). Light regulates COP1-mediated degradation of HFR1, a transcription factor essential for light signaling in Arabidopsis. Plant Cell. 17, 804-821.
206. Yano, K., et al. (2009). CERBERUS, a novel U-box protein containing WD-40 repeats, is required for formation of the infection thread and nodule development in the legume-Rhizobium symbiosis. Plant J. 60, 168-180.
207. Yoshida, H., Nagata, M., Saito, K., Wang, K.L., and Ecker, J.R. (2005). Arabidopsis ETO1 specifically interacts with and negatively regulates type 2 1-aminocyclopropane-1-carboxylate synthases. BMC Plant Biol. 5, 14.
208. Yuan, S., et al. (2012). A ubiquitin ligase of symbiosis receptor kinase involved in nodule organogenesis. Plant Physiol. 160, 106-117.
209. Zeng, L.R., Park, C.H., Venu, R.C., Gough, J., and Wang, G.L. (2008). Classification, expression pattern, and E3 ligase activity assay of rice U-box-containing proteins. Mol. Plant. 1, 800-815.
210. Zhang, W., Ito, H., Quint, M., Huang, H., Noel, L.D., and Gray, W.M. (2008a). Genetic analysis of CAND1-CUL1 interactions in Arabidopsis supports a role for CAND1-mediated cycling of the SCFTIR1 complex. Proc. Natl Acad. Sci. U S A. 105, 8470-8475.
211. Zhang, X., Chen, S., and Mou, Z. (2010a). Nuclear localization of NPR1 is required for regulation of salicylate tolerance, isochorismate synthase 1 expression and salicylate accumulation in Arabidopsis. J. Plant Physiol. 167, 144-148.
212. Zhang, Y., Feng, S.,Chen, F., Chen, H., Wang, J., McCall, C., Xiong, Y., and Deng, X.W. (2008b). Arabidopsis DDB1-CUL4 ASSOCIATED FACTOR1 forms a nuclear E3 ubiquitin ligase with DDB1 and CUL4 that is involved in multiple plant developmental processes. Plant Cell. 20, 1437-1455.
213. Zhang, Z., Roe, S.M., Diogon, M., Kong, E., El Alaoui, H., and Barford, D. (2010b). Molecular structure of the N-terminal domain of the APC/C subunit Cdc27 reveals a homo-dimeric tetratricopeptide repeat architecture. J. Mol. Biol. 397, 1316-1328.
214. Zheng, J., Yang, X., Harrell, J.M., Ryzhikov, S.,Shim, E.H., Lykke- Andersen, K.,Wei, N.,Sun, H.,Kobayashi, R., and Zhang, H. (2002a). CAND1 binds to unneddylated CUL1 and regulates the formation of SCF ubiquitin E3 ligase complex. Mol. Cell. 10, 1519-1526.
215. Zheng, N., et al. (2002b). Structure of the Cul1-Rbx1-Skp1-F box- Skp2 SCF ubiquitin ligase complex: N6east COP9/signalosome suppresses cullin activity through recruitment of the deubiquitylating enzyme Ubp12p. Mol. Cell. 11, 927-938.
216. Nature. 416, 703-709.
217. Zhou, C., Wee , S., Rhee, E., Naumann, M.,Dubiel, W., and Wolf, D.A. (2003). Fission yeast COP9/signalosome suppresses cullin activity through recruitment of the deubiquitylating enzyme Ubp12p. Mol. Cell. Cell. 11, 927-938.