Overexpression of a directed mutant of 14-3-3u in Arabidopsis leaves affects phosphorylation and protein content of nitrate reductase

Botany

Volumn 87, Issue 7, 2009, Pages 691-701

  Oh, Man Ho ^a   Huber, Joan L ^a   Shen, Wei ^b   Athwal, Gurdeep S ^b   Wu, Xia ^a   Huber, Steven C ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

14 3 3 Protein; Arabidopsis thaliana; B glucosidase; Glutathione S transferase; Site directed mutagenesis; Two dimensional difference gel electrophoresis

Indexed keywords

ELECTROKINESIS; ENZYME ACTIVITY; GENE EXPRESSION; HERB; MUTATION; PROTEIN; SIGNALING;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

EID: 68349106875     PISSN: 19162804     EISSN: None     Source Type: Journal    
DOI: 10.1139/B09-003     Document Type: Article

References (47)

1. Alexander, R.D., and Morris, P.C. 2006. A proteomic analysis of 14-3-3 binding proteins from developing barley grains. Proteomics, 6: 1886-1896. doi:10.1002/pmic.200500548. PMID:16470656.
2. Athwal, G.S., and Huber, S.C. 2002. Divalent cations and polyamines bind to loop 8 of 14-3-3 proteins, modulating their interaction with phosphorylated nitrate reductase. Plant J. 29: 119-129. doi:10.1046/j.0960-7412.2001.01200.x. PMID:11851916.
3. Athwal, G.S., Lombardo, C., Huber, J.L., Masters, S.C., Fu, H., and Huber, S.C. 2000. Modulation of 14-3-3 protein interactions with target polypeptides by physical and metabolic effectors. Plant Cell Physiol. 41: 523-533. PMID:10845467. (Pubitemid 30319618)
4. Bachmann, M., Huber, J.L., Athwal, G.S., Wu, K., Ferl, R.J., and Huber, S.C. 1996a. 14-3-3 proteins associate with the regulatory phosphorylation site of spinach leaf nitrate reductase in an isoform-specific manner and reduce dephosphorylation by endogenous protein phosphatases. FEBS Lett. 398: 26-30. doi:10. 1016/S0014-5793(96)01188-X. PMID:8946947. (Pubitemid 26400336)
5. Bachmann, M., Huber, J.L., Liao, P.-C., Gage, D.A., and Huber, S.C. 1996b. The inhibitor protein of phosphorylated nitrate reductase from spinach (Spinacia oleracea) leaves is a 14-3-3 protein. FEBS Lett. 387: 127-131. doi:10.1016/0014-5793(96) 00478-4. PMID:8674533. (Pubitemid 26178907)
6. Bachmann, M., Shiraishi, N., Campbell, W.H., Yoo, B.-C., Harmon, A.C., and Huber, S.C. 1996c. Identification of Ser-543 as the major regulatory phosphorylation site in spinach leaf nitrate reductase. Plant Cell, 8: 505-517. doi:10.1105/tpc.8.3.505. PMID:8721752. (Pubitemid 126635923)
7. Bunney, T.D., van Walraven, H.S., and de Boer, A.H. 2001. 14-3-3 protein is a regulator of the mitochondrial and chloroplast ATP synthase. Proc. Natl. Acad. Sci. U.S.A. 98: 4249-4254. doi:10. 1073/pnas.061437498. PMID:11274449.
8. 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. doi:10.1046/j.1365-313x.1998.00343. x. PMID:10069079. (Pubitemid 128418620)
9. Cotelle, V., Meek, S.E.M., Provan, F., Milne, F.C., Morrice, N., and MacKintosh, C. 2000. 14-3-3s regulate global cleavage of their diverse binding partners in sugar-starved Arabidopsis cells. EMBO J. 19: 2869-2876. doi:10.1093/emboj/19.12.2869. PMID: 10856232. (Pubitemid 30386759)
10. Cummins, I., Cole, D.J., and Edwards, R. 1999. A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J. 18: 285-292. doi:10.1046/j.1365-313X.1999. 00452.x. PMID:10377994. (Pubitemid 129516621)
11. Douglas, P., Morrice, N., and MacKintosh, C. 1995. Identification of a regulatory phosphorylation site in the hinge 1 region of nitrate reductase from spinach (Spinacea oleracea) leaves. FEBS Lett. 377: 113-117. doi:10.1016/0014-5793(95)01300-8. PMID: 8543031. (Pubitemid 26015056)
12. Ferl, R.J. 2004. 14-3-3 proteins: regulation of signal-induced events. Physiol. Plant. 120: 173-178. doi:10.1111/j.0031-9317. 2004.0239.x. PMID:15032850.
13. Gibon, Y., Blaesing, O.E., Hannemann, J., Carillo, P., Höhne, M., Hendriks, J.H.M., Palacios, N., Cross, J., Selbig, J., and Stitt, M. 2004. A robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell, 16: 3304-3325. doi:10.1105/tpc.104.025973. PMID:15548738. (Pubitemid 41096008)
14. Glaab, J., and Kaiser, W.M. 1995. Inactivation of nitrate reductase involves NR-protein phosphorylation and subsequent 'binding' of an inhibitor protein. Planta, 195: 514-518. doi:10.1007/BF00195708.
15. Glaab, J., and Kaiser, W.M. 1996. The protein kinase, protein phosphatase and inhibitor protein of nitrate reductase are ubiquitous in higher plants and independent of nitrate reductase expression and turnover. Planta, 199: 57-63. doi:10.1007/BF00196881. (Pubitemid 126579534)
16. Gruhler, A., Schulze, W.X., Matthiesen, R., Mann, M., and Jensen, O.N. 2005. Stable isotope labeling of Arabidopsis thaliana cells and quantitative proteomics by mass spectrometry. Mol. Cell. Proteomics, 4: 1697-1709. doi:10.1074/mcp.M500190-MCP200. PMID:16088002. (Pubitemid 41749263)
17. Hoagland, D. R., and Arnon, D. I. 1950. Calif Agric Exp Stn Bull, Circular 347.
18. 2+ and 5'-AMP. Planta, 193: 358-364. doi:10. 1007/BF00201813.
19. Kaiser, W.M., and Huber, S.C. 2001. Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. J. Exp. Bot. 52: 1981-1989. doi:10.1093/jexbot/52.363.1981. PMID:11559733.
20. Kulma, A., Villadsen, D., Campbell, D.G., Meek, S.E.M., Harthill, J.E., Nielsen, T.M., and MacKintosh, C. 2004. Phosphorylation and 14-3-3 binding of Arabidopsis 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase. Plant J. 37: 654-667. doi:10.1111/j. 1365-313X.2003.01992.x. PMID:14871307. (Pubitemid 38300511)
21. Lillo, C., Lea, U.S., Leydecker, M.-T., and Meyer, C. 2003. Mutation of the regulatory phosphorylation site of tobacco nitrate reductase results in constitutive activation of the enzyme in vivo and nitrite accumulation. Plant J. 35: 566-573. doi:10.1046/j. 1365-313X.2003.01828.x. PMID:12940950. (Pubitemid 37110712)
22. Lima, L., Seabra, A., Melo, P., Cullimore, J., and Carvalho, H. 2006. Phosphorylation and subsequent interaction with 14-3-3 proteins regulate plastid glutamine synthetase in Medicago truncatula. Planta, 223: 558-567. doi:10.1007/s00425-005-0097-8. PMID:16136328. (Pubitemid 43327626)
23. Lu, G., Sehnke, P.C., and Ferl, R.J. 1994. Phosphorylation and calcium binding properties of an Arabidopsis GF14 brain protein homolog. Plant Cell, 6: 501-510. doi:10.1105/tpc.6.4.501. PMID:8205002. (Pubitemid 24987214)
24. MacKintosh, C. 2004. Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem. J. 381: 329-342. doi:10.1042/BJ20031332. PMID: 15167810.
25. MacKintosh, C., and Meek, S.E.M. 2001. Regulation of NR activity by reversible phosphorylation, 14-3-3 proteins and proteolysis. Cell. Mol. Life Sci. 58: 205-214. doi:10.1007/PL00000848. PMID:11289302. (Pubitemid 32217352)
26. Man, H.-M., and Kaiser, W.M. 2001. Increased glutamine synthetase activity and changes in amino acid pools in leaves treated with 5-aminoimidazole-4-carboxamide ribonucleoside (AICAR). Physiol. Plant. 111: 291-296. doi:10.1034/j.1399-3054.2001. 1110305.x. PMID:11240912. (Pubitemid 32169988)
27. Manak, M.S., and Ferl, R.J. 2007. Divalent cation effects on interactions between multiple Arabidopsis 14-3-3 isoforms and phosphopeptide targets. Biochemistry, 46: 1055-1063. doi:10.1021/bi061366c. PMID:17240989.
28. Moorhead, G., Douglas, P., Morrice, N., Scarabel, M., Aitken, A., and MacKintosh, C. 1996. Phosphorylated nitrate reductase from spinach leaves is inhibited by 14-3-3 proteins and activated byfusicoccin. Curr. Biol. 6: 1104-1113. doi:10.1016/S0960-9822(02)70677-5. PMID:8805370. (Pubitemid 26368744)
29. Moorhead, G., Douglas, P., Cotelle, V., Harthill, J., Morrice, N., Meek, S., Deiting, U., Stitt, M., Scarabel, M., Aitken, A., and MacKintosh, C. 1999. Phosphorylation-dependent interactions between enzymes of plant metabolism and 14-3-3 proteins. Plant J. 18: 1-12. doi:10.1046/j.1365-313X.1999.00417.x. PMID: 10341439. (Pubitemid 29194965)
30. Muslin, A.J., Tanner, J.W., Allen, P.M., and Shaw, A.S. 1996. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell, 84: 889-897. doi:10.1016/S0092-8674(00)81067-3. PMID:8601312.
31. Roberts, M.R. 2003. 14-3-3 proteins find new partners in plant cell signaling. Trends Plant Sci. 8: 218-223. doi:10.1016/S1360-1385(03)00056-6. PMID:12758039.
32. Roxas, V.P., Smith, R.K.J., Allen, E.R., and Allen, R.D. 1997. Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat. Biotechnol. 15: 988-991. doi:10.1038/nbt1097-988. PMID:9335051.
33. Roxas, V.P., Lodhi, S.A., Garrett, D.K., Mahan, J.R., and Allen, R.D. 2000. Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol. 41: 1229-1234. doi:10.1093/pcp/pcd051. PMID:11092907.
34. Schoonheim, P.J., Veiga, H., da Costa Pereira, D., Friso, G., van Wijk, K.J., and de Boer, A.H. 2007. A comprehensive analysis of the 14-3-3 interactome in barley leaves using a complementary proteomics and two-hybrid approach. Plant Physiol. 143: 670-683. doi:10.1104/pp.106.090159. PMID:17172288. (Pubitemid 46940961)
35. Sehnke, P.C., Chung, H.-J., Wu, K., and Ferl, R.J. 2001. Regulation of starch accumulation by granule-associated plant 14-3-3 proteins. Proc. Natl. Acad. Sci. U.S.A. 98: 765-770. doi:10. 1073/pnas.021304198. PMID:11149942. (Pubitemid 32105117)
36. Shen, W., and Huber, S.C. 2006. Polycations globally enhance binding of 14-3-3u to target proteins in spinach leaves. Plant Cell Physiol. 47: 764-771. doi:10.1093/pcp/pcj050. PMID:16621845. (Pubitemid 43946306)
37. Shen, W., Clark, A.C., and Huber, S.C. 2003. The C-terminal tail of Arabidopsis 14-3-3 omega functions as an autoinhibitor and may contain a tenth alpha-helix. Plant J. 34: 473-484. doi:10. 1046/j.1365-313X.2003.01739.x. PMID:12753586. (Pubitemid 36631878)
38. Sinnige, M.P., Roobeek, I., Bunney, T.D., Visser, A.J.W.G., Mol, J.N.M., and de Boer, A.H. 2005. Single amino acid variation in barley 14-3-3 proteins leads to functional isoform specificity in the regulation of nitrate reductase. Plant J. 44: 1001-1009. doi:10.1111/j.1365-313X.2005.02599.x. PMID:16359392. (Pubitemid 43906727)
39. Stotz, H.U., Pittendrigh, B.R., Kroymann, J., Weniger, K., Fritsche, J., Bauke, A., and Mitchell-Olds, T. 2000. Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiol. 124: 1007-1017. doi:10.1104/pp.124.3.1007. PMID:11080278. (Pubitemid 30841558)
40. Su, W., Huber, S.C., and Crawford, N.M. 1996. Identification in vitro of a post-translational regulatory site in the hinge 1 region of Arabidopsis nitrate reductase. Plant Cell, 8: 519-527. doi:10. 1105/tpc.8.3.519. PMID:8721753. (Pubitemid 126635924)
41. Szopa, J. 2002. Transgenic 14-3-3 isoforms in plants: the metabolite profiling of repressed 14-3-3 protein synthesis in transgenic potato plants. Biochem. Soc. Trans. 30: 405-410. doi:10.1042/BST0300405. PMID:12196104. (Pubitemid 35001566)
42. 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. doi:10.1074/jbc.R100059200. PMID:11709560. (Pubitemid 34953163)
43. Weiner, H.K., and Kaiser, W.M. 1999. 14-3-3 proteins control proteolysis of nitrate reductase in spinach leaves. FEBS Lett. 455: 75-78. doi:10.1016/S0014-5793(99)00868-6. PMID:10428475.
44. Weiner, H., and Kaiser, W.M. 2001. Antibodies to assess phosphorylation of spinach leaf nitrate reductase on serine 543 and its binding to 14-3-3 proteins. J. Exp. Bot. 52: 1165-1172. doi:10. 1093/jexbot/52.359.1165. PMID:11432934. (Pubitemid 32646428)
45. Wilker, E.W., Grant, R.A., Artim, S.C., and Yaffe, M.B. 2005. A structural basis for 14-3-3s functional specificity. J. Biol. Chem. 280: 18891-18898. doi:10.1074/jbc.M500982200. PMID: 15731107.
46. Xu, Z., Escamilla-Treviño, L.L., Zeng, L., Lalgondar, L., Bevan, D.R., Winkel, B.S.J., Mohamed, A., Cheng, C.-L., Shih, M.-C., Poulton, J.E., and Esen, A. 2004. Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 1. Plant Mol. Biol. 55: 343-367. doi:10.1007/s11103-004-0790-1. PMID: 15604686. (Pubitemid 40660263)
47. Yan, J., He, C., Wang, J., Mao, Z., Holaday, S.A., Allen, R.D., and Zhang, H. 2004. Overexpression of the Arabidopsis 14-3-3 protein GF14 lambda in cotton leads to a "stay-green" phenotype and improves stress tolerance under moderate drought conditions. Plant Cell Physiol. 45: 1007-1014. doi:10.1093/pcp/pch115. PMID:15356326. (Pubitemid 39260278)