Skip to main content
Log in

Tomato SlMPK4 is required for resistance against Botrytis cinerea and tolerance to drought stress

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Mitogen-activated protein kinases (MPKs) play important roles in biotic and abiotic stress responses. In the present study, we identified a tomato MPK gene, SlMPK4, a possible homolog of Arabidopsis AtMPK4, and performed functional analysis to examine its possible roles in biotic and abiotic responses. Expression of SlMPK4 was induced by infection with Botrytis cinerea and by exogenous application of jasmonic acid and ethylene precursor 1-amino cyclopropane-1-carboxylic acid. Knockdown of the endogenous SlMPK4 expression through virus-induced gene silencing in tomato plants (TRV-SlMPK4) resulted in increased susceptibility to B. cinerea. Expression of defense-related genes SlPR1a and SlPR1b were up-regulated in the SlMPK4-silenced plants. Furthermore, silencing of the SlMPK4 gene also resulted in reduced tolerance against drought stress, leading to earlier wilting symptom under drought stress condition, as compared with the control plants. These results suggest important roles for SlMPK4 in disease resistance against B. cinerea and tolerance to drought stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abuqamar S, Chai MF, Luo H, Song F, Mengiste T (2008) Tomato protein kinase 1b mediates signaling of plant responses to necrotrophic fungi and insect herbivory. Plant Cell 20:1964–1983

    Article  PubMed  CAS  Google Scholar 

  • Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NH, Zhu S, Qiu JL, Micheelsen P, Rocher A, Petersen M, Newman MA, Bjørn-Nielsen H, Hirt H, Somssich I, Mattsson O, Mundy J (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J 24:2579–2589

    Article  PubMed  CAS  Google Scholar 

  • Benito EP, ten Have A, van’t Klooster JW, van Kan JAL (1998) Fungal and plant gene expression during synchronized infection of tomato leaves by Botrytis cinerea. Eur J Plant Pathol 104:207–220

    Article  CAS  Google Scholar 

  • Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744

    Article  PubMed  CAS  Google Scholar 

  • Brodersen P, Petersen M, Bjørn-Nielsen H, Zhu S, Newman MA, Shokat KM, Rietz S, Parker J, Mundy J (2006) Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J 47:532–546

    Article  PubMed  CAS  Google Scholar 

  • Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J 413:217–226

    Article  PubMed  CAS  Google Scholar 

  • Cui H, Wang Y, Xue L, Chu J, Yan C, Fu J, Chen M, Innes RW, Zhou JM (2010) Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4. Cell Host Microbe 7:164–175

    Article  PubMed  CAS  Google Scholar 

  • del Pozo O, Pedley KF, Martin GB (2004) MAPKKKα is a positive regulator of cell death associated with both plant immunity and disease. EMBO J 23:3072–3082

    Article  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  PubMed  CAS  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    Article  PubMed  CAS  Google Scholar 

  • El Oirdi M, El Rahman TA, Rigano L, El Hadrami A, Rodriguez MC, Daayf F, Vojnov A, Bouarab K (2011) Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell 23:2405–2421

    Google Scholar 

  • Gao M, Liu J, Bi D, Zhang Z, Cheng F, Chen S, Zhang Y (2008) MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res 18:1190–1198

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  PubMed  CAS  Google Scholar 

  • 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 46:1902–1914

    Article  PubMed  CAS  Google Scholar 

  • Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751–757

    Article  PubMed  CAS  Google Scholar 

  • Han L, Li GJ, Yang KY, Mao G, Wang R, Liu Y, Zhang S (2010) Mitogen-activated protein kinase 3 and 6 regulate Botrytis cinerea-induced ethylene production in Arabidopsis. Plant J 64:114–127

    PubMed  CAS  Google Scholar 

  • Hettenhausen C, Baldwin IT, Wu J (2012) Silencing MPK4 in Nicotiana attenuata enhances photosynthesis and seed production but compromises abscisic acid-induced stomatal closure and guard cell-mediated resistance to Pseudomonas syringae pv. tomato DC3000. Plant Physiol 158:759–776

    Article  PubMed  CAS  Google Scholar 

  • Holley SR, Yalamanchili RD, Moura DS, Ryan CA, Stratmann JW (2003) Convergence of signaling pathways induced by systemin, oligosaccharide elicitors, and ultraviolet-B radiation at the level of mitogen-activated protein kinases in Lycopersicon peruvianum suspension-cultured cells. Plant Physiol 132:1728–1738

    Article  PubMed  CAS  Google Scholar 

  • Ichimura K, Casais C, Peck SC, 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 281:36969–36976

    Article  PubMed  CAS  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • 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 USA 104:12205–12210

    Article  PubMed  CAS  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 doi:10.1016/j.gene.2012.01.048

  • Liu Y, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31:777–786

    Article  PubMed  CAS  Google Scholar 

  • Liu JZ, Horstman HD, Braun E, Graham MA, Zhang C, Navarre D, Qiu WL, Lee Y, Nettleton D, Hill JH, Whitham SA (2011) Soybean homologs of MPK4 negatively regulate defense responses and positively regulate growth and development. Plant Physiol 157:1363–1378

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Marten H, Hyun T, Gomi K, Seo S, Hedrich R, Roelfsema MR (2008) Silencing of NtMPK4 impairs CO-induced stomatal closure, activation of anion channels and cytosolic Ca signals in Nicotiana tabacum guard cells. Plant J 55:698–708

    Article  PubMed  CAS  Google Scholar 

  • Mengiste T (2012) Plant immunity to necrotrophs. Annu Rev Phytopathol. doi:10.1146/annurev-phyto-081211-172955

  • Mengiste T, Chen X, Salmeron J, Dietrich R (2003) The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15:2551–2565

    Article  PubMed  CAS  Google Scholar 

  • Meszaros T, Helfer A, Hatzimasoura E, Magyar Z, Serazetdinova L, Rios G, Bardoczy 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 48:485–498

    Article  PubMed  CAS  Google Scholar 

  • Moniz de Sá M, Drouin G (1996) Phylogeny and substitution rates of angiosperm actin genes. Mol Biol Evol 13:1198–1212

    Article  PubMed  Google Scholar 

  • Nakagami H, Soukupova H, Schikora A, Zarsky V, Hirt H (2006) A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J Biol Chem 281:38697–38704

    Article  PubMed  CAS  Google Scholar 

  • Nambeesan S, AbuQamar S, Laluk K, Mattoo AK, Mickelbart MV, Ferruzzi MG, Mengiste T, Handa AK (2012) Polyamines attenuate ethylene-mediated defense responses to abrogate resistance to Botrytis cinerea in tomato. Plant Physiol 158:1034–1045

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen HB, Lacy M, Austin MJ, Parker JE, Sharma SB, Klessig DF, Martienssen R, Mattsson O, Jensen AB, Mundy J (2000) Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103:1111–1120

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pitzschke A, Schikora A, Hirt H (2009b) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12:421–426

    Article  PubMed  CAS  Google Scholar 

  • Pokalsky AR, Hiatt WR, Ridge N, Rasmussen R, Houck CM, Shewmaker CK (1989) Structure and expression of elongation factor 1 alpha in tomato. Nucl Acids Res 17:4661–4673

    Article  PubMed  CAS  Google Scholar 

  • Prins TW, Tudzynski P, Tiedemann AV, Tudzynski B, ten-Have A, Hansen ME, Tenberge K, Van-Kan JAL (2000) Infection strategies of Botrytis cinerea and related necrotrophic pathogens. In: Kronstad JW (ed) Fungal pathology. Kluwer Academic Publishers, Dordrecht, pp 33–64

    Chapter  Google Scholar 

  • Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S, Palma K, Suarez-Rodriguez MC, Sandbech-Clausen S, Lichota J, Brodersen P, Grasser KD, Mattsson O, Glazebrook J, Mundy J, Petersen M (2008a) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27:2214–2221

    Article  PubMed  CAS  Google Scholar 

  • Qiu JL, Zhou L, Yun BW, Nielsen HB, Fiil BK, Petersen K, Mackinlay J, Loake GJ, Mundy J, Morris PC (2008b) Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol 148:212–222

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez MC, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649

    Article  PubMed  CAS  Google Scholar 

  • Shen XL, Yuan B, Liu HB, Li XH, Xu CG, Wang SP (2010) Opposite functions of a rice mitogen-activated protein kinase during the process of resistance against Xanthomonas oryzae. Plant J 64:86–99

    PubMed  CAS  Google Scholar 

  • Sinha AK, Jaggi M, Raghuram B, Tuteja N (2011) Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal Behav 6:196–203

    Article  PubMed  CAS  Google Scholar 

  • Song FM, Zhang HJ, Zhang SQ (2009) Mitogen-activated protein kinase cascades in plant defence responses. In: Bouarab K, Brisson N, Daayf F (eds) Molecular plant-microbe interactions. CAB International, London, pp 36–58

    Chapter  Google Scholar 

  • Stulemeijer IJE, Stratmann JW, Joosten MHAJ (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

    Article  PubMed  CAS  Google Scholar 

  • Suarez-Rodriguez MC, Adams-Phillips L, Liu Y, Wang H, Su SH, Jester PJ, Zhang S, Bent AF, Krysan PJ (2007) MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Physiol 143:661–669

    Article  PubMed  CAS  Google Scholar 

  • Taj G, Agarwal P, Grant M, Kumar A (2010) MAPK machinery in plants: recognition and response to different stresses through multiple signal transduction pathways. Plant Signal Behav 5:1370–1378

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Mao H, Dong C, Ji R, Cai L, Fu H, Liu S (2009) Overexpression of Brassica napus MPK4 enhances resistance to Sclerotinia sclerotiorum in oilseed rape. Mol Plant Microbe Interact 22:235–244

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yuan B, Shen X, Li X, Xu C, Wang S (2007) Mitogen-activated protein kinase OsMPK6 negatively regulates rice disease resistance to bacterial pathogens. Planta 226:953–960

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Basic Research Program of China (2009CB119005), the National Key Technology R & D Program of China (2011BAD12B04) and the National Natural Science Foundation of China (no. 30971880).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fengming Song.

Additional information

Communicated by B. Barna.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Virk, N., Liu, B., Zhang, H. et al. Tomato SlMPK4 is required for resistance against Botrytis cinerea and tolerance to drought stress. Acta Physiol Plant 35, 1211–1221 (2013). https://doi.org/10.1007/s11738-012-1160-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-012-1160-2

Keywords

Navigation