Skip to main content

Examining Protein Stability and Its Relevance for Plant Growth and Development

  • Protocol
Plant Signal Transduction

Part of the book series: Methods in Molecular Biology ((MIMB,volume 479))

Abstract

Eukaryotes control many aspects of growth and development such as cell cycle progression and gene expression through the selective degradation of regulatory proteins by way of the 26S proteasome. Generally, proteasomal degradation requires the poly-ubiquitylation of degradation targets by El ubiquitin activating enzymes, E2 ubiquitin conjugating enzymes, and E3 ubiquitin ligases. Specificity is brought to the process by E3 ubiquitin ligases, which engage in direct interactions with the degradation substrate to bring it into the proximity of the E2 enzyme. The abundance of genes encoding E3 ligase subunits in plant genomes invites the hypothesis that protein degradation plays an important role in the control of many plant growth processes, and it is therefore not surprising that proteasomal degradation has already been implicated in several important response pathways. However, most of the genes with a predicted role in the ubiquitin-proteasome pathway still remain to be characterized and the identity of their degradation substrates needs to be revealed. In this chapter, we give an overview of the ubiquitin-proteasome system and the pathway proteins that have been examined in Arabidopsis to date. We review the methods required to identify and characterize the proteins that play a role in protein degradation or that are the target for proteasomal degradation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Hershko, A., and Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67,425–479.

    Article  PubMed  CAS  Google Scholar 

  2. Reinstein, E., and Ciechanover, A. (2006) Protein degradation and human diseases: the ubiquitin connection. Ann. Intern. Med. 145,676–684.

    Article  PubMed  Google Scholar 

  3. Bachmair, A., Novatchkova, M., Potuschak, T., and Eisenhaber, F. (2001) Ubiquitylation in plants: a post-genomic look at a posttranslational modification. Trends Plant Set. 6, 463–470.

    Article  CAS  Google Scholar 

  4. Schwechheimer, C., and Villalobos, L. I. (2004) Cullin-containing E3 ubiquitin ligases in plant development. Curr. Opin. Plant Biol. 7, 677–686.

    Article  PubMed  CAS  Google Scholar 

  5. Willems, A. R., Schwab, M., and Tyers, M. (2004) A hitchhiker’s guide to the cullin ubiquitin ligases: SCF and its kin. Biochim. Biophys. Acta 1695,133–170.

    Article  PubMed  CAS  Google Scholar 

  6. 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. USA 99,11519–11524.

    Article  PubMed  CAS  Google Scholar 

  7. Kuroda, H., Takahashi, N., Shimada, H., Seki, M., Shinozaki, K., and Matsui, M. (2002) Classification and expression analysis of Arabidopsis F-box-containing protein genes. Plant Cell Physiol. 43,1073–1085.

    Article  PubMed  CAS  Google Scholar 

  8. Hermand, D. (2006) F-box proteins: more than baits for the SCF> Cell Div. 1, 30.

    Google Scholar 

  9. Kepinski, S., and Leyser, O. (2004) Auxininduced SCF™ -AUX/IAAinteraction involves stable modification of the SCFTIR1 complex. Proc. Natl. Acad. Sci. USA 101, 12381– 12386.

    Article  PubMed  CAS  Google Scholar 

  10. Dharmasiri, N., Dharmasiri, S., and Estelle, M. (2005) The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445.

    Article  PubMed  CAS  Google Scholar 

  11. Kepinski, S., and Leyser, O. (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446–451.

    Article  PubMed  CAS  Google Scholar 

  12. Gray, W. M., Kepinski, S., Rouse, D., Leyser, O., and Estelle, M. (2001) Auxin regulates SCF(TIRl)-dependent degradation of AUX/IAA proteins. Nature 414, 271–276.

    Article  PubMed  CAS  Google Scholar 

  13. Ruegger, M., Dewey, E., Gray, W. M., Hobbie, L., Turner, J., and Estelle, M. (1998) The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast GRRlp. Genes Dev. 12, 198–207.

    Article  PubMed  CAS  Google Scholar 

  14. Guo, H., and Ecker, J. R. (2003) Plant responses to ethylene gas are mediated by SCF(EBFl/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115, 667–677.

    Article  PubMed  CAS  Google Scholar 

  15. 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.

    Article  PubMed  CAS  Google Scholar 

  16. 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. Set. USA 101, 6803–6808.

    Article  CAS  Google Scholar 

  17. 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 SLEEPT1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15, 1120–1130.

    Article  PubMed  CAS  Google Scholar 

  18. Strader, L. C., Ritchie, S., Soule, J. D., McGinnis, K. M., and Steber, C. M. (2004) Recessive-interfering mutations in the gibberellin signaling gene SLEEPT1 are rescued by overexpression of its homologue, SNEEZY. Proc. Natl. Acad. Sci. USA 101, 12771–12776.

    Article  PubMed  CAS  Google Scholar 

  19. 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.

    Article  PubMed  CAS  Google Scholar 

  20. Itoh, H., Matsuoka, M., and Steber, C. M. (2003) A role for the ubiquitin-26S-proteasome pathway in gibberellin signaling. Trends Plant Sci. 8, 492–497.

    Article  PubMed  CAS  Google Scholar 

  21. Fu, X., Richards, D. E., Fleck, B., Xie, D., Burton, N., and Harberd, N. P. (2004) The Arabidopsis mutant SLEEPYlgar2_1 protein promotes plant growth by increasing the affinity of the SCFSLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 16,1406–1418.

    Article  PubMed  CAS  Google Scholar 

  22. 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.

    Article  PubMed  CAS  Google Scholar 

  23. Dieterle, M., Zhou, Y. C., Schafer, E., Funk, M., and Kretsch, T. (2001) EID1, an F-box protein involved in phytochrome A-specific light signaling. Genes Dev. 15, 939–944.

    Article  PubMed  CAS  Google Scholar 

  24. del Pozo, J. C., Boniotti, M. B., and 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, 3057–3071.

    Article  PubMed  CAS  Google Scholar 

  25. 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.

    Article  PubMed  CAS  Google Scholar 

  26. 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.

    Article  PubMed  CAS  Google Scholar 

  27. 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.

    Article  PubMed  CAS  Google Scholar 

  28. Bernhardt,A.,Lechner,E.,Hano,P.,Schade, V., Dieterle, M., Anders, M., Dubin, M. J., Benvenuto, G., Bowler, C., Genschik, P., and Hellmann, H. (2006) CUL4 associates with DDB1 and DET1 and its downregulation affects diverse aspects of development in Arabidopsis thaliana. Plant J. 47, 591–603.

    Article  PubMed  CAS  Google Scholar 

  29. Chen, H., Shen, Y., Tang, X., Yu, L., Wang, J., Guo, L., Zhang, Y., Zhang, H., Feng, S., Strickland, E., Zheng, N., and Deng, X. W. (2006) Arabidopsis CULLIN4 forms an E3 ubiquitin ligase with RBX1 and the CDD complex in mediating light control of development. Plant Cell 18, 1991–2004.

    Article  PubMed  CAS  Google Scholar 

  30. Serralbo, O., Fülöp, K., Frugier, F., Parmentier, Y., Dong, A., Lecureuil, A., Guerche, P., Kondorosi, E., Scheres, B., and Genschik, P. (2003) The Arabidopsis anaphase-promoting complex or cyclosome: molecular and genetic characterization of the APC2 subunit. Plant Cell 15, 2370–2382.

    Article  PubMed  CAS  Google Scholar 

  31. Eloy, N. B., Coppens, F., Beemster, G. T., Hemerly, A. S., and Ferreira, P. C. (2006) The Arabidopsis anaphase promoting complex (APC): regulation through subunit availability in plant tissues. Cell Cycle 5, 1957–1965.

    Article  PubMed  CAS  Google Scholar 

  32. Fulop, K., Tarayre, S., Kelemen, Z., Horvath, G., Kevei, Z., Nikovics, K., Bako, L., Brown, S., Kondorosi, A., and Kondorosi, E. (2005) Arabidopsis anaphase-promoting complexes: multiple activators and wide range of substrates might keep APC perpetually busy. Cell Cycle A, 1084-1092.

    Google Scholar 

  33. Kwee, H. S., and Sundaresan, V. (2003) The NOMEG A gene required for female gametophyte development encodes the putative APC6/CDC16 component of the Anaphase Promoting Complex in Arabidopsis. Plant J. 36, 853–866.

    Article  PubMed  CAS  Google Scholar 

  34. Capron, A., Serralbo, O., Fulop, K., Frugier, F., Parmentier, Y., Dong, A., Lecureuil, A. , Guerche, P., Kondorosi, E., Scheres, B., and Genschik, P. (2003) The Arabidopsis anaphase-promoting complex or cyclosome: molecular and genetic characterization of the APC2 subunit. Plant Cell 15, 2370–2382.

    Article  PubMed  CAS  Google Scholar 

  35. 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.

    Article  PubMed  CAS  Google Scholar 

  36. 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.

    Article  PubMed  CAS  Google Scholar 

  37. 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.

    Article  PubMed  CAS  Google Scholar 

  38. El Refy, A., Perazza, D., Zekraoui, L., Valay, J. G., Bechtold, N., Brown, S., Hiilskamp, 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. Gen. 270, 403–414.

    Article  CAS  Google Scholar 

  39. 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.

    Article  PubMed  CAS  Google Scholar 

  40. 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.

    Article  PubMed  CAS  Google Scholar 

  41. Stone, S. L., Williams, L. A., Farmer, L. M., Vierstra, R. D., and Callis, J. (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 18,3415–3428.

    Article  PubMed  CAS  Google Scholar 

  42. 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.

    Article  PubMed  CAS  Google Scholar 

  43. Mladek, C., Guger, K, and Hauser, M. T. (2003) Identification and characterization of the ARIADNE gene family in Arabidopsis. A group of putative E3 ligases. Plant Physiol. 131, 27–40.

    Article  CAS  Google Scholar 

  44. Andersen, P., Kragelund, B. B., Olsen, A. N., Larsen, F. H., Chua, N. H., Poulsen, F. M., and Skriver, K. (2004) Structure and biochemical function of a prototypical Arabidopsis U-box domain. J. Biol. Chem. 279, 40053–40061.

    Article  PubMed  CAS  Google Scholar 

  45. 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.

    Article  PubMed  CAS  Google Scholar 

  46. Yang, P., Fu, H., Walker, J., Papa, C. M., Smalle, J., Ju, Y. M., and Vierstra, R D. (2004) Purification of the Arabidopsis 26 S proteasome: biochemical and molecular analyses revealed the presence of multiple isoforms. J. Biol. Chem. 279, 6401–6413.

    Article  PubMed  CAS  Google Scholar 

  47. Fu, H., Girod, P. A., Doelling, J. H., van Nocker, S., Hochstrasser, M., Finley, D., and Vierstra, R. D. (1999) Structure and functional analysis of the 26S proteasome subunits from plants. Mol. Biol. Rep. 26, 137–146.

    Article  PubMed  CAS  Google Scholar 

  48. Huang, W., Pi, L., Liang, W., Xu, B., Wang, H., Cai, R, and Huang, H. (2006) The proteolytic function of the Arabidopsis 26S proteasome is required for specifying leaf adaxial identity. Plant Cell 18, 2479–2492.

    Article  PubMed  CAS  Google Scholar 

  49. Jin, H., Li, S., and Villegas, A., Jr. (2006) Down-regulation of the 26S proteasome subunit RPN9 inhibits viral systemic transport and alters plant vascular development. Plant Physiol. 142, 651–661.

    Article  PubMed  CAS  Google Scholar 

  50. Brukhin, V., Gheyselinck, J., Gagliardini, V., Genschik, P., and Grossniklaus, U. (2005) The RPN1 subunit of the 26S proteasome in Arabidopsis is essential for embryogenesis. Plant Cell 17, 2723–2737.

    Article  PubMed  CAS  Google Scholar 

  51. Smalle, J., Kurepa, J., Yang, P., Emborg, T. J., Babiychuk, E., Kushnir, S., and Vierstra, R. D. (2003) The pleiotropic role of the 26S proteasome subunit RPN10 in Arabidopsis growth and development supports a substrate-specific function in abscisic acid signaling. Plant Cell 15, 965–980.

    Article  PubMed  CAS  Google Scholar 

  52. Smalle, J., Kurepa, J., Yang, P., Babiychuk, E. , Kushnir, S., Durski, A., and Vierstra, R. D. (2002) Cytokinin growth responses in Arabidopsis involve the 26S proteasome subunit RPN12. Plant Cell 14,17–32.

    Article  PubMed  CAS  Google Scholar 

  53. Ueda, M., Matsui, K, Ishiguro, S., Sano, R, Wada, T., Paponov, I., Palme, K, and Okada, K. (2004) The HALTED ROOT gene encoding the 26S proteasome subunit RPT2a is essential for the maintenance of Arabidopsis meristems. Development 131, 2101–2111.

    Article  PubMed  CAS  Google Scholar 

  54. Schwechheimer, C. (2004) The COP9 signalosome (CSN): an evolutionary conserved proteolysis regulator in eukaryotic development. Biochim Biophys Acta 1695, 45–54.

    Article  PubMed  CAS  Google Scholar 

  55. Kwok, S. F., Piekos, B., Misera, S., and Deng, X. -W. (1996) A complement of ten essential and pleiotropic Arabidopsis COP/ DET/FUS genes is necessary for repression of photomorphogenesis in darkness. Plant Physiol. 110, 731–742.

    Article  PubMed  CAS  Google Scholar 

  56. Wei, N., Chamovitz, D. A., and Deng, X. -W. (1994) Arabidopsis COP9 is a component of a novel signaling complex mediating light control of development. Cell 78, 117–124.

    Article  PubMed  CAS  Google Scholar 

  57. Chamovitz, D. A., and Deng, X. -W. (1995) The novel components of the Arabidopsis light signalling pathway may define a group of general developmental regulators shared by both animal and plant kingdoms. Cell 82, 353–354.

    Article  PubMed  CAS  Google Scholar 

  58. Chamovitz, D. A., Wei, N., Osterlund, M. T., von Arnim, A. G., Staub, J. M., Matsui, M., and Deng, X. -W. (1996) The COP9 complex, a novel multisubunit nuclear regulator involved in light control of a plant developmental switch. Cell 86, 115–121.

    Article  PubMed  CAS  Google Scholar 

  59. Schwechheimer, C., and Deng, X. -W. (2001) COP9 signalosome revisited: a novel mediator of protein degradation. Trends Cell Biol. 11, 420–426.

    Article  PubMed  CAS  Google Scholar 

  60. Dohmann, E. M., Kuhnle, C., and Schwechheimer, C. (2005) Loss of the CONSTITUTTVEPHOTOMORPHOGENIC9signalosome subunit 5 is sufficient to cause the cop/det/ fus mutant phenotype in Arabidopsis. Plant Cell 17,1967–1978.

    Article  PubMed  CAS  Google Scholar 

  61. Wang, X., Feng, S., Nakayama, N., Crosby, W. L., Irish, V., Deng, X. W., and Wei, N. (2003) The COP9 signalosome interacts with SCF UFO and participates in Arabidopsis flower development. Plant Cell 15, 1071–1082.

    Article  PubMed  CAS  Google Scholar 

  62. Feng, S.,Ma, L.,Wang,X.,Xie, D., Dinesh-Kumar, S. P., Wei, N., and Deng, X. W. (2003) The COP9 signalosome interacts physically with SCFCOI1 and modulates jasmonate responses. Plant Cell 15, 1083–1094.

    Article  PubMed  CAS  Google Scholar 

  63. Liu, Y., Schiff, M., Serino, G., Deng, X. W., and Dinesh-Kumar, S. P. (2002) Role of SCF ubiquitin-ligase and the COP9 signalosome in the N gene-mediated resistance response to Tobacco mosaic virus. Plant Cell 14,1483–1496.

    Article  PubMed  CAS  Google Scholar 

  64. Schwechheimer, C., Serino, G., Callis, J., Crosby, W. L., Lyapina, S., Deshaies, R. J., Gray, W. M., Estelle, M., and Deng, X. -W. (2001) Interactions of the COP9 signalosome with the E3 ubiquitin ligase SCFTIR1 in mediating auxin response. Science 292, 1379–1382.

    Article  PubMed  CAS  Google Scholar 

  65. Lyapina, S., Cope, G., Shevchenko, A., Serino, G., Zhou, C., Wolf, D. A., Wei, N., Shevchenko, A., and Deshaies, R. J. (2001) COP9 signalosome promotes cleavage of NEDD8-CUL1 conjugates. Science 292, 1382–1385.

    Article  PubMed  CAS  Google Scholar 

  66. Bornstein, G., Ganoth, D., and Hershko, A. (2006) Regulation of neddylation and deneddylation of cullinl in SCFSKP2 ubiquitin ligase by F-box protein and substrate. Proc. Natl. Acad. Sci. USA 103,11515–11520.

    Article  PubMed  CAS  Google Scholar 

  67. Wu, J. T., Lin, H. C., Hu, Y. C., and Chien, C. T. (2005) Neddylation and deneddylation regulate Cull and Cul3 protein accumulation. Nat. Cell Biol. 7, 1014–1020.

    Article  PubMed  CAS  Google Scholar 

  68. Pan, Z. Q., Kentsis, A., Dias, D. C., Yamoah, K, and Wu, K. (2004) Nedd8 on cullin: building an expressway to protein destruction. Oncogene 23,1985–1997.

    Article  PubMed  CAS  Google Scholar 

  69. Chiba, T., and Tanaka, K. (2004) Cullin- based ubiquitin ligase and its control by NEDD8--conjugating system. Curr. Protein Pept. Sci. 5,177–184.

    Article  PubMed  CAS  Google Scholar 

  70. 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.

    Article  PubMed  CAS  Google Scholar 

  71. Liu, J., Furukawa, M., Matsumoto, T., and Xiong, Y. (2002) NEDD8 modification of CUL1 dissociates pl20 (CAND1), an inhibitor of CUL1-SKP1 binding and SCF ligases. Mol. Cell 10,1511–1518.

    Article  PubMed  CAS  Google Scholar 

  72. Kawakami, T., Chiba, T., Suzuki, T., Iwai, K., Yamanaka, H., Minato, N., Suzuki, H., Shimbara, N., Hidaka, Y., Osaka, F., Omata, M., and Tanaka, K. (2001) NEDD8 recruits E2-ubiquitin to SCF E3 ligase. EMBO J. 20, 1–10.

    Article  Google Scholar 

  73. Podust, V. N., Brownell, J. E., Gladysheva, T. B., Luo, R. -S., Wang, C., Coggins, M. B. , Pierce, J. W., Lightcap, E. S., Chau, V. (2000) A Nedd8 conjugation pathway is essential for proteolytic targeting of p27Kpl by ubiquitination. Proc. Natl. Acad. Sci. USA. 97,4579–4584.

    Article  PubMed  CAS  Google Scholar 

  74. Osaka, F., Saeki, M., Katayama, S., Aida, N., Toh-e, A., Kominami, K., Toda, T., Suzuki, T., Chiba, T., Tanaka, K., and Kato, S. (2000) Covalent modifier NEDD8 is essential for SCF ubiquitin-ligase in fission yeast. EMBOJ. 19, 3475–3484.

    Article  CAS  Google Scholar 

  75. Schwechheimer, C., Serino, G., and Deng, X. W. (2002) Multiple ubiquitin ligase-mediated processes require COP9 signalosome and AXR1 function. Plant Cell 14, 2553–2563.

    Article  PubMed  CAS  Google Scholar 

  76. Criqui, M. C., Parmentier, Y., Derevier, A. , Shen, W. H., Dong, A., and Genschik, P. (2000) Cell cycle-dependent proteolysis and ectopic overexpression of cyclin B1 in tobacco BY2 cells. Plant J. 24, 763–773.

    Article  PubMed  CAS  Google Scholar 

  77. Planchais, S., Samland, A. K., and Murray, J. A. (2004) Differential stability of Arabidopsis D-type cyclins: CYCD3;1 is a highly unstable protein degraded by a proteasome-dependent mechanism. Plant J. 38, 616–625.

    Article  PubMed  CAS  Google Scholar 

  78. Zhang, X., Garreton, V., and Chua, N. H. (2005) The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev. 19, 1532–1543.

    Article  PubMed  CAS  Google Scholar 

  79. Willige, B. C., Ghosh, S., Nill, C., Zourelidou, M., Dohmann, E. M., Maier, A., and Schwechheimer, C. (2007) The DELLA Domain of GA INSENSITIVE Mediates the Interaction with the GA INSENSITIVE DWARF 1A Gibberellin Receptor of Arabidopsis. Plant Cell 19,1209–1220.

    Article  PubMed  CAS  Google Scholar 

  80. Shen, Y., Feng, S., Ma, L., Lin, R, Qu, L. J., Chen, Z., Wang, H., and Deng, X. W. (2005) Arabidopsis FHY1 protein stability is regulated by light via phytochrome A and 26S proteasome. Plant Physiol. 139, 1234–1243.

    Article  PubMed  CAS  Google Scholar 

  81. Shen, H., Moon, J., and Huq, E. (2005) PIF1 is regulated by light-mediated degradation through the ubiquitin-26S proteasome pathway to optimize photomorphogenesis of seedlings in Arabidopsis. Plant J. 44, 1023–1035.

    Article  PubMed  CAS  Google Scholar 

  82. Al-Sady, B., Ni, W., Kircher, S., Schafer, E. , and Quail, P. H. (2006) Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol. CelllZ, 439-446.

    Google Scholar 

  83. del Pozo, J. C., Diaz-Trivino, S., Cisneros, N., and Gutierrez, C. (2006) The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. Plant Cell 18, 2224–2235.

    Article  PubMed  CAS  Google Scholar 

  84. Zenser, N., Ellsmore, A., Leasure, C., and Callis, J. (2001) Auxin modulates the degradation rate of AUX/IAA proteins. Proc. Natl. Acad. Sci. USA9S, 11795–11800.

    Article  Google Scholar 

  85. Earley, K. W., Haag, J. R., Pontes, O., Opper, K., Juehne, T., Song, K., and Pikaard, C. S. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616–629.

    Article  PubMed  CAS  Google Scholar 

  86. Curtis, M. D., and Grossniklaus, U. (2003) A gateway cloning vector set for high- throughput functional analysis of genes in planta. Plant Physiol. 133,462–469.

    Article  PubMed  CAS  Google Scholar 

  87. Calderon-Villalobos, L. I., Kuhnle, C., Li, H. , Rosso, M., Weisshaar, B., and Schwechheimer, C. (2006) LucTrap vectors are tools to generate luciferase fusions for the quantification of transcript and protein abundance in vivo. Plant Physiol. 141, 3–14.

    Article  PubMed  CAS  Google Scholar 

  88. Zuo, J., Niu, Q. W., and Chua, N. H. (2000) Technical advance: An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 24, 265–273.

    Article  PubMed  CAS  Google Scholar 

  89. Aoyama, T., and Chua, N. H. (1997) A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11, 605–612.

    Article  PubMed  CAS  Google Scholar 

  90. de Ruijter, N. C. A., Verhees, J., van Leeuwen, W., and van der Krol, A. R (2003) Evaluation and comparison of the GUS, LUC and GFP reporter system for gene expression studies in plants. Plant Biol. 5,103–115.

    Article  Google Scholar 

  91. Haseloff, J., and Amos, B. (1995) GFP in plants. Trends Genet. 11, 328–329.

    Article  PubMed  CAS  Google Scholar 

  92. Shaner, N. C., Steinbach, P. A., and Tsien, R. Y. (2005) A guide to choosing fluorescent proteins. Nat. Methods 2, 905–909.

    Article  PubMed  CAS  Google Scholar 

  93. Millar, A. J., Short, S. R.,Chua,N. -H.,and Kay, S. A. (1992) A novel circadian phenotype based on firefly luciferase expression in transgenic plants. Plant Cell 4, 1075–1087.

    PubMed  CAS  Google Scholar 

  94. Holm, M., Ma, L., Qu, L. -J., and Deng, X. W. (2002) Two interacting bZIP proteins are direct targets of COP 1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev. 16, 1247–1259.

    Article  PubMed  CAS  Google Scholar 

  95. Reed, J. (2001) Roles and activities of AUX/IAA proteins in Arabidopsis. Trends Plant Sci. 6, 420–425.

    Article  PubMed  CAS  Google Scholar 

  96. Weijers, D., Benkova, E., Jager, K. E., Schlereth, A., Hamann, T., Kientz, M., Wilmoth, J. C., Reed, J. W., and Jurgens, G. (2005) Developmental specificity of auxin response by pairs of ARF and AUX/ IAA transcriptional regulators. EMBO J. 24, 1874–1885.

    Article  PubMed  CAS  Google Scholar 

  97. Overvoorde, P. J., Okushima, Y., Alonso, J. M., Chan, A., Chang, C., Ecker, J. R, Hughes, B., Liu, A., Onodera, C., Quach, H. , Smith, A., Yu, G., and Theologis, A. (2005) Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana. Plant Cell 17, 3282–3300.

    Article  PubMed  CAS  Google Scholar 

  98. Dharmasiri, N., Dharmasiri, S., Weijers, D. , Lechner, E., Yamada, M., Hobbie, L., Ehrismann, J. S., Jürgens, G., and Estelle, M. (2005) Plant development is regulated by a family of auxin receptor F-box proteins. Dev. Cell 9, 109–119.

    Article  PubMed  CAS  Google Scholar 

  99. Ramos, J. A., Zenser, N., Leyser, O., and Callis, J. (2001) Rapid degradation of AUXIN/INDOLEACETIC ACID proteins requires conserved amino acids of domain II and is proteasome dependent. Plant Cell 13, 2349–2360.

    PubMed  CAS  Google Scholar 

  100. Zenser, N., Dreher, K. A., Edwards, S. R, and Callis, J. (2003) Acceleration of AUX/ IAA proteolysis is specific for auxin and independent of AXR1. Plant J. 35, 285–294.

    Article  PubMed  CAS  Google Scholar 

  101. Peng, J., Carol, P., Richards, D. E., King, K. E. , Cowling, R. J., Murphy, G. P., and Harberd, N. P. (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev. 11, 3194–3205.

    Article  PubMed  CAS  Google Scholar 

  102. Griffiths, J., Murase, K., Rieu, I., Zentella, R, Zhang, Z. L., Powers, S. J., Gong, F., Phillips, A. L., Hedden, P., Sun, T. P., and Thomas, S. G. (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18, 3399–3414.

    Article  PubMed  CAS  Google Scholar 

  103. Kawasaki, T., Nam, J., Boyes, D. C., Holt, B. F. , 3rd, Hubert, D. A., Wiig, A., and Dangl, J. L. (2005) A duplicated pair of Arabidopsis RING-finger E3 ligases contribute to the RPM1- and RPS2-mediated hypersensitive response. Plant J. 44, 258–270.

    Article  PubMed  CAS  Google Scholar 

  104. Hardtke, C. S., Okamoto, H., Stoop-Myer, C. , and Deng, X. W. (2002) Biochemical evidence for ubiquitin ligase activity of the Arabidopsis COP1 interacting protein 8 (CIP8). Plant J. 30, 385–394.

    Article  PubMed  CAS  Google Scholar 

  105. Xie, Q., Guo, H. -S., Dallman, G., Fang, S., Weissman, A. M., and Chua, N. -H. (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419,167–170.

    Article  PubMed  CAS  Google Scholar 

  106. Dong, C. H., Agarwal, M., Zhang, Y., Xie, Q., and Zhu, J. K. (2006) The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE 1. Proc. Natl. Acad. Sci. USA 103, 8281–8286.

    Article  PubMed  CAS  Google Scholar 

  107. Disch, S., Anastasiou, E., Sharma, V. K., Laux, T., Fletcher, J. C., and Lenhard, M. (2006) The E3 ubiquitin ligase BIG BROTHER controls Arabidopsis organ size in a dosage-dependent manner. Curr. Biol. 16, 272–279.

    Article  PubMed  CAS  Google Scholar 

  108. Shen, W. H., Parmentier, Y., Hellmann, H., Lechner, E., Dong, A., Masson, J., Granier, F. , Lepiniec, L., Estelle, M., and Genschik, P. (2002) Null mutation of AtCULl causes arrest in early embryogenesis in Arabidopsis. Mol. Biol. Cell 13, 1916–1928.

    Article  PubMed  CAS  Google Scholar 

  109. Hellmann, H., Hobbie, L., Chapman, A., Dharmasiri, S., Dharmasiri, N., del Pozo, C. , Reinhardt, D., and Estelle, M. (2003) Arabidopsis AXR6 encodes CUL1 implicating SCF E3 ligases in auxin regulation of embryogenesis. EMBO J. 22, 3314–3325.

    Article  PubMed  CAS  Google Scholar 

  110. Quint, M., Ito, H., Zhang, W., and Gray, W. M. (2005) Characterization of a novel temperature-sensitive allele of the CUL1/ AXR6 subunit of SCF ubiquitin-ligases. Plant J. 43, 371–383.

    Article  PubMed  CAS  Google Scholar 

  111. Hobbie, L., McGovern, M., Hurwitz, L. R, Pierro, A., Liu, N. Y., Bandyopadhyay, A., and Estselle, M. (2000) The axr6mutants of Arabidopsis thaliana define a gene involved in auxin response and early development. Development 127, 23–32.

    PubMed  CAS  Google Scholar 

  112. Moon, J., Zhao,Y., Dai, X., Zhang,W., Gray, W. M., Huq, E., and Estelle, M. (2007) A new cullinl mutant has altered responses to hormones and light in Arabidopsis. Plant Physiol. 143, 684–696.

    Article  PubMed  CAS  Google Scholar 

  113. Ren, C., Pan, J., Peng, W., Genschik, P., Hobbie, L., Hellmann, H., Estelle, M., Gao, B. , Peng, J., Sun, C., and Xie, D. (2005) Point mutations in Arabidopsis CTJL- LIN1 reveal its essential role in jasmonate response. Plant J. 42, 514–524.

    Article  PubMed  CAS  Google Scholar 

  114. Ni, W., Xie, D., Hobbie, L., Feng, B., Zhao, D. , Akkara, J., and Ma, H. (2004) Regulation of flower development in Arabidopsis by SCF complexes. Plant Physiol. 134, 1574– 1585.

    Article  PubMed  CAS  Google Scholar 

  115. Thomann, A., Brukhin, V., Dieterle, M., Gheyeselinck, J., Vantard, M., Grossniklaus, U., and Genschik, P. (2005) Arabidopsis CUL3A and CUL3B genes are essential for normal embryogenesis. Plant J. 43, 437–448.

    Article  PubMed  CAS  Google Scholar 

  116. Lechner, E., Xie, D., Grava, S., Pigaglio, E., Planchais, S., Murray, J. A., Parmentier, Y., Mutterer, J., Dubreucq, B., Shen, W. H., and Genschik, P. (2002) The AtRBXl protein is part of plant SCF complexes, and its down-regulation causes severe growth and developmental defects. J. Biol. Chem. 277, 50069–50080.

    Article  PubMed  CAS  Google Scholar 

  117. 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.

    Article  PubMed  CAS  Google Scholar 

  118. Liu, F., Ni, W., Griffith, M. E., Huang, Z., Chang, C., Peng, W., Ma, H., and Xie, D. (2004) The ASK1 and ASK2 genes are essential for Arabidopsis early development. Plant Cell 16, 5–20.

    Article  PubMed  CAS  Google Scholar 

  119. Yang, M., Hu, Y., Lodhi, M., McCombie, W. R, and Ma, H. (1999) The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation. Proc. Natl. Acad. Sci. USA 96, 11416–11421.

    Article  PubMed  CAS  Google Scholar 

  120. Zhao, D., Yu, Q., Chen, M., and Ma, H. (2001) The ASK1 gene regulates B function gene expression in cooperation with UFO and LEAFY in Arabidopsis. Development 128,2735–2746.

    PubMed  CAS  Google Scholar 

  121. Walsh, T. A., Neal, R, Merlo, A. O., Honma, M., Hicks, G. R, Wolff, K., Matsumura, W., and Davies, J. P. (2006) Mutations in an auxin receptor homolog AFB5 and in SGTlb confer resistance to synthetic picolinate auxins and not to 2,4-dichlorophenoxyacetic acid or indole-3-acetic acid in Arabidopsis. Plant Physiol. 142, 542–552.

    Article  PubMed  CAS  Google Scholar 

  122. Gray, W. M., Muskett, P. R, Chuang, H. W., and Parker, J. E. (2003) Arabidopsis SGTlb is required for SCF(TIRl)-mediated auxin response. Plant Cell 15, 1310–1319.

    Article  PubMed  CAS  Google Scholar 

  123. Austin, M. J., Muskett, P. R, Kahn, K, Feys, B. F., Jones, J. D. G., and Parker, J. E. (2002) Regulatory role of SGT1 in early R gene-mediated plant defenses. Science 295, 2077–2080.

    Article  PubMed  CAS  Google Scholar 

  124. Coates, J. C., Laplaze, L., and Haseloff, J. (2006) Armadillo-related proteins promote lateral root development in Arabidopsis. Proc. Natl. Acad. Sci. USA 103,1621–1626.

    Article  PubMed  CAS  Google Scholar 

  125. Kim, S., Choi, H. I., Ryu, H. J., Park, J. H. , Kim, M. D., and Kim, S. Y. (2004) ARIA, an Arabidopsis arm repeat protein interacting with a transcriptional regulator of abscisic acid-responsive gene expression, is a novel abscisic acid signaling component. Plant Physiol. 136, 3639–3648.

    Article  PubMed  CAS  Google Scholar 

  126. Ha, C. M., Jun, J. H., Nam, H. G., and Fletcher, J. C. (2004) BLADE-ON-PETIOLE1 encodes a BTB/POZ domain protein required for leaf morphogenesis in Arabidopsis thaliana. Plant Cell Physiol 45, 1361–1370.

    Article  PubMed  CAS  Google Scholar 

  127. Dong, L., Wang, L., Zhang, Y., Zhang, Y., Deng, X., and Xue, Y. (2006) An auxininducible F-box protein CEGENDUO negatively regulates auxin-mediated lateral root formation in Arabidopsis. Plant Mol. Biol. 60, 599–615.

    Article  PubMed  CAS  Google Scholar 

  128. Seo, H. S., Watanabe, E., Tokutomi, S., Nagatani, A., and Chua, N. H. (2004) Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes Dev. 18, 617–622.

    Article  PubMed  CAS  Google Scholar 

  129. Xu, L., Liu, F., Lechner, E., Genschik, P., Crosby, W. L., Ma, H., Peng, W., Huang, D. , and Xie, D. (2002) The SCF(COIl) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14, 1919–1935.

    Article  PubMed  CAS  Google Scholar 

  130. Mayer, R, Raventos, D., and Chua, N. -H. (1996) detl, copl, and cop9 mutations cause inappropriate expression of several gene sets. Plant CellS, 1951-1959.

    Google Scholar 

  131. Pepper, A., Delaney, T., Wahsburn, T., Poole, D., and Chory, J. (1994) DET1, a negative regulator of light-mediated development and gene expression in Arabidopsis, encodes a novel nuclear-localized protein. Cell 78, 109–116.

    Article  PubMed  CAS  Google Scholar 

  132. Wang, K. L. -C., Yoshida, H., Lurin, C., and Ecker, J. R. (2004) Regulation of ethylene gas biosynthesis by the Arabidopsis ETOl protein. Nature 428, 945–950.

    Article  PubMed  CAS  Google Scholar 

  133. Calderon-Villalobos, L. I., Nill, C., Marrocco, K, Kretsch, T., and Schwechheimer, C. (2007) The evolutionarily conserved Arabidopsis thaliana F-box protein AtFBP7 is required for efficient translation during temperature stress. Gene 392, 106–116.

    Article  PubMed  CAS  Google Scholar 

  134. Nelson, D. C., Lasswell, J., Rogg, L. E., Cohen, M. A., and Bartel, B. (2000) FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101, 331–340.

    Article  PubMed  CAS  Google Scholar 

  135. 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.

    Article  PubMed  CAS  Google Scholar 

  136. Imaizumi, T., Tran, H. G., Swartz, T. E., Briggs, W. R, and Kay, S. A. (2003) FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis. Nature 426, 302–306.

    Article  PubMed  CAS  Google Scholar 

  137. Fleury, D., Himanen, K., Cnops, G., Nelissen, H., Boccardi, T. M., Maere, S., Beemster, G. T., Neyt, P., Anami, S., Robles, R, Micol, J. L., Inze, D., and Van Lijsebettens, M. (2007) The Arabidopsis thaliana homolog of yeast BRE1 has a function in cell cycle regulation during early leaf and root growth. Plant Cell 19, 417–432.

    Article  PubMed  CAS  Google Scholar 

  138. Lee, H., Xiong, L., Gong, Z., Ishitani, M., Stevenson, B., and Zhu, J. K. (2001) The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold- regulated nucleo-cytoplasmic partitioning. Genes Dev. 15,912–924.

    Google Scholar 

  139. Schultz, T. F., Kiyosue, T., Yanovsky, M., Wada, M., and Kay, S. A. (2001) A role for LKP2 in the circadian clock of Arabidopsis. Plant Cell 13, 2659–2670.

    PubMed  CAS  Google Scholar 

  140. Rochon, A., Boyle, R, Wignes, T., Fobert, R R, and Despres, C. (2006) The coactivator function of Arabidopsis NPR1 requires the core of its BTB/POZ domain and the oxidation of C-terminal cysteines. Plant Cell 18,3670–3685.

    Article  PubMed  CAS  Google Scholar 

  141. 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.

    Article  PubMed  CAS  Google Scholar 

  142. Stirnberg, P., van De Sande, K, and Leyser, H. M. (2002) MAXI and MAX2 control shoot lateral branching in Arabidopsis. Development 129,1131–1141.

    PubMed  CAS  Google Scholar 

  143. 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.

    PubMed  CAS  Google Scholar 

  144. Potuschak, T., Stary, S., Schlögelhofer, P., Becker, F., Nehjinskaia, V., and Bachmair, A. (1998) PRT1 of Arabidopsis thaliana encodes a component of the plant N-end rule pathway. Proc. Natl. Acad. Sci. USA 95, 7904–7908.

    Article  PubMed  CAS  Google Scholar 

  145. Kim, H. S., and Delaney, T. P. (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, 1469–1482.

    Article  PubMed  CAS  Google Scholar 

  146. Laubinger, S., Marchal, V., Le Gourrierec, J., Wenkel, S., Adrian, J., Jang, S., Kulajta, C., Braun, H., Coupland, G., and Hoecker, U. (2006) Arabidopsis SPA proteins regulate photoperiodic flowering and interact with the floral inducer CONSTANS to regulate its stability. Development 133,3213–3222.

    Article  PubMed  CAS  Google Scholar 

  147. Yang, J., Lin, R, Hoecker, U., Liu, B., Xu, L., and Wang, H. (2005) Repression of light signaling by Arabidopsis SPA1 involves post-translational regulation of HFR1 protein accumulation. Plant J. 43, 131–141.

    Article  PubMed  CAS  Google Scholar 

  148. Hoecker, U., Tepperman, J. M., and Quail, P. H. (1999) SPA1, a WD-repeat protein specific to phytochrome A signal transduction. Science 284, 496–499.

    Article  PubMed  CAS  Google Scholar 

  149. 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.

    Article  PubMed  CAS  Google Scholar 

  150. Lai, C. P., Lee, C. L., Chen, P. H., Wu, S. H., Yang, C. C., and Shaw, J. F. (2004) Molecular analyses of the Arabidopsis TUBBY-like protein gene family. Plant Physiol. 134, 1586–1597.

    Article  PubMed  CAS  Google Scholar 

  151. Samach, A., Klenz, J. E., Kohalmi, S. E., Risseeuw, E., Haughn, G. W., and Crosby, W. L. (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, 433–445.

    Article  PubMed  CAS  Google Scholar 

  152. Schwager, K. M., Calderon-Villalobos, L. I., Dohmann, E. M., Willige, B. C., Knierer, S., Nill, C., and Schwechheimer, C. (2007) Characterization of the VIER F-BOX PROTEINE genes from Arabidopsis reveals their importance for plant growth and development. Plant Cell 19,1163–1178.

    Article  PubMed  CAS  Google Scholar 

  153. Nodzon, L. A., Xu, W. H., Wang, Y., Pi, L. Y., Chakrabarty, P. K, and Song, W. Y. (2004) The ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis. Plant J. 40, 996–1006.

    Article  PubMed  CAS  Google Scholar 

  154. Ko, J. H., Yang, S. H., and Han, K. H. (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J. 47, 343–355.

    Article  PubMed  CAS  Google Scholar 

  155. Somers, D. E., Schultz, T. F., Milnamow, M., and Kay, S. A. (2000) ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 101, 319–329.

    Article  PubMed  CAS  Google Scholar 

  156. del Pozo, J. C., Timpte, C., Tan, S., Callis, J., and Estelle, M. (1998) The ubiquitin- related protein RUB1 and auxin response in Arabidopsis. Science 280,1760–1763.

    Article  PubMed  CAS  Google Scholar 

  157. del Pozo, J. L., and Estelle, M. (1999) The Arabidopsis cullin AtCULl is modified by the ubiquitin-related protein RUB1. Proc. Natl. Acad. Scie. USA96,15342–15347.

    Article  Google Scholar 

  158. Woodward, A. W., Ratzel, S. E., Woodward, E. E., Shamoo, Y., and Bartel, B. (2007) Mutation of El-CONJUGATING ENZYME-RELATED 1 decreases RUB conjugation and alters auxin response and development. Plant Physiol. 144, 976–987.

    Article  PubMed  CAS  Google Scholar 

  159. 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.

    Article  PubMed  CAS  Google Scholar 

  160. Alonso-Peral, M. M., Candela, H., del Pozo, J. C., Martinez-Laborda, A., Ponce, M. R, and Micol, J. L. (2006) The HVE/CAND1 gene is required for the early patterning of leaf venation in Arabidopsis. Development 133,3755–3766.

    Article  PubMed  CAS  Google Scholar 

  161. Wang, X., Kang, D., Feng, S., Serino, G., Schwechheimer, C., and Wei, N. (2002) CSN1 N-terminal-dependent activity is required for Arabidopsis development but not for Rubl/Nedd8 deconjugation of cullins: A structure-function study of CSN1 subunit of COP9 signalosome. Mol. Biol. Cell 13, 646–655.

    Article  PubMed  CAS  Google Scholar 

  162. 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.

    Article  PubMed  CAS  Google Scholar 

  163. Peng, Z., Serino, G., and Deng, X. -W. (2001) A role of Arabidopsis COP9 signalosome in multifaceted developmental processes revealed by the characterization of its subunit 3. Development 128, 4277–4288.

    PubMed  CAS  Google Scholar 

  164. Serino, G., Tsuge, T., Kwok, S., Matsui, M., Wei, N., and Deng, X. -W. (1999) Arabidopsis cop8 and fus4 muations define the same gene that encodes subunit 4 of the COP9 signalosome. Plant Cell 11,1967–1979.

    PubMed  CAS  Google Scholar 

  165. Gusmaroli, G., Feng, S., and Deng, X. W. (2004) The Arabidopsis CSN5A and CSN5B subunits are present in distinct COP9 signalosome complexes, and mutations in their JAMM domains exhibit differential dominant negative effects on development. Plant Cell 16, 2984–3001.

    Article  PubMed  CAS  Google Scholar 

  166. 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.

    Article  PubMed  CAS  Google Scholar 

  167. Peng, Z., Serino, G., and Deng, X. -W. (2001) Molecular characterization of subunit 6 of the COP9 signalosome and its role in multifaceted development processes in Arabidopsis. Plant Cell 13, 2393–2407.

    PubMed  CAS  Google Scholar 

  168. Karniol, B., Malec, P., and Chamovitz, D. A. (1999) Arabidopsis FUSCA5 encodes a novel phosphoprotein that is a component of the COP9 complex. Plant Cell 11, 839–848.

    PubMed  CAS  Google Scholar 

  169. Wei, N., and Deng, X. -W. (1992) COP9. A new genetic locus involved in light-regulated development and gene expression in Arabidopsis. Plant Cell 4, 1507–1518.

    CAS  Google Scholar 

  170. Suzuki, G., Yanagawa, Y., Kwok, S., Matsui, M., and Deng, X. W. (2002) Arabidopsis COP 10 is an ubiquitin-conjugating enzyme variant that acts together with COP1 and the COP9 signalosome in repressing photomorphogenesis. Genes Dev. 16, 554–559.

    Article  PubMed  CAS  Google Scholar 

  171. Yanagawa, Y., Sullivan, J. A., Komatsu, S., Gusmaroli, G., Suzuki, G., Yin, J., Ishibashi, T., Saijo, Y., Rubio, V., Kimura, S., Wang, J., and Deng, X. W. (2004) Arabidopsis COP 10 forms a complex with DDB1 and DET1 in vivo and enhances the activity of ubiquitin conjugating enzymes. Genes Dev. 18,2172–2181.

    Article  PubMed  CAS  Google Scholar 

  172. Vogel, J. P., Schuerman, P., Woeste, K, Brandstatter, I., and Kieber, J. J. (1998) Isolation and characterization of Arabidopsis mutants defective in the induction of ethylene biosynthesis by cytokinin. Genetics 149, 417–427.

    PubMed  CAS  Google Scholar 

  173. Perales, M., Portoles, S., and Mas, P. (2006) The proteasome-dependent degradation of CKB4 is regulated by the Arabidopsis biological clock. Plant J. 46, 849–860.

    Article  PubMed  CAS  Google Scholar 

  174. 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.

    Article  PubMed  CAS  Google Scholar 

  175. Kim, W. Y., Geng, R, and Somers, D. E. (2003) Circadian phase-specific degradation of the F-box protein ZTL is mediated by the proteasome. Proc. Natl. Acad. Sci. USA 100,4933–4938.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Humana Press, a part of Springer Science+Business Media, LLC

About this protocol

Cite this protocol

Schwechheimer, C., Willige, B., Zourelidou, M., Dohmann, E. (2009). Examining Protein Stability and Its Relevance for Plant Growth and Development. In: Pfannschmidt, T. (eds) Plant Signal Transduction. Methods in Molecular Biology, vol 479. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-59745-289-2_10

Download citation

  • DOI: https://doi.org/10.1007/978-1-59745-289-2_10

  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-58829-943-7

  • Online ISBN: 978-1-59745-289-2

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics