Turnover of LeACS2, a wound-inducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation

Plant Journal

Volumn 64, Issue 1, 2010, Pages 140-150

  Kamiyoshihara, Yusuke ^a   Iwata, Mineko ^a   Fukaya, Tomoko ^a   Tatsuki, Miho ^a,b   Mori, Hitoshi ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF FRUIT TREE SCIENCE   (Japan)

Author keywords

1 aminocyclopropane 1 carboxylic acid synthase; calcium dependent protein kinase; protein phosphorylation; protein turnover

Indexed keywords

1-AMINO-CYCLOPROPANE- 1-CARBOXYLIC ACIDS; 1-AMINOCYCLOPROPANE-1- CARBOXYLIC ACID SYNTHASE; CALCIUM-DEPENDENT PROTEIN KINASE; DEGRADATION PATHWAYS; DEPHOSPHORYLATIONS; ENZYMATIC ACTIVITIES; ETHYLENE BIOSYNTHESIS; ETHYLENE PRODUCTION; IN-VIVO; MITOGEN ACTIVATED PROTEIN KINASE; PROTEASOMES; PROTEIN KINASE; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN TURNOVER; RATE-LIMITING ENZYMES; SOLANUM LYCOPERSICUM; SYNTHASES; TOMATO FRUITS; TRANSLATIONAL REGULATION; UBIQUITIN;

BIOCHEMISTRY; CALCIUM; CARBOXYLIC ACIDS; ETHYLENE; FRUITS; ORGANIC ACIDS; PHOSPHORYLATION; PLANTS (BOTANY);

PROTEINS;

1 AMINOCYCLOPROPANECARBOXYLATE SYNTHASE; 1-AMINOCYCLOPROPANECARBOXYLATE SYNTHASE; LYASE; VEGETABLE PROTEIN;

ARTICLE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; TOMATO;

GENE EXPRESSION REGULATION, PLANT; LYASES; LYCOPERSICON ESCULENTUM; PHOSPHORYLATION; PLANT PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY;

LYCOPERSICON ESCULENTUM; SOLANUM;

EID: 77957226474     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04316.x     Document Type: Article

References (56)

1. Abeles, F.B., Morgan, P.W. Saltveit, M.E.J. (1992) Ethylene in Plant Biology. San Diego: Academic Press.
2. Argueso, C.T., Hansen, M. Kieber, J.J. (2007) Regulation of ethylene biosynthesis. J. Plant Growth Regul. 26, 92 105. (Pubitemid 47165740)
3. Barry, C.S., Llop-Tous, M.I. Grierson, D. (2000) The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol. 123, 979 986. (Pubitemid 30466849)
4. Botella, J.R., Arteca, J.M., Somodevilla, M. Arteca, R.N. (1996) Calcium-dependent protein kinase gene expression in response to physical and chemical stimuli in mungbean (Vigna radiata). Plant Mol. Biol. 30, 1129 1137. (Pubitemid 26310786)
5. Boualem, A., Fergany, M., Fernandez, R. et al. (2008) A conserved mutation in an ethylene biosynthesis enzyme leads to andromonoecy in melons. Science, 321, 836 838.
6. Boualem, A., Troadec, C., Kovalski, I., Sari, M.A., Perl-Treves, R. Bendahmane, A. (2009) A conserved ethylene biosynthesis enzyme leads to andromonoecy in two cucumis species. PLoS ONE, 4, e6144.
7. Chae, H.S. Kieber, J.J. (2005) Eto brute? Role of ACS turnover in regulating ethylene biosynthesis. Trends Plant Sci. 10, 291 296.
8. Chae, H.S., Faure, F. 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)
9. 2+-dependent protein kinase and endogenous substrate proteins from bitter gourd seeds. Plant Sci. 105, 31 44.
10. Chappell, J., Hahlbrock, K. Boller, T. (1984) Rapid induction of ethylene biosynthesis in cultured parsley cells by fungal elicitor and its relationship to the induction of phenylalanine-lyase. Planta, 161, 475 480.
11. Chen, Y.F., Shakeel, S.N., Bowers, J., Zhao, X.C., Etheridge, N. Schaller, G.E. (2007) Ligand-induced degradation of the ethylene receptor ETR2 through a proteasome-dependent pathway in Arabidopsis. J. Biol. Chem. 282, 24752 24758. (Pubitemid 47347555)
12. Cheng, S.H., Willmann, M.R., Chen, H.C. Sheen, J. (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol. 129, 469 485. (Pubitemid 34689138)
13. Chico, J.M., Raices, M., Tellez-Inon, M.T. Ulloa, R.M. (2002) A calcium-dependent protein kinase is systemically induced upon wounding in tomato plants. Plant Physiol. 128, 256 270. (Pubitemid 34115327)
14. Christians, M.J., Gingerich, D.J., Hansen, M., Binder, B.M., Kieber, J.J. 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.
15. Collins, T., Stone, J.R. Williams, A.J. (2001) All in the family: the BTB/POZ, KRAB, and SCAN domains. Mol. Cell. Biol. 21, 3609 3615. (Pubitemid 32466975)
16. D'Andrea, L.D. Regan, L. (2003) TPR proteins: the versatile helix. Trends Biochem. Sci. 28, 655 662. (Pubitemid 37500900)
17. Felix, G., Grosskopf, D.G., Regenass, M., Basse, C.W. Boller, T. (1991) Elicitor-induced ethylene biosynthesis in tomato cells. Characterization and use as a bioassay for elicitor action. Plant Physiol. 97, 19 25. (Pubitemid 21914178)
18. Ge, L., Liu, J.Z., Wong, W.S., Hsiao, W.L.W., Chong, K., Xu, Z.K., Yang, S.F., Kung, S.D. Li, N. (2000) Identification of a novel multiple environmental factor-responsive 1-aminocyclopropane-1-carboxylate synthase gene, NT-ACS2, from tobacco. Plant Cell Environ. 23, 1169 1182.
19. Guo, H.W. 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.
20. Higgins, R., Lockwood, T., Holley, S., Yalamanchili, R. Stratmann, J.W. (2007) Changes in extracellular pH are neither required nor sufficient for activation of mitogen-activated protein kinases (MAPKs) in response to systemin and fusicoccin in tomato. Planta, 225, 1535 1546. (Pubitemid 46632356)
21. Joo, S., Liu, Y., Lueth, A. Zhang, S.Q. (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)
22. Katou, S., Yoshioka, H., Kawakita, K., Rowland, O., Jones, J.D.G., Mori, H. Doke, N. (2005) Involvement of PPS3 phosphorylated by elicitor-responsive mitogen-activated protein kinases in the regulation of plant cell death. Plant Physiol. 139, 1914 1926. (Pubitemid 43899827)
23. Kende, H. (1993) Ethylene biosynthesis. Annu. Rev. Plant Biol. 44, 283 307.
24. Kende, H. Boller, T. (1981) Wound ethylene and 1-aminocyclopropane-1- carboxylate synthase in ripening tomato fruit. Planta, 151, 476 481.
25. Kim, W.T. Yang, S.F. (1992) Turnover of 1-aminocyclopropane-1-carboxylic acid synthase protein in wounded tomato fruit tissue. Plant Physiol. 100, 1126 1131.
26. Kinoshita, E., Kinoshita-Kikuta, E., Takiyama, K. Koike, T. (2006) Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell Proteomics, 5, 749 757.
27. Knight, H. Knight, M.R. (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci. 6, 262 267.
28. Li, Z., Huang, S.W., Liu, S.Q. et al. (2009) Molecular isolation of the M Gene suggests that a conserved-residue conversion induces the formation of bisexual flowers in cucumber plants. Genetics, 182, 1381 1385.
29. Liu, Y.D. Zhang, S.Q. (2004) Phosphorylation of 1-aminocyclopropane-1- carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell, 16, 3386 3399.
30. Lizada, M.C.C. Yang, S.F. (1979) Simple and sensitive assay for 1-aminocyclopropane-1-carboxylic acid. Anal. Biochem. 100, 140 145. (Pubitemid 10157643)
31. Llop-Tous, I., Barry, C.S. Grierson, D. (2000) Regulation of ethylene biosynthesis in response to pollination in tomato flowers. Plant Physiol. 123, 971 978. (Pubitemid 30466848)
32. Lupas, A. (1996) Coiled coils: new structures and new functions. Trends Biochem. Sci. 21, 375 382. (Pubitemid 26338674)
33. Matsuo, R., Ochiai, W., Nakashima, K. Taga, T. (2001) A new expression cloning strategy for isolation of substrate-specific kinases by using phosphorylation site-specific antibody. J. Immunol. Methods, 247, 141 151. (Pubitemid 32057051)
34. Mayrose, M., Bonshtien, A. Sessa, G. (2004) LeMPK3 is a mitogen-activated protein kinase with dual specificity induced during tomato defense and wounding responses. J. Biol. Chem. 279, 14819 14827. (Pubitemid 38618871)
35. Nakatsuka, A., Murachi, S., Okunishi, H., Shiomi, S., Nakano, R., Kubo, Y. Inaba, A. (1998) Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiol. 118, 1295 1305. (Pubitemid 128653063)
36. Oetiker, J.H., Olson, D.C., Shiu, O.Y. Yang, S.F. (1997) Differential induction of seven 1-aminocyclopropane-1-carboxylate synthase genes by elicitor in suspension cultures of tomato (Lycopersicon esculentum). Plant Mol. Biol. 34, 275 286.
37. Romeis, T., Ludwig, A.A., Martin, R. Jones, J.D.G. (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J. 20, 5556 5567. (Pubitemid 33010033)
38. Rutschmann, F., Stalder, U., Piotrowski, M., Oecking, C. Schaller, A. (2002) LeCPK1, a calcium-dependent protein kinase from tomato. Plasma membrane targeting and biochemical characterization. Plant Physiol. 129, 156 168. (Pubitemid 34527317)
39. Sebastia, 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.
40. Spanu, P., Felix, G. Boller, T. (1990) Inactivation of stress-induced 1-aminocyclopropane-1-carboxylate synthase in vivo differs from substrate-dependent inactivation in vitro. Plant Physiol. 93, 1482 1485. (Pubitemid 120029977)
41. 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. (Pubitemid 2164124)
42. Tatsuki, M. Mori, H. (1999) Rapid and transient expression of 1-aminocyclopropane-1-carboxylate synthase isogenes by touch and wound stimuli in tomato. Plant Cell Physiol. 40, 709 715. (Pubitemid 29360686)
43. 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. (Pubitemid 37391504)
44. Tsuchisaka, A. Theologis, A. (2004) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol. 136, 2982 3000. (Pubitemid 41096300)
45. Tuomainen, J., Betz, C., Kangasjarvi, J., Ernst, D., Yin, Z.H., Langebartels, C. Sandermann, H. (1997) Ozone induction of ethylene emission in tomato plants: regulation by differential accumulation of transcripts for the biosynthetic enzymes. Plant J. 12, 1151 1162. (Pubitemid 28000574)
46. Van der Straeten, D., Rodrigues-Pousada, R.A., Villarroel, R., Hanley, S., Goodman, H.M. Van Montagu, M. (1992) Cloning, genetic-mapping, and expression analysis of an Arabidopsis thaliana gene that encodes 1-aminocyclopropane-1-carboxylate synthase. Proc. Natl Acad. Sci. USA, 89, 9969 9973.
47. Vogel, J.P., Woeste, K.E., Theologis, A. 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)
48. 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. (Pubitemid 38568096)
49. Woeste, K.E., Ye, C. Kieber, J.J. (1999) Two Arabidopsis mutants that overproduce ethylene are affected in the posttranscriptional regulation of 1-aminocyclopropane-1-carboxylic acid synthase. Plant Physiol. 119, 521 529. (Pubitemid 29384542)
50. Yang, S.F. Hoffman, N.E. (1984) Ethylene biosynthesis and its regulation in higher plants. Ann. Rev. Plant Biol. 35, 155 189.
51. Yoon, G.M., Cho, H.S., Ha, H.J., Liu, J.R. Lee, H.S.P. (1999) Characterization of NtCDPK1, a calcium-dependent protein kinase gene in Nicotiana tabacum, and the activity of its encoded protein. Plant Mol. Biol. 39, 991 1001. (Pubitemid 29207773)
52. Yoshida, H., Nagata, M., Saito, K., Wang, K.L.C. Ecker, J.R. (2005) Arabidopsis ETO1 specifically interacts with and negatively regulates type 2 1-aminocyclopropane-1-carboxylate synthases. BMC Plant Biol. 5, 13. (Pubitemid 41261266)
53. 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. (Pubitemid 44454917)
54. Yoshii, H. Imaseki, H. (1982) Regulation of auxin-induced ethylene biosynthesis. Repression of inductive formation of 1-aminocyclopropane-1- carboxylate synthase by ethylene. Plant Cell Physiol. 23, 639 649.
55. Zarembinski, T.I. Theologis, A. (1994) Ethylene biosynthesis and action: a case of conservation. Plant Mol. Biol. 26, 1579 1597.
56. Zhang, S.Q. Klessig, D.F. (2001) MAPK cascades in plant defense signaling. Trends Plant Sci. 6, 520 527.