Abstract
DnaJ-like proteins are molecular chaperones that regulate Hsp70 ATPase activity both in protein folding, assembly and disassembly of protein complexes. Here we report the isolation of MsJ1, an alfalfa gene encoding a protein homologous to cytosolic DnaJ-like proteins. MsJ1 was induced under heat-shock treatment in both leaves and stems of adult plants. In the absence of heat shock MsJ1 expression was tissue-specific with the highest levels of mRNA in roots and in embryonal structures. High levels of transcript were also detected in cotyledons where active degradation of storage protein occurs. In synchronized alfalfa suspension-cultured cells the MsJ1 transcript was actively expressed and showed a phase-specific modulation during cell cycle with a 2-fold induction in G2/M. These findings suggest that DnaJ-like proteins play an active role in regulating normal cellular events like protein degradation, morphogenesis and cell cycle progression.
Similar content being viewed by others
References
Amino, S., Fujimura, T. and Komamine, A. 1983. Synchrony induced by double phosphate starvation in suspension cultures of Catharanthus roseus. Physiol. Plant. 59: 393-396.
Atencio, D.P. and Yaffe, M.P. 1992. MAS5, a yeast homologue of DnaJ involved in mitochondrial protein import. Mol. Cell. Biol. 12: 283-291.
Bessoule, J.J. 1993. Occurrence and sequence of a DnaJ protein in plant (Allium porrum) epidermal cells. FEBS Lett. 323: 51-54.
Blumberg, H. and Silver, P.A. 1991. A homologue of the bacterial heat-shock gene DnaJ that alters protein sorting in yeast. Nature 349: 627-629.
Bond, U. and Schlesinger, M.J. 1987. Heat shock proteins and development. Adv. Genet. 24: 1-29.
Caplan, A.J. and Douglas, M.G. 1991. Characterization of YDJ1: a yeast homologue of the bacterial DnaJ protein. J. Cell Biol. 114: 609-621.
Chirwing, J.M., Przybyla, A.E., MacDonald, R.J. and Rutter, W.J. 1979. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294-5299.
Chomczynski, P. 1992. One-hour downward alkaline capillary transfer for blotting of DNA and RNA. Anal. Biochem. 201: 134-139.
Corpas, F.J. and Trelease, R.N. 1997. The plant 73 kDa peroxisomal membrane protein (PMP73) is immunorelated to molecular chaperones. Eur. J. Cell Biol. 73: 49-57.
Cyr, D.M., Langer, T. and Douglas, M.G. 1994. DnaJ-like proteins: molecular chaperones and specific regulators of Hsp70. Trends Biochem Sci. 19: 176-181.
de Kochko, A. and Hamon, S. 1990. A rapid and efficient method for the isolation of restrictable total DNA from plants of the genus Abelmoschus. Plant Mol. Biol. Rep.8(1): 3-7.
DeRocher, A.E. and Vierling, E. 1994. Developmental control of small heat shock protein expression during pea seed maturation. Plant J. 5: 93-102.
DeRocher, A.E. and Vierling, E. 1995. Cytoplasmic Hsp70 homologues of pea: differential expression in vegetative and embryonic organs. Plant Mol. Biol. 27: 441-456.
Gething, M. and Sambrook, J. 1992. Protein folding in the cell. Nature 355: 33-45.
Grundemann, D. and Koepsell, H. 1994. Ethidium bromide staining during denaturation with glyoxal for sensitive detection of RNA in agarose gel electrophoresis.Anal. Biochem. 216: 459-461.
Hang, H., He, L. and Fox, M.H. 1995. Cell cycle variation of Hsp70 levels in HeLa cells at 37 _C and after a heat shock. Cell Physiol 165: 367-375.
Hartl, F.U. 1996. Molecular chaperones in cellular protein folding. Nature 381: 571-581.
Hendrick, J.P. and Hartl, F.U. 1993. Molecular chaperone functions of heat-shock proteins. Annu. Rev. Biochem. 62: 349-384.
Karlseder, J., Wissing, D., Holzer, G., Orel, L., Sliutz, G., Auer, H., Jaattela, M. and Simon, M.M. 1996. HSP70 overexpression mediates the escape of a doxorubicin-induced G2 cell cycle arrest. Biochem. Biophys. Res. Commun. 220: 153-159.
Kroczynska, B., Zhu, R., Clifford, W. and Miernyk, J.A. 1996. AtJ1, a mitochondrial homologue of the Escherichia coli DnaJ protein. Plant Mol. Biol. 31: 619-629.
Liang, P. and Pardee, A.B. 1992. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257: 967-971.
Lindquist, S. 1986. The heat shock response. Annu. Rev. Biochem. 55: 1151-1191.
Lu, Z. and Cyr, D.M. 1998. The conserved carboxyl terminus and the zinc finger-like domain of the co-chaperone Ydj1 assist Hsp70 in protein folding. J. Biol. Chem. 6: 5970-5978.
Luke, M.M., Sutton, A. and Arndt, K. 1991. Characterization of SIS1, a Saccharomyces cerevisiae homologue of bacterial DnaJ proteins. J. Cell. Biol. 114: 623-638.
Nover, L. 1991. Control of Hsp synthesis. In: L. Nover (Ed.), Heat Shock Response, CRC Press, Boca Raton, FL, pp. 237-279.
Nover, L. and Scharf, K.D. 1997. Heat stress proteins and transcription factors. Cell Mol. Life Sci 53: 80-103.
Pierpaoli, E.V., Sandmeier, E., Schonfeld, H.J. and Christen, P. 1998. Control of the DnaK chaperone cycle by substoichiometric concentrations of the co-chaperones DnaJ and GrpE. J. Biol. Chem. 273: 6643-6649.
Preisig-Muller, R. and Kindl, H. 1993. Plant dnaJ homologue: molecular cloning, bacterial expression, and expression analysis in tissues of cucumber seedlings. Arch. Biochem. Biophys. 305: 30-37.
Preisig-Muller, R., Muster, G. and Kindl, H. 1994. Heat shock enhances the amount of prenylated DnaJ protein at membranes of glyoxysomes. Eur. J. Biochem. 219: 57-63.
Reindl, A., Schoffl, F., Schell, J., Koncz, C. and Bako, L. 1997. Phosphorylation of a cyclin-dependent kinase modulates DNA binding of the Arabidopsis heat-shock transcription factor HSF1 in vitro. Plant Physiol. 115: 93-100.
Qian, D., Zhou, D., Ju, R., Cramer, C.L. and Yang, Z. 1996. Protein farnesyltransferase in plants: molecular characterization and involvement in cell cycle control. Plant Cell 8: 2381-2394.
Sanger, F., Nicklen, S. and Coulson, A.R. 1997. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463-5467.
Schlicher, T. and Soll, J. 1997. Chloroplastic isoforms of DnaJ and GrpE in pea. Plant Mol. Biol. 33: 181-185.
Uchimiya, H. and Murashige, T. 1974. Evaluation of parameters in the isolation of viable protoplasts from cultured tobacco cells. Plant Physiol. 54: 936-944.
Vierling, E. 1991. The roles of heat shock proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 579-620.
Yaglom, J.A., Goldberg, A.L., Finley, D. and Sherman, M.Y. 1996. The molecular chaperone Ydj1 is required for the p34CDC28-dependent phosphorylation of the cyclin Cln3 that signals its degradation. Mol. Cell. Biol. 16: 3679-3684.
Zarzov, P., Boucherie, H. and Mann, C. 1997. A yeast heat shock transcription factor (Hsf1) mutant is defective in both Hsc82/Hsp82 synthesis and spindle pole body duplication. J. Cell Sci. 110: 1879-1891.
Zhu, J.K., Shi, J.S., Bressan, R.A. and Hasegawa, P.M. 1993a. Expression of an Atriplex nummularia gene encoding a protein homologous to the bacterial molecular chaperone DnaJ. Plant Cell 5: 341-349.
Zhu, J.K., Bressan, R.A. and Hasegawa, P.M. 1993b. Isoprenylation of the plant molecular chaperone ANJ1 facilitates membrane association and function at high temperature. Proc. Natl. Acad. Sci. USA 90: 8557-8561.
Zhu, R., Kroczynska, B., Hayman, G.T. and Miernyk, J.A. 1995. AtJ2, an Arabidopsis homolog of Escherichia coli dnaJ. Plant Physiol. 108: 821-822.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Frugis, G., Mele, G., Giannino, D. et al. MsJ1, an alfalfa DnaJ-like gene, is tissue-specific and transcriptionally regulated during cell cycle. Plant Mol Biol 40, 397–408 (1999). https://doi.org/10.1023/A:1006215231492
Issue Date:
DOI: https://doi.org/10.1023/A:1006215231492