A plastid-localized glycogen synthase kinase 3 modulates stress tolerance and carbohydrate metabolism

Plant Journal

Volumn 49, Issue 6, 2007, Pages 1076-1090

  Kempa, Stefan ^a   Rozhon, Wilfried ^a   Šamaj, Jozef ^b,c   Erban, Alexander ^d   Baluška, František ^c   Becker, Thomas ^e   Haselmayer, Joachim ^f   Schleiff, Enrico ^e   Kopka, Joachim ^d   Hirt, Heribert ^f   Jonak, Claudia ^a  

^a GREGOR MENDEL INSTITUTE OF MOLECULAR PLANT BIOLOGY   (Austria)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

^c UNIVERSITY OF BONN   (Germany)

^d MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^e UNIVERSITY OF MUNICH   (Germany)

^f UNIVERSITY OF VIENNA   (Austria)

Author keywords

Protein phosphorylation; Signal transduction; Starch

Indexed keywords

BIODIVERSITY; CARBOHYDRATES; GLUCOSE; METABOLISM;

CARBOHYDRATE METABOLISM; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STARCH METABOLISM;

ENZYME KINETICS;

GLYCOGEN SYNTHASE KINASE 3; INORGANIC SALT; STARCH;

ARTICLE; CARBOHYDRATE METABOLISM; CHEMISTRY; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PLASTID; SIGNAL TRANSDUCTION;

CARBOHYDRATE METABOLISM; GENE EXPRESSION REGULATION, PLANT; GLYCOGEN SYNTHASE KINASE 3; METABOLIC NETWORKS AND PATHWAYS; PLASTIDS; SALTS; SIGNAL TRANSDUCTION; STARCH;

CARBOHYDRATES; GLYCOGENS; MAMMALS; METABOLISM; PLASTIDS; STARCH;

MAMMALIA; MEDICAGO SATIVA;

EID: 33847385457     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2006.03025.x     Document Type: Article

References (93)

1. Arbona, V., Marco, A.J., Iglesias, D.J., López-Climent, M.F., Talon, M. and Gómez-Cadenas, A. (2005) Carvohydrate depletion in roots and leaves of salt-stressed potted Citrus clementina L. Plant Growth Regul. 46, 153-160.
2. Balibrea, M.E., Rus-Alvarez, A.M., Bolarín, M.C. and Pérez-Alfocea, F. (1997) Fast changes in soluble carbohydrates and proline contents in tomato seedlings in response to ionic and non-ionic iso-osmotic stresses. J. Plant Physiol. 151, 221-226.
3. Bécard, G. and Fortin, J.A. (1988) Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol. 108, 211-218.
4. Bohnert, H.J. and Sheveleva, E. (1998) Plant stress adaptations - making metabolism move. Curr. Opin. Plant Biol. 1, 267-274.
5. Boisson-Dernier, A., Chabaud, M., Garcia, F., Becard, G., Rosenberg, C. and Barker, D.G. (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen- fixing and endomycorrhizal symbiotic associations. Mol. Plant-Microbe Interact. 14, 695-700.
6. Boudsocq, M., Barbier-Brygoo, H. and Lauriere, C. (2004) Identification of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. J. Biol. Chem. 279, 41758-41766.
7. Boyer, J.S. (1982) Plant productivity and environment. Science, 218, 443-448.
8. Castonguay, Y. and Nadeau, P. (1998) Enzymatic control of soluble carbohydrate accumulation in cold-acclimated crowns of alfalfa. Crop Sci. 38, 1183-1189.
9. Chia, T., Thorneycroft, D., Chapple, A., Messerli, G., Chen, J., Zeeman, S.C., Smith, S.M. and Smith, A.M. (2004) A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant J. 37, 853-863.
10. Choe, S., Schmitz, R.J., Fujioka, S., Takatsuto, S., Lee, M.O., Yoshida, S., Feldmann, K.A. and Tax, F.E. (2002) Arabidopsis brassinosteroid-insensitive dwarf12 mutants are semidominant and defective in a glycogen synthase kinase 3beta-like kinase. Plant Physiol. 130, 1506-1515.
11. 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.
12. Cohen, P. and Frame, S. (2001) The renaissance of GSK3. Nature Rev. Mol. Cell Biol. 2, 769-776.
13. Cook, D., Fowler, S., Fiehn, O. and Thomashow, M.F. (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc. Natl Acad. Sci. USA, 101, 15243-15248.
14. Debnam, P.M., Fernie, A.R., Leisse, A., Golding, A., Bowsher, C.G., Grimshaw, C., Knight, J.S. and Emes, M.J. (2004) Altered activity of the P2 isoform of plastidic glucose 6-phosphate dehydrogenase in tobacco (Nicotiana tabacum cv. Samsun) causes changes in carbohydrate metabolism and response to oxidative stress in leaves. Plant J. 38, 49-59.
15. Doble, B.W. and Woodgett, J.R. (2003) GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 116, 1175-1186.
16. Dornelas, M.C., Van Lammeren, A.A. and Kreis, M. (2000) Arabidopsis thaliana SHAGGY-related protein kinases (AtSK11 and 12) function in perianth and gynoecium development. Plant J. 21, 419-429.
17. Droillard, M.J., Thibivilliers, S., Cazale, A.C., Barbier-Brygoo, H. and Lauriere, C. (2000) Protein kinases induced by osmotic stresses and elicitor molecules in tobacco cell suspensions: two crossroad MAP kinases and one osmoregulation-specific protein kinase. FEBS Lett. 474, 217-222.
18. Embi, N., Rylatt, D.B. and Cohen, P. (1980) Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase. Eur. J. Biochem. 107, 519-527.
19. Fernandez-Sanchez, M.E., Criado-Garcia, O., Heath, K.E., Garcia-Fojeda, B., Medrano-Fernandez, I., Gomez-Garre, P., Sanz, P., Serratosa, J.M. and Rodriguez de Cordoba, S. (2003) Laforin, the dual-phosphatase responsible for Lafora disease, interacts with R5 (PTG), a regulatory subunit of protein phosphatase-1 that enhances glycogen accumulation. Hum. Mol. Genet. 12, 3161-3171.
20. Fiehn, O., Kopka, J., Dormann, P., Altmann, T., Trethewey, R.N. and Willmitzer, L. (2000) Metabolite profiling for plant functional genomics. Nature Biotechnol. 18, 1157-1161.
21. Fougere, F., Le Rudulier, D. and Streeter, J.G. (1991) Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids, and cytosol of alfalfa (Medicago sativa L.). Plant Physiol. 96, 1228-1236.
22. Geigenberger, P., Reimholz, H., Geiger, M., Merlo, M., Canale, V. and Stitt, M. (1997) Regulation of sucrose and starch metabolism in potato tubers in response to short-term water deficit. Planta, 201, 502-518.
23. Gilbert, G.A., Wilson, C. and Madore, M.A. (1997) Root-zone salinity alters raffinose oligosaccharide metabolism and transport in coleus. Plant Physiol. 115, 1267-1276.
24. Hasegawa, P., Bressan, R., Zhu, J.K. and Bohnert, H. (2000) Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 463-499.
25. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S. and Mullineaux, P.M. (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819-832.
26. Hoyos, M.E. and Zhang, S. (2000) Calcium-independent activation of salicylic acid-induced protein kinase and a 40-kilodalton protein kinase by hyperosmotic stress. Plant Physiol. 122, 1355-1363.
27. Ichimura, K., Mizoguchi, T., Yoshida, R., Yuasa, T. and Shinozaki, K. (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J. 24, 655-665.
28. Jonak, C. and Hirt, H. (2002) Glycogen synthase kinase 3/SHAGGY-like kinases in plants: an emerging family with novel functions. Trends Plant Sci. 7, 457-461.
29. Jonak, C., Heberle-Bors, E. and Hirt, H. (1995) Inflorescence-specific expression of AtK-1, a novel Arabidopsis thaliana homologue of shaggy/glycogen synthase kinase-3. Plant Mol. Biol. 27, 217-221.
30. Jonak, C., Beisteiner, D., Beyerly, J. and Hirt, H. (2000) Wound-induced expression and activation of WIG, a novel glycogen synthase kinase 3. Plant Cell, 12, 1467-1476.
31. Jope, R.S. and Johnson, G.V. (2004) The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci. 29, 95-102.
32. Jouve, L., Hoffmann, L. and Hausman, J.F. (2004) Polyamine, carbohydrate, and proline content changes during salt stress exposure of aspen (Populus tremula L.): involvement of oxidation and osmoregulation metabolism. Plant Biol. 6, 74-80.
33. Kaplan, F. and Guy, C.L. (2004) β-Amylase induction and the protective role of maltose during temperature shock. Plant Physiol. 135, 1674-1684.
34. Kaplan, F. and Guy, C.L. (2005) RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J. 44, 730-743.
35. Kaplan, F., Kopka, J., Haskell, D.W., Zhao, W., Schiller, K.C., Gatzke, N., Sung, D.Y. and Guy, C.L. (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol. 136, 4159-4168.
36. Kawasaki, S., Borchert, C., Deyholos, M., Wang, H., Brazille, S., Kawai, K., Galbraith, D. and Bohnert, H.J. (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell, 13, 889-905.
37. Kerk, D., Conley, T.R., Rodriguez, F.A., Tran, H.T., Nimick, M., Muench, D.G. and Moorhead, G.B. (2006) A chloroplast-localized dual-specificity protein phosphatase in Arabidopsis contains a phylogenetically dispersed and ancient carbohydrate-binding domain, which binds the polysaccharide starch. Plant J. 46, 400-413.
38. Kiegerl, S., Cardinale, F., Siligan, C. et al. (2000) SIMKK, a mitogen-activated protein kinase (MAPK) kinase, is a specific activator of the salt stress-induced MAPK, SIMK. Plant Cell, 12, 2247-2258.
39. Kopka, J., Schauer, N., Krueger, S. et al. (2005) GMD@CSB.DB: the Golm metabolome database. Bioinformatics, 21, 1635-1638.
40. Kotting, O., Pusch, K., Tiessen, A., Geigenberger, P., Steup, M. and Ritte, G. (2005) Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiol. 137, 242-252.
41. Li, J. and Nam, K.H. (2002) Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science, 295, 1299-1301.
42. Liska, A.J., Shevchenko, A., Pick, U. and Katz, A. (2004) Enhanced photosynthesis and redox energy production contribute to salinity tolerance in Dunaliella as revealed by homology-based proteomics. Plant Physiol. 136, 2806-2817.
43. Lloyd, J.R., Kossmann, J. and Ritte, G. (2005) Leaf starch degradation comes out of the shadows. Trends Plant Sci. 10, 130-137.
44. Lohi, H., Ianzano, L., Zhao, X.C., Chan, E.M., Turnbull, J., Scherer, S.W., Ackerley, C.A. and Minassian, B.A. (2005) Novel glycogen synthase kinase 3 and ubiquitination pathways in progressive myoclonus epilepsy. Hum. Mol. Genet. 14, 2727-2736.
45. Lorberth, R., Ritte, G., Willmitzer, L. and Kossmann, J. (1998) Inhibition ofastarch-granule-bound protein leads to modified starch and repression of cold sweetening. Nature Biotechnol. 16, 473-477.
46. Lu, Y. and Sharkey, T.D. (2004) The role of amylomaltase in maltose metabolism in the cytosol of photosynthetic cells. Planta, 218, 466-473.
47. Matsuoka, D., Nanmori, T., Sato Ki, K., Fukami, Y., Kikkawa, U. and Yasuda, T. (2002) Activation of AtMEK1, an Arabidopsis mitogen-activated protein kinase kinase, in vitro and in vivo: analysis of active mutants expressed in E. coli and generation of the active form in stress response in seedlings. Plant J. 29, 637-647.
48. Mikkelsen, R. and Blennow, A. (2005) Functional domain organization of the potato alpha-glucan, water dikinase (GWD): evidence for separate site catalysis as revealed by limited proteolysis and deletion mutants. Biochem. J. 385, 355-361.
49. Mikolajczyk, M., Awotunde, O.S., Muszynska, G., Klessig, D.F. and Dobrowolska, G. (2000) Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. Plant Cell, 12, 165-178.
50. Morsy, M.R., Jouve, L., Hausman, J.F., Hoffmann, L. and Stewart, J.M. (2006) Alteration of oxidative and carbohydrate metabolism under abiotic stress in two rice (Oryza sativa L.) genotypes contrasting in chilling tolerance. J. Plant Physiol. 2006 Feb 23; [Epub ahead of print].
51. Mu-Forster, C., Huang, R., Powers, J.R., Harriman, R.W., Knight, M., Singletary, G.W., Keeling, P.L. and Wasserman, B.P. (1996) Physical association of starch biosynthetic enzymes with starch granules of maize endosperm. Granule-associated forms of starch synthase I and starch branching enzyme II. Plant Physiol. 111, 821-829.
52. Munnik, T., Ligterink, W., Meskiene, I., Calderini, O., Beyerly, J., Musgrave, A. and Hirt, H. (1999) Distinct osmo-sensing protein kinase pathways are involved in signalling moderate and severe hyper-osmotic stress. Plant J. 20, 381-388.
53. Munns, R. (2002) Comparative physiology of salt and water stress. Plant Cell Environ. 25, 239-250.
54. Ndimba, B.K., Chivasa, S., Simon, W.J. and Slabas, A.R. (2005) Identification of Arabidopsis salt and osmotic stress responsive proteins using two-dimensional difference gel electrophoresis and mass spectrometry. Proteomics, 5, 4185-4196.
55. Niittyla, T., Messerli, G., Trevisan, M., Chen, J., Smith, A.M. and Zeeman, S.C. (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science, 303, 87-89.
56. Niittyla, T., Comparot-Moss, S., Lue, W.L. et al. (2006) Similar protein phosphatases control starch metabolism in plants and glycogen metabolism in mammals. J. Biol. Chem. 281, 11815- 11818.
57. Oparka, K.J. and Wright, K.M. (1988) Osmotic regulation of starch synthesis in potato tubers. Planta, 174, 123-126.
58. Pay, A., Jonak, C., Bogre, L., Meskiene, I., Mairinger, T., Szalay, A., Heberle-Bors, E. and Hirt, H. (1993) The MsK family of alfalfa protein kinase genes encodes homologues of shaggy/glycogen synthase kinase-3 and shows differential expression patterns in plant organs and development. Plant J. 3, 847-856.
59. Perez-Perez, J.M., Ponce, M.R. and Micol, J.L. (2002) The UCU1 Arabidopsis gene encodes a SHAGGY/GSK3-like kinase required for cell expansion along the proximodistal axis. Dev. Biol. 242, 161-173.
60. Piao, H.L., Pih, K.T., Lim, J.H., Kang, S.G., Jin, J.B., Kim, S.H. and Hwang, I. (1999) An Arabidopsis GSK3/shaggy-like gene that complements yeast salt stress-sensitive mutants is induced by NaCl and abscisic acid. Plant Physiol. 119, 1527-1534.
61. Piao, H.L., Lim, J.H., Kim, S.J., Cheong, G.W. and Hwang, I. (2001) Constitutive over-expression of AtGSK1 induces NaCl stress responses in the absence of NaCl stress and results in enhanced NaCl tolerance in Arabidopsis. Plant J. 27, 305-314.
62. Qbadou, S., Tien, R., Soll, J. and Schleiff, E. (2003) Membrane insertion of the chloroplast outer envelope protein, Toc34: constrains for insertion and topology. J. Cell Sci. 116, 837-846.
63. Ritte, G., Lorberth, R. and Steup, M. (2000) Reversible binding of the starch-related R1 protein to the surface of transitory starch granules. Plant J. 21, 387-391.
64. Ritte, G., Lloyd, J.R., Eckermann, N., Rottmann, A., Kossmann, J. and Steup, M. (2002) The starch-related R1 protein is an alpha-glucan, water dikinase. Proc. Natl Acad. Sci. USA, 99, 7166-7171.
65. Rivett, A.J., Palmer, A. and Knecht, E. (1992) Electron microscopic localization of the multicatalytic proteinase complex in rat liver and in cultured cells. J. Histochem. Cytochem. 40, 1165-1172.
66. Rongine De Fekete, M.A., Leloir, L.F. and Cardini, C.E. (1960) Mechanism of starch biosynthesis. Nature, 187, 918-919.
67. Schauer, N., Steinhauser, D., Strelkov, S. et al. (2005) GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett. 579, 1332-1337.
68. Scheidig, A., Frohlich, A., Schulze, S., Lloyd, J.R. and Kossmann, J. (2002) Downregulation of a chloroplast-targeted beta-amylase leads to a starch-excess phenotype in leaves. Plant J. 30, 581-591.
69. Schleiff, E., Tien, R., Salomon, M. and Soll, J. (2001) Lipid composition of outer leaflet of chloroplast outer envelope determines topology of OEP7. Mol. Biol. Cell, 12, 4090-4102.
70. Seki, M., Narusaka, M., Ishida, J. et al. (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31, 279-292.
71. Smith, A.M. (2001) The biosynthesis of starch granules. Biomacromolecules, 2, 335-341.
72. Smith, A.M., Zeeman, S.C. and Smith, S.M. (2005) Starch degradation. Annu. Rev. Plant Biol. 56, 73-97.
73. Sokolov, L.N., Dominguez-Solis, J.R., Allary, A.L., Buchanan, B.B. and Luan, S. (2006) A redox-regulated chloroplast protein phosphatase binds to starch diurnally and functions in its accumulation. Proc. Natl Acad. Sci. USA, 103, 9732-9737.
74. Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M., Yamaguchi-Shinozaki, K. and Shinozaki, K. (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 29, 417-426.
75. Teige, M., Scheikl, E., Eulgem, T., Doczi, R., Ichimura, K., Shinozaki, K., Dangl, J.L. and Hirt, H. (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol. Cell, 15, 141-152.
76. Tetlow, I.J., Morell, M.K. and Emes, M.J. (2004a) Recent developments in understanding the regulation of starch metabolism in higher plants. J. Exp. Bot. 55, 2131-2145.
77. Tetlow, I.J., Wait, R., Lu, Z., Akkasaeng, R., Bowsher, C.G., Esposito, S., Kosar-Hashemi, B., Morell, M.K. and Emes, M.J. (2004b) Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein-protein interactions. Plant Cell, 16, 694-708.
78. Todaka, D., Matsushima, H. and Morohashi, Y. (2000) Water stress enhances beta-amylase activity in cucumber cotyledons. J. Exp. Bot. 51, 739-745.
79. Umezawa, T., Yoshida, R., Maruyama, K., Yamaguchi-Shinozaki, K. and Shinozaki, K. (2004) SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 101, 17306-17311.
80. Vert, G. and Chory, J. (2006) Downstream nuclear events in brassinosteroid signalling. Nature, 441, 96-100.
81. Wagner, C., Sefkow, M. and Kopka, J. (2003) Construction and application of a mass spectral and retention time index database generated from plant GC/EI-TOF-MS metabolite profiles. Phytochemistry, 62, 887-900.
82. Weber, A.P. (2004) Solute transporters as connecting elements between cytosol and plastid stroma. Curr. Opin. Plant Biol. 7, 247-253.
83. Weber, A., Servaites, J.C., Geiger, D.R., Kofler, H., Hille, D., Groner, F., Hebbeker, U. and Flugge, U.I. (2000) Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell, 12, 787-802.
84. Weise, S.E., Weber, A.P. and Sharkey, T.D. (2004) Maltose is the major form of carbon exported from the chloroplast at night. Planta, 218, 474-482.
85. Woodgett, J.R. and Cohen, P. (1984) Multisite phosphorylation of glycogen synthase. Molecular basis for the substrate specificity of glycogen synthase kinase-3 and casein kinase-II (glycogen synthase kinase-5). Biochim. Biophys. Acta, 788, 339-347.
86. Xiong, L., Schumaker, K.S. and Zhu, J.K. (2002) Cell signaling during cold, drought, and salt stress. Plant Cell, 14, S165-S183.
87. Yancey, P.H. (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208, 2819-2830.
88. Yano, R., Nakamura, M., Yoneyama, T. and Nishida, I. (2005) Starch-related alpha-glucan/water dikinase is involved in the cold-induced development of freezing tolerance in Arabidopsis. Plant Physiol. 138, 837-846.
89. Yu, T.S., Kofler, H., Hausler, R.E. et al. (2001) The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell, 13, 1907-1918.
90. Zenner, R. and Stitt, M. (1991) Comparison of the effect of rapidly and gradually developing water-stress on carbohydrate metabolism in spinach leaves. Plant Cell Environ. 14, 939-946.
91. Zhu, J.K. (2001) Plant salt tolerance. Trends Plant Sci. 6, 66-71.
92. Zhu, J.K. (2002) Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247-273.
93. Zhu, J.K., Liu, J. and Xiong, L. (1998) Genetic analysis of salt tolerance in Arabidopsis. Evidence for a critical role of potassium nutrition. Plant Cell, 10, 1181-1191.