Improvement of stress tolerance in plants by genetic manipulation of mitogen-activated protein kinases

Biotechnology Advances

Volumn 31, Issue 1, 2013, Pages 118-128

  Šamajová, Olga ^a   Plíhal, Ondřej ^a   Al Yousif, Mohamed ^b   Hirt, Heribert ^b,c   Šamaj, Jozef ^a  

^a PALACKÝ UNIVERSITY   (Czech Republic)

^b KING SAUD UNIVERSITY   (Saudi Arabia)

^c UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

Author keywords

Arabidopsis; Biotechnology; Crops; Mitogen activated protein kinase; Omics approaches; Signaling; Stress tolerance; Transgenic plants

Indexed keywords

ARABIDOPSIS; MITOGEN ACTIVATED PROTEIN KINASE; OMICS APPROACHES; STRESS TOLERANCE; TRANSGENIC PLANTS;

BIOTECHNOLOGY; CROPS; PHOSPHORYLATION; SIGNALING; TRANSCRIPTION FACTORS;

ENZYME ACTIVITY;

MITOGEN ACTIVATED PROTEIN KINASE; PHYTOHORMONE;

BIOTECHNOLOGY; CEREAL; CROP IMPROVEMENT; CROP PLANT; DICOTYLEDON; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; GENETIC ENGINEERING; GENOMICS; PHYTOCHEMISTRY; PROTEIN; SIGNALING; TOBACCO; TOLERANCE; TRANSGENIC PLANT;

ARABIDOPSIS; CROP; GENETIC ENGINEERING; GENETICS; METABOLISM; METHODOLOGY; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT PHYSIOLOGY; REVIEW; TRANSGENIC PLANT;

ARABIDOPSIS; CROPS, AGRICULTURAL; GENETIC ENGINEERING; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PLANT GROWTH REGULATORS; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS, GENETICALLY MODIFIED; STRESS, PHYSIOLOGICAL;

ARABIDOPSIS; NICOTIANA TABACUM;

EID: 84871933536     PISSN: 07349750     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biotechadv.2011.12.002     Document Type: Review

References (143)

1. Agrawal G.K., Agrawal S.K., Shibato J., Iwahashi H., Rakwal R. Novel rice MAP kinases OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation. Biochem Biophys Res Commun 2003, 300:775-783.
2. Agrawal G.K., Rakwal R., Iwahashi H. Isolation of novel rice (Oryza sativa L.) multiple stress responsive MAP kinase gene, OsMSRMK2, whose mRNA accumulates rapidly in response to environmental cues. Biochem Biophys Res Commun 2002, 294:1009-1016.
3. Ahlfors R., Macioszek V., Rudd J., Brosché M., Schlichting R., Scheel D., et al. Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J 2004, 40:512-522.
4. Andreasson E., Jenkins T., Brodersen P., Thorgrimsen S., Petersen N.H.T., Zhu S., et al. The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J 2005, 24:2579-2589.
5. Asai T., Tena G., Plotnikova J., Willmann M.R., Chiu W.L., Gomez-Gomez L., et al. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 2002, 415:977-983.
6. Asai S., Ohta K., Yoshioka H. MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell 2008, 20:1390-1406.
7. Bayer M., Nawy T., Giglione C., Galli M., Meinnel T., Lukowitz W. Paternal control of embryonic patterning in Arabidopsis thaliana. Science 2009, 323(5920):1485-1488.
8. Beck M., Komis G., Müller J., Menzel D., Šamaj J. Arabidopsis homologs of nucleus- and phragmoplast-localized kinase 2 and 3 and mitogen-activated protein kinase 4 are essential for microtubule organization. Plant Cell 2010, 22:755-771.
9. Beck M., Komis G., Ziemann A., Menzel D., Šamaj J. Mitogen-activated protein kinase 4 is involved in the regulation of mitotic and cytokinetic microtubule transitions in Arabidopsis thaliana. New Phytol 2011, 189:1069-1083.
10. Bergmann D.C., Lukowitz W., Somerville C.R. Stomatal development and pattern controlled by a MAPKK kinase. Science 2004, 304:1494-1497.
11. Binder B.M., Walker J.M., Gagne J.M., Emborg T.J., Hemmann G., Bleecker A.B., et al. The Arabidopsis EIN3 binding F-Box proteins EBF1 and EBF2 have distinct but overlapping roles in ethylene signaling. Plant Cell 2007, 19:509-523.
12. Bögre L., Ligterink W., Meskiene I., Barker P.J., Heberle-Bors E., Huskisson N.S., et al. Wounding induces the rapid and transient activation of a specific MAP kinase pathway. Plant Cell 1997, 9:75-83.
13. Bögre L., Calderini O., Binarova P., Mattauch M., Till S., Kiegerl S., et al. A MAP kinase is activated late in plant mitosis and becomes localized to the plane of cell division. Plant Cell 1999, 11:101-113.
14. Brader G., Djamei A., Teige M., Palva E.T., Hirt H. The MAP kinase kinase MKK2 affects disease resistance in Arabidopsis. Mol Plant Microbe Interact 2007, 20:589-596.
15. Bush S.M., Krysan P.J. Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo development. J Exp Bot 2007, 58:2181-2191.
16. Calderini O., Bögre L., Vicente O., Binarova P., Heberle-Bors E., Wilson C. A cell cycle regulated MAP kinase with a possible role in cytokinesis in tobacco cells. J Cell Sci 1998, 111:3091-3100.
17. Cardinale F., Jonak C., Ligterink W., Niehaus K., Boller T., Hirt H. Differential activation of four specific MAPK pathways by distinct elicitors. J Biol Chem 2000, 275:36734-36740.
18. Cardinale F., Meskiene I., Ouaked F., Hirt H. Convergence and divergence of stress-induced mitogen-activated protein kinase signaling pathways at the level of two distinct mitogen-activated protein kinase kinases. Plant Cell 2002, 14:703-711.
19. Chao Q., Rothenberg M., Solano R., Roman G., Terzaghi W., Ecker J.R. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 1997, 89:1133-1144.
20. Chinchilla D., Zipfel C., Robatzek S., Kemmerling B., Nurnberger T., Jones J., et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 2007, 448:497-500.
21. Ciolkowski I., Wanke D., Birkenbihl R.P., Somssich I.E. Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol Biol 2008, 68:81-92.
22. Clark K.L., Larsen P.B., Wang X., Chang C. Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ET receptors. Proc Natl Acad Sci USA 1998, 95:5401-5406.
23. Dai Y., Wang H., Li B., Huang J., Liu X., Zhou Y., et al. Increased expression of MAP KINASE KINASE7 causes deficiency in polar auxin transport and leads to plant architectural abnormality in Arabidopsis. Plant Cell 2006, 18:308-320.
24. del Pozo O., Pedley K.F., Martin G.B. MAPKKKα is a positive regulator of cell death associated with both plant immunity and disease. EMBO J 2004, 23:3072-3082.
25. Desikan R., Clarke A., Atherfold P., Hancock J.T., Neill S.J. Harpin induces mitogen-activated protein kinase activity during defence responses in Arabidopsis thaliana suspension cultures. Planta 1999, 210:97-103.
26. Desikan R., Hancock J.T., Ichimura K., Shinozaki K., Neill S.J. Harpin induces activation of the Arabidopsis mitogen-activated protein kinases AtMPK4 and AtMPK6. Plant Physiol 2001, 126:1579-1587.
27. Djamei A., Pitzschke A., Nakagami H., Rajh I., Hirt H. Trojan horse strategy in Agrobacterium transformation: abusing MAPK defense signaling. Science 2007, 318:453-456.
28. Doczi R., Brader G., Pettko-Szandtner A., Rajh I., Djamei A., Pitzschke A., et al. The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell 2007, 19:3266-3279.
29. Droillard M., Boudsocq M., Barbier-Brygoo H., Lauriere C. Different protein kinase families are activated by osmotic stresses in Arabidopsis thaliana cell suspensions. Involvement of the MAP kinases AtMPK3 and AtMPK6. FEBS Lett 2002, 527:43-50.
30. Droillard M.J., Boudsocq M., Barbier-Brygoo H., Lauriere C. Involvement of MPK4 in osmotic stress response pathways in cell suspensions and plantlets of Arabidopsis thaliana: activation by hypoosmolarity and negative role in hyperosmolarity tolerance. FEBS Lett 2004, 574:42-48.
31. Feilner T., Hultschig C., Lee J., Meyer S., Immink R.G., Koenig A., et al. High throughput identification of potential Arabidopsis mitogen-activated protein kinases substrates. Mol Cell Proteomics 2005, 4:1558-1568.
32. Felix G., Duran J.D., Volko S., Boller T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 1999, 18:265-276.
33. Fu S.F., Chou W.C., Huang D.D., Huang H.J. Transcriptional regulation of a rice mitogen-activated protein kinase gene, OsMAPK4, in response to environmental stresses. Plant Cell Physiol 2002, 43:958-963.
34. Fujita M., Fujita Y., Noutoshi Y., Takahashi F., Narusaka Y., Yamaguchi-Shinozaki K., et al. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 2006, 9:436-442.
35. Gao Z., Chen Y.F., Randlett M.D., Zhao X.C., Findell J.L., Kieber J.J., et al. Localization of the Raf-like kinase CTR1 to the endoplasmic reticulum of Arabidopsis through participation in ethylene receptor signaling complexes. J Biol Chem 2003, 278:34725-34732.
36. Gao M., Liu J., Bi D., Zhang Z., Cheng F., Chen S., et al. MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res 2008, 18:1190-1198.
37. Gomez-Gomez L., Boller T. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 2000, 5:1003-1011.
38. Gomi K., Ogawa D., Katou S., Kamada H., Nakajima N., Saji H., et al. A mitogen-activated protein kinase NtMPK4 activated by SIPKK is required for jasmonic acid signaling and involved in ozone tolerance via stomatal movement in tobacco. Plant Cell Physiol 2005, 46:1902-1914.
39. Gudesblat G.E., Iusem N.D., Morris P.C. Arabidopsis MPK3, a key signalling intermediate in stomatal function. Plant Signal Behav 2007, 2:271-272.
40. Gudesblat G.E., Iusem N.D., Morris P.C. Guard cell-specific inhibition of Arabidopsis MPK3 expression causes abnormal stomatal responses to abscisic acid and hydrogen peroxide. New Phytol 2007, 173:713-721.
41. Holley S.R., Yalamanchili R.D., Moura D.S., Ryan C.A., Stratmann J.W. Convergence of signaling pathways induced by systemin, oligosaccharide elicitors, and ultraviolet-B radiation at the level of mitogen-activated protein kinases in Lycopersicon peruvianum suspension-cultured cells. Plant Physiol 2003, 132:1728-1738.
42. Hua J., Meyerowitz E.M. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 1998, 94:261-271.
43. Huang Y., Li H., Hutchison C.E., Laskey J., Kieber J.J. Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis. Plant J 2003, 33:221-233.
44. Ichimura K., Casais C., Peck S.C., Shinozaki K., Shirasu K. MEKK1 is required for MPK4 activation and regulates tissue-specific and temperature-dependent cell death in Arabidopsis. J Biol Chem 2006, 281:36969-36976.
45. Ichimura K., Mizoguchi T., Irie K., Morris P., Giraudat J., Matsumoto K., et al. Isolation of ATMEKK1 (a MAP kinase kinase kinase)-interacting proteins and analysis of a MAP kinase cascade in Arabidopsis. Biochem Biophys Res Commun 1998, 253:532-543.
46. Ichimura K., Mizoguchi T., Yoshida R., Yuasa T., Shinozaki K. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J 2000, 24:655-665.
47. Ikeda Y., Men S., Fischer U., Stepanova A.N., Alonso J.M., Ljung K., et al. Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nat Cell Biol 2009, 11:731-740.
48. Jiang M., Zhang J. Cross-talk between calcium and reactive oxygen species originated from NADPH oxidase in abscisic acid-induced antioxidant defence in leaves of maize seedlings. Plant Cell Environ 2003, 26:929-939.
49. Jonak C., Kiegerl S., Ligterink W., Barker P.J., Huskisson N.S., Hirt H. Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci USA 1996, 93:11274-11279.
50. Jonak C., Ökrész L., Bögre L., Hirt H. Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 2002, 5:415-424.
51. Jonak C., Nakagami H., Hirt H. Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol 2004, 136:3276-3283.
52. Jones J.D., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
53. Joo S., Liu Y., Lueth A., Zhang S. 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 26 S proteasome pathway. Plant J 2008, 54:129-140.
54. Kieber J.J., Rothenberg M., Roman G., Feldmann K.A., Ecker J.R. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 1993, 72:427-441.
55. Kiegerl S., Cardinale F., Siligan C., Gross A., Baudouin E., Liwosz A., et al. SIMKK, a mitogen-activated protein kinase (MAPK) kinase, is a specific activator of the salt stress-induced MAPK, SIMK. Plant Cell 2000, 12:2247-2258.
56. Kim J.A., Agrawal G.K., Rakwal R., Han K.S., Kim K.N., Yun C.H., et al. Molecular cloning and mRNA expression analysis of a novel rice (Oryza sativa L.) MAPK kinase kinase, OsEDR1, an ortholog of Arabidopsis AtEDR1, reveal its role in defense/stress signalling pathways and development. Biochem Biophys Res Commun 2003, 300:868-876.
57. Kosetsu K., Matsunaga S., Nakagami H., Colcombet J., Sasabe M., Soyano T., et al. The MAP kinase MPK4 is required for cytokinesis in Arabidopsis thaliana. Plant Cell 2010, 22:3778-3790.
58. Kovtun Y., Chiu W.L., Tena G., Sheen J. Functional analysis of oxidative stress-activated mitogen activated protein kinase cascade in plants. Proc Natl Acad Sci USA 2000, 97:2940-2945.
59. Kovtun Y., Chiu W.L., Zeng W., Sheen J. Suppression of auxin signal transduction by a MAPK cascade in higher plants. Nature 1998, 395:716-720.
60. Krysan P.J., Jester P.J., Gottwald J.R., Sussman M.R. An Arabidopsis mitogen-activated protein kinase kinase kinase gene family encodes essential positive regulators of cytokinesis. Plant Cell 2002, 14:1109-1120.
61. Kunze G., Zipfel C., Robatzek S., Niehaus K., Boller T., Felix G. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 2004, 16:3496-3507.
62. Lampard G.R., Macalister C.A., Bergmann D.C. Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 2008, 322:1113-1116.
63. Lampard G.R., Lukowitz W., Ellis B.E., Bergmann D.C. Novel and expanded roles for MAPK signaling in Arabidopsis stomatal cell fate revealed by cell type-specific manipulations. Plant Cell 2009, 21:3506-3517.
64. Lee J., Rudd J.J., Macioszek V.K., Scheel D. Dynamic changes in the localization of MAPK cascade components controlling pathogenesis-related (PR) gene expression during innate immunity in parsley. J Biol Chem 2004, 279:22440-22448.
65. Lee J.S., Ellis B.E. Arabidopsis MAPK phosphatase 2 (MKP2) positively regulates oxidative stress tolerance and inactivates the MPK3 and MPK6 MAPKs. J Biol Chem 2007, 282:25020-25029.
66. Lee J.S., Wang S., Sritubtim S., Chen J.G., Ellis B.E. Arabidopsis mitogen-activated protein kinase MPK12 interacts with the MAPK phosphatase IBR5 and regulates auxin signaling. Plant J 2009, 57:975-985.
67. Lee S.K., Kim B.G., Kwon T.R., Jeong M.J., Park S.R., Lee J.W., et al. Overexpression of the mitogen-activated protein kinase gene OsMAPK33 enhances sensitivity to salt stress in rice (Oryza sativa L.). J Biosci 2011, 36:139-151.
68. Lin F., Ding H., Wang J., Zhang H., Zhang A., Zhang Y., et al. Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J Exp Bot 2009, 60:3221-3238.
69. Liu Y., Schiff M., Dinesh-Kumar S.P. Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. Plant J 2004, 38:800-809.
70. Liu Y., Zhang S. Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ET biosynthesis in Arabidopsis. Plant Cell 2004, 16:3386-3399.
71. Lukowitz W., Roeder A., Parmenter D., Somerville C. A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 2004, 116:109-119.
72. Mao G., Meng X., Liu Y., Zheng Z., Chen Z., Zhang S. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 2011, 23:1639-1653.
73. Matsuoka D., Nanmori T., Sato K., Fukami Y., Kikkawa U., Yasuda T. 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 2002, 29:637-647.
74. Mayrose M., Bonshtien A., Sessa G. LeMPK3 is a mitogen-activated protein kinase with dual specificity induced during tomato defense and wounding responses. J Biol Chem 2004, 279:14819-14827.
75. Menke F.L., van Pelt J.A., Pieterse C.M., Klessig D.F. Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. Plant Cell 2004, 16:897-907.
76. Mészáros T., Helfer A., Hatzimasoura E., Magyar Z., Serazetdinova L., Rios G., et al. The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin. Plant J 2006, 48:485-498.
77. Miles G.P., Samuel M.A., Zhang Y., Ellis B.E. RNA interference-based (RNAi) suppression of AtMPK6, an Arabidopsis mitogen-activated protein kinase, results in hypersensitivity to ozone and misregulation of AtMPK3. Environ Pollut 2005, 138:230-237.
78. Miya A., Albert P., Shinya T., Desaki Y., Ichimura K., Shirasu K., et al. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 2007, 104:19613-19618.
79. Mizoguchi T., Irie K., Hirayama T., Hayashida N., Yamaguchi-Shinozaki K., Matsumoto K., et al. A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proc Natl Acad Sci USA 1996, 93:765-769.
80. Mockaitis K., Howell S.H. Auxin induces mitogenic activated protein kinase (MAPK) activation in roots of Arabidopsis seedlings. Plant J 2000, 24:785-796.
81. Moon H., Lee B., Choi G., Shin D., Prasad D.T., Lee O., et al. NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proc Natl Acad Sci USA 2003, 100:358-363.
82. Müller J., Beck M., Mettbach U., Komis G., Hause G., Menzel D., et al. 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 2010, 61:234-248.
83. Nakagami H., Kiegerl S., Hirt H. OMTK1, a novel MAPKKK, channels oxidative stress signaling through direct MAPK interaction. J Biol Chem 2004, 279:26959-26966.
84. Nakagami H., Pitzschke A., Hirt H. Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci 2005, 10:339-346.
85. Nakagami H., Soukupová H., Schikora A., Zárský V., Hirt H. A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J Biol Chem 2006, 281:38697-38704.
86. Ning J., Li X., Hicks L.M., Xiong L. A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol 2010, 152:876-890.
87. Nishihama R., Ishikawa M., Araki S., Soyano T., Asada T., Machida Y. The NPK1 mitogen-activated protein kinase kinase kinase is a regulator of cell-plate formation in plant cytokinesis. Genes Dev 2001, 15:352-363.
88. Nishihama R., Soyano T., Ishikawa M., Araki S., Tanaka H., Asada T., et al. Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex. Cell 2002, 109:87-99.
89. Novikova G.V., Moshkov I.E., Smith A.R., Hall M.A. The effect of ET on MAPKinase-like activity in Arabidopsis thaliana. FEBS Lett 2000, 474:29-32.
90. Nuhse T.S., Peck S.C., Hirt H., Boller T. Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK 6. J Biol Chem 2000, 275:7521-7526.
91. Ortiz-Masia D., Perez-Amador M.A., Carbonell J., Marcote M.J. Diverse stress signals activate the C1 subgroup MAP kinases of Arabidopsis. FEBS Lett 2007, 581:1834-1840.
92. Ouaked F., Rozhon W., Lecourieux D., Hirt H. A MAPK pathway mediates ET signaling in plants. EMBO J 2003, 22:1282-1288.
93. Pedley K.F., Martin G.B. Identification of MAPKs and their possible MAPK kinase activators involved in the Pto-mediated defense response of tomato. J Biol Chem 2004, 279:49229-49235.
94. Petersen M., Brodersen P., Naested H., Andreasson E., Lindhart U., Johansen B., et al. Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell 2000, 103:1111-1120.
95. Petersen K., Qiu J.L., Lutje J., Fiil B.K., Hansen S., Mundy J., et al. Arabidopsis MKS1 is involved in basal immunity and requires an intact N-terminal domain for proper function. PLoS One 2010, 5:e14364.
96. Pitzschke A., Djamei A., Bitton F., Hirt H. A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol Plant 2009, 2:120-137.
97. Pitzschke A., Djamei A., Teige M., Hirt H. VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression. Proc Natl Acad Sci USA 2009, 106:18414-18419.
98. Popescu S.C., Popescu G.V., Bachan S., Zhang Z., Gerstein M., Snyder M., et al. MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev 2009, 23:80-92.
99. Prasad T.K., Anderson M.D., Martin B.A., Stewart C.R. Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 1994, 6:65-74.
100. Qiu J.L., Fiil B.K., Petersen K., Nielsen H.B., Botanga C.J., Thorgrimsen S., et al. Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 2008, 27:2214-2221.
101. Qiu J.L., Zhou L., Yun B.W., Nielsen H.B., Fiil B.K., Petersen K., et al. Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol 2008, 148:212-222.
102. Qutob D., Kemmerling B., Brunner F., Kufner I., Engelhardt S., Gust A.A., et al. Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell 2006, 18:3721-3744.
103. Ren D., Liu Y., Yang K.Y., Han L., Mao G., Glazebrook J., et al. A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 2008, 105:5638-5643.
104. Ren D., Yang K.Y., Li G.J., Liu Y., Zhang S. Activation of Ntf4, a tobacco mitogen-activated protein kinase, during plant defense response and its involvement in hypersensitive response-like cell death. Plant Physiol 2006, 141:1482-1493.
105. Ren D., Yang H., Zhang S. Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem 2002, 277:559-565.
106. Robatzek S., Chinchilla D., Boller T. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 2006, 20:537-542.
107. Rudd J.J., Keon J., Hammond-Kosack K.E. The wheat mitogen-activated protein kinases TaMPK3 and TaMPK6 are differentially regulated at multiple levels during compatible disease interactions with Mycosphaerella graminicola. Plant Physiol 2008, 147:802-815.
108. Rushton P.J., Reinstadler A., Lipka V., Lippok B., Somssich I.E. Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signaling. Plant Cell 2002, 14:749-762.
109. Samuel M.A., Miles G.P., Ellis B.E. Ozone treatment rapidly activates MAP kinase signalling in plants. Plant J 2000, 22:367-376.
110. Sasabe M., Soyano T., Takahashi Y., Sonobe S., Igarashi H., Itoh T.J., et al. Phosphorylation of NtMAP65-1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells. Genes Dev 2006, 20:1004-1014.
111. Sasabe M., Kosetsu K., Hidaka M., Murase A., Machida Y. Arabidopsis thaliana MAP65-1 and MAP65-2 function redundantly with MAP65-3/PLEIADE in cytokinesis downstream of MPK4. Plant Signal Behav 2011, 6:743-747.
112. Šamaj J., Ovecka M., Hlavacka A., Lecourieux F., Meskiene I., Lichtscheidl I., et al. Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip growth. EMBO J 2002, 21:3296-3306.
113. Schweighofer A., Kazanaviciute V., Scheikl E., Teige M., Doczi R., Hirt H., et al. The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis. Plant Cell 2007, 19:2213-2224.
114. Sharma P.C., Ito A., Shimizu T., Terauchi R., Kamoun S., Saitoh H. Virus-induced silencing of WIPK and SIPK genes reduces resistance to a bacterial pathogen, but has no effect on the INF1-induced hypersensitive response (HR) in Nicotiana benthamiana. Mol Genet Genomics 2003, 269:583-591.
115. Shou H., Bordallo P., Fan J.B., Yeakley J.M., Bibikova M., Sheen J., et al. Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize. Proc Natl Acad Sci U S A 2004, 101:3298-3303.
116. Shou H., Bordallo P., Wang K. Expression of the Nicotiana protein kinase (NPK1) enhanced drought tolerance in transgenic maize. J Exp Bot 2004, 55:1013-1019.
117. Soyano T., Nishihama R., Morikiyo K., Ishikawa M., Machida Y. NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK-mediated MAPK cascade and is required for plant cytokinesis. Genes Dev 2003, 17:1055-1067.
118. Smertenko A.P., Chang H.Y., Sonobe S., Fenyk S.I., Weingartner M., Bögre L., et al. Control of the AtMAP65-1 interaction with microtubules through the cell cycle. J Cell Sci 2006, 119:3227-3237.
119. Suarez-Rodriguez M.C., Adams-Phillips L., Liu Y., Wang H., Su S.H., Jester P.J., et al. MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Physiol 2007, 143:661-669.
120. Takahashi F., Yoshida R., Ichimura K., Mizoguchi T., Seo S., Yonezawa M., et al. The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. Plant Cell 2007, 19:805-818.
121. Takahashi Y., Soyano T., Kosetsu K., Sasabe M., Machida Y. HINKEL kinesin, ANP MAPKKKs and MKK6/ANQ MAPKK, which phosphorylates and activates MPK4 MAPK, constitute a pathway that is required for cytokinesis in Arabidopsis thaliana. Plant Cell Physiol 2010, 51:1766-1776.
122. Tang D., Innes R.W. Overexpression of a kinase-deficient form of the EDR1 gene enhances powdery mildew resistance and ethylene-induced senescence in Arabidopsis. Plant J 2002, 32:975-983.
123. Teige M., Scheikl E., Eulgem T., Dóczi R., Ichimura K., Shinozaki K., et al. The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 2004, 15:141-152.
124. Walia A., Lee J.S., Wasteneys G., Ellis B. Arabidopsis mitogen-activated protein kinase MPK18 mediates cortical microtubule functions in plant cells. Plant J 2009, 59:565-575.
125. Wang H., Ngwenyama N., Liu Y., Walker J.C., Zhang S. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 2007, 19:63-73.
126. Wang J., Ding H., Zhang A., Ma F., Cao J., Jiang M. A novel mitogen-activated protein kinase gene in maize (Zea mays), ZmMPK3, is involved in response to diverse environmental cues. J Integr Plant Biol 2010, 52:442-452.
127. Wen J.Q., Oono K., Imai R. Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice. Plant Physiol 2002, 129:1880-1891.
128. 2 production in Arabidopsis. J Exp Bot 2007, 58:2969-2981.
129. 2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J 2008, 54:440-451.
130. Xing Y., Jia W., Zhang J. AtMKK1 and AtMPK6 are involved in abscisic acid and sugar signaling in Arabidopsis seed germination. Plant Mol Biol 2009, 70:725-736.
131. Xiong L., Yang Y. Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 2003, 15:745-759.
132. Yanagisawa S., Yoo S.D., Sheen J. Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 2003, 425:521-525.
133. Yang K.Y., Liu Y., Zhang S. Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc Natl Acad Sci U S A 2001, 98:741-746.
134. Yeh C.M., Chien P.S., Huang H.J. Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. J Exp Bot 2007, 58:659-671.
135. Yoo S.D., Cho Y.H., Tena G., Xiong Y., Sheen J. Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 2008, 451:789-795.
136. Yuasa T., Ichimura K., Mizoquchi T., Shinozaki K. Oxidative stress activates ATMPK6, an Arabidopsis homologue of MAP kinase. Plant Cell Physiol 2001, 42:1012-1026.
137. Zaïdi I., Ebel C., Touzri M., Herzog E., Evrard J.L., Schmit A.C., et al. TMKP1 is a novel wheat stress responsive MAP kinase phosphatase localized in the nucleus. Plant Mol Biol 2010, 73:325-338.
138. Zhang A., Jiang M., Zhang J., Ding H., Xu S., Hu X., et al. Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytol 2007, 175:36-50.
139. Zhang S., Klessig D.F. Resistance gene N-mediated de novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection. Proc Natl Acad Sci USA 1998, 95:7433-7438.
140. Zhang S., Klessig D.F. The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc Natl Acad Sci U S A 1998, 95:7225-7230.
141. Zhang S., Liu Y., Klessig D.F. Multiple levels of tobacco WIPK activation during the induction of cell death by fungal elicitins. Plant J 2000, 23:339-347.
142. Zhang L., Xi D., Luo L., Meng F., Li Y., Wu C.A., et al. Cotton GhMPK2 is involved in multiple signaling pathways and mediates defense responses to pathogen infection and oxidative stress. FEBS J 2011, 278:1367-1378.
143. Zipfel C., Robatzek S., Navarro L., Oakeley E.J., Jones J.D., Felix G., et al. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 2004, 428:764-767.