Soybean MAPK, GMK1 is dually regulated by phosphatidic acid and hydrogen peroxide and translocated to nucleus during salt stress

Molecules and Cells

Volumn 34, Issue 3, 2012, Pages 271-278

  Im, Jong Hee ^a   Lee, Hyoungseok ^a,b   Kim, Jitae ^a,c   Kim, Ho Bang ^a,d   An, Chung Sun ^a  

^a Seoul National University   (South Korea)

^b Korea Polar Research Institute (KOPRI)   (South Korea)

^c Department of Obstetrics Gynecology   (United States)

^d Life Sciences Research Institute   (South Korea)

Author keywords

GMK1; Hydrogen peroxide; Phosphatidic acid; Salt stress; Soybean

Indexed keywords

DIPHENYLIODONIUM SALT; ENZYME; GMK1; HYDROGEN PEROXIDE; MACROGOL; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PHOSPHATIDIC ACID; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; IMMUNOLOCALIZATION; IMMUNOPRECIPITATION; PLANT SEED; PROTEIN EXPRESSION; PROTOPLAST; PROTOPLAST ISOLATION; RESPIRATORY BURST; SALT STRESS; SIGNAL TRANSDUCTION; SOYBEAN; YEAST CELL;

CELL NUCLEUS; HYDROGEN PEROXIDE; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDIC ACIDS; PLANT PROTEINS; PLANT ROOTS; PROTEIN TRANSPORT; REACTIVE OXYGEN SPECIES; SODIUM CHLORIDE; SOYBEANS; STRESS, PHYSIOLOGICAL; TIME FACTORS;

GLYCINE MAX;

EID: 84870378359     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.1007/s10059-012-0092-4     Document Type: Article

References (49)

1. Ahlfors, R., Macioszek, V., Rudd, J., Brosche, M., Schlichting, R., Scheel, D., and Kangasjarvi, J. (2004). Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J. 40, 512-522.
2. Alvarez, M.E., Pennell, R.I., Meijer, P.J., Ishikawa, A., Dixon, R.A., and Lamb, C. (1998). Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773-784.
3. An, L.Z., Yang, Y.L., Xua, S.J., and Chen, N.L. (2007). NADPH oxidase-dependent hydrogen peroxide production, induced by salinity stress, may be involved in the regulation of total calcium in roots of wheat. J. Plant Physiol. 164, 1429-1435.
4. Asai, S., Ohta, K., and Yoshioka, H. (2008). MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell 20, 1390-1406.
5. Balestrasse, K.B., Zilli, C.G., and Tomaro, M.L. (2008). Signal transduction pathways and haem oxygenase induction in soybean leaves subjected to salt stress. Redox Rep. 13, 255-262.
6. Broughton, W.J., and Dilworth, M.J. (1971). Control of leghaemoglobin synthesis in snake beans. Biochem. J. 125, 1075-1080.
7. Coronado, M.J., Gonzalez-Melendi, P., Segui, J.M., Ramirez, C., Barany, I., Testillano, P.S., and Risueno, M.C. (2002). MAPKs entry into the nucleus at specific interchromatin domains in plant differentiation and proliferation processes. J. Struct. Biol. 140, 200-213.
8. Dat, J.F., Lopez-Delgado, H., Foyer, C.H., and Scott, I.M. (1998). Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol. 116, 1351-1357.
9. Delledonne, M., Zeier, J., Marocco, A., and Lamb, C. (2001). Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl. Acad. Sci. USA 98, 13454-13459.
10. Farooq, A., and Zhou, M.M. (2004). Structure and regulation of MAPK phosphatases. Cell. Signal. 16, 769-779.
11. Fernandez-Pascual, M., Lucas, M.M., de Felipe, M.R., Bosca, L., Hirt, H., and Golvano, M.P. (2006). Involvement of mitogen-activated protein kinases in the symbiosis Bradyrhizobium-Lupinus. J. Exp. Bot. 57, 2735-2742.
12. Foyer, C.H., and Noctor, G. (2005). Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell 17, 1866-1875.
13. Gupta, R., Huang, Y., Kieber, J., and Luan, S. (1998). Identification of a dual-specificity protein phosphatase that inactivates a MAP kinase from Arabidopsis. Plant J. 16, 581-589.
14. Im, J.H., Lee, H., Kim, J., Kim, H.B., Kim, S., Kim, B.M., and An, C.S. (2012). A salt stress-activated mitogen-activated protein kinase in soybean is regulated by phosphatidic acid in early stages of the stress response. J. Plant Biol. 55, 303-309.
15. Jiang, M.Y., Zhang, A.Y., Zhang, J.H., Tan, M.P., and Hu, X.L. (2006). Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol. 141, 475-487.
16. Katsuhara, M., Otsuka, T., and Ezaki, B. (2005). Salt stress-induced lipid peroxidation is reduced by glutathione S-transferase, but this reduction of lipid peroxides is not enough for a recovery of root growth in Arabidopsis. Plant Sci. 169, 369-373.
17. Lee, S., Hirt, H., and Lee, Y. (2001). Phosphatidic acid activates a wound-activated MAPK in Glycine max. Plant J. 26, 479-486.
18. Lee, J., Rudd, J.J., Macioszek, V.K., and Scheel, D. (2004). Dynamic changes in the localization of MAPK cascade components controlling pathogenesis-related (PR) gene expression during innate immunity in parsley. J. Biol. Chem. 279, 22440-22448.
19. Lee, H., Kim, J., Im, J.H., Kim, H.B., Oh, C.J., and An, C.S. (2008). Mitogen-activated protein kinase is involved in the symbiotic interaction between Bradyrhizobium japonicum USDA110 and soybean. J. Plant Biol. 51, 291-296.
20. Lee, B.H., Alam, I., Sharmin, S.A., Kim, K.H., Yang, J.K., and Choi, M.S. (2010) Proteome analysis of soybean roots subjected to short-term drought stress. Plant Soil 333, 491-505.
21. Levine, A., Leshem, Y., and Seri, L. (2007). Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J. 51, 185-197.
22. Liu, J.Z., Horstman, H.D., Braun, E., Graham, M.A., Zhang, C.Q., Navarre, D., Qiu, W.L., Lee, Y., Nettleton, D., Hill, J.H., et al. (2011). Soybean homologs of MPK4 negatively regulate defense responses and positively regulate growth and development. Plant Physiol. 157, 1363-1378.
23. Misra, H.P., and Fridovich, I. (1977). Superoxide-dismutase and peroxidase-positive activity stain applicable to polyacrylamidegel electropherograms. Arch. Biochem. Biophys. 183, 511-515.
24. Nakagami, H., Kiegerl, S., and Hirt, H. (2004). OMTK1, a novel MAPKKK, channels oxidative stress signaling through direct MAPK interaction. J. Biol. Chem. 279, 26959-26966.
25. Neill, S., Desikan, R., and Hancock, J. (2002). Hydrogen peroxide signalling. Curr. Opin. Plant Biol. 5, 388-395.
26. Nishizuka Y. (1995). Protein kinase C and lipid signaling for sustained cellular responses. FASEB J. 9, 484-496.
27. Ogasawara, Y., Kaya, H., Hiraoka, G., Yumoto, F., Kimura, S., Kadota, Y., Hishinuma, H., Senzaki, E., Yamagoe, S., Nagata, K., et al. (2008). Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J. Biol. Chem. 283, 8885-8892.
28. Pitzschke, A., and Hirt, H. (2006). Mitogen-activated protein kinases and reactive oxygen species signaling in plants. Plant Physiol. 141, 351-356.
29. Pitzschke, A., and Hirt, H. (2009). Disentangling the complexity of mitogen-activated protein kinases and reactive oxygen species signaling. Plant Physiol. 149, 606-615.
30. Plotnikov, A., Zehorai, E., Procaccia, S., and Seger, R. (2011). The MAPK cascades: Signaling components, nuclear roles and mechanisms of nuclear translocation. BBA-Mol. Cell Res. 1813, 1619-1633.
31. Raho, N., Ramirez, L., Lanteri, M.L., Gonorazky, G., Lamattina, L., ten Have, A., and Laxalt, A.M. (2011). Phosphatidic acid production in chitosan-elicited tomato cells, via both phospholipase D and phospholipase C/diacylglycerol kinase, requires nitric oxide. J. Plant Physiol. 168, 534-539.
32. Reichheld, J.P., Vernoux, T., Lardon, F., Van Montagu, M., and Inze, D. (1999). Specific checkpoints regulate plant cell cycle progression in response to oxidative stress. Plant J. 17, 647-656.
33. Rentel, M.C., Lecourieux, D., Ouaked, F., Usher, S.L., Petersen, L., Okamoto, H., Knight, H., Peck, S.C., Grierson, C.S., Hirt, H., et al. (2004). OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427, 858-861.
34. Samaj, J., Ovecka, M., Hlavacka, A., Lecourieux, F., Meskiene, I., Lichtscheidl, I., Lenart, P., Salaj, J., Volkmann, D., Bogre, L., et al. (2002). Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip growth. EMBO J. 21, 3296-3306.
35. Takahashi, F., Mizoguchi, T., Yoshida, R., Ichimura, K., and Shinozaki, K. (2011). Calmodulin-dependent activation of MAP kinase for ROS homeostasis in Arabidopsis. Mol. Cell 41, 649-660.
36. Tester, M., and Davenport, R. (2003). Na(+) tolerance and Na(+) transport in higher plants. Ann. Bot. 91, 503-527.
37. Torres, M.A., and Dangl, J.L. (2005). Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr. Opin. Plant Biol. 8, 397-403.
38. Ulm, R., Ichimura, K., Mizoguchi, T., Peck, S.C., Zhu, T., Wang, X., Shinozaki, K., and Paszkowski, J. (2002). Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO J. 21, 6483-6493.
39. Xia, X.J., Wang, Y.J., Zhou, Y.H., Tao, Y., Mao, W.H., Shi, K., Asami, T., Chen, Z.X., and Yu, J.Q. (2009). Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol. 150, 801-814.
40. Yamamizo, C., Kuchimura, K., Kobayashi, A., Katou, S., Kawakita, K., Jones, J.D.G., Doke, N., and Yoshioka, H. (2006). Rewiring mitogen-activated protein kinase cascade by positive feedback confers potato blight resistance. Plant Physiol. 140, 681-692.
41. Yang, Y.L., Xua, S.J., An, L.Z., and Chen, N.L. (2007). NADPH oxidase-dependent hydrogen peroxide production, induced by salinity stress, may be involved in the regulation of total calcium in roots of wheat. J. Plant Physiol. 164, 1429-1435.
42. Yang, K.Y., Liu, Y.D., and Zhang, S.Q. (2001). Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl. Acad. Sci. USA 98, 741-746.
43. 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.
44. Yoshioka, H., Asai, S., Yoshioka, M., and Kobayashi, M. (2009). Molecular mechanisms of generation for nitric oxide and reactive oxygen species, and role of the radical burst in plant immunity. Mol. Cells 28, 321-329.
45. Yoshioka, H., Sugie, K., Park, H.J., Maeda, H., Tsuda, N., Kawakita, K., and Doke, N. (2001) Induction of plant gp91 phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Mol. Plant Microbe Interact. 14, 725-736.
46. Yu, L., Nie, J., Cao, C., Jin, Y., Yan, M., Wang, F., Liu, J., Xiao, Y., Liang, Y., and Zhang, W. (2010). Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol. 188, 762-773.
47. Zhang, W.H., Wang, C.X., Qin, C.B., Wood, T., Olafsdottir, G., Welti, R., and Wang, X.M. (2003). The oleate-stimulated phospholipase D, PLD delta, and phosphatidic acid decrease H2O2-induced cell death in arabidopsis. Plant Cell 15, 2285-2295.
48. Zhang, A.Y., Jiang, M.Y., Zhang, J.H., Tan, M.P., and Hu, X.L. (2006). Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol. 141, 475-487.
49. Zhang, Y., Zhu, H., Zhang, Q., Li, M., Yan, M., Wang, R., Wang, L., Welti, R., Zhang, W., and Wang, X. (2009). Phospholipase D alpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21, 2357-2377.