The Arabidopsis RING-type E3 ligase XBAT32 mediates the proteasomal degradation of the ethylene biosynthetic enzyme, 1-aminocyclopropane-1- carboxylate synthase 7

Plant Journal

Volumn 71, Issue 1, 2012, Pages 23-34

  Lyzenga, Wendy J ^a   Booth, Judith K ^a   Stone, Sophia L ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

ACC synthase; Arabidopsis; ethylene; proteasomal degradation; RING type E3 ligase; ubiquitination

Indexed keywords

ACC-SYNTHASE; ARABIDOPSIS; E3 LIGASE; PROTEASOMAL DEGRADATION; UBIQUITINATION;

BIOSYNTHESIS; ENZYMES; ETHYLENE; PROTEINS;

DEGRADATION;

1 AMINOCYCLOPROPANECARBOXYLATE SYNTHASE; 1-AMINOCYCLOPROPANECARBOXYLATE SYNTHASE; ARABIDOPSIS PROTEIN; ATP DEPENDENT 26S PROTEASE; LYASE; PROTEASOME; UBIQUITIN PROTEIN LIGASE; XBAT32 PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; LYASES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITIN-PROTEIN LIGASES;

ARABIDOPSIS;

EID: 84862509597     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04965.x     Document Type: Article

References (55)

1. Abramoff, M.D., Magalhaes, P., and, Ram, S.J., (2004) Image processing with ImageJ. Biophoton Int. 11, 36-43.
2. Alonso, J.M., Stepanova, A.N., Leisse, T.J., et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657. (Pubitemid 36927950)
3. An, F., Zhao, Q., Ji, Y., 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.
4. Argueso, C.T., Hansen, M., and, Kieber, J.J., (2007) Regulation of ethylene biosynthesis. J. Plant Growth Regul. 26, 92-105. (Pubitemid 47165740)
5. Benkirane, M., Sardet, C., and, Coux, O., (2010) Lessons from interconnected ubiquitylation and acetylation of p53: think metastable networks. Biochem. Soc. Trans. 38, 98-103.
6. 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. (Pubitemid 46941675)
7. Bork, P., (1993) Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally? Proteins, 17, 363-374.
8. Bostick, M., Lochhead, S.R., Honda, A., Palmer, S., and, Callis, J., (2004) Related to ubiquitin 1 and 2 are redundant and essential and regulate vegetative growth, auxin signaling, and ethylene production in Arabidopsis. Plant Cell, 16, 2418-2432. (Pubitemid 39247082)
9. Chae, H.S., and, Kieber, J.J., (2005) Eto Brute? Role of ACS turnover in regulating ethylene biosynthesis Trends Plant Sci. 10, 291-296. (Pubitemid 40793515)
10. Chae, H.S., Faure, F., and, Kieber, J.J., (2003) The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell, 15, 545-559. (Pubitemid 36230004)
11. Chang, I.F., Curran, A., Woolsey, R., Quilici, D., Cushman, J.C., Mittler, R., Harmon, A., and, Harper, J.F., (2009) Proteomic profiling of tandem affinity purified 14-3-3 protein complexes in Arabidopsis thaliana. Proteomics, 9, 2967-2985.
12. 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.
13. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
14. De Smet, I., Tetsumura, T., De Rybel, B., et al. (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development, 134, 681-690. (Pubitemid 46437910)
15. Dong, H., Zhen, Z., Peng, J., Chang, L., Gong, Q., and, Wang, N.N., (2011) Loss of ACS7 confers abiotic stress tolerance by modulating ABA sensitivity and accumulation in Arabidopsis. J. Exp. Bot. 62, 4875-4887.
16. Dubrovsky, J.G., Sauer, M., Napsucialy-Mendivil, S., Ivanchenko, M.G., Friml, J., Shishkova, S., Celenza, J., and, Benková, E., (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc. Natl Acad. Sci. USA, 105, 8790-8794. (Pubitemid 351987758)
17. 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. (Pubitemid 43373712)
18. Freemont, P.S., (1993) The RING finger. A novel protein sequence motif related to the zinc finger. Ann. NY Acad. Sci. 684, 174-192. (Pubitemid 23218950)
19. Han, L., Li, G.J., Yang, K.Y., Mao, G., Wang, R., Liu, Y., and, Zhang, S., (2010) Mitogen-activated protein kinase 3 and 6 regulate Botrytis cinerea-induced ethylene production in Arabidopsis. Plant J. 64, 114-1127.
20. Joo, S., Liu, Y., Lueth, A., and, Zhang, S., (2008) MAPK phosphorylation-induced stabilization of ACS6 protein is mediated by the non-catalytic C-terminal domain, which also contains the cis-determinant for rapid degradation by the 26S proteasome pathway. Plant J. 54, 129-140. (Pubitemid 351406020)
21. Kamiyoshihara, Y., Iwata, M., Fukaya, T., Tatsuki, M., and, Mori, H., (2010) Turnover of LeACS2, a wound-inducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation. Plant J. 64, 140-150.
22. Kieber, J.J., Rothenberg, M., Roman, G., Feldmann, K.A., and, Ecker, J.R., (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell, 72, 427-441. (Pubitemid 23059412)
23. Kosarev, P., Mayer, K.F., and, Hardtke, C.S., (2002) Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome. Genome Biol. 3, RESEARCH0016.1-RESEARCH0016.12.
24. Le, J., Vandenbussche, F., Van Der Straeten, D., and, Verbelen, J.P., (2001) In the early response of Arabidopsis roots to ethylene, cell elongation is up and down regulated and uncoupled from differentiation. Plant Physiol. 125, 519-522. (Pubitemid 32169858)
25. Lee, J.H., Yoon, H.J., Terzaghi, W., Martinez, C., Dai, M., Li, J., Byun, M.O., and, Deng, X.W., (2010) DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell, 22, 1716-1732.
26. Lehman, A., Black, R., and, Ecker, J.R., (1996) HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell, 85, 183-194.
27. Lewis, D.R., Negi, S., Sukumar, P., and, Muday, G.K., (2011) Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development, 138, 3485-3495.
28. Liu, H., and, Stone, S.L., (2010) Abscisic acid increases Arabidopsis ABI5 transcription factor levels by promoting KEG E3 ligase self-ubiquitination and proteasomal degradation. Plant Cell, 22, 2630-2641.
29. Liu, Y., and, Zhang, S., (2004) Phosphorylation of ACC synthase by MPK6, a stress-responsive MAPK, induces ethylene biosynthesis in Arabidopsis. Plant Cell, 16, 3386-3399.
30. Lorick, K.L., Jensen, J.P., Fang, S., Ong, A.M., Hatakeyama, S., and, Weissman, A.M., (1999) RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc. Natl Acad. Sci. USA, 96, 11364-11369. (Pubitemid 29487386)
31. Masucci, J.D., and, Schiefelbein, J.W., (1994) The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin- and ethylene-associated process. Plant Physiol. 106, 1335-1346. (Pubitemid 24986558)
32. Negi, S., Ivanchenko, M.G., and, Muday, G.K., (2008) Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J. 55, 175-187.
33. 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. (Pubitemid 40047637)
34. Péret, B., De Rybel, B., Casimiro, I., Benková, E., Swarup, R., Laplaze, L., Beeckman, T., and, Bennett, M.J., (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci. 14, 399-408.
35. Prasad, M.E., and, Stone, S.L., (2010) Further analysis of XBAT32, an Arabidopsis RING E3 ligase, involved in ethylene biosynthesis. Plant Signal Behav. 11, 1425-1429.
36. Prasad, M.E., Schofield, A., Lyzenga, W., Liu, H., and, Stone, S.L., (2010) Arabidopsis RING E3 ligase XBAT32 regulates lateral root production through its role in ethylene biosynthesis. Plant Physiol. 153, 1587-1596.
37. Santner, A., and, Estelle, M., (2010) The ubiquitin-proteasome system regulates plant hormone signaling. Plant J. 61, 1029-1040.
38. Sebastià, C.H., Hardin, S.C., Clouse, S.D., Kieber, J.J., and, Huber, S.C., (2004) Identification of a new motif for CDPK phosphorylation in vitro that suggests ACC synthase may be a CDPK substrate. Arch. Biochem. Biophys. 428, 81-91. (Pubitemid 38844911)
39. Stepanova, A.N., Yun., J., Likhacheva, A.V., and, Alonso, J.M., (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell, 19, 2169-2185. (Pubitemid 47347460)
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. (Pubitemid 43034286)
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. (Pubitemid 46464902)
42. Sun, L., and, Chen, Z.J., (2004) Novel functions of ubiquitination in signaling. Curr. Opin. Cell Biol. 16, 119-126.
43. Tanimoto, M., Roberts, K., and, Dolan, L., (1995) Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. Plant J. 8, 943-948. (Pubitemid 3009654)
44. Tatsuki, M., and, Mori, H., (2001) Phosphorylation of tomato 1-aminocyclopropane-1-carboxylic acid synthase, LE-ACS2, at the C-terminal region. J. Biol. Chem. 276, 28051-28057.
45. Tsuchisaka, A., Yu, G., Jin, H., Alonso, J.M., Ecker, J.R., Zhang, W., Gao, S., and, Theologis, A., (2009) A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics, 183, 979-1003.
46. Vandenbussche, F., Petrásek, J., Zádníková, P., et al. (2010) The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apicalhook development in Arabidopsis thaliana seedlings. Development, 137, 597-606.
47. Vierstra, R.D., (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10, 385-397.
48. Vogel, J.P., Woeste, K.W., Theologis, A., and, Kieber, J.J., (1998) Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc. Natl Acad. Sci. USA, 95, 4766-4771. (Pubitemid 28207988)
49. Wang, K.L., Li, H., and, Ecker, J.R., (2002) Ethylene biosynthesis and signaling networks. Plant Cell, 14, S131-S151. (Pubitemid 34609235)
50. Wang, K.L., Yoshida, H., Lurin, C., and, Ecker, J.R., (2004) Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature, 428, 945-950. (Pubitemid 38568096)
51. Wang, F., Zhu, D., Huang, X., Li, S., Gong, Y., Yao, Q., Fu, X., Fan, L.M., and, Deng, X.W., (2009) Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. Plant Cell, 21, 2378-2390.
52. Yamagami, T., Tsuchisaka, A., Yamada, K., Haddon, W.F., Harden, L.A., and, Theologis, A., (2003) Biochemical diversity among the 1-amino-cyclopropane- 1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. J. Biol. Chem. 278, 49102-49112.
53. Yang, S.F., and, Hoffman, N.E., (1984) Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35, 155-189.
54. 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.
55. Yoshida, H., Wang, K.L., Chang, C.M., Mori, K., Uchida, E., and, Ecker, J.R., (2006) The ACC synthase TOE sequence is required for interaction with ETO1 family proteins and destabilization of target proteins. Plant Mol. Biol. 62, 427-437. (Pubitemid 44454917)