Abstract
Medicago truncatula, a model for legume genomics, can be regenerated by somatic embryogensis by the use of a suitable genotype and an auxin plus cytokinin. The stress response induced by explant wounding and culture is increasingly recognized as an important component of somatic embryo induction. We have cloned and investigated the stress kinase gene MtSK1 in relation to somatic embryogenesis in M. truncatula, using the highly embryogenic mutant Jemalong 2HA (2HA) and its progenitor Jemalong. The main features of the MtSK1 protein of 351 amino acids are an N-terminal kinase domain and a C-terminal glutamic acid-rich region, which is predicted to be a coiled-coil. MtSK1 is a member of the SnRK2 subgroup of the SnRK group of plant kinases. Members of the SnRK2 kinases play a role in stress responses of plants. MtSKI expression is induced by wounding in the cultured tissue independent of auxin or cytokinin. However, in both 2HA and Jemalong, as the callus develops in response to auxin plus cytokinin, MtSK1 expression continues to increase. MtSK1 responds to salt stress in vivo, consistent with its role as a stress kinase. The likely role of MtSK1 in stress-induced signaling will facilitate the relating of stress–response pathways to auxin and cytokinin-induced signaling in the understanding of the molecular mechanisms involved in the induction of somatic embryogenesis in M. truncatula.
Similar content being viewed by others
References
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Anderberg RJ, Walker-Simmons MK (1992) Isolation of a wheat cDNA clone for an abscisic acid-inducible transcript with homology to protein kinases. PNAS 89:10183–10187
Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795
Bonetta D, McCourt P (1998) Genetic analysis of ABA signal transduction pathways. Trends Plant Sci 3:231–235
Burkhard P, Stetefeld J, Strelkov SV (2001) Coiled coils: A highly versatile protein folding motif. Trends Cell Biol 11:82–88
Chabaud M, Larsonneau C, Marmouget C, Huguet T (1996) Transformation of Barrel Medic (Medicago truncatula Gaertn) By Agrobacterium tumefaciens and regeneration via somatic embryogenesis of transgenic plants with the Mtenod12 nodulin promoter fused to the Gus reporter gene. Plant Cell Rep 15:305–310
das Neves LO, Duque SRL, de Almeida JS, Fevereiro PS (1999) Repetitive somatic embryogenesis in Medicago truncatula ssp. Narbonensis and M-truncatula Gaertn cv. Jemalong. Plant Cell Rep 18:398–405
Emanuelsson O, Nielsen H, Von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978–984
Feher A, Pasternak TP, Dudits D (2003) Transition of somatic plant cells to an embryogenic state. Plant Cell Tissue Organ Cult 74:201–228
Felsenstein J (1989) PHYLIP—Phylogeny inference package (Version 3.2). Cladistics 5:164–166
Frugoli J, Harris J (2001) Medicago truncatula on the move! Plant Cell 13:458–463
Halford NG, Hardie DG (1998) SNF1-related protein kinases: Global regulators of carbon metabolism in plants? Plant Mol Biol 37:735–748
Halford NG, Hey S, Jhurreea D, Laurie S, McKibbin RS, Paul M, Zhang Y (2003) Metabolic signalling and carbon partitioning: Role of Snf1-related (SnRK1) protein kinase. J Exp Bot 54:467–475
Hanks SK, Hunter T (1995) The eukaryotic protein kinase superfamily: Kinase (catalytic) domain structure and classification. FASEB J 9:576–596
Hardie DG (1999) Plant protein serine threonine kinases: Classification and functions. Annu Rev Plant Physiol Plant Molec Biol 50:97–131
Hofmann K, Bucher P, Falquet L, Bairoch A (1999) The PROSITE database, its status in 1999. Nucleic Acids Res 27:215–219
Holappa LD, Walker-Simmons MK (1995) The wheat abscisic acid-responsive protein kinase mRNA, PKABA1, is up-regulated by dehydration, cold temperature, and osmotic stress. Plant Physiol 108:1203–1210
Holappa LD, Walker-Simmons MK (1997) The wheat protein kinase gene, TaPK3, of the PKABA1 subfamily is differentially regulated in greening wheat seedlings. Plant Mol Biol 33:935–941
Hrabak EM, Chan CWM, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu J-K, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680
Hrabak EM, Dickmann LJ, Satterlee JS, Sussman MR (1996) Characterization of eight new members of the calmodulin-like domain protein kinase gene family from Arabidopsis thaliana. Plant Mol Biol 31:405–412
Iantcheva A, Vlahova M, Trinh TH, Brown SC, Slater A, Elliot MC, Atanassov A (2001) Assessment of polysomaty, embryo formation and regeneration in liquid media for various species of diploid annual Medicago. Plant Sci 160:621–627
Imin N, De Jong F, Mathesius U, van Noorden G, Saeed NA, Wang X-D, Rose RJ, Rolfe BG (2004) Proteome reference maps of Medicago truncatula embryogenic cell cultures generated from single protoplasts. Proteomics 4:1883–1896
Imin N, Nizamidin M, Daniher D, Nolan KE, Rose RJ, Rolfe BG (2005) Proteomic analysis of somatic embryogenesis in Medicago truncatula. Plant Physiol 137:1250–1260
Kamada H, Ishikawa K, Saga H, Harada H (1993) Induction of somatic embryogenesis in carrot by osmotic stress. Plant Tissue Cult Lett 10:38–44
Kamada H, Tachikawa Y, Saitou T, Harada H (1994) Heat stresses induction of carrot somatic embryogenesis. Plant Tissue Cult Lett 11:229–232
Kiyosue T, Kamada H, Harada H (1989) Induction of somatic embryogenesis by salt stress in carrot. Plant Tissue Cult Lett 6:162–164
Laurie S, Halford NG (2001) The role of protein kinases in the regulation of plant growth and development. Plant Growth Regul 34:253–265
Lee EK, Cho DY, Soh WY (2001) Enhanced production and germination of somatic embryos by temporary starvation in tissue cultures of Daucus carota. Plant Cell Rep 20:408–415
Lupas A (1996) Coiled coils: New structures and new functions. Trends Biochem Sci 21:375–382
Lupas A, Vandyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252:1162–1164
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
Mustilli A-C, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089–3099
Nakai K, Kanehisa M (1992) A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14:897–911
Nishiwaki M, Fujino K, Koda Y, Masuda K, Kikuta Y (2000) Somatic embryogenesis induced by the simple application of abscisic acid to carrot (Daucus carota L.) seedlings in culture. Planta 211:756–759
Nolan KE, Irwanto RR, Rose RJ (2003) Auxin up-regulates MtSERK1 expression in both medicago truncatula root-forming and embryogenic cultures. Plant Physiol 133:218–230
Nolan KE, Rose RJ (1998) Plant regeneration from cultured Medicago truncatula with particular reference to abscisic acid and light treatments. Aust J Bot 46:151–160
Nolan KE, Rose RJ, Gorst JE (1989) Regeneration of Medicago truncatula from tissue culture: increased somatic embryogenesis from regenerated plants. Plant Cell Rep 8:278–281
Page RDM (1996) TREEVIEW: An application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Park YS, Hong SW, Oh SA, Kwak JM, Lee HH, Nam HG (1993) Two putative protein kinases from Arabidopsis thaliana contain highly acidic domains. Plant Mol Biol 22:615–624
Quatrano RS, Bartels D, Ho THD, Pages M (1997) New insights into ABA-mediated processes. Plant Cell 9:470–475
Rose RJ (2004) Somatic embryogenesis in plants. In: Goodman RM (ed) Encyclopedia of plant and crop science. Marcel Dekker Inc., New York, pp 1165–1168
Rose RJ, Nolan KE, Bicego L (1999) The development of the highly regenerable seed line Jemalong 2HA for transformation of Medicago truncatula—Implications for regenerability via somatic embryogenesis. J Plant Physiol 155:788–791
Schafleitner R, Wilhelm E (2002) Isolation of wound inducible genes from Castanea sativa stems and expression analysis in the bark tissue. Plant Physiol Biochem 40:235–245
Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7:41–48
Thompson MR, Johnson LB, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Touraev A, Vicente O, Heberlebors E (1997) Initiation of microspore embryogenesis by stress. Trends Plant Sci 2:297–302
Yoon HW, Kim MC, Shin PG, Kim JS, Kim CY, Lee SY, Hwang I, Bahk JD, Hong JC, Han C, Cho MJ (1997) Differential expression of two functional serine/threonine protein kinases from soyabean that have an unusual acidic domain at the carboxy terminus. Mol Gen Genet 255:359–371
Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker JR, Shinozaki K (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol 43:1473–1483
Acknowledgements
The authors would like to thank Dr Thomas Kaiser of Corbett Research for his assistance with Real Time PCR and Professor Barry Rolfe (Australian National University, Canberra) for helpful discussions. This work was supported by an Australian Research Council Centre of Excellence grant to the University of Newcastle node of the Centre of Excellence for Integrative Legume Research (to RJR).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P. Lakshmanan
Rights and permissions
About this article
Cite this article
Nolan, K.E., Saeed, N.A. & Rose, R.J. The stress kinase gene MtSK1 in Medicago truncatula with particular reference to somatic embryogenesis. Plant Cell Rep 25, 711–722 (2006). https://doi.org/10.1007/s00299-006-0135-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-006-0135-4