14-3-3 regulates 1-aminocyclopropane-1-carboxylate synthase protein turnover in Arabidopsis

Plant Cell

Volumn 25, Issue 3, 2013, Pages 1016-1028

  Yoon, Gyeong Mee ^a   Kieber, Joseph J ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84876747163     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.110106     Document Type: Article

References (69)

1. Abeles, F.B., Morgan, P.W., and Saltveit, M.E., Jr. (1992). Ethylene in Plant Biology. (San Diego, CA: Academic Press).
2. 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.
3. Aoyama, T., and Chua, N.-H. (1997). A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11: 605-612.
4. Argueso, C.T., Hansen, M., and Kieber, J.J. (2007). Regulation of ethylene biosynthesis. J. Plant Growth Regul. 26: 92-105.
5. Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.L., Gomez-Gomez, L., Boller, T., Ausubel, F.M., and Sheen, J. (2002). MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977-983.
6. 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.
7. Chae, H.S., and Kieber, J.J. (2005). Eto Brute? Role of ACS turnover in regulating ethylene biosynthesis. Trends Plant Sci. 10: 291-296.
8. 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.
9. Chevalier, D., Morris, E.R., and Walker, J.C. (2009). 14-3-3 and FHA domains mediate phosphoprotein interactions. Annu. Rev. Plant Biol. 60: 67-91.
10. 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.
11. Coll, N.S., Vercammen, D., Smidler, A., Clover, C., Van Breusegem, F., Dangl, J.L., and Epple, P. (2010). Arabidopsis type I metacaspases control cell death. Science 330: 1393-1397.
12. 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.
13. Darling, D.L., Yingling, J., and Wynshaw-Boris, A. (2005). Role of 14-3-3 proteins in eukaryotic signaling and development. Curr. Top. Dev. Biol. 68: 281-315.
14. Denison, F.C., Paul, A.L., Zupanska, A.K., and Ferl, R.J. (2011). 14-3-3 proteins in plant physiology. Semin. Cell Dev. Biol. 22: 720-727.
15. Dougherty, M.K., and Morrison, D.K. (2004). Unlocking the code of 14-3-3. J. Cell Sci. 117: 1875-1884.
16. Fang, S., Jensen, J.P., Ludwig, R.L., Vousden, K.H., and Weissman, A.M. (2000). Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53. J. Biol. Chem. 275: 8945-8951.
17. Folta, K.M., Paul, A.L., Mayfield, J.D., and Ferl, R.J. (2008). 14-3-3 isoforms participate in red light signaling and photoperiodic flowering. Plant Signal. Behav. 3: 304-306.
18. Freeman, A.K., and Morrison, D.K. (2011). 14-3-3 proteins: Diverse functions in cell proliferation and cancer progression. Semin. Cell Dev. Biol. 22: 681-687.
19. 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. USA 101: 6803-6808.
20. Galan, J.-M., and Peter, M. (1999). Ubiquitin-dependent degradation of multiple F-box proteins by an autocatalytic mechanism. Proc. Natl. Acad. Sci. USA 96: 9124-9129.
21. Gampala, S.S., et al. (2007). An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev. Cell 13: 177-189.
22. 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.
23. 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.
24. Hansen, M., Chae, H.S., and Kieber, J.J. (2009). Regulation of ACS protein stability by cytokinin and brassinosteroid. Plant J. 57: 606-614.
25. Ho, M.S., Ou, C., Chan, Y.R., Chien, C.T., and Pi, H. (2008). The utility F-box for protein destruction. Cell. Mol. Life Sci. 65: 1977-2000.
26. Huber, S.C., MacKintosh, C., and Kaiser, W.M. (2002). Metabolic enzymes as targets for 14-3-3 proteins. Plant Mol. Biol. 50: 1053-1063.
27. Joo, S., Liu, Y., Lueth, A., and Zhang, S. (2008). MAPK phosphory-lation-induced stabilization of ACS6 protein is mediated by the noncatalytic C-terminal domain, which also contains the cis-determinant for rapid degradation by the 26S proteasome pathway. Plant J. 54: 129-140.
28. Lee, M.H., and Lozano, G. (2006). Regulation of the p53-MDM2 pathway by 14-3-3 sigma and other proteins. Semin. Cancer Biol. 16: 225-234.
29. Li, J.J., Zhang, T.P., Meng, Y., Du, J., and Li, H.H. (2011). Stability of F-box protein atrogin-1 is regulated by p38 mitogen-activated protein kinase pathway in cardiac H9c2 cells. Cell. Physiol. Biochem. 27: 463-470.
30. Liu, Y., and Zhang, S. (2004). Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogenactivated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16: 3386-3399.
31. 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-1carboxylate synthase 7. Plant J. 71: 23-34.
32. Masters, S.C., and Fu, H. (2001). 14-3-3 proteins mediate an essential anti-apoptotic signal. J. Biol. Chem. 276: 45193-45200.
33. Mattoo, A.K., and Suttle, J.C. (1991). The Plant Hormone Ethylene. (Boca Raton, FL: CRC Press).
34. Mayfield, J.D., Folta, K.M., Paul, A.-L., and Ferl, R.J. (2007). The 14-3-3 proteins mu and upsilon influence transition to flowering and early phytochrome response. Plant Physiol. 145: 1692-1702.
35. Mayfield, J.D., Paul, A.L., and Ferl, R.J. (2012). The 14-3-3 proteins of Arabidopsis regulate root growth and chloroplast development as components of the photosensory system. J. Exp. Bot. 63: 3061-3070.
36. Nakashima, A., Hayashi, N., Kaneko, Y.S., Mori, K., Sabban, E.L., Nagatsu, T., and Ota, A. (2007). RNAi of 14-3-3eta protein increases intracellular stability of tyrosine hydroxylase. Biochem. Biophys. Res. Commun. 363: 817-821.
37. Oecking, C., and Jaspert, N. (2009). Plant 14-3-3 proteins catch up with their mammalian orthologs. Curr. Opin. Plant Biol. 12: 760-765.
38. Oh, C.S., Pedley, K.F., and Martin, G.B. (2010). Tomato 14-3-3 protein 7 positively regulates immunity-associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKK alpha. Plant Cell 22: 260-272.
39. Paul, A.L., Denison, F.C., Schultz, E.R., Zupanska, A.K., and Ferl, R.J. (2012). 14-3-3 phosphoprotein interaction networks - Does isoform diversity present functional interaction specification? Front. Plant Sci. 3: 190.
40. Paul, A.L., Sehnke, P.C., and Ferl, R.J. (2005). Isoform-specific subcellular localization among 14-3-3 proteins in Arabidopsis seems to be driven by client interactions. Mol. Biol. Cell 16: 1735-1743.
41. 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.
42. Purwestri, Y.A., Ogaki, Y., Tamaki, S., Tsuji, H., and Shimamoto, K. (2009). The 14-3-3 protein GF14c acts as a negative regulator of flowering in rice by interacting with the florigen Hd3a. Plant Cell Physiol. 50: 429-438.
43. Roberts, M.R., and de Bruxelles, G.L. (2002). Plant 14-3-3 protein families: Evidence for isoform-specific functions? Biochem. Soc. Trans. 30: 373-378.
44. Ryu, H., Kim, K., Cho, H., Park, J., Choe, S., and Hwang, I. (2007). Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling. Plant Cell 19: 2749-2762.
45. Santner, A., and Estelle, M. (2010). The ubiquitin-proteasome system regulates plant hormone signaling. Plant J. 61: 1029-1040.
46. Sepúlveda-García, E., and Rocha-Sosa, M. (2012). The Arabidopsis F-box protein AtFBS1 interacts with 14-3-3 proteins. Plant Sci. 195: 36-47.
47. Stone, S.L., and Callis, J. (2007). Ubiquitin ligases mediate growth and development by promoting protein death. Curr. Opin. Plant Biol. 10: 624-632.
48. Su, C.H., Zhao, R., Velazquez-Torres, G., Chen, J., Gully, C., Yeung, S.C., and Lee, M.H. (2010). Nuclear export regulation of COP1 by 14-3-3s in response to DNA damage. Mol. Cancer 9: 243.
49. Su, C.H., Zhao, R., Zhang, F., Qu, C., Chen, B., Feng, Y.H., Phan, L., Chen, J., Wang, H., Wang, H., Yeung, S.C., and Lee, M.H. (2011). 14-3-3s exerts tumor-suppressor activity mediated by regulation of COP1 stability. Cancer Res. 71: 884-894.
50. Tseng, T.S., Whippo, C., Hangarter, R.P., and Briggs, W.R. (2012). The role of a 14-3-3 protein in stomatal opening mediated by PHOT2 in Arabidopsis. Plant Cell 24: 1114-1126.
51. Tzivion, G., and Avruch, J. (2002). 14-3-3 proteins: Active cofactors in cellular regulation by serine/threonine phosphorylation. J. Biol. Chem. 277: 3061-3064.
52. Vierstra, R.D. (2009). The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10: 385-397.
53. Vogel, J.P., Schuerman, P., Woeste, K.W., Brandstatter, I., and Kieber, J.J. (1998b). Isolation and characterization of Arabidopsis mutants defective in the induction of ethylene biosynthesis by cytokinin. Genetics 149: 417-427.
54. Vogel, J.P., Woeste, K.E., Theologis, A., and Kieber, J.J. (1998a). 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.
55. Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33: 949-956.
56. Wang, B., Yang, H., Liu, Y.C., Jelinek, T., Zhang, L., Ruoslahti, E., and Fu, H. (1999). Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry 38: 12499-12504.
57. Wang, K.L.-C., Yoshida, H., Lurin, C., and Ecker, J.R. (2004). Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428: 945-950.
58. 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.
59. Wei, W., Ayad, N.G., Wan, Y., Zhang, G.J., Kirschner, M.W., and Kaelin, W.G.J., Jr. (2004). Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphase-promoting complex. Nature 428: 194-198.
60. Weiner, H., and Kaiser, W.M. (1999). 14-3-3 proteins control proteolysis of nitrate reductase in spinach leaves. FEBS Lett. 455: 75-78.
61. Xu, W., Shi, W., Jia, L., Liang, J., and Zhang, J. (2012). TFT6 and TFT7, two different members of tomato 14-3-3 gene family, play distinct roles in plant adaption to low phosphorus stress. Plant Cell Environ. 35: 1393-1406.
62. Yang, H.Y., Wen, Y.Y., Lin, Y.I., Pham, L., Su, C.H., Yang, H., Chen, J., and Lee, M.H. (2007). Roles for negative cell regulator 14-3-3sigma in control of MDM2 activities. Oncogene 26: 7355-7362.
63. Yang, J.L., Chen, W.W., Chen, L.Q., Qin, C., Jin, C.W., Shi, Y.Z., and Zheng, S.J. (2013). The 14-3-3 protein GENERAL REGULATORY FACTOR11 (GRF11) acts downstream of nitric oxide to regulate iron acquisition in Arabidopsis thaliana. New Phytol. 197: 815-824.
64. Yang, S.F., and Hoffman, N.E. (1984). Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35: 155-189.
65. Yang, Y., Li, R., and Qi, M. (2000). In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves. Plant J. 22: 543-551.
66. Yi, C., and Deng, X.W. (2005). COP1 From plant photomorphogenesis to mammalian tumorigenesis. Trends Cell Biol. 15: 618-625.
67. Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat. Protoc. 2: 1565-1572.
68. 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.
69. 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