Plant mitogen-activated protein kinases and their roles in mediation of signal transduction in abiotic stresses

Abstract

Mitogen-activated protein kinase (MAPK) cascade plays a central role in transfer information from diverse receptors/sensors to a wide range of cellular responses in plants. MAP kinases are organized into a complex network for efficient transmission of specific stimuli, including the abiotic stress signaling. In recent years, the mutants of loss-of-function and gain-of-function, and other additional tools are used to investigate the plant MAPK cascades. This review has summarized the recent progress on the MAPK cascade involved in mediation of the transduction of several pronounced abiotic stress signalings, such as salt, drought, low and high temperature, wound, hormone, and deficient nutrients. Currently, although part of the components of the MAPK cascade responding to the abiotic stresses have been identified, the integral molecular mechanisms of the abiotic stresses signaling transduction mediated via MAPK cascade are largely unknown and need to be elucidated further in the future.

Keywords

MAP kinase / abiotic stress / signaling / signal transduction / molecular mechanism

References

[1] Ahlfors R, Macioszek V, Rudd J, Brosché M, Schlichting R, Scheel D, Kangasjärvi J (2004). Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J, 40(4): 512–522

[2] Apel K, Hirt H (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol, 55(1): 373–399

[3] Bartels S, Anderson J C, González Besteiro M A, Carreri A, Hirt H, Buchala A, Métraux J P, Peck S C, Ulm R (2009). MAP kinase phosphatase1 and protein tyrosine phosphatase1 are repressors of salicylic acid synthesis and SNC1-mediated responses in Arabidopsis. Plant Cell, 21(9): 2884–2897

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

[5] Blanco F A, Zanetti M E, Casalongué C A, Daleo G R (2006). Molecular characterization of a potato MAP kinase transcriptionally regulated by multiple environmental stresses. Plant Physiol Biochem, 44(5-6): 315–322

[6] Bogre L, Ligterink W, Meskiene I, Barker P J, Heberle-Bors E, Huskisson N S, Hirt H (1997). Wounding induces the rapid and transient activation of a specific MAP kinase pathway. Plant Cell, 9(1): 75–83

[7] 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

[8] Burnett E C, Desikan R, Moser R C, Neill S J (2000). ABA activation of an MBP kinase in Pisum sativum epidermal peels correlates with stomatal responses to ABA. J Exp Bot, 51(343): 197–205

[9] Chen Z, Gibson T B, Robinson F, Silvestro L, Pearson G, Xu B, Wright A, Vanderbilt C, Cobb M H (2001). MAP kinases. Chem Rev, 101(8): 2449–2476

[10] Cobb M H, Goldsmith E J (1995). How MAP kinases are regulated. J Biol Chem, 270(25): 14843–14846

[11] Davis R J (2000). Signal transduction by the JNK group of MAP kinases. Cell, 103(2): 239–252

[12] Droillard M J, Thibivilliers S, Cazalé A C, Barbier-Brygoo H, Laurière C (2000). Protein kinases induced by osmotic stresses and elicitor molecules in tobacco cell suspensions: two crossroad MAP kinases and one osmoregulation-specific protein kinase. FEBS Lett, 474(2-3): 217–222

[13] 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

[14] 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

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

[16] Jiang J, Han S, Song C P (2007). SB202190 modulate salicylic acid-induced H2O2 generation in Vicia guard cells. Chin Bull Bot, 24(4): 444–451 (in Chinese)

[17] Jonak C, Kiegerl S, Ligterink W, Barker P J, Huskisson N S, 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(20): 11274–11279

[18] Jonak C, Ligterink W, Hirt H (1999). MAP kinases in plant signal transduction. Cell Mol Life Sci, 55(2): 204–213

[19] Jonak C, Nakagami H, Hirt H (2004). Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol, 136(2): 3276–3283

[20] 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

[21] Katou S, Kuroda K, Seo S, Yanagawa Y, Tsuge T, Yamazaki M, Miyao A, Hirochika H, Ohashi Y (2007). A calmodulin-binding mitogen-activated protein kinase phosphatase is induced by wounding and regulates the activities of stress-related mitogen-activated protein kinases in rice. Plant Cell Physiol, 48(2): 332–344

[22] Knetsch M L W, Wang M, Snaar-Jagalska B E, Heimovaara-Dijkstra S (1996). Abscisic acid induces mitogen-activated protein kinase activation in barley aleurone protoplasts. Plant Cell, 8(6): 1061–1067

[23] Kovtun Y, Chiu W L, Tena G, Sheen J (2000). Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA, 97(6): 2940–2945

[24] 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

[25] Lee M O, Cho K, Kim S H, Jeong S H, Kim J A, Jung Y H, Shim J, Shibato J, Rakwal R, Tamogami S, Kubo A, Agrawal G K, Jwa N S (2008). Novel rice OsSIPK is a multiple stress responsive MAPK family member showing rhythmic expression at mRNA level. Planta, 227(5): 981–990

[26] Lin C W, Chang H B, Huang H J (2005). Zinc induces mitogen-activated protein kinase activation mediated by reactive oxygen species in rice roots. Plant Physiol Biochem, 43(10-11): 963–968

[27] Lu C, Han M H, Guevara-Garcia A, Fedoroff N V (2002). Mitogen-activated protein kinase signaling in postgermination arrest of development by abscisic acid. Proc Natl Acad Sci USA, 99(24): 15812–15817

[28] Lu W J, Li R J, Wang X Y, Li X J, Guo C J, Gu J T, Xiao K (2009). Cloning and expression analysis of a wheat Mitogen-activated protein kinase gene of TaMPK1a-1 that responding to deficient-Pi. Scientia Agric Sinica, 42(7): 2601–2607 (in Chinese)

[29] Miles G P, Samuel M A, Zhang Y, Ellis B E (2005). RNA interference-based (RNAi) suppression of AtMPK6, an mitogen-activated protein kinase, results in hypersensitivity to ozone and misregulation of AtMPK3. Environ Pollut, 138(2): 230–237

[30] 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(2): 765–769

[31] Munnik T, Ligterink W, Meskiene I 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

[32] Nakagami H, Pitzschke A, Hirt H (2005). Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci, 10(7): 339–346

[33] 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

[34] Ning J, Yuan B, Xie K B, Hu H H, Wu C Q, Xiong L Z (2006). Isolation and identification of SA and JA inducible protein kinase gene OsSJMK1 in rice. Acta Genetica Sinica, 33(7): 625–633

[35] Ouaked F, Rozhon W, Lecourieux D, Hirt H (2003). A MAPK pathway mediates ethylene signaling in plants. EMBO J, 22(6): 1282–1288

[36] Peng L X, Gu L K, Zheng C C, Li D Q, Shu H R (2006). Expression of MaMAPK gene in seedlings of Malus L. under water stress. Acta Biochim Biophys Sin (Shanghai), 38(4): 281–286

[37] Peng L X, Zheng C C, Li D Q, Gu L K, Shu H R (2003). Cloning and expression characteristics of MaMAPK gene of Malus micromalus. J Plant Physiol Mol Biol, 29(5): 431–436 (in Chinese)

[38] Pitzschke A, Djamei A, Bitton F, Hirt H (2009). A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol Plant, 2(1): 120–137

[39] Pöpping B, Gibbons T, Watson M D (1996). The Pisum sativum MAP kinase homologue (PsMAPK) rescues the Saccharomyces cerevisiae hog1 deletion mutant under conditions of high osmotic stress. Plant Mol Biol, 31(2): 355–363

[40] Reyna N S, Yang Y N (2006). Molecular analysis of the rice MAP kinase gene family in relation to Magnaporthe grisea infection. Mol Plant Microbe Interact, 19(5): 530–540

[41] Samuel M A, Ellis B E (2002). Double jeopardy: both overexpression and suppression of a redox-activated plant mitogen-activated protein kinase render tobacco plants ozone sensitive. Plant Cell, 14(9): 2059–2069

[42] Samuel M A, Miles G P, Ellis B E (2000). Ozone treatment rapidly activates MAP kinase signalling in plants. Plant J, 22(4): 367–376

[43] Sangwan V, Orvar B L, Beyerly J, Hirt H, Dhindsa R S (2002). Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J, 31(5): 629–638

[44] Seo S, Katou S, Seto H, Gomi K, Ohashi Y (2007). The mitogen-activated protein kinases WIPK and SIPK regulate the levels of jasmonic and salicylic acids in wounded tobacco plants. Plant J, 49(5): 899–909

[45] Seo S, Okamoto M, Seto H, Ishizuka K, Sano H, Ohashi Y (1995). Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science, 270(5244): 1988–1992

[46] 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

[47] Suzuki N, Rizhsky L, Liang H, Shuman J, Shulaev V, Mittler R (2005). Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiol, 139(3): 1313–1322

[48] 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

[49] 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

[50] Usami S, Banno H, Ito Y, Nishihama R, Machida Y (1995). Cutting activates a 46-kilodalton protein kinase in plants. Proc Natl Acad Sci USA, 92(19): 8660–8664

[51] Wang M M, Zhang Y, Wang J, Wu X L, Guo X Q (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(3): 325–332

[52] Wang W, Vinocur B, Altman A (2003). Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta, 218(1): 1–14

[53] Widmann C, Gibson S, Jarpe M B, Johnson G L (1999). Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev, 79(1): 143–180

[54] Wu J Q, Hettenhausen C, Meldau S, Baldwin I T (2007). Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell, 19(3): 1096–1122

[55] 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

[56] 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

[57] 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

[58] Xu S C, Ding H D, Sang J R (2007). Reactive oxygen species, metabolism, and signal transduction in plant cells. Acta Botanica Yunnanica, 29(3): 355–365 (in Chinese)

[59] Yeh C M, Chien P S, Huang H J (2006). Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. J Exp Bot, 58(3): 659–671

[60] 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

[61] Yu S W, Tang K X (2004). MAP kinase cascades responding to environmental stress in plants. Acta Bot Sin, 46(2): 127–136

[62] Zhang A Y, Jiang M Y, Zhang J H, Tan M P, Hu X L (2006). Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol, 141(2): 475–487

[63] 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

[64] Zong X J, Li D P, Gu L K, Li D Q, Liu L X, Hu X L (2009). 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, 229(3): 485–495

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 30971773) and Key Laboratory of Crop Growth Regulation of Hebei Province.

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2014 Higher Education Press and Springer-Verlag Berlin Heidelberg