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MAPK cascades and major abiotic stresses

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Abstract

Plants have evolved with complex signaling circuits that operate under multiple conditions and govern numerous cellular functions. Stress signaling in plant cells is a sophisticated network composed of interacting proteins organized into tiered cascades where the function of a molecule is dependent on the interaction and the activation of another. In a linear scheme, the receptors of cell surface sense the stimuli and convey stress signals through specific pathways and downstream phosphorylation events controlled by mitogen-activated protein (MAP) kinases and second messengers, leading to appropriate adaptive responses. The specificity of the pathway is guided by scaffolding proteins and docking domains inside the interacting partners with distinctive structures and functions. The flexibility and the fine-tuned organization of the signaling molecules drive the activated MAP kinases into the appropriate location and connection to control and integrate the information flow. Here, we overview recent findings of the involvement of MAP kinases in major abiotic stresses (drought, cold and temperature fluctuations) and we shed light on the complexity and the specificity of MAP kinase signaling modules.

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Abbreviations

MAP:

Mitogen activated protein

MAPK:

Mitogen activated protein kinase

MAP2K, MEK, MKK, or MAPKK:

MAPK kinase

MAP3K, MEKK, MKKK or MAPKKK:

MAPK kinase kinase

MAP4K, MEKKK, MKKKK or MAPKKKK:

MAPK kinase kinase kinase

S/T:

Serine/threonine

T(E/D)Y:

Threonine(glutamate/aspartate)tyrosine

References

  • Abele D, Heise K, Portner HO, Puntarulo S (2002) Temperature-dependence of mitochondrial function and production of reactive oxygen species in the intertidal mud clam Mya arenaria. J exp biol 205:1831–1841

    CAS  PubMed  Google Scholar 

  • Agarwal PK, Gupta K, Jha B (2010) Molecular characterization of the Salicornia brachiata SbMAPKK gene and its expression by abiotic stress. Mol Biol Rep 37:981–986

    Article  CAS  PubMed  Google Scholar 

  • Agrawal GK, Rakwal R, Iwahashi H (2002) 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 294:1009–1016

    Article  CAS  PubMed  Google Scholar 

  • Agrawal GK, Agrawal SK, Shibato J, Iwahashi H, Rakwal R (2003) Novel rice MAP kinases OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation. Biochem Biophys Res Commun 300:775–783

    Article  CAS  PubMed  Google Scholar 

  • Alzwiy IA, Morris PC (2007) A mutation in the Arabidopsis MAP kinase kinase 9 gene results in enhanced seedling stress tolerance. Plant Sci 173:302–308

    Article  CAS  Google Scholar 

  • An D, Yang J, Zhang P (2012) Transcriptome profiling of low temperature-treated cassava apical shoots showed dynamic responses of tropical plant to cold stress. BMC Genom 13:64

    Article  CAS  Google Scholar 

  • Berberich T, Sano H, Kusano T (1999) Involvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maize. Mol Gen Genet MGG 262:534–542

    Article  CAS  Google Scholar 

  • Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273

    Article  PubMed Central  PubMed  Google Scholar 

  • Blanco FA, Zanetti ME, Casalongue CA, Daleo GR (2006) Molecular characterization of a potato MAP kinase transcriptionally regulated by multiple environmental stresses. Plant Physiol Biochem PPB/Societe francaise de physiologie vegetale 44:315–322

    Article  CAS  Google Scholar 

  • Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stress. In: Buchanan B, Grussem W, Jones R (eds) Biochemistry and molecular biology of plants, p 1158–1203

  • Droillard M, Boudsocq M, Barbier-Brygoo H, Lauriere C (2002) Different protein kinase families are activated by osmotic stresses in Arabidopsis thaliana cell suspensions. Involvement of the MAP kinases AtMPK3 and AtMPK6. FEBS Lett 527:43–50

    Article  CAS  PubMed  Google Scholar 

  • Droillard MJ, Boudsocq M, Barbier-Brygoo H, Lauriere C (2004) 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 574:42–48

    Article  CAS  PubMed  Google Scholar 

  • Edmunds JW, Mahadevan LC (2004) MAP kinases as structural adaptors and enzymatic activators in transcription complexes. J Cell Sci 117:3715–3723

    Article  CAS  PubMed  Google Scholar 

  • Feilner T, Hultschig C, Lee J, Meyer S, Immink RG, Koenig A, Possling A, Seitz H, Beveridge A, Scheel D, Cahill DJ, Lehrach H, Kreutzberger J, Kersten B (2005) High throughput identification of potential Arabidopsis mitogen-activated protein kinases substrates. Mol Cell Proteomics MCP 4:1558–1568

    Article  CAS  Google Scholar 

  • Fu SF, Chou WC, Huang DD, Huang HJ (2002) Transcriptional regulation of a rice mitogen-activated protein kinase gene, OsMAPK4, in response to environmental stresses. Plant Cell Physiol 43:958–963

    Article  CAS  PubMed  Google Scholar 

  • Gao L, Xiang CB (2008) The genetic locus At1g73660 encodes a putative MAPKKK and negatively regulates salt tolerance in Arabidopsis. Plant Mol Biol 67:125–134

    Article  CAS  PubMed  Google Scholar 

  • Gu L, Liu Y, Zong X, Liu L, Li DP, Li DQ (2010) Overexpression of maize mitogen-activated protein kinase gene, ZmSIMK1 in Arabidopsis increases tolerance to salt stress. Mol Biol Rep 37:4067–4073

    Article  CAS  PubMed  Google Scholar 

  • Hoang MHT, Nguyen XC, Lee K, Kwon YS, Pham HTT, Park HC, Yun D-J, Lim CO, Chung WS (2012) Phosphorylation by AtMPK6 is required for the biological function of AtMYB41 in Arabidopsis. Biochem Biophys Res Commun 422:181–186

    Article  CAS  PubMed  Google Scholar 

  • Hua ZM, Yang X, Fromm ME (2006) Activation of the NaCl- and drought-induced RD29A and RD29B promoters by constitutively active Arabidopsis MAPKK or MAPK proteins. Plant Cell Environ 29:1761–1770

    Article  CAS  PubMed  Google Scholar 

  • Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J Cell Mol Biol 24:655–665

    Article  CAS  Google Scholar 

  • Ichimura K, Shinozaki K, Tena G, Sheen J, Henry Y, Champion A, Kreis M, Zhang S, Hirt H, Wilson C, Heberle-Bors E, Ellis BE, Morris PC, Innes RW, Ecker JR, Scheel D, Klessig DF, Machida Y, Mundy J, Ohashi Y, Walker JC (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–308

    Article  CAS  Google Scholar 

  • Jammes F, Song C, Shin D, Munemasa S, Takeda K, Gu D, Cho D, Lee S, Giordo R, Sritubtim S, Leonhardt N, Ellis BE, Murata Y, Kwak JM (2009) MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. Proc Natl Acad Sci USA 106:20520–20525

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jeong M-J, Lee S-K, Kim B-G, Kwon T-R, Cho W-S, Park Y-T, Lee J-O, Kwon H-B, Byun M-O, Park S-C (2006) A rice (Oryza sativa L.) MAP kinase gene, OsMAPK44, is involved in response to abiotic stresses. Plant Cell Tissue Organ Cult 85:151–160

    Article  CAS  Google Scholar 

  • Jonak C, Kiegerl S, Ligterink W, Barker PJ, Huskisson NS, Hirt H (1996) Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci USA 93:11274–11279

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Karlson D, Imai R (2003) Conservation of the cold shock domain protein family in plants. Plant Physiol 131:12–15

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kiegerl S, Cardinale F, Siligan C, Gross A, Baudouin E, Liwosz A, Eklof S, Till S, Bogre 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 12:2247–2258

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kim JA, Agrawal GK, Rakwal R, Han KS, Kim KN, Yun CH, Heu S, Park SY, Lee YH, Jwa NS (2003) 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 300:868–876

    Article  CAS  PubMed  Google Scholar 

  • Kim SH, Woo DH, Kim JM, Lee SY, Chung WS, Moon YH (2011) Arabidopsis MKK4 mediates osmotic-stress response via its regulation of MPK3 activity. Biochem Biophys Res Commun 412:150–154

    Article  CAS  PubMed  Google Scholar 

  • Kim J-M, Woo D-H, Kim S-H, Lee S-Y, Park H-Y, Seok H-Y, Chung W, Moon Y-H (2012) Arabidopsis MKKK20 is involved in osmotic stress response via regulation of MPK6 activity. Plant Cell Rep 31:217–224

    Article  CAS  PubMed  Google Scholar 

  • Kong X, Pan J, Zhang M, Xing X, Zhou Y, Liu Y, Li D (2011a) ZmMKK4, a novel group C mitogen-activated protein kinase kinase in maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis. Plant Cell Environ 34:1291–1303

    Article  CAS  PubMed  Google Scholar 

  • Kong X, Sun L, Zhou Y, Zhang M, Liu Y, Pan J, Li D (2011b) ZmMKK4 regulates osmotic stress through reactive oxygen species scavenging in transgenic tobacco. Plant Cell Rep 30:2097–2104

    Article  CAS  PubMed  Google Scholar 

  • Kong F, Wang J, Cheng L, Liu S, Wu J, Peng Z, Lu G (2012) Genome-wide analysis of the mitogen-activated protein kinase gene family in Solanum lycopersicum. Gene 499:108–120

    Article  CAS  PubMed  Google Scholar 

  • Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608

    Article  CAS  PubMed  Google Scholar 

  • Kumar K, Rao KP, Sharma P, Sinha AK (2008) Differential regulation of rice mitogen activated protein kinase kinase (MKK) by abiotic stress. Plant Physiol Biochem PPB/Societe francaise de physiologie vegetale 46:891–897

    Article  CAS  Google Scholar 

  • Lee SK, Kim BG, Kwon TR, Jeong MJ, Park SR, Lee JW, Byun MO, Kwon HB, Matthews BF, Hong CB, Park SC (2011) Overexpression of the mitogen-activated protein kinase gene OsMAPK33 enhances sensitivity to salt stress in rice (Oryza sativa L.). J Biosci 36:139–151

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Yue H, Xing D (2012) MAP Kinase 6-mediated activation of vacuolar processing enzyme modulates heat shock-induced programmed cell death in Arabidopsis. New Phytol 195:85–96

    Article  CAS  PubMed  Google Scholar 

  • Link V, Sinha AK, Vashista P, Hofmann MG, Proels RK, Ehness R, Roitsch T (2002) A heat-activated MAP kinase in tomato: a possible regulator of the heat stress response. FEBS Lett 531:179–183

    Article  CAS  PubMed  Google Scholar 

  • Mikolajczyk M, Awotunde OS, Muszynska G, Klessig DF, Dobrowolska G (2000) Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. Plant Cell 12:165–178

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mizoguchi T, Irie K, Hirayama T, Hayashida N, Yamaguchi-Shinozaki K, Matsumoto K, Shinozaki K (1996) 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 93:765–769

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Moustafa K, Lefebvre-De Vos D, Leprince A-S, Savourée A, Laurière C (2008) Analysis of the Arabidopsis mitogen-activated protein kinase families: organ specificity and transcriptional regulation upon water stresses. Sch Res Exch. p 12. doi:10.3814/2008/143656

  • Nakagami H, Kiegerl S, Hirt H (2004) OMTK1, a novel MAPKKK, channels oxidative stress signaling through direct MAPK interaction. J Biol Chem 279:26959–26966

    Article  CAS  PubMed  Google Scholar 

  • Ning J, Li X, Hicks LM, Xiong L (2010) A raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol 152:876–890

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pan J, Zhang M, Kong X, Xing X, Liu Y, Zhou Y, Liu Y, Sun L, Li D (2012) ZmMPK17, a novel maize group D MAP kinase gene, is involved in multiple stress responses. Planta 235:661–676

    Article  CAS  PubMed  Google Scholar 

  • Pastenes C, Horton P (1996) Effect of high temperature on photosynthesis in beans (I. oxygen evolution and chlorophyll fluorescence). Plant Physiol 112:1245–1251

    CAS  PubMed Central  PubMed  Google Scholar 

  • Peng LX, Gu LK, Zheng CC, Li DQ, Shu HR (2006) Expression of MaMAPK gene in seedlings of Malus L. under water stress. Acta Biochim Biophys Sin (Shanghai) 38:281–286

    Article  CAS  Google Scholar 

  • Rengasamy P (2006) World salinization with emphasis on Australia. J Exp Bot 57:1017–1023

    Article  CAS  PubMed  Google Scholar 

  • Roberts EH (1988) Temperature and seed germination. Symp Soc Exp Biol 42:109–132

    CAS  PubMed  Google Scholar 

  • Sangwan V, Dhindsa RS (2002) In vivo and in vitro activation of temperature-responsive plant map kinases. FEBS Lett 531:561–564

    Article  CAS  PubMed  Google Scholar 

  • Sangwan V, Orvar BL, Beyerly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J Cell Mol Biol 31:629–638

    Article  CAS  Google Scholar 

  • Shi J, Zhang L, An H, Wu C, Guo X (2011) GhMPK16, a novel stress-responsive group D MAPK gene from cotton, is involved in disease resistance and drought sensitivity. BMC Mol Biol 12:22

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shou H, Bordallo P, Wang K (2004) Expression of the Nicotiana protein kinase (NPK1) enhanced drought tolerance in transgenic maize. J Exp Bot 55:1013–1019

    Article  CAS  PubMed  Google Scholar 

  • Suri SS, Dhindsa RS (2008) A heat-activated MAP kinase (HAMK) as a mediator of heat shock response in tobacco cells. Plant Cell Environ 31:218–226

    Article  CAS  PubMed  Google Scholar 

  • Tanoue T, Adachi M, Moriguchi T, Nishida E (2000) A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat Cell Biol 2:110–116

    Article  CAS  PubMed  Google Scholar 

  • Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152

    Article  CAS  PubMed  Google Scholar 

  • Vierling E (1991) The role of heat-shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620

    Article  CAS  Google Scholar 

  • Wang M, Zhang Y, Wang J, Wu X, Guo X (2007) A novel MAP kinase gene in cotton (Gossypium hirsutum L.), GhMAPK, is involved in response to diverse environmental stresses. J Biochem Mol Biol 40:325–332

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Ding H, Zhang A, Ma F, Cao J, Jiang M (2010) A novel mitogen-activated protein kinase gene in maize (Zea mays), ZmMPK3, is involved in response to diverse environmental cues. J Integr Plant Biol 52:442–452

    CAS  PubMed  Google Scholar 

  • Wen JQ, 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 129:1880–1891

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Went FW (1953) The effect of temperature on plant growth. Annu Rev Plant Physiol 4:347–362

    Article  Google Scholar 

  • Wu T, Kong X-P, Zong X-J, Li D-P, Li D-Q (2011) Expression analysis of five maize MAP kinase genes in response to various abiotic stresses and signal molecules. Mol Biol Rep 38:3967–3975

    Article  CAS  PubMed  Google Scholar 

  • Xie G, Kato H, Imai R (2012) Biochemical identification of the OsMKK6-OsMPK3 signalling pathway for chilling stress tolerance in rice. Biochem J 443:95–102

    Article  CAS  PubMed  Google Scholar 

  • 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 15:745–759

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xiong L, Ishitani M, Zhu JK (1999) Interaction of osmotic stress, temperature, and abscisic acid in the regulation of gene expression in Arabidopsis. Plant Physiol 119:205–212

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xu J, Chua NH (2012) Dehydration stress activates Arabidopsis MPK6 to signal DCP1 phosphorylation. EMBO J 31:1975–1984

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 283:26996–27006

    Article  CAS  PubMed  Google Scholar 

  • Xu H, Li K, Yang F, Shi Q, Wang X (2010) Overexpression of CsNMAPK in tobacco enhanced seed germination under salt and osmotic stresses. Mol Biol Rep 37:3157–3163

    Article  CAS  PubMed  Google Scholar 

  • Yamazaki T, Kawamura Y, Uemura M (2009) Extracellular freezing-induced mechanical stress and surface area regulation on the plasma membrane in cold-acclimated plant cells. Plant Signal Behav 4:231–233

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yu L, Nie J, Cao C, Jin Y, Yan M, Wang F, Liu J, Xiao Y, Liang Y, Zhang W (2010) Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New phytol 188:762–773

    Article  CAS  PubMed  Google Scholar 

  • Zhang T, Liu Y, Xue L, Xu S, Chen T, Yang T, Zhang L, An L (2006) Molecular cloning and characterization of a novel MAP kinase gene in Chorispora bungeana. Plant Physiol Biochem PPB/Societe francaise de physiologie vegetale 44:78–84

    Article  CAS  Google Scholar 

  • Zhang L, Xi D, Li S, Gao Z, Zhao S, Shi J, Wu C, Guo X (2011) A cotton group C MAP kinase gene, GhMPK2, positively regulates salt and drought tolerance in tobacco. Plant Mol Biol 77:17–31

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Institut National de la Santé et de la Recherche Médicale (INSERM), Créteil, France

    Khaled Moustafa

  2. United Arab Emirates University, Al Ain, United Arab Emirates

    Synan AbuQamar

  3. University of Modern Sciences, Dubai, United Arab Emirates

    Mohammad Jarrar

  4. Jazan University, Jazan, Saudi Arabia

    Abdul Jabbar Al-Rajab

  5. Université François-Rabelais, Tours, France

    Jocelyne Trémouillaux-Guiller

Authors
  1. Khaled Moustafa
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  2. Synan AbuQamar
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  3. Mohammad Jarrar
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  4. Abdul Jabbar Al-Rajab
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  5. Jocelyne Trémouillaux-Guiller
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Correspondence to Khaled Moustafa.

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Communicated by N. Stewart.

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Moustafa, K., AbuQamar, S., Jarrar, M. et al. MAPK cascades and major abiotic stresses. Plant Cell Rep 33, 1217–1225 (2014). https://doi.org/10.1007/s00299-014-1629-0

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