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.
Similar content being viewed by others
References
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
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
Andreasson E, Ellis B (2010). Convergence and specificity in the Arabidopsis MAPK nexus. Trends Plant Sci, 15(2): 106–113
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
Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel F M, Sheen J (2002). MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415(6875): 977–983
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
Bergmann D C, Lukowitz W, Somerville C R (2004). Stomatal development and pattern controlled by a MAPKK kinase. Science, 304(5676): 1494–1497
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
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
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
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
Chang L, Karin M (2001). Mammalian MAP kinase signalling cascades. Nature, 410(6824): 37–40
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Liu Y, Zhang S (2004). Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogenactivated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell, 16(12): 3386–3399
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
MacRobbie E A, Kurup S (2007). Signalling mechanisms in the regulation of vacuolar ion release in guard cells. New Phytol, 175(4): 630–640
MAPK Group (2002). Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci, 7(7): 301–308
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
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
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
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
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
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
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
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
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
Pitzschke A, Hirt H (2006). Mitogen-activated protein kinases and reactive oxygen species signaling in plants. Plant Physiol, 141(2): 351–356
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
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 mitogenactivated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol, 148(1): 212–222
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
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
Rodriguez MC, Petersen M, Mundy J (2010). Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol, 61(1): 621–649
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
Seo S, Sano H, Ohashi Y (1999). Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogenactivated protein kinase. Plant Cell, 11(2): 289–298
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
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
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
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
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
Turner J G, Ellis C, Devoto A (2002). The jasmonate signal pathway. Plant Cell, 14(Suppl): S153–S164
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
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
Wang P, Du Y, Li Y, Ren D, Song C P (2010). Hydrogen peroxidemediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell, 22(9): 2981–2998
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
Whitmarsh A J (2007). Regulation of gene transcription by mitogenactivated protein kinase signaling pathways. Biochim Biophys Acta, 1773(8): 1285–1298
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
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
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
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
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
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
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
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
Zhang S, Klessig D F (1998). The tobacco wounding-activated mitogenactivated protein kinase is encoded by SIPK. Proc Natl Acad Sci USA, 95(12): 7225–7230
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
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Kumar, K., Wankhede, D.P. & Sinha, A.K. Signal convergence through the lenses of MAP kinases: paradigms of stress and hormone signaling in plants. Front. Biol. 8, 109–118 (2013). https://doi.org/10.1007/s11515-012-1207-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11515-012-1207-1