DOI QR코드

DOI QR Code

A Novel MAP Kinase Gene in Cotton (Gossypium hirsutum L.), GhMAPK, is Involved in Response to Diverse Environmental Stresses

  • Wang, Meimei (Shandong Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University) ;
  • Zhang, Ying (Shandong Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University) ;
  • Wang, Jian (Shandong Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University) ;
  • Wu, Xiaoliang (Shandong Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University) ;
  • Guo, Xingqi (Shandong Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University)
  • Published : 2007.05.31

Abstract

The mitogen-activated protein kinase (MAPK) cascade is one of the major and evolutionally conserved signaling pathways and plays pivotal role in the regulation of stress and developmental signals in plants. Here, a novel gene, termed Gossypium hirsutum MAPK (GhMAPK), was isolated from cotton. The full-length cDNA of GhMAPK encodes for a 372 amino acid protein that contains all 11 of the MAPK conserved subdomains and the phosphorylationactivation motif, TEY. Amino acid sequence alignment revealed that GhMAPK shared high identity with group-C MAPK in plants and showed 83~89% similarities with MAPKs from Arabidopsis, apricot, pea, petunia, and tobacco. Southern blot analysis indicated that the GhMAPK belonged to a multygene family in cotton. Two introns were found within the region of genomic sequence. Northern blot analysis revealed that the transcripts of GhMAPK accumulated markedly when the cotton seedlings were subjected to various abiotic stimuli such as wounding, cold (4$^{\circ}C$), or salinity stress; Furthermore, GhMAPK was upregulated by the exogenous signaling molecules, such as salicylic acid (SA) and hydrogen peroxide ($H_2O_2C$), as well as pathogen attacks. These results indicate that the GhMAPK, which has a high degree of identity with group-C plant MAPKs, may also play an important role in response to environmental stresses.

Keywords

References

  1. Agrawal, G. K., Agrawal, S. K., Shibato, J., Iwahashi, H. and Rakwal, R. (2003) Novel rice MAPK kinase OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation. Biochem. Biophys. Res. Commun. 300, 775-783 https://doi.org/10.1016/S0006-291X(02)02868-1
  2. Agrawal, G. K., Rakwal, R. and 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 https://doi.org/10.1016/S0006-291X(02)00571-5
  3. Apel, K. and Hirt, H. (2004) Reactive oxygen species, metabolism, oxidative stress, and signal transduction. Annu Rev. Plant Biol. 55, 373-399 https://doi.org/10.1146/annurev.arplant.55.031903.141701
  4. Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W. L., Gomez-Gomez, L., Boller, T., Ausubel, F. M. and Sheen, J. (2002) MAP kinase signaling cascade in Arabidopsis innate immunity. Nature 415, 977-983 https://doi.org/10.1038/415977a
  5. Baogre, L., Calderini, O., Binarova, P., Matlauch, M., Till, S., Kiegerl, S., Jonack, C., Pollaschek, C., Baker, P., Huskisson, NS., Hirt, H. and Heberle-Bors, E., (1999) A MAP kinase is activated late in mitosis and becomes localised to the plane of cell division. Plant Cell 11, 5-14 https://doi.org/10.1105/tpc.11.1.5
  6. Champin, A., Picaud, A., and Henry, Y. (2005) Reassessing the MAP3K and MAP4K relationships. Thends in plant Sci. 9, 123-128
  7. Cheong, Y. H., Chang, H. S., Gupta, R., Wang, X., Zhu, T. and Luan, S., (2002) Transcriptional Profiling Reveals Novel Interactions between Wounding, Pathogen, Abiotic Stress, and Hormonal Responses in Arabidopsis. Plant Physiol. 129, 661-677 https://doi.org/10.1104/pp.002857
  8. Cheong, Y. H., Moon, B. C., Kim, J. K., Kim, C. Y., Kim, M. C., Kim, I. H., Park, C. Y., Kim, J. C., Park, B. O., Koo, S. C., Yoon, H. W., Chung, W. S., Lim, C. O., Lee, S. Y. and Cho, M. J. (2003) BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiol. 132, 1961-1972 https://doi.org/10.1104/pp.103.023176
  9. Cobb, M. H. and Goldsmith, E. J. (1995) How MAP kinase are regulated. J. Biol. Chem. 270, 14843-14846 https://doi.org/10.1074/jbc.270.25.14843
  10. Decroocq-Ferrant, V., Decroocq, S., van Went, J., Schmidt, E. and Kreis, M. (1995) A homologue of the MAP/ERK family of protein kinase genes is expressed in vegetative and in female reproductive organs of Petunia hybrida. Plant Mol. Biol. 27, 339-350 https://doi.org/10.1007/BF00020188
  11. Dowd, C, Wilson, I. W. and McFadden, H. (2004) Gene expression profile changes in cotton root and hypocotyl tissues in response to infection with Fusarium oxysporum f. sp. vasinfectum. Mol Plant Microbe Interact. 17, 654-667 https://doi.org/10.1094/MPMI.2004.17.6.654
  12. Fu, S. F., Chou, W. C., Huang, D. D. and Huang, H. J. (2002) Transcriptional regulation of a rice mitogen-activated protein kinase gene, OsMAPK4, in response to environmental stress. Plant Cell Physiol. 43, 958-963 https://doi.org/10.1093/pcp/pcf111
  13. He, C., Fong, S. H. T., Yang, D. and Wang, G. L. (1999) BWMK1, a novel MAP kinase induced by fungal infection and mechanical wounding in rice. Mol. Plant Microbe Interact. 12, 1064-1073 https://doi.org/10.1094/MPMI.1999.12.12.1064
  14. Hirt, H. (1997) Multiple roles of MAP kinases in plant signal transduction. Trends Plant Sci. 2, 11-15 https://doi.org/10.1016/S1360-1385(96)10048-0
  15. Halim, V. A., Vess, A., Scheel, D. and Rosahl, S. (2006) The role of salicylic acid and jasmonic acid in pathogen defence. Plant Biol(stuttq). 8(3), 307-313 https://doi.org/10.1055/s-2006-924025
  16. Jeong, M. J., Lee, S. K., Kim, B. J., Kwon, T. R., Cho W. S., Park, Y. T., Lee, J. O., Kwon, H. B., Byun, M. O. and Park, S. C. (2006) A rice (Oryza stativa L.) MAP kinase gene, OsMAPK44, is involved in response to abiotic stresses. Plant Cell, Tissue and Organ Culture 85, 151-160 https://doi.org/10.1007/s11240-005-9064-0
  17. Jonak, C., Kiegerl, S., Ligterink, W., Baker, P. J., Huskisson, N. S. and 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 https://doi.org/10.1073/pnas.93.20.11274
  18. Jonak, C., Ligterink, W. and Hirt, H. (1999) MAP kinase in plant signal transduction. Cell. Mol. Life Sci. 55, 204-213 https://doi.org/10.1007/s000180050285
  19. Jonak, C., Okresz, L., Boger, H. and Hirt, H. (2002) Complexity cross talk and integration of plant MAP kinase signaling. Curr. Opin. Plant Biol. 5, 415-424 https://doi.org/10.1016/S1369-5266(02)00285-6
  20. Jonak, C., Nakagami, H. and Hirt, H. (2004) Heavy metal stress. Activation of destinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol., 136, 3276-3283 https://doi.org/10.1104/pp.104.045724
  21. Kovtun, Y., Chiu, W. L., Tena, G. and Sheen, J. (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA 97, 2940-2945 https://doi.org/10.1073/pnas.97.6.2940
  22. MAPK Group. (2002) Mitogen-activated protein kinase cascades in plants: A new nomenclature. Trends Plant Sci. 7, 301-308 https://doi.org/10.1016/S1360-1385(02)02302-6
  23. Mizoguchi, T., Irie, K., Hirayama, T., Hayashida, N., Yamaguchi-Shinozaki, K., Matsumoto, K. and 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 S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 93, 765-769 https://doi.org/10.1073/pnas.93.2.765
  24. Nakagami, H., Pitzschke, A. and Hirt, H (2005) Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci. 10, 339-346 https://doi.org/10.1016/j.tplants.2005.05.009
  25. Reyna, N. S. and Yang, Y. N. (2006) Molecular analysis of the rice MAP kinase gene family in relation to Magnaporthe grisea infection. Mol. Plant Microbe Interact. 19, 530-540 https://doi.org/10.1094/MPMI-19-0530
  26. Ouaked. F., Rozhon, W., Lecourieux, D. and Hirt, H. (2003) A MAPK pathway mediates ethylene signaling in plants. EMBO J. 22, 1282-1288 https://doi.org/10.1093/emboj/cdg131
  27. Ryals, J.A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H.-Y. and Hunt, M. D. (1996) systemic acquired resistance. Plant cell 8, 1809-1819 https://doi.org/10.1105/tpc.8.10.1809
  28. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989) Molecular Cloning, A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, New York, USA
  29. Samuel, M. A., Miles, G. P. and Ellis, B. E. (2000) Ozone treatment rapidly activates MAP kinase signalling in plants. Plant J. 22, 367-376 https://doi.org/10.1046/j.1365-313x.2000.00741.x
  30. Seo, S., Sano, H. and Ohashi, Y. (1999) Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinase. Plant Cell 11, 289-298 https://doi.org/10.1105/tpc.11.2.289
  31. Song, F. and Goodman, R. M. (2002) OsBIMK1, a rice MAP kinase gene involved in disease resistance responses. Planta 215, 997-1005 https://doi.org/10.1007/s00425-002-0794-5
  32. Stone, J. M. and Walker, J. C. (1995). Plant protein kinase families and signal transduction. Plant Physiol. 108, 451-457 https://doi.org/10.1104/pp.108.2.451
  33. Tanoue, T., Adachi. M., Moriguchi, T. and Nishida, E. (2000) A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat. Cell Biol. 2, 110-116 https://doi.org/10.1038/35000065
  34. Taylor, A. T., Kim, J. and Low, P. S. (2001) Involvement of mitogen-activated protein kinase activation in the signaltransduction pathways of the soya bean oxidative burst. Biochem. J. 355, 795-803 https://doi.org/10.1042/bj3550795
  35. Trewavas, A. and Gilroy, S. (1991) Signal transduction in plant cells. Trends Genet. 7, 356-361 https://doi.org/10.1016/0168-9525(91)90255-O
  36. Wilson, V., Voronin, A., Touraev, O., Vincente, E. and Heberle-Bors. (1997) A developmentally regulated MAP kinase activated by hydration in tobacco pollen. Plant Cell 9, 2093-2100 https://doi.org/10.1105/tpc.9.11.2093
  37. Widmann, C., Gibson, S., Jarpe, M. B. and Johnson, G. L. (1999) Mitogen-activated protein kinase, conservation of a three-kinase module from yeast to human. Physiol. Rev. 79, 143-180 https://doi.org/10.1152/physrev.1999.79.1.143
  38. Xiong, L. and Yang, Y. (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acidinducible mitogen-activated protein kinase. Plant Cell 15, 745-759 https://doi.org/10.1105/tpc.008714
  39. Yu, S. W., Zhang, L. D., Zuo, K. J., Tang, D. Q. and Tang, K. X. (2005) Isolation and characterization of an oilseed rape MAP kinase BnMPK3 involved in diverse environmental stresses. Plant Sci. 169, 413-421 https://doi.org/10.1016/j.plantsci.2005.04.005
  40. Zhang, S. and Klessig, D. F. (1998) The tobacco woundingactivated mitogen-activated protein kinase is encoded by SIPK. Proc. Natl. Acad. Sci. USA 95, 7225-7230 https://doi.org/10.1073/pnas.95.12.7225
  41. Zhang, S. and Klessig, D. F. (2001) MAPK cascades in plant defense signaling. Trends Plant Sci. 6, 520-527 https://doi.org/10.1016/S1360-1385(01)02103-3

Cited by

  1. Cotton GhMPK2 is involved in multiple signaling pathways and mediates defense responses to pathogen infection and oxidative stress vol.278, pp.8, 2011, https://doi.org/10.1111/j.1742-4658.2011.08056.x
  2. Cotton mitogen-activated protein kinase4 (GhMPK4) confers the transgenic Arabidopsis hypersensitivity to salt and osmotic stresses vol.123, pp.3, 2015, https://doi.org/10.1007/s11240-015-0865-5
  3. Expression Profile of Early Responsive Genes Under Salt Stress in Upland Cotton (Gossypium hirsutum L.) vol.29, pp.3, 2011, https://doi.org/10.1007/s11105-010-0269-y
  4. Differential contributions to the transcriptome of duplicated genes in response to abiotic stresses in natural and synthetic polyploids vol.190, pp.4, 2011, https://doi.org/10.1111/j.1469-8137.2011.03650.x
  5. GhMPK16, a novel stress-responsive group D MAPK gene from cotton, is involved in disease resistance and drought sensitivity vol.12, pp.1, 2011, https://doi.org/10.1186/1471-2199-12-22
  6. A cotton mitogen-activated protein kinase (GhMPK6) is involved in ABA-induced CAT1 expression and H2O2 production vol.38, pp.11, 2011, https://doi.org/10.1016/j.jgg.2011.10.003
  7. Mulberry MnMAPK1, a group C mitogen-activated protein kinase gene, endowed transgenic Arabidopsis with novel responses to various abiotic stresses vol.131, pp.1, 2017, https://doi.org/10.1007/s11240-017-1272-x
  8. The pearl millet mitogen-activated protein kinase PgMPK4 is involved in responses to downy mildew infection and in jasmonic- and salicylic acid-mediated defense vol.87, pp.3, 2015, https://doi.org/10.1007/s11103-014-0276-8
  9. Comparative genomic analysis of mitogen activated protein kinase gene family in grapevine vol.32, pp.3, 2010, https://doi.org/10.1007/s13258-010-0010-0
  10. GhMPK7, a novel multiple stress-responsive cotton group C MAPK gene, has a role in broad spectrum disease resistance and plant development vol.74, pp.1-2, 2010, https://doi.org/10.1007/s11103-010-9661-0
  11. Molecular characterization of RsMPK2, a C1 subgroup mitogen-activated protein kinase in the desert plant Reaumuria soongorica vol.48, pp.10-11, 2010, https://doi.org/10.1016/j.plaphy.2010.07.001
  12. Plant mitogen-activated protein kinases and their roles in mediation of signal transduction in abiotic stresses vol.5, pp.2, 2011, https://doi.org/10.1007/s11703-011-1072-8
  13. ZmMPK17, a novel maize group D MAP kinase gene, is involved in multiple stress responses vol.235, pp.4, 2012, https://doi.org/10.1007/s00425-011-1510-0
  14. An in silico strategy identified the target gene candidates regulated by dehydration responsive element binding proteins (DREBs) in Arabidopsis genome vol.69, pp.1-2, 2009, https://doi.org/10.1007/s11103-008-9414-5
  15. Functional analysis reveals effects of tobacco alternative oxidase gene (NtAOX1a) on regulation of defence responses against abiotic and biotic stresses vol.29, pp.6, 2009, https://doi.org/10.1042/BSR20080133
  16. ZmMKK3, a novel maize group B mitogen-activated protein kinase kinase gene, mediates osmotic stress and ABA signal responses vol.169, pp.15, 2012, https://doi.org/10.1016/j.jplph.2012.06.008
  17. A cotton group C MAP kinase gene, GhMPK2, positively regulates salt and drought tolerance in tobacco vol.77, pp.1-2, 2011, https://doi.org/10.1007/s11103-011-9788-7
  18. De novo zygotic transcription in wheat (Triticum aestivum L.) includes genes encoding small putative secreted peptides and a protein involved in proteasomal degradation vol.26, pp.3, 2013, https://doi.org/10.1007/s00497-013-0229-4
  19. MAPK cascades and major abiotic stresses vol.33, pp.8, 2014, https://doi.org/10.1007/s00299-014-1629-0
  20. Mitogen-activated protein kinase signaling in plants under abiotic stress vol.6, pp.2, 2011, https://doi.org/10.4161/psb.6.2.14701