Salt Stress in arabidopsis: Lipid transfer protein AZI1 and its control by mitogen-activated protein Kinase MPK3

Molecular Plant

Volumn 7, Issue 4, 2014, Pages 722-738

  Pitzschke, Andrea ^a   Datta, Sneha ^a   Persak, Helene ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

Arabidopsis; AZI1; in vivo interaction.; lipid transfer protein; MAPK; MPK3; phosphorylation; salt stress

Indexed keywords

ARABIDOPSIS PROTEIN; ATMPK3 PROTEIN, ARABIDOPSIS; AZI1 PROTEIN, ARABIDOPSIS; MITOGEN ACTIVATED PROTEIN KINASE KINASE; SODIUM CHLORIDE;

ARABIDOPSIS; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PHOSPHORYLATION; SODIUM CHLORIDE;

EID: 84898721686     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sst157     Document Type: Article

References (84)

1. Andreasson, E., and Ellis, B. (2010). Convergence and specificity in the Arabidopsis MAPK nexus. Trends Plant Sci. 15, 106-113.
2. Arisz, S.A., van Wijk, R., Roels, W., Zhu, J.K., Haring, M.A., and Munnik, T. (2013). Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase. Frontiers in Plant Science. 4, 1.
3. Atkinson, N.J., and Urwin, P.E. (2012). The interaction of plant biotic and abiotic stresses: from genes to the field. J. Exp. Bot. 63, 3523-3543.
4. Ballif, B.A., and Blenis, J. (2001). Molecular mechanisms mediating mammalian mitogen-activated protein kinase (MAPK) kinase (MEK)-MAPK cell survival signals. Cell Growth & Differentiation: The Molecular Biology Journal of the American Association for Cancer Research. 12, 397-408.
5. Beck, M., Komis, G., Muller, J., Menzel, D., and Samaj, J. (2010). Arabidopsis homologs of nucleus- and phragmoplast-localized kinase 2 and 3 and mitogen-activated protein kinase 4 are essential for microtubule organization. Plant Cell. 22, 755-771.
6. Beck, M., Komis, G., Ziemann, A., Menzel, D., and Samaj, J. (2011). Mitogen-activated protein kinase 4 is involved in the regulation of mitotic and cytokinetic microtubule transitions in Arabidopsis thaliana. The New Phytologist. 189, 1069-1083.
7. Beckers, G.J., Jaskiewicz, M., Liu, Y., Underwood, W.R., He, S.Y., Zhang, S., and Conrath, U. (2009). Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell. 21, 944-953.
8. Blanco-Portales, R., Lopez-Raez, J.A., ellido, M.L., Moyano, E., Dorado, G., Gonzalez-Reyes, J.A., Caballero, J.L., and Munoz- Blanco, J. (2004). A strawberry fruit-specific and ripeningrelated gene codes for a HyPRP protein involved in polyphenol anchoring. Plant Mol. Biol. 55, 763-780.
9. Brock, A.K., Willmann, R., Kolb, D., Grefen, L., Lajunen, H.M., Bethke, G., Lee, J., Nurnberger, T., and Gust, A.A. (2010). The Arabidopsis mitogen-activated protein kinase phosphatase PP2C5 affects seed germination, stomatal aperture, and abscisic acid-inducible gene expression. Plant Physiol. 153, 1098-1111.
10. Buhot, N., et al. (2001). A lipid transfer protein binds to a receptor involved in the control of plant defence responses. FEBS Lett. 509, 27-30.
11. Cameron, K.D., Teece, M.A., and Smart, L.B. (2006). Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco. Plant Physiol. 140, 176-183.
12. Carvalho, A.d.O., and Gomes, V.M. (2007). Role of plant lipid transfer proteins in plant cell physiology: a concise review. Peptides. 28, 1144-1153.
13. 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.
14. Colcombet, J., and Hirt, H. (2008). Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem. J. 413, 217-226.
15. Djamei, A., Pitzschke, A., Nakagami, H., Rajh, I., and Hirt, H. (2007). Trojan horse strategy in Agrobacterium transformation: abusing MAPK defense signaling. Science. 318, 453-456.
16. Dvorakova, L., Srba, M., Opatrny, Z., and Fischer, L. (2012). Hybrid proline-rich proteins: novel players in plant cell elongation? Annals Bot. (Lond.). 109, 453-462.
17. Ezhova, T.A., Soldatova, O.P., Mamanova, L.B., Musin, S.M., Grimm, B., and Shestakov, S.V. (2001). [Collection of Arabidopsis thaliana mutants with altered sensitivity to oxidative stress inductors]. Izvestiia Akademii nauk. Seriia biologicheskaia/Rossiiskaia akademiia nauk., 533-543.
18. Fernandez-Calvino, L., Faulkner, C., Walshaw, J., Saalbach, G., Bayer, E., Benitez-Alfonso, Y., and Maule, A. (2011). Arabidopsis plasmodesmal proteome. PloS One. 6, e18880.
19. Gechev, T.S., Dinakar, C., Benina, M., Toneva, V., and Bartels, D. (2012). Molecular mechanisms of desiccation tolerance in resurrection plants. Cell Mol. Life Sci. 69, 3175-3186.
20. Heazlewood, J.L., Verboom, R.E., Tonti-Filippini, J., Small, I., and Millar, A.H. (2007). SUBA: the Arabidopsis Subcellular Database. Nucleic Acids Res. 35, D213-D218.
21. Hijazi, M., Durand, J., Pichereaux, C., Pont, F., Jamet, E., and Albenne, C. (2012). Characterization of the arabinogalactan protein 31 (AGP31) of Arabidopsis thaliana: new advances on the Hyp-O-glycosylation of the Pro-rich domain. J. Biol. Chem. 287, 9623-9632.
22. Hollenbach, B., Schreiber, L., Hartung, W., and Dietz, K.J. (1997). Cadmium leads to stimulated expression of the lipid transfer protein genes in barley: implications for the involvement of lipid transfer proteins in wax assembly. Planta. 203, 9-19.
23. Hong, Z., Jin, H., Tzfira, T., and Li, J. (2008). Multiple mechanismmediated retention of a defective brassinosteroid receptor in the endoplasmic reticulum of Arabidopsis. Plant Cell. 20, 3418-3429.
24. Huang, G.T., Ma, S.L., Bai, L.P., Zhang, L., Ma, H., Jia, P., Liu, J., Zhong, M., and Guo, Z.F. (2012). Signal transduction during cold, salt, and drought stresses in plants. Mol. Biol. Rep. 39, 969-987.
25. Joo, S., Liu, Y., Lueth, A., and Zhang, S. (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.
26. Jose-Estanyol, M., Gomis-Ruth, F.X., and Puigdomenech, P. (2004). The eight-cysteine motif, a versatile structure in plant proteins. Plant Physiology and Biochemistry: PPB/Societe francaise de physiologie vegetale. 42, 355-365.
27. Jung, H.W., Tschaplinski, T.J., Wang, L., Glazebrook, J., and Greenberg, J.T. (2009). Priming in systemic plant immunity. Science. 324, 89-91.
28. Kant, P., Gordon, M., Kant, S., Zolla, G., Davydov, O., Heimer, Y.M., Chalifa-Caspi, V., Shaked, R., and Barak, S. (2008). Functional-genomics-based identification of genes that regulate Arabidopsis responses to multiple abiotic stresses. Plant, Cell & Environment. 31, 697-714.
29. Kim, S.H., Woo, D.H., Kim, J.M., Lee, S.Y., Chung, W.S., and Moon, Y.H. (2011). Arabidopsis MKK4 mediates osmotic-stress response via its regulation of MPK3 activity. Biochem. Biophys. Res. Commun. 412, 150-154.
30. Kohorn, B.D., Kohorn, S.L., Todorova, T., Baptiste, G., Stansky, K., and McCullough, M. (2012). A dominant allele of Arabidopsis pectinbinding wall-associated kinase induces a stress response suppressed by MPK6 but not MPK3 mutations. Mol. Plant. 5, 841-851.
31. Krishnaswamy, S., Verma, S., Rahman, M.H., and Kav, N.N. (2011). Functional characterization of four APETALA2-family genes (RAP2.6, RAP2.6L, DREB19 and DREB26) in Arabidopsis. Plant Mol. Biol. 75, 107-127.
32. Kyriakis, J.M., and Avruch, J. (2012). Mammalian MAPK signal transduction pathways activated by stress and inflammation: a 10-year update. Physiol. Rev. 92, 689-737.
33. Li, L., Zhang, C., Xu, D., Schlappi, M., and Xu, Z.Q. (2012). Expression of recombinant EARLI1, a hybrid proline-rich protein of Arabidopsis, in Escherichia coli and its inhibition effect to the growth of fungal pathogens and Saccharomyces cerevisiae. Gene. 506, 50-61.
34. Lindorff-Larsen, K., Lerche, M.H., Poulsen, F.M., Roepstorff, P., and Winther, J.R. (2001). Barley lipid transfer protein, LTP1, contains a new type of lipid-like post-translational modification. J. Biol. Chem. 276, 33547-33553.
35. Liu, Y., and Zhang, S. (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.
36. Lopez-Marques, R.L., Poulsen, L.R., and Palmgren, M.G. (2012). A putative plant aminophospholipid flippase, the Arabidopsis P4 ATPase ALA1, localizes to the plasma membrane following association with a beta-subunit. PloS One. 7, e33042.
37. Magome, H., Yamaguchi, S., Hanada, A., Kamiya, Y., and Oda, K. (2004). dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. Plant J. 37, 720-729.
38. Mahajan, S., and Tuteja, N. (2005). Cold, salinity and drought stresses: an overview. Arch. Biochem. Biophys. 444, 139-158.
39. Maldonado, A.M., Doerner, P., Dixon, R.A., Lamb, C.J., and Cameron, R.K. (2002). A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature. 419, 399-403.
40. Mao, G., Meng, X., Liu, Y., Zheng, Z., Chen, Z., and Zhang, S. (2011). Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell. 23, 1639-1653.
41. Mitra, S.K., Walters, B.T., Clouse, S.D., and Goshe, M.B. (2009). An efficient organic solvent based extraction method for the proteomic analysis of Arabidopsis plasma membranes. J. Proteome Res. 8, 2752-2767.
42. Molina, A., and Garcia-Olmedo, F. (1997). Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2. Plant J. 12, 669-675.
43. Muller, J., Beck, M., Mettbach, U., Komis, G., Hause, G., Menzel, D., and Samaj, J. (2010). Arabidopsis MPK6 is involved in cell division plane control during early root development, and localizes to the pre-prophase band, phragmoplast, trans-Golgi network and plasma membrane. Plant J. 61, 234-248.
44. Munnik, T., and Vermeer, J.E. (2010). Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. Plant, Cell & Environment. 33, 655-669.
45. Nieuwland, J., Feron, R., Huisman, B.A., Fasolino, A., Hilbers, C.W., Derksen, J., and Mariani, C. (2005). Lipid transfer proteins enhance cell wall extension in tobacco. Plant Cell. 17, 2009-2019.
46. Oparka, K.J. (1994). Plasmolysis: new insights into an old process. New Phytologist. 126, 571-591.
47. Osakabe, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., and Tran, L.S. (2013). Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J. Exp. Bot. 64, 445-458.
48. Panadero, J., Pallotti, C., Rodriguez-Vargas, S., Randez-Gil, F., and Prieto, J.A. (2006). A downshift in temperature activates the high osmolarity glycerol (HOG) pathway, which determines freeze tolerance in Saccharomyces cerevisiae. J. Biol. Chem. 281, 4638-4645.
49. Park, S.Y., and Lord, E.M. (2003). Expression studies of SCA in lily and confirmation of its role in pollen tube adhesion. Plant Mol. Biol. 51, 183-189.
50. Persak, H., and Pitzschke, A. (2013). Tight interconnection and multi-level control of Arabidopsis MYB44 in MAPK cascade signalling. PloS One. 8, e57547.
51. Pitzschke, A. (2013). Tropaeolum tops tobacco: simple and efficient transgene expression in the order brassicales. PloS One. 8, e73355.
52. Pitzschke, A., and Persak, H. (2012). Poinsettia protoplasts-a simple, robust and efficient system for transient gene expression studies. Plant Methods. 8, 14.
53. Pitzschke, A., Djamei, A., Bitton, F., and Hirt, H. (2009a). A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol. Plant. 2, 120-137.
54. Pitzschke, A., Djamei, A., Teige, M., and Hirt, H. (2009b). VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression. Proc. Natl Acad. Sci. U S A. 106, 18414-18419.
55. Pitzschke, A., Schikora, A., and Hirt, H. (2009c). MAPK cascade signalling networks in plant defence. Curr. Opin. Plant Biol. 12, 421-426.
56. Qiu, J.L., Zhou, L., Yun, B.W. Nielsen, H.B., Fiil, B.K., Petersen, K., Mackinlay, J., Loake, G.J., Mundy, J., and Morris, P.C. (2008). Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol. 148, 212-222.
57. Regente, M.C., Giudici, A.M., Villalain, J., and de la Canal, L. (2005). The cytotoxic properties of a plant lipid transfer protein involve membrane permeabilization of target cells. Lett. Appl. Microbiol. 40, 183-189.
58. Rodriguez, M.C., Petersen, M., and Mundy, J. (2010). Mitogenactivated protein kinase signaling in plants. Annu. Rev. Plant Biol. 61, 621-649.
59. Samajova, O., Plihal, O., Al-Yousif, M., Hirt, H., and Samaj, J. (2013). Improvement of stress tolerance in plants by genetic manipulation of mitogen-activated protein kinases. Biotechnol. Adv. 31, 118-128.
60. Schweighofer, A., et al. (2007). The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis. Plant Cell. 19, 2213-2224.
61. Segura, A., Moreno, M., and Garcia-Olmedo, F. (1993). Purification and antipathogenic activity of lipid transfer proteins (LTPs) from the leaves of Arabidopsis and spinach. FEBS Lett. 332, 243-246.
62. Silverstein, K.A., Moskal, W.A., Jr., Wu, H.C., Underwood, B.A., Graham, M.A., Town, C.D., and VandenBosch, K.A. (2007). Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant J. 51, 262-280.
63. Sinha, A.K., Jaggi, M., Raghuram, B., and Tuteja, N. (2011). Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signaling & Behavior. 6, 196-203.
64. Smallwood, M., Yates, E.A., Willats, W.G.T., Martin, H., and Knox, J.P. (1996). Immunochemical comparison of membrane-associated and secreted arabinogalactan-proteins in rice and carrot. Planta. 198, 452-459.
65. Snider, C., Jayasinghe, S., Hristova, K., and White, S.H. (2009). MPEx: a tool for exploring membrane proteins. Protein Sci. 18, 2624-2628.
66. Suarez-Rodriguez, M.C., Adams-Phillips, L., Liu, Y., Wang, H., Su, S.H., Jester, P.J., Zhang, S., Bent, A.F., and Krysan, P.J. (2007). MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Physiol. 143, 661-669.
67. Tanoue, T., and Nishida, E. (2003). Molecular recognitions in the MAP kinase cascades. Cell. Signal. 15, 455-462.
68. Teige, M., et al. (2004). The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol. Cell. 15, 141-152.
69. Testerink, C., and Munnik, T. (2011). Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J. Exp. Bot. 62, 2349-2361.
70. Tsugama, D., Liu, S., and Takano, T. (2011). A rapid chemical method for lysing Arabidopsis cells for protein analysis. Plant Methods. 7, 22.
71. Tsugama, D., Liu, S., and Takano, T. (2012). A bZIP protein, VIP1, is a regulator of osmosensory signaling in Arabidopsis. Plant Physiol. 159, 144-155.
72. Verslues, P.E., Agarwal, M., Katiyar-Agarwal, S., Zhu, J., and Zhu, J.K. (2006). Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J. 45, 523-539.
73. Walia, A., Lee, J.S., Wasteneys, G., and Ellis, B. (2009). Arabidopsis mitogen-activated protein kinase MPK18 mediates cortical microtubule functions in plant cells. Plant J. 59, 565-575.
74. Wang, H., Ngwenyama, N., Liu, Y., Walker, J.C., and Zhang, S. (2007). Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell. 19, 63-73.
75. Wilson, I.B. (2002). Glycosylation of proteins in plants and invertebrates. Curr. Opin. Struct. Biol. 12, 569-577.
76. Xu, D., Huang, X., Xu, Z.Q., and Schlappi, M. (2011a). The HyPRP gene EARLI1 has an auxiliary role for germinability and early seedling development under low temperature and salt stress conditions in Arabidopsis thaliana. Planta. 234, 565-577.
77. Xu, J., Tan, L., Lamport, D.T., Showalter, A.M., and Kieliszewski, M.J. (2008). The O-Hyp glycosylation code in tobacco and Arabidopsis and a proposed role of Hyp-glycans in secretion. Phytochemistry. 69, 1631-1640.
78. Xu, Z.Y., Zhang, X., Schlappi, M., and Xu, Z.Q. (2011b). Coldinducible expression of AZI1 and its function in improvement of freezing tolerance of Arabidopsis thaliana and Saccharomyces cerevisiae. J. Plant Physiol. 168, 1576-1587.
79. Yeats, T.H., and Rose, J.K. (2008). The biochemistry and biology of extracellular plant lipid-transfer proteins (LTPs). Protein Sci. 17, 191-198.
80. Yu, K., Soares, J.M., Mandal, M.K., Wang, C., Chanda, B., Gifford, A.N., Fowler, J.S., Navarre, D., Kachroo, A., and Kachroo, P. (2013). A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. Cell Reports. 3, 1266-1278.
81. Zhang, Y., and Schlappi, M. (2007). Cold responsive EARLI1 type HyPRPs improve freezing survival of yeast cells and form higher order complexes in plants. Planta. 227, 233-243.
82. Zi, Z., Liebermeister, W., and Klipp, E. (2010). A quantitative study of the Hog1 MAPK response to fluctuating osmotic stress in Saccharomyces cerevisiae. PloS One. 5, e9522.
83. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and Gruissem, W. (2004). GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.
84. Zulawski, M., Braginets, R., and Schulze, W.X. (2013). PhosPhAt goes kinases: searchable protein kinase target information in the plant phosphorylation site database PhosPhAt. Nucleic Acids Res. 41, D1176-D1184.