Abstract
Interaction between Medicago spp. and Sinorhizobium meliloti leads to the development of a novel organ, the root nodule. A gene, Msapk1, encoding a novel type of plant protein kinase containing a N-terminal region with an ankyrin domain, was identified and shown to be expressed both in S. meliloti-infected and spontaneous nodules in alfalfa. This gene is not exclusively associated to nodulation since its expression was detected in other plant organs. Several genes coding for ankyrin protein kinases (APKs) were detected in various plants and animals. Three closest A. thaliana homologues of Msapk1 were identified in databases and two of them were shown to express differentially in various organs using gene-specific RT-PCR. In contrast, Southern analysis suggests that a single-copy gene exists in diploid M. truncatula. By screening a M. truncatula BAC library the Mtapk1 genomic region was isolated and sequenced. Two neighbouring genes showing homologies to previously identified sequences in data banks were detected in the vicinity of the Mtapk1 gene and compared to similar regions of the three Atapk genes. The distribution of exons/introns was the same for all expressed genes of both species although Mtapk1 contained larger introns. Upon osmotic stress Msapk1 expression was induced in roots of alfalfa starting from three hours up to two days of treatment. These data suggest that Msapk1, involved in alfalfa osmotic stress responses, belongs to a novel class of plant protein kinases.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bennett, V. 1992. Ankyrins. J Biol Chem 267: 8703–8706.
Bevan, M., Mayer, K., White, O., Eisen, J., Preuss, D., Bureau, T., Salzberg, S.L. and Mewes, H-W. 2001. Sequence and analysis of the Arabidopsis genome. Curr Opin Plant Biol 4: 105–110.
Bögre, L., Calderini, O., Binarova, P., Mattauch, M., Till, S., Kiegerl, S., Jonak, C., Pollaschek, C., Barker, P., Huskisson, N.S., Hirt, H. and Heberle-Bors, E. 1999. A MAP kinase is activated late in plant mitosis and becomes localized to the plane of cell division. Plant Cell 11: 101–113.
Charon, C., Sousa, C., Crespi, M. and Kondorosi, A. 1999. Alteration of enod40 expression modifies Medicago truncatula root nodule development induced by Sinorhizobium meliloti. Plant Cell 11: 1953–1966.
Chang, C. 1996. The ethylene signal transduction pathway in Arabidopsis: an emerging paradigm ? Trends Biol Sci 21: 129–131.
Church, G.M. and Gilbert, W. 1984. Genomic sequencing. Proc Natl Acad Sci USA 81: 1991–1995.
Covitz, P.A., Smith, L. and Long, S. 1998. Expressed sequence tags from a root hair-enriched Medicago truncatula cDNA library. Plant Physiol 117: 1325–1332.
Davis, J.Q. and Bennett, V. 1984. Brain ankyrin: a membraneassociated protein with binding sites for spectrin, tubulin, and the cytoplasmic domain of the erythrocyte anion channel. J Biol Chem 259: 13550–13559.
Frugier, F., Kondorosi, A. and Crespi, M. 1998. Identification of novel putative regulatory genes induced during alfalfa nodule development with a cold-plaque screening procedure. Mol Plant-Microbe Interact 11: 358–366.
Frugier, F., Poirier, S., Satiat-Jeunemaitre, B., Kondorosi, A. and Crespi, M. (2000) A Krüppel-like zinc finger protein is involved in nitrogen-fixing root nodule organogenesis. Genes Dev 14: 475–482.
Glazebrook, J., Ichige, A. and Walker, G.C. 1993. A Rhizobium meliloti homologue of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroïd development. Genes Dev 7: 1485–1497.
Gyorgyey, J., Vaubert, D., Jiménez-Zurdo, J.I., Charon, C., Troussard, L., Kondorosi, A. and Kondorosi, E. 2000. Analysis of Medicago truncatula nodule expressed sequence tags. Mol Plant Microbe Interact 13: 62–71.
Hanks, S.K., Quinn, A.M. and Hunter, T. 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241: 42–52.
Hirsch, A.M. 1992. Developmental biology of legume nodulation. New Phytol 122: 211–237
Hirt, H. 1997. Multiple roles of MAP kinases in plant signal transduction. Trends Plant Sci 2: 11–15.
Hoyos, M.E. and Zhang, S. 2000. Calcium-independent activation of salicylic acid-induced protein kinase and a 40-kilodalton protein kinase by hyperosmotic stress. Plant Physiol 122: 1355–1363.
Ichimura, K., Mizoguchi, T., Yoshida, R., Yuasa, T. and Shinozaki K. 2000. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J 24: 655–665.
Jimenez-Zurdo, J.I., Frugier, F., Crespi, M.D. and Kondorosi, A. 2000. Expression profiles of 22 novel molecular markers for organogenetic pathways acting in alfalfa nodule development. Mol Plant Microbe Interact 13: 96–106.
Jonak, C., Kiegerl, S., Ligterink, W., Barker, 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 U S A 93: 11274–11279.
Kondorosi, E., Banfalvi, Z. and Kondorosi, A. 1984. Physical and genetic analysis of a symbiotic region of Rhizobium meliloti: Identification of nodulation genes. Mol Gen Genet 193: 445–452.
Kovacs, I., Ayaydin, F., Oberschall, A., Ipacs, I., Bottka, S., Pongor, S., Dudits, D. and Toth, E.C. 1998. Immunolocalisation of a novel annexin-like protein encoded by a stress and abscissic acid responsive gene in alfalfa. Plant J 15:185–197.
Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Promé, J.C., Dénarié, J. 1990. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344: 781–784.
Liu, J., Ishitani, M., Halfter, U., Kim, C.S. and Zhu, J.K. 2000. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA 97: 3730–3734.
Michaely, P. and Bennett, V. 1992. The ANK repeat: a ubiquitous motif involved in macromolecular recognition. Trends Cell Biol 33: 615–624.
Mikolajczyk, M., Awotunde, O.S., Muszynska, G., Klessig, D.F. and Dobrowolska, G. 2000. Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homologue of protein kinase ASK1 in tobacco cells. Plant Cell 12: 165–78.
Munnik, T., Ligterink, W., Meskiene, I., Calderini, O., Beyerly, J., Musgrave, A. and Hirt, H. 1999. Distinct osmo-sensing protein kinase pathways are involved in signalling moderate and severe hyper-osmotic stress. Plant J 20: 381–388.
Newman, T., de Bruijn, F.J., Green, P., Keegstra, K., Kende, H., McIntosh, L., Ohlrogge, J., Raikhel, N., Somerville, S. and Thomashow, M. 1994. Genes galore: a summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones. Plant Physiol 106: 1241–1255.
Somerville, S. and Thomashow, M. 1994. Genes galore: a summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones. Plant Physiol 106: 1241–1255.
Pay, A., Heberle-Bors, E. and Hirt, H. 1992. An alfalfa cDNA encodes a protein with homology to translationally controlled human tumor protein. Plant Mol Biol 19: 501–503.
Romeis, T., Piedras, P., Zhang, S., Klessig, D.F., Hirt, H. and Jones, J.D. 1999. Rapid Avr9-and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell 11: 273–287.
Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
Sedgwick, S.G., Smerdon, S.J. 1999. The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci 24: 311–316.
Shinozaki, K. and Yamaguchi-Shinozaki, K. 1997. Gene expression and signal transduction in water-stress response. Plant Physiol 115: 327–334.
Suzuki, H., Verma, D.P. 1989. Nodule-specific kinases phosphorylating nuclear factors in isolated nuclei. Plant Cell 1: 373–379.
Winicov, I. 2000. Alfin1 transcription factor overexpression enhances plant root growth under normal and saline conditions and improves salt tolerance in alfalfa. Planta 210: 416–422.
Wu, C. and Dedhar, S. 2001. Integrin-linked kinase (ILK) and its interactors: a new paradigm for the coupling of extracellular matrix to actin cytoskeleton and signalling complexes. J Cell Biol 155: 505–510.
Zhang, S. and Klessig, D.F. 1998. The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc Natl Acad Sci U S A 95(12): 7225–30.
Zhu, J. 2001. Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol. 4(5): 401–406.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Chinchilla, D., Merchan, F., Megias, M. et al. Ankyrin protein kinases: a novel type of plant kinase gene whose expression is induced by osmotic stress in alfalfa. Plant Mol Biol 51, 555–566 (2003). https://doi.org/10.1023/A:1022337221225
Issue Date:
DOI: https://doi.org/10.1023/A:1022337221225