Regulation of ACS protein stability by cytokinin and brassinosteroid

Plant Journal

Volumn 57, Issue 4, 2009, Pages 606-614

  Hansen, Maureen ^b   Chae, Hyun Sook ^a,b   Kieber, Joseph J ^b  

^a SYNGENTA BIOTECHNOLOGY INC   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

ACC synthase; Brassinosteroid; Ethylene; Protein stability

Indexed keywords

1 AMINOCYCLOPROPANECARBOXYLATE SYNTHASE; 1-AMINOCYCLOPROPANECARBOXYLATE SYNTHASE; ARABIDOPSIS PROTEIN; BRASSINOLIDE; CHOLESTANOL; CYTOKININ; ETHYLENE; ETHYLENE DERIVATIVE; HETEROCYCLIC STEROID; LYASE; PHYTOHORMONE;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROTEIN STABILITY; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHOLESTANOLS; CYTOKININS; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; LYASES; PLANT GROWTH REGULATORS; PLANTS, GENETICALLY MODIFIED; PROTEIN STABILITY; STEROIDS, HETEROCYCLIC;

EID: 59149105869     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03711.x     Document Type: Article

References (53)

1. Abel, S., Nguyen, M.D., Chow, W. Theologis, A. (1995) ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. J. Biol. Chem. 270, 19093 19099.
2. Abeles, F.B., Morgan, P.W. Saltveit, M.E. Jr. (1992) Ethylene in Plant Biology, 2nd edn. San Diego, CA : Academic Press Inc.
3. Adams, D.O. Yang, S.F. (1979) Ethylene biosynthesis: identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proc. Natl. Acad. Sci. U.S.A. 76, 170 174.
4. Aoyama, T. Chua, N.H. (1997) A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11, 605 612.
5. Argueso, C.T., Hansen, M. Kieber, J.J. (2007) Regulation of ethylene biosynthesis. J. Plant Growth Regul. 26, 92 105.
6. Arteca, R.N. Arteca, J.M. (2008) Effects of brassinosteroid, auxin, and cytokinin on ethylene production in Arabidopsis thaliana plants. J. Exp. Bot. 59, 3019 3026.
7. Belkhadir, Y., Wang, X. Chory, J. (2006) Brassinosteroid signaling pathway. Sci STKE, 2006, 364.
8. Bostick, M., Lochhead, S.R., Honda, A., Palmer, S. 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.
9. Cano-Delgado, A., Yin, Y., Yu, C., Vafeados, D., Mora-Garcia, S., Cheng, J.C., Nam, K.H., Li, J. Chory, J. (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development, 131, 5341 5351.
10. Cary, A.J., Liu, W. Howell, S.H. (1995) Cytokinin action is coupled to ethylene in its effects on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings. Plant Physiol. 107, 1075 1082.
11. Chae, H.S. Kieber, J.J. (2005) Eto Brute? The role of ACS turnover in regulating ethylene biosynthesis. Trends Plant Sci. 10, 291 296.
12. Chae, H.S., Faure, F. Kieber, J.J. (2003) The eto1, eto2 and eto3 mutations and cytokinin treatment elevate ethylene biosynthesis in Arabidopsis by increasing the stability of the ACS5 protein. Plant Cell, 15, 545 559.
13. Christians, M., Gingerich, D., Hansen, M., Binder, B., Kieber, J.J. Vierstra, R.D. (2008) 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. doi:, in press.
14. Clough, S.J. Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsisthaliana. Plant J. 16, 735 743.
15. De Grauwe, L., Vandenbussche, F., Tietz, O., Palme, K. Van Der Straeten, D. (2005) Auxin, ethylene and brassinosteroids: tripartite control of growth in the Arabidopsis hypocotyl. Plant Cell Physiol. 46, 827 836.
16. Fujioka, S. Yokota, T. (2003) Biosynthesis and metabolism of brassinosteroids. Annu. Rev. Plant Biol. 54, 137 164.
17. Gingerich, D.J., Gagne, J.M., Salter, D.W., Hellmann, H., Estelle, M., Ma, L. 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.
18. Guzman, P. Ecker, J.R. (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell, 2, 513 523.
19. Hutchison, C.E., Li, J., Argueso, C. et al. (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell, 18, 3073 3087.
20. Joo, S., Liu, Y., Lueth, A. 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.
21. Kakimoto, T. (2003) Perception and signal transduction of cytokinins. Annu. Rev. Plant Biol. 54, 605 627.
22. Larsen, P.B. Cancel, J.D. (2004) A recessive mutation in the RUB1-conjugating enzyme, RCE1, reveals a requirement for RUB modification for control of ethylene biosynthesis and proper induction of basic chitinase and PDF1.2 in Arabidopsis. Plant J. 38, 626 638.
23. Li, J. (2003) Brassinosteroids signal through two receptor-like kinases. Curr. Opin. Plant Biol. 6, 494 499.
24. Li, J. Jin, H. (2007) Regulation of brassinosteroid signaling. Trends Plant Sci. 12, 37 41.
25. Liang, X., Abel, S., Keller, J.A., Shen, N.F. Theologis, A. (1992) The 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana. Proc. Natl Acad. Sci. U.S.A. 89, 11046 11050.
26. Liu, Y. Zhang, S. (2004) Phosphorylation of ACC synthase by MPK6, a stress-responsive MAPK, induces ethylene biosynthesis in Arabidopsis. Plant Cell, 16, 3386 3399.
27. Mason, M.G., Li, J., Mathews, D.E., Kieber, J.J. Schaller, G.E. (2004) Type-B response regulators display overlapping but distinct expression patterns in Arabidopsis. Plant Physiol. 135, 927 937.
28. Mason, M.G., Mathews, D.E., Argyros, D.A., Maxwell, B.B., Kieber, J.J., Alonso, J.M., Ecker, J.R. Schaller, G.E. (2005) Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell, 17, 3007 3018.
29. Pintard, L., Willems, A. Peter, M. (2004) Cullin-based ubiquitin ligases: Cul3-BTB complexes join the family. EMBO J. 23, 1681 1687.
30. Rashotte, A.M., Carson, S.D.B., To, J.P.C. Kieber, J.J. (2003) Expression profiling of cytokinin action in Arabidopsis. Plant Physiol. 123, 184 194.
31. Rashotte, A.M., Mason, M.G., Hutchison, C.E., Ferreira, F.J., Schaller, G.E. Kieber, J.J. (2006) A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc. Natl Acad. Sci. U.S.A. 103, 11081 11085.
32. Sebastià, C.H., Hardin, S.C., Clouse, S.D., Kieber, J.J. 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.
33. Spanu, P., Grosskopf, D.G., Felix, G. Boller, T. (1994) The apparent turnover of 1-aminocyclopropane-1-carboxylate synthase in tomato cells is regulated by protein phosphorylation and dephosphorylation. Plant Physiol. 106, 529 535.
34. Tatsuki, M. 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.
35. To, J.P.C. Kieber, J.J. (2008) Cytokinin signaling: two-components and more. Trends Plant Sci. 13, 85 92.
36. To, J.P.C., Haberer, G., Ferreira, F.J., Deruère, J., Mason, M.G., Schaller, G.E., Alonso, J.M., Ecker, J.R. Kieber, J.J. (2004) Type-A ARRs are partially redundant negative regulators of cytokinin signaling in Arabidopsis. Plant Cell, 16, 658 671.
37. Tsuchisaka, A. Theologis, A. (2004a) Heterodimeric interactions among the 1-amino-cyclopropane-1-carboxylate synthase polypeptides encoded by the Arabidopsis gene family. Proc. Natl Acad. Sci. U.S.A. 101, 2275 2280.
38. Tsuchisaka, A. Theologis, A. (2004b) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol. 136, 2982 3000.
39. Vogel, J.P., Schuerman, P., Woeste, K.W., Brandstatter, I. Kieber, J.J. (1998a) Isolation and characterization of Arabidopsis mutants defective in induction of ethylene biosynthesis by cytokinin. Genetics, 149, 417 427.
40. Vogel, J.P., Woeste, K.W., Theologis, A. Kieber, J.J. (1998b) Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc. Natl Acad. Sci. U.S.A. 95, 4766 4771.
41. Wang, K.L.-C., Yoshida, H., Lurin, C. Ecker, J.R. (2004) Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature, 428, 945 950.
42. Wang, N., Shih, M. Li, N. (2005) The GUS reporter-aided analysis of the promoter activities of Arabidopsis ACC synthase genes AtACS4, AtACS5, and AtACS7 induced by hormones and stresses. J. Exp. Bot. 56, 909 920.
43. Weber, H., Bernhardt, A., Dieterle, M., Hano, P., Mutlu, A., Estelle, M., Genschik, P. Hellmann, H. (2004) Arabidopsis AtCUL3a and AtCUL3b form complexes with members of the BTB/POZ-MATH protein family. Plant Physiol. 137, 83 93.
44. Woeste, K., Vogel, J.P. Kieber, J.J. (1999a) Factors regulating ethylene biosynthesis in etiolated Arabidopsis thaliana seedlings. Physiol. Plant. 105, 478 484.
45. Woeste, K., Ye, C. Kieber, J.J. (1999b) Two Arabidopsis mutants that overproduce ethylene are affected in the post-transcriptional regulation of ACC synthase. Plant Physiol. 119, 521 530.
46. Woodward, A.W., Ratzel, S.E., Woodward, E.E., Shamoo, Y. Bartel, B. (2007) Mutation of E1-CONJUGATING ENZYME-RELATED1 decreases RELATED TO UBIQUITIN conjugation and alters auxin response and development. Plant Physiol. 144, 976 987.
47. Yamagami, T., Tsuchisaka, A., Yamada, K., Haddon, W.F., Harden, L.A. 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.
48. Yang, S.F. Hoffman, N.E. (1984) Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35, 155 189.
49. Yi, H.C., Joo, S., Nam, K.H., Lee, J.S., Kang, B.G. Kim, W.T. (1999) Auxin and brassinosteroid differentially regulate the expression of the three members of the 1-aminocyclopropane-1-carboxylate synthase family in mung bean (Vigna radiata L.). Plant Mol. Biol. 41, 443 454.
50. Yoshida, H., Nagata, M., Saito, K. Ecker, J. (2005) Arabidopsis ETO1 specifically interacts with and negatively regulates type 2 1-aminocyclopropane- 1-carboxylate synthases. BMC Plant Biol. 5, 14.
51. Yoshida, H., Wang, K.L.C., Chang, C.M., Mori, K., Uchida, E. 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.
52. Zhou, A., Wang, H., Walker, J.C. Li, J. (2004) BRL1, a leucine-rich repeat receptor-like protein kinase, is functionally redundant with BRI1 in regulating Arabidopsis brassinosteroid signaling. Plant J. 40, 399 409.
53. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L. Gruissem, W. (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621 2632.