Signal convergence through the lenses of MAP kinases: paradigms of stress and hormone signaling in plants

Abstract

Common mechanisms plants use to translate the external stimuli into cellular responses are the activation of mitogen-activated protein kinase (MAPK) cascade. These MAPK cascades are highly conserved in eukaryotes and consist of three subsequently acting protein kinases, MAP kinase kinase kinase (MAPKKK), MAP kinase kinase (MAPKK) and MAP kinase (MAPK) which are linked in various ways with upstream receptors and downstream targets. Plant MAPK cascades regulate numerous processes, including various environmental stresses, hormones, cell division and developmental processes. The number of MAPKKs in Arabidopsis and rice is almost half the number of MAPKs pointing important role of MAPKKs in integrating signals from several MAPKKKs and transducing signals to various MAPKs. The cross talks between different signal transduction pathways are concentrated at the level of MAPKK in the MAPK cascade. Here we discussed the insights into MAPKK mediated response to environmental stresses and in plant growth and development.

Keywords

environmental stresses / abiotic stress / biotic stress / mitogen-activated protein kinase kinase / MAPKK / mitogen-activated protein kinase / MAPK / plant signaling

References

[1] Alonso J M, Stepanova A N, Solano R, Wisman E, Ferrari S, Ausubel F M, Ecker J R (2003). Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc Natl Acad Sci USA, 100(5): 2992–2997

[2] Alzwiy I A, Morris P C (2007). A mutation in the Arabidopsis MAP kinase kinase 9 gene results in enhanced seedling stress tolerance. Plant Sci, 173(3): 302–308

[3] Andreasson E, Ellis B (2010). Convergence and specificity in the Arabidopsis MAPK nexus. Trends Plant Sci, 15(2): 106–113

[4] Asai S, Ohta K, Yoshioka H (2008). MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell, 20(5): 1390–1406

[5] Asai T, Tena G, Plotnikova J, Willmann M R, Chiu W L, Gomez-Gomez L, Boller T, Ausubel F M, Sheen J (2002). MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415(6875): 977–983

[6] Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W (2009). Paternal control of embryonic patterning in Arabidopsis thaliana. Science, 323(5920): 1485–1488

[7] Bergmann D C, Lukowitz W, Somerville C R (2004). Stomatal development and pattern controlled by a MAPKK kinase. Science, 304(5676): 1494–1497

[8] Boudsocq M, Willmann M R, McCormack M, Lee H, Shan L, He P, Bush J, Cheng S H, Sheen J (2010). Differential innate immune signalling via Ca²⁺ sensor protein kinases. Nature, 464(7287): 418–422

[9] Brader G, Djamei A, Teige M, Palva E T, Hirt H (2007). The MAP kinase kinase MKK2 affects disease resistance in Arabidopsis. Mol Plant Microbe Interact, 20(5): 589–596

[10] Calderini O, Glab N, Bergounioux C, Heberle-Bors E, Wilson C (2001). A novel tobacco mitogen-activated protein (MAP) kinase kinase, NtMEK1, activates the cell cycle-regulated p43Ntf6 MAP kinase. J Biol Chem, 276(21): 18139–18145

[11] Cardinale F, Meskiene I, Ouaked F, Hirt H (2002). 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, 14(3): 703–711

[12] Chang L, Karin M (2001). Mammalian MAP kinase signalling cascades. Nature, 410(6824): 37–40

[13] Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker J R (1997). Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell, 89(7): 1133–1144

[14] Clark K L, Larsen P B, Wang X, Chang C (1998). Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc Natl Acad Sci USA, 95(9): 5401–5406

[15] Clarke A, Desikan R, Hurst R D, Hancock J T, Neill S J (2000). NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant J, 24(5): 667–677

[16] Dai Y, Wang H, Li B, Huang J, Liu X, Zhou Y, Mou Z, Li J (2006). Increased expression of MAP KINASE KINASE7 causes deficiency in polar auxin transport and leads to plant architectural abnormality in Arabidopsis. Plant Cell, 18(2): 308–320

[17] Dóczi R, Brader G, Pettkó-Szandtner A, Rajh I, Djamei A, Pitzschke A, Teige M, Hirt H (2007). The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell, 19(10): 3266–3279

[18] Ekengren S K, Liu Y, Schiff M, Dinesh-Kumar S P, Martin G B (2003). Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J, 36(6): 905–917

[19] Gadjev I, Vanderauwera S, Gechev T S, Laloi C, Minkov I N, Shulaev V, Apel K, Inzé D, Mittler R, Van Breusegem F (2006). Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol, 141(2): 436–445

[20] Gómez-Gómez L, Boller T (2000). FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell, 5(6): 1003–1011

[21] Gomi K, Ogawa D, Katou S, Kamada H, Nakajima N, Saji H, Soyano T, Sasabe M, Machida Y, Mitsuhara I, Ohashi Y, Seo S (2005). 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, 46(12): 1902–1914

[22] Hamel L P, Nicole M C, Sritubtim S, Morency M J, Ellis M, Ehlting J, Beaudoin N, Barbazuk B, Klessig D, Lee J, Martin G, Mundy J, Ohashi Y, Scheel D, Sheen J, Xing T, Zhang S, Seguin A, Ellis B E (2006). Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci, 11(4): 192–198

[23] Huang Y, Li H, Hutchison C E, Laskey J, Kieber J J (2003). Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis. Plant J, 33(2): 221–233

[24] Ichimura K, Casais C, Peck S C, Shinozaki K, Shirasu K (2006). MEKK1 is required for MPK4 activation and regulates tissue-specific and temperature-dependent cell death in Arabidopsis. J Biol Chem, 281(48): 36969–36976

[25] Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000). Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J, 24(5): 655–665

[26] Jonak C, Okrész L, Bögre L, Hirt H (2002). Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol, 5(5): 415–424

[27] Khokhlatchev A V, Canagarajah B, Wilsbacher J, Robinson M, Atkinson M, Goldsmith E, Cobb M H (1998). Phosphorylation of the MAP kinase ERK2 promotes its homodimerization and nuclear translocation. Cell, 93(4): 605–615

[28] Kieber J J, Rothenberg M, Roman G, Feldmann K A, Ecker J R (1993). CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell, 72(3): 427–441

[29] Kiegerl S, Cardinale F, Siligan C, Gross A, Baudouin E, Liwosz A, Eklöf S, Till S, Bögre L, Hirt H, Meskiene I (2000). SIMKK, a mitogen-activated protein kinase (MAPK) kinase, is a specific activator of the salt stress-induced MAPK, SIMK. Plant Cell, 12(11): 2247–2258

[30] Kishi-Kaboshi M, Okada K, Kurimoto L, Murakami S, Umezawa T, Shibuya N, Yamane H, Miyao A, Takatsuji H, Takahashi A, Hirochika H (2010). A rice fungal MAMP-responsive MAPK cascade regulates metabolic flow to antimicrobial metabolite synthesis. Plant J, 63(4): 599–612

[31] Kumar D, Klessig D F (2000). Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid. Mol Plant Microbe Interact, 13(3): 347–351

[32] Kumar K, Rao K P, Biswas D K, Sinha A K (2011). Rice WNK1 is regulated by abiotic stress and involved in internal circadian rhythm. Plant Signal Behav, 6(3): 316–320

[33] Kumar K, Rao K P, Sharma P, Sinha A K (2008). Differential regulation of rice mitogen activated protein kinase kinase (MKK) by abiotic stress. Plant Physiol Biochem, 46(10): 891–897

[34] Lee J S, Huh K W, Bhargava A, Ellis B E (2008). Comprehensive analysis of protein-protein interactions between Arabidopsis MAPKs and MAPK kinases helps define potential MAPK signalling modules. Plant Signal Behav, 3(12): 1037–1041

[35] Liu Y, Jin H, Yang K Y, Kim C Y, Baker B, Zhang S (2003). Interaction between two mitogen-activated protein kinases during tobacco defense signaling. Plant J, 34(2): 149–160

[36] Liu Y, 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(12): 3386–3399

[37] Liu Y K, Liu Y B, Zhang M Y, Li D Q (2010). Stomatal development and movement: the roles of MAPK signaling. Plant Signal Behav, 5(10): 1176–1180

[38] MacRobbie E A, Kurup S (2007). Signalling mechanisms in the regulation of vacuolar ion release in guard cells. New Phytol, 175(4): 630–640

[39] MAPK Group (2002). Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci, 7(7): 301–308

[40] Matsuoka D, Nanmori T, Sato K I, Fukami Y, Kikkawa U, 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(5): 637–647

[41] Mészáros T, Helfer A, Hatzimasoura E, Magyar Z, Serazetdinova L, Rios G, Bardóczy V, Teige M, Koncz C, Peck S, Bögre L (2006). The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin. Plant J, 48(4): 485–498

[42] Mockaitis K, Howell S H (2000). Auxin induces mitogenic activated protein kinase (MAPK) activation in roots of Arabidopsis seedlings. Plant J, 24(6): 785–796

[43] Mou Z, Wang X, Fu Z, Dai Y, Han C, Ouyang J, Bao F, Hu Y, Li J (2002). Silencing of phosphoethanolamine N-methyltransferase results in temperature-sensitive male sterility and salt hypersensitivity in Arabidopsis. Plant Cell, 14(9): 2031–2043

[44] Munnik T, Ligterink W, Meskiene I, Calderini O, Beyerly J, Musgrave A, Hirt H (1999). Distinct osmo-sensing protein kinase pathways are involved in signalling moderate and severe hyper-osmotic stress. Plant J, 20(4): 381–388

[45] Nakagami H, Soukupová H, Schikora A, Zárský V, Hirt H (2006). A Mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J Biol Chem, 281(50): 38697–38704

[46] Neill S J, Desikan R, Clarke A, Hurst R D, Hancock J T (2002). Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot, 53(372): 1237–1247

[47] Pedley K F, Martin G B (2004). Identification of MAPKs and their possible MAPK kinase activators involved in the Pto-mediated defense response of tomato. J Biol Chem, 279(47): 49229–49235

[48] Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen H B, Lacy M, Austin M J, Parker J E, Sharma S B, Klessig D F, Martienssen R, Mattsson O, Jensen A B, Mundy J (2000). Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell, 103(7): 1111–1120

[49] Pitzschke A, Hirt H (2006). Mitogen-activated protein kinases and reactive oxygen species signaling in plants. Plant Physiol, 141(2): 351–356

[50] Popescu S C, Popescu G V, Bachan S, Zhang Z, Gerstein M, Snyder M, Dinesh-Kumar S P (2009). MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev, 23(1): 80–92

[51] Qiu J L, Zhou L, Yun B W, Nielsen H B, Fiil B K, Petersen K, Mackinlay J, Loake G J, Mundy J, 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(1): 212–222

[52] Rao K P, Richa T, Kumar K, Raghuram B, Sinha A K (2010). In silico analysis reveals 75 members of mitogen-activated protein kinase kinase kinase gene family in rice. DNA Res, 17(3): 139–153

[53] Rao K P, Vani G, Kumar K, Wankhede D P, Misra M, Gupta M, Sinha A K (2011). Arsenic stress activates MAP kinase in rice roots and leaves. Arch Biochem Biophys, 506(1): 73–82

[54] Rodriguez M C, Petersen M, Mundy J (2010). Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol, 61(1): 621–649

[55] Saito N, Nakamura Y, Mori I C, Murata Y (2009). Nitric oxide functions in both methyl jasmonate signaling and abscisic acid signaling in Arabidopsis guard cells. Plant Signal Behav, 4(2): 119–120

[56] Seo S, Sano H, Ohashi Y (1999). Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinase. Plant Cell, 11(2): 289–298

[57] Sinha A K, Jaggi M, Raghuram B, Tuteja N (2011). Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal Behav, 6(2): 196–203

[58] Suarez-Rodriguez M C, Adams-Phillips L, Liu Y, Wang H, Su S H, Jester P J, Zhang S, Bent A F, Krysan P J (2007). MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Physiol, 143(2): 661–669

[59] Takahashi F, Yoshida R, Ichimura K, Mizoguchi T, Seo S, Yonezawa M, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K (2007). The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. Plant Cell, 19(3): 805–818

[60] Teige M, Scheikl E, Eulgem T, Dóczi R, Ichimura K, Shinozaki K, Dangl J L, Hirt H (2004). The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell, 15(1): 141–152

[61] Thoma I, Loeffler C, Sinha A K, Gupta M, Krischke M, Steffan B, Roitsch T, Mueller M J (2003). Cyclopentenone isoprostanes induced by reactive oxygen species trigger defense gene activation and phytoalexin accumulation in plants. Plant J, 34(3): 363–375

[62] Turner J G, Ellis C, Devoto A (2002). The jasmonate signal pathway. Plant Cell, 14(Suppl): S153–S164

[63] Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inzé D, Van Breusegem F (2005). Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol, 139(2): 806–821

[64] Wang H, Ngwenyama N, Liu Y, Walker J C, Zhang S (2007). Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell, 19(1): 63–73

[65] Wang P, Du Y, Li Y, Ren D, Song C P (2010). Hydrogen peroxide-mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell, 22(9): 2981–2998

[66] Wen J Q, Oono K, Imai R (2002). Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice. Plant Physiol, 129(4): 1880–1891

[67] Whitmarsh A J (2007). Regulation of gene transcription by mitogen-activated protein kinase signaling pathways. Biochim Biophys Acta, 1773(8): 1285–1298

[68] Xing Y, Jia W, Zhang J (2008). AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J, 54(3): 440–451

[69] Xiong L, Yang Y (2003). Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell, 15(3): 745–759

[70] Xu J, Li Y, Wang Y, Liu H, Lei L, Yang H, Liu G, Ren D (2008). Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. J Biol Chem, 283(40): 26996–27006

[71] Yamamoto A, Katou S, Yoshioka H, Doke N, Kawakita K (2004). Involvement of nitric oxide generation in hypersensitive cell death induced by elicitin in tobacco cell suspension culture. J Gen Plant Pathol, 70(2): 85–92

[72] Yang K Y, Liu Y, Zhang S (2001). Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc Natl Acad Sci USA, 98(2): 741–746

[73] Yoo S D, Cho Y H, Tena G, Xiong Y, Sheen J (2008). Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature, 451(7180): 789–795

[74] You M K, Oh S L, Ok S H, Cho S K, Shin H Y, Jeung J U, Shin J S (2007). Identification of putative MAPK Kinase in Oryza minuta and O. sativa responsive to biotic stresses. Mol Cell, 23(1): 108–114

[75] Zhang A, Jiang M, Zhang J, Ding H, Xu S, Hu X, Tan M (2007a). 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, 175(1): 36–50

[76] Zhang S, Klessig D F (1998). The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc Natl Acad Sci USA, 95(12): 7225–7230

[77] Zhang X, Dai Y, Xiong Y, DeFraia C, Li J, Dong X, Mou Z (2007). Overexpression of Arabidopsis MAP kinase kinase 7 leads to activation of plant basal and systemic acquired resistance. Plant J, 52(6): 1066–1079

Acknowledgments

Senior research fellowship to K. K. and D. P. W. during Ph.D. program from University Grants Commission, India is gratefully acknowledged. We apologize to colleagues whose work was not discussed owing to space constraints.

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2014 Higher Education Press and Springer-Verlag Berlin Heidelberg