Abstract
Low temperature is one of the most common environmental stresses affecting plant growth and agricultural production. The mitogen-activated protein kinase (MAPK) cascade plays a pivotal role in diverse signaling pathways related to plant development and stress responses. In this study, a novel MAPK gene, SlMPK7, in tomato (Solanum lycopersicum) belonging to group B MAPK was isolated and functionally characterized. QRT-PCR analysis revealed that transcription of the MAPK SlMPK7 in tomato leaves was triggered by abiotic stresses and exogenous signaling molecules. Moreover, hydrogen peroxide (H2O2) and Ca2+ mediated 4 °C-induced upregulated expression of SlMPK7 at the messenger RNA (mRNA) level. SlMPK7 was predominantly localized in the nucleus. Transgenic tomato overexpressing SlMPK7 accumulated less reactive oxygen species (ROS), more superoxide dismutase, peroxidase, catalase activities, more proline and soluble sugar contents, and more stress-responsive gene expression, leading to enhanced chilling stress tolerance compared with the wild-type plants. Collectively, these data demonstrate that SlMPK7 acts as a positive regulator in the response to chilling stress by regulating ROS homeostasis through activation of cellular antioxidant systems and modulating the transcription of stress-associated genes.
Similar content being viewed by others
References
Agell N, Bachs O, Rocamora N, Villalonga P (2002) Modulation of the Ras/Raf/MEK/ERK pathway by Ca2+ and calmodulin. Cell Signal 14:649–654
Ahlfors R, Macioszek V, Rudd J, Brosche M, Schlichting R, Scheel D, Kangasjarvi J (2004) Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J 40:512–522
Bari R, Jones JD (2009) Role of plant hormones in plant defense responses. Plant Mol Biol 69:473–488
Beckers GJ, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, Conrath U (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21:944–953
Cargnello M, Roux P (2011) Activation and function of the MAPKs and their substrates, the MAPK activated protein kinases. Microbiol Mol Biol Rev 75:50–83
Couee I, Sulmon C, Gouesbet G, Amrani AE (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459
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
Du XM, Zhao XL, Li XJ, Guo CJ, Lu WJ, Gu JT, Xiao K (2013) Overexpression of TaSRK2C1, a wheat SNF1 related protein kinase 2 gene, increases tolerance to dehydration, salt, and low temperature in transgenic tobacco. Plant Mol Biol Rep 31:810–821
Duan KX, Yang HQ, Ran K, You SZ, Zhao HZ, Jiang QQ (2009) Characterization of a novel stress-response member of the MAPK family in Malus hupehensis Rehd. Plant Mol Biol Rep 27:69–78
Duan M, Feng HL, Wang LY, Li D, Meng QW (2012) Overexpression of thylakoidal ascorbate peroxidase shows enhanced resistance to chilling stress in tomato. J Plant Physiol 169:867–877
Einset J, Winge P, Bones A (2007) ROS signaling pathways in chilling stress. Plant Signal Behav 2:365–367
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. Mole Cell Proteom 4:1558–1568
Fillatti JJ, Kiser J, Rose R, Comai L (1987) Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Biotechnology 5:726–730
Hamel LP, Nicole MC, Sritubtim S, Morency MJ, Ellis M, Ehlting J (2006) Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci 11:192–198
Heidarvand L, Amiri RM (2010) What happens in plant molecular responses to cold stress? Acta Physiol Plant 32:419–431
Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231
Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J 24:655–665
Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2002) Mitogen activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–308
Irigoyen JJ, Emerich DW, Sanchez DM (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60
Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defense system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273
Jonak C, Ökrész L, Bogre L, Hirt H (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 5:415–424
Kandoth PK, Ranf S, Pancholi SS, Jayanty S, Walla MD, Miller W, Howe GA, Lincoln DE, Stratmann JW (2007) Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systemin mediated defense response against herbivorous insects. Proc Natl Acad Sci 104:12205–12210
Knight MR, Campbell AK, Smith SM, Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352:524–526
Kong X, Pan J, Zhang M, Xing X, Zhou Y, Liu Y, Li D, Li D (2011) 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
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
Kumar KR, Srinivasan T, Kirti PB (2009) A mitogen-activated protein kinase gene, AhMPK3 of peanut: molecular cloning, genomic organization, and heterologous expression conferring resistance against Spodoptera litura in tobacco. Mol Genet Genomics 282:65–81
Kumar K, Wankhede DP, Sinha AK (2013) Signal convergence through the lenses of MAP kinases: paradigms of stress and hormone signaling in plants. Front Biol 8:109–118
Lee JT, Prasad V, Yang PT, Wu JF, David HTH, Charng YY, Chan MT (2003) Expression of Arabidopsis CBF1 regulated by an ABA/stress inducible promoter in transgenic tomato confers stress tolerance without affecting yield. Plant Cell Environ 26:1181–1190
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
Li JT, Wang N, Xin HP, Li SH (2013) Overexpression of VaCBF4, a transcription factor from Vitis amurensis, improves cold tolerance accompanying increased resistance to drought and salinity in Arabidopsis. Plant Mol Biol Rep 31:1518–1528
Liu J, Zhu JK (1997) Proline accumulation and salt stress induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol 114:591–596
Liu JH, Kitashiba H, Wang J, Ban Y, Moriguchi T (2007) Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnol 24:117–126
Liu HY, Feng DR, Liu B, He YM, Wang HB, Wang JF (2009a) Studies on subcellular localization of MpASR in onion epidermal cells mediated by Agrobacterium (in Chinese). J Trop Subtrop Bot 17:218–222
Liu LX, Hu X, Song J, Zong X, Li DP, Li DQ (2009b) Over-expression of a Zea mays L. protein phosphatase 2C gene (ZmPP2C) in Arabidopsis thaliana decreases tolerance to salt and drought. J Plant Physiol 166:531–542
Liu X, Wang Z, Wang L, Wu R, Phillips J, Deng X (2009c) LEA4 group genes from the resurrection plant Boea hygrometrica confer dehydration tolerance in transgenic tobacco. Plant Sci 176:90–98
Liu YK, Zhang D, Wang L, Li DQ (2013) Genome wide analysis of mitogen-activated protein kinase gene family in maize. Plant Mol Biol Rep 31:1446–1460
Maria H, Ian T, Baldwin WJQ (2012) Three MAPK kinases, MEK1, SIPKK, and NPK2, are not involved in activation of SIPK after wounding and herbivore feeding but important for accumulation of trypsin proteinase inhibitors. Plant Mol Biol Rep 30:731–740
Mayrose M, Bonshtien A, Sessa G (2004) LeMPK3 is a mitogen-activated protein kinase with dual specificity induced during tomato defense and wounding responses. J Biol Chem 279:14819–14827
Melech BS, Sessa G (2011) The SlMKK2 and SlMPK2 genes play a role in tomato disease resistance to Xanthomonas campestris pv. Vesicatoria. Plant Signal Behav 6:154–156
Nadarajah K, Sidek HM (2010) The green MAPKs. Asian J Plant Sci 9:1–10
Patterson BD, Mutton L, Paull RE, Nguyen VQ (1987) Tomato pollen development: stages sensitive to chilling and a natural environment for the selection of resistant genotypes. Plant Cell Environ 10:363–368
Pedley KF, Martin GB (2004) Identification of MAPKs and their possible MAPK kinase activators involved in the Pto-mediated defense response of tomato. J Biol Chem 279:49229–49235
Pitzschke A, Djamei A, Bitton F, Hirt H (2009) A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signaling. Mol Plant 2:120–137
Pozo DO, Pedley KF, Martin GB (2004) MAPKKKa is a positive regulator of cell death associated with both plant immunity and disease. EMBO J 23:3072–3082
Rodriguez MC, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Physiol Plant Mol Biol 161:621–649
Rohila JS, Yang YN (2007) Rice mitogen-activated protein kinase gene family and its role in biotic and abiotic stress response. J Integr Plant Biol 49:751–759
Shan DP, Huang JG, Yang YT, Guo YH, Wu CA, Yang GD, Gao Z, Zheng CC (2007) Cotton GhDREB1 increases plant tolerance to low temperature and is negatively regulated by gibberellic acid. New Phytol 176:70–81
Song F, Goodman RM (2002) OsBIMK1, a rice MAP kinase gene involved in disease resistance responses. Planta 215:997–1005
Stulemeijer IJ, Stratmann JW, Joosten MH (2007) Tomato mitogen-activated protein kinases LeMPK1, LeMPK2, and LeMPK3 are activated during the Cf-4/Avr4-induced hypersensitive response and have distinct phosphorylation specificities. Plant Physiol 144:1481–1494
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
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
Wurzinger B, Mair A, Pfister B, Teige M (2011) Cross-talk of calcium-dependent protein kinase and MAP kinase signaling. Plant Signal Behav 6:8–12
Xing Y, Jia WS, Zhang JH (2008) AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J 54:440–451
Yuasa T, Ichimura K, Mizoguchi T, Shinozaki K (2001) Oxidative stress activates ATMPK6, an Arabidopsis homologue of MAP kinase. Plant Cell Physiol 42:1012–1016
Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6:520–527
Zhang A, Jiang M, Zhang J, Tan M, Hu X (2006a) 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 141:475–487
Zhang T, Liu Y, Yang T, Zhang L, Xu S, Xue L (2006b) Diverse signals converge at MAPK cascades in plant. Plant Physiol Biochem 44:274–283
Zhou Y, Zhang D, Pan JW, Kong XP, Liu YK, Sun LP, Wang L, Li DQ (2012) Overexpression of a multiple stress-responsive gene, ZmMPK4, enhances tolerance to low temperature in transgenic tobacco. Plant Physiol Biochem 58:174–181
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Zong XJ, Li DP, Gu LK, Liu LX, Hu XL, Li DQ (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 229:485–495
Acknowledgments
We thank the editors and reviewers for their critical reading and constructive suggestions. This work was funded by Shanghai Academy of Agricultural Sciences Fund for Young Scholars (Nong Ke Qing Nian Ke Ji NO.2012-06), Special Fund for Agro-scientific Research in the Public Interest (NO.201403032), and Young Talents Plan in Shanghai Agricultural System (Hu Nong Qing Zi NO.2015-1-19).
Author information
Authors and Affiliations
Corresponding author
Additional information
Li Yu, Jun Yan and Yanjuan Yang contributed equally to this work.
Rights and permissions
About this article
Cite this article
Yu, L., Yan, J., Yang, Y. et al. Enhanced Tolerance to Chilling Stress in Tomato by Overexpression of a Mitogen-Activated Protein Kinase, SlMPK7 . Plant Mol Biol Rep 34, 76–88 (2016). https://doi.org/10.1007/s11105-015-0897-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-015-0897-3