Mitogen-activated protein kinase signaling in plants under abiotic stress

Plant Signaling and Behavior

Volumn 6, Issue 2, 2011, Pages 196-203

  Sinha, Alok Krishna ^a   Jaggi, Monika ^a   Raghuram, Badmi ^a   Tuteja, Narendra ^b  

^a NATIONAL INSTITUTE OF PLANT GENOME RESEARCH   (India)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

Abiotic stress; Cross talk; Heat map; MAPK signaling; Mitogen activated protein kinases; Signal transduction; Stress signaling

Indexed keywords

ENZYMOLOGY; PHYSIOLOGICAL STRESS; PLANT; REVIEW; SIGNAL TRANSDUCTION;

MAP KINASE SIGNALING SYSTEM; PLANTS; RECEPTOR CROSS-TALK; STRESS, PHYSIOLOGICAL;

EID: 79956226797     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.6.2.14701     Document Type: Review

References (91)

1. Chinnusamy V, Schumaker K, Zhu JK. Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 2004; 55:225-236.
2. Sreenivasulu N, Sopory SK, Kavi Kishor PB. Deciphering the regulatory mechanisms of abiotic stress tolerance in plants by genomic approaches. Gene 2007; 388:1-13.
3. Tena G, Asai T, Chiu WL, Sheen J. Plant mitogen-activated protein kinase signaling cascades. Curr Opin Plant Biol 2001; 4:392-400.
4. Jonak C, Okrész L, Bögre L, Hirt H. Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 2002; 5:415-424.
5. Mishra NS, Tuteja R, Tuteja N. Signaling through MAP kinase networks in plants. Arch Biochem Biophys 2006; 452:55-68.
6. Rodriguez MC, Petersen M, Mundy J. Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 2010; 61:621-649.
7. Dan I, Watanabe NM, Kusumi A. The Ste20 group kinases as regulators of MAP kinase cascades. Trends Cell Biol 2001; 11:220-230.
8. Chang L, Karin M. Mammalian MAP kinase signaling cascades. Nature 2001; 410:37-40.
9. Whitmarsh AJ, Davis RJ. Structural organization of MAP-kinase signaling modules by scaffold proteins in yeast and mammals. Trends Biochem Sci 1998; 23:481-485.
10. Bardwell AJ, Flatauer LJ, Matsukuma K, Thorner J, Bardwell L. A conserved docking site in MEKs mediates high-affinity binding to MAP kinases and cooperates with a scaffold protein to enhance signal transmission. J Biol Chem 2001; 276:10374-10386.
11. Takekawa M, Tatebayashi K, Saito H. Conserved docking site is essential for activation of mammalian MAP kinase kinases by specific MAP kinase kinase kinases. Mol Cell 2005; 18:295-306.
12. Ulm R, Ichimura K, Mizoguchi T, Peck SC, Zhu T, Wang X, et al. Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO J 2002; 21:6483-6493.
13. 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.
14. 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.
15. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, et al. MAP kinase signaling cascade in Arabidopsis innate immunity. Nature 2002; 415:977-983.
16. Yoo SD, Cho YH, Tena G, Xiong Y, Sheen J. Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signaling. Nature 2008; 451:789-795.
17. Zhu JK. Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 2002; 53:247-273.
18. Tuteja N. Mechanisms of high salinity tolerance in plants. Methods Enzymol 2007; 428:419-438.
19. 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 ribo-somal protein kinase by touch, cold and water stress in Arabidopsis thaliana. Proc Natl Acad Sci USA 1996; 93:765-769.
20. 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.
21. 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.
22. Munnik T, Ligterink W, Meskiene II, Calderini O, Beyerly J, Musgrave A, Hirt H. Distinct osmo-sensing protein kinase pathways are involved in signaling moderate and severe hyper-osmotic stress. Plant J 1999; 20:381-388.
23. 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.
24. Mikołajczyk M, Awotunde OS, Muszynska G, Klessig DF, Dobrowolska G. Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. Plant Cell 2000; 12:165-178.
25. Droillard M, Boudsocq M, Barbier-Brygoo H, Laurière 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.
26. Droillard MJ, Boudsocq M, Barbier-Brygoo H, Lauriere C. Involvement of MPK4 in osmotic stress response pathways in cell suspensions and plantlets of A. thaliana: activation by hypoosmolarity and negative role in hyperosmolarity tolerance. FEBS Lett 2004; 574:42-48.
27. Ding HD, Zhang XH, Xu SC, Sun LL, Jiang MY, Zhang AY, Jin YG. Induction of protection against paraquat-induced oxidative damage by abscisic acid in maize leaves is mediated through mitogen-activated protein kinase. J Integr Plant Biol 2009; 51:961-972.
28. Gu L, Liu Y, Zong X, Liu L, Li DP, Li DQ. Overexpression of maize mitogen-activated protein kinase gene, ZmSIMK1 in Arabidopsis increases tolerance to salt stress. Mol Biol Rep 2010; In press.
29. 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.
30. 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.
31. Zhang T, Liu Y, Xue L, Xu S, Chen T, Yang T, et al. Molecular cloning and characterization of a novel MAP kinase gene in Chorispora bungeana. Plant Physiol Biochem 2006; 44:78-84.
32. Shi J, An HL, Zhang L, Gao Z, Guo XQ. GhMPK7, a novel multiple stress-responsive cotton group C MAPK gene, has a role in broad spectrum disease resistance and plant development. Plant Mol Biol 2010; 74:1-17.
33. Boyer JS. Plant productivity and environment. Science 1982; 218:443-448.
34. Mahajan S, Tuteja N. Cold, salinity and drought stresses: An overview. Arch Biochem Biophys 2005; 444:139-158.
35. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, et al. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 2008; 20:2238-2251.
36. Lee HK, Cho SK, Son O, Xu Z, Hwang I, Kim WT Drought stress-induced Rma1H1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquapo-rin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell 2009; 21:622-641.
37. Jonak C, Kiegerl S, Ligterink W, Barker PJ, Huskisson NS, 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.
38. Agrawal GK, 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.
39. Ning J, Li X, Hicks LM, Xiong L. A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol 2010; 152:876-890.
40. Peng LX, Gu LK, Zheng CC, Li DQ, Shu HR. Expression of MaMAPK gene in seedlings of Malus L. under water stress. Acta Biochim Biophys Sin (Shanghai) 2006; 38:281-286.
41. Mizoguchi T, Ichimura K, Yoshida R, Shinozaki K. MAP kinase cascades in Arabidopsis: their roles in stress and hormone responses, in: Hirt H, (Ed.), Results and Problems in Cell Di Verentiation: MAP Kinases in Plant Signal Transduction, Heidelberg, Springer 2000; 29-38.
42. Berberich T, Sano H, Kusano T. Involvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maize. Mol Gen Genet 1999; 262:534-542.
43. Ding H, Zhang A, Wang J, Lu R, Zhang H, Zhang J, Jiang M. Identity of an ABA-activated 46 kDa mitogen-activated protein kinase from Zea mays leaves: partial purification, identification and characterization. Planta 2009; 230:239-251.
44. Agarwal PK, Gupta K, Jha B. Molecular characteriza-tion of the Salicornia brachiata SbMAPKK gene and its expression by abiotic stress. Mol Biol Rep 2010 37:981-986.
45. Ciais P, Reichstein M, Viovy N, Granier A, Ogée J, Allard V, et al. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 2005; 437:529-533.
46. Sangwan V, Orvar BL, Beyerly J, Hirt H, Dhindsa RS. Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J 2002; 31:629-638.
47. Link V, Sinha AK, Vashista P, Hofmann MG, Proels RK, Ehness R, Roitsch T. A heat-activated MAP kinase in tomato: a possible regulator of the heat stress response. FEBS Lett 2002; 531:179-183.
48. Rao KP, Vani G, Kumar K, Sinha AK Rhythmic expression of mitogen activated protein kinase activity in rice. Mol Cells 2009; 28:417-422.
49. Blanco FA, Zanetti ME, Casalongué CA, Daleo GR. Molecular characterization of a potato MAP kinase transcriptionally regulated by multiple environmental stresses. Plant Physiol Biochem 2006; 44:315-322.
50. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 2002; 7:405-410.
51. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 2010; In press.
52. Xing Y, Jia W, Zhang J. AtMEK1 mediates stress-induced gene expression of CAT1 catalase by triggering HO production in Arabidopsis. J Exp Bot 2007; 58:2969-2981.
53. Xing Y, Jia W, Zhang J. AtMKK1 mediates ABA-induced CAT1 expression and HO production via AtMPK6-coupled signaling in Arabidopsis. Plant J 2008; 54:440-451.
54. Pitzschke A, Hirt H. Disentangling the complexity of mitogen-activated protein kinases and reactive oxygen species signaling. Plant Physiol 2009; 149:606-615.
55. Nakagami H, Soukupova H, Schikora A, Zarsky V, Hirt H. A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J Biol Chem 2006; 281:38697-38704.
56. Kovtun Y, Chiu WL, 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.
57. 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.
58. Zong XJ, Li DP, Gu LK, Li DQ, Liu LX, Hu XL. Abscisic acid and hydrogen peroxide induce a novel maize group C MAP kinase gene, ZmMPK7, which is responsible for the removal of reactive oxygen species. Planta 2009; 229:485-495.
59. Ortiz-Masia D, Perez-Amador MA, Carbonell P, Aniento F, Carbonell J, Marcote MJ. Characterization of PsMPK2, the first C1 subgroup MAP kinase from pea (Pisum sativum L.). Planta 2008; 227:1333-1342.
60. Lumbreras V, Vilela B, Irar S, Solé M, Capellades M, Valls M, et al. MAPK phosphatase MKP2 mediates disease responses in Arabidopsis and functionally interacts with MPK3 and MPK6. Plant J 2010; 63:1017-1030.
61. Samuel MA, Miles GP, Ellis BE. Ozone treatment rapidly activates MAP kinase signaling in plants. Plant J 2000; 22:367-376.
62. Samuel MA, Ellis BE. Double jeopardy: both over-expression and suppression of a redox-activated plant mitogen-activated protein kinase render tobacco plants ozone sensitive. Plant Cell 2002; 14:2059-2069.
63. Ahlfors R, Macioszek V, Rudd J, Brosché M, Schlichting R, Scheel D, Kangasjärvi J. Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J 2004; 40:512-522.
64. Miles GP, Samuel MA, Zhang Y, Ellis BE. 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.
65. 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 sto-matal movement in tobacco. Plant Cell Physiol 2005; 46:1902-1914.
66. Hamel LP, Miles GP, Samuel MA, Ellis BE, Séguin A, Beaudoin N. Activation of stress-responsive mitogen-activated protein kinase pathways in hybrid poplar (Populus trichocarpa x Populus deltoides). Tree Physiol 2005; 25:277-288.
67. Lee JS, Ellis BE. Arabidopsis MAPK phosphatase 2 (MKP2) positively regulates oxidative stress tolerance and inactivates the MPK3 and MPK6 MAPKs. J Biol Chem 2007; 282:25020-25029.
68. Lawton MA, Lamb CJ. Transcriptional activation of plant defense genes by fungal elicitor, wounding and infection. Mol Cell Biol 1987; 7:335-341.
69. Brederode FT, Linthorst HJ, Bol JF. Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Mol Biol 1991; 17:1117-1125.
70. Seo S, Okamoto M, Seto H, Ishizuka K, Sano H, Ohashi Y. Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science 1995; 270:1988-1992.
71. Bogre L, Ligterink W, Meskiene I, Barker PJ, Heberle-Bors E, Huskisson NS, et al. Wounding induces the rapid and transient activation of a specific MAP kinase Pathway. Plant Cell 1997; 9:75-83.
72. He C, Fong SH, Yang D, Wang GL. BWMK1, a novel MAP kinase induced by fungal infection and mechanical wounding in rice. Mol Plant Microbe Interact 1999; 12:1064-1073.
73. Xing T, Malik K, Martin T, Miki BL. Activation of tomato PR and wound-related genes by a mutagenized tomato MAP kinase kinase through divergent pathways. Plant Mol Biol 2001; 46:109-120.
74. Lee S, Hirt H, Lee Y. Phosphatidic acid activates a wound-activated MAPK in Glycine max. Plant J 2001; 26:479-486.
75. Wang M, Zhang Y, Wang J, Wu X, Guo X A novel MAP kinase gene in cotton (Gossypium hirsutum L.), GhMAPK, is involved in response to diverse environmental stresses. J Biochem Mol Biol 2007; 40:325-332.
76. Yeh CM, Hsiao LJ, Huang HJ. Cadmium activates a mitogen-activated protein kinase gene and MBP kinases in rice. Plant Cell Physiol 2004; 45:1306-1312.
77. 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.
78. Gupta M, Sharma P, Sarin NB, Sinha AK. Differential response of arsenic stress in two varieties of Brassica juncea L. Chemosphere 2009; 74:1201-1208.
79. Rao KP, Vani G, Kumar K, Wankhede DP, Mishra M, Gupta M, Sinha AK. Arsenic stress activates MAP kinase in rice roots and leaves. Arch Biochem Biophys 2010; In press.
80. Flowers TJ. Improving crop salt tolerance. J Exp Bot 2004; 55:307-319.
81. Bartels D, Sunkar R. Drought and salt tolerance in plants. Crit Rev Plant Sci 2005; 24:23-58.
82. Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 2006; 17:113-122.
83. Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M, Snyder M, Dinesh-Kumar SP. MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev 2009; 23:80-92.
84. Ding X, Richter T, Chen M, Fujii H, Seo YS, Xie M, et al. A rice kinase-protein interaction map. Plant Physiol 2009; 149:1478-1492.
85. Lee JS, Huh KW, Bhargava A, Ellis BE. Comprehensive analysis of protein-protein interactions between Arabidopsis MAPKs and MAPK kinases helps define potential MAPK signaling modules. Plant Signal Behav 2008; 3:1037-1041.
86. Jung KH, Cao P, Seo YS, Dardick C, Ronald PC. The Rice Kinase Phylo-genomics Database: a guide for systematic analysis of the rice kinase super-family Trends Plant Sci 2010; 15:595-599.
87. Dardick C, Chen J, Richter T, Ouyang S, Ronald P The rice kinase database. A phylogenomic database for the rice kinome. Plant Physiol 2007; 143:579-586.
88. Rao KP, Richa T, Kumar K, Raghuram B, Sinha AK. In silico analysis reveals 75 members of mitogen-activated protein kinase kinase kinase gene family in rice. DNA Res 2010; 17:139-153.
89. Liu Y, Li X, Tan H, Liu M, Zhao X, Wang J. Molecular characterization of RsMPK2, a C1 subgroup mitogen-activated protein kinase in the desert plant Reaumuria soongorica. Plant Physiol Biochem 2010; 48:836-844.
90. Taj G, Agarwal P, Grant M, Kumar A. MAPK machinery in plants: Recognition and response to different stresses through multiple signal transduction pathways. Plant Signal Behav 2010; In press.
91. Gao F, Su Q, Fan Y, Wang L. Expression pattern and core region analysis of AtMPK3 promoter in response to environmental stresses. Sci China Life Sci 2010; 53:1315-1321.