Molecular Cloning and Expression of a cDNA Encoding a Hybrid Histidine Kinase Receptor in Tropical Periwinkle Catharanthus roseus

Abstract

Signalling pathways involving histidine kinase receptors (HKRs) are widely used by prokaryotes and fungi to regulate a large palette of biological processes. In plants, HKRs are known to be implicated in cytokinin, ethylene, and osmosensing transduction pathways. In this work, a full length cDNA named CrCIK was isolated from the tropical species Catharanthus roseus (L.) G. Don. It encodes a 1205 amino acid protein that belongs to the hybrid HKR family. The deduced amino acid sequence shows the highest homology with AtHK1, an osmosensing HKR in Arabidopsis thaliana. In return, CrCIK protein shares very low identity with the other 10 Arabidopsis HKRs. Southern blot analysis indicates that the CrCIK corresponding gene is either present in multiple copies or has very close homologues in the genome of the tropical periwinkle. The gene is widely expressed in the plant. In C. roseus C20D cell suspension, it is slightly induced after exposure to low temperature, pointing to a putative role in cold-shock signal transduction.

Key words

Catharanthus roseus - histidine kinase receptor - monoterpene indole alkaloids - multistep phosphorelay - osmosensing

References

• 1 Chang C., Kwok S. F., Bleecker A. B., Meyerowitz E. M.. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators.  Science. (1993);  262 539-544
• 2 Courtois D., Guern J.. Temperature exposure of Catharanthus roseus cells cultivated in liquid medium.  Plant Science Letters. (1980);  17 473-482
• 3 Gamble R. L., Coonfield M. L., Schaller G. E.. Histidine kinase activity of the ETR1 ethylene receptor from Arabidopsis. .  Proceedings of the National Academy of Sciences of the USA. (1998);  95 7825-7829
• 4 Gamble R. L., Qu X., Schaller G. E.. Mutational analysis of the ethylene receptor ETR1. Role of the histidine kinase domain in dominant ethylene insensitivity.  Plant Physiology. (2002);  128 1428-1438
• 5 Gamborg O. L., Miller R. A., Ojima K.. Nutrient requirement of suspension cultures of soybean root cells.  Experimental Cell Research. (1968);  50 151-158
• 6 Geourjon C., Deleage G.. SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments.  Computer Applications in the Biosciences. (1995);  11 681-684
• 7 Hejatko J., Pernisova M., Eneva T., Palme K., Brzobohaty B.. The putative sensor histidine kinase CKI1 is involved in female gametophyte development in Arabidopsis. .  Molecular Genetics and Genomics. (2003);  69 443-453
• 8 Hua J., Sakai H., Nourizadeh S., Chen Q. G., Bleecker A. B., Ecker J. R., Meyerowitz E. M.. EIN4 and ERS2 are members of the putative receptor gene family in Arabidopsis. .  Plant Cell. (1998);  10 1321-1332
• 9 Inoue T., Higuchi M., Hashimoto Y., Seki M., Kobayashi M., Kato T., Tabata S., Shinozaki K., Kakimoto T.. Identification of CRE1 as a cytokinin receptor from Arabidopsis.  Nature. (2001);  409 1060-1063
• 10 Kakimoto T.. CKI1, a histidine kinase homolog implicated in cytokinin signal transduction.  Science. (1996);  274 982-985
• 11 Kozak M.. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs.  Nucleic Acids Research. (1984);  12 857-872
• 12 Krogh A., Larsson B., von Heijne G., Sonnhammer E. L.. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes.  Journal of Molecular Biology. (2001);  305 567-580
• 13 Lütcke H. A., Chow K. C., Mickel F. S., Moss K. A., Kern H. F., Scheele G. A.. Selection of AUG initiation codons differs in plants and animals.  European Molecular Biology Organization Journal. (1987);  6 43-48
• 14 Mérillon J. M., Rideau M., Chénieux J. C.. Influence of sucrose on levels of ajmalicine, serpentine, and tryptamine in Catharanthus roseus cells in vitro. .  Planta Medica. (1984);  48 497-502
• 15 Mikami K., Kanesaki Y., Suzuki I., Murata N.. The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp. PCC 6803.  Molecular Microbiology. (2002);  46 905-915
• 16 Ouélhazi L., Filali M., Chénieux J. C., Rideau M.. Differential protein accumulation in zeatin- and 2,4-D treated cells of Catharanthus roseus. Correlation with alkaloid biosynthesis.  Plant Physiology and Biochemistry. (1994);  31 421-434
• 17 Page R. D.. TreeView: an application to display phylogenetic trees on personal computers.  Computer Applications in the Biosciences. (1996);  12 357-358
• 18 Papon N., Bremer J., Vansiri A., Andreu F., Rideau M., Crèche J.. Cytokinin and ethylene control indole alkaloid production at the level of the MEP/terpenoid pathway in Catharanthus roseus suspension cells.  Planta Medica. (2005);  71 572-574
• 19 Papon N., Clastre M., Andreu F., Gantet P., Rideau M., Chénieux J. C., Crèche J.. Expression analysis in plant and cell suspensions of CrCKR1, a cDNA encoding a histidine kinase receptor homologue in Catharanthus roseus (L.) G. Don.  Journal of Experimental Botany. (2002);  53 1989-1990
• 20 Papon N., Clastre M., Gantet P., Rideau M., Chénieux J. C., Crèche J.. Inhibition of the plant cytokinin transduction pathway by bacterial histidine kinases inhibitors in Catharanthus roseus cell cultures.  Federation of European Biochemical Societies Letters. (2003);  537 101-105
• 21 Papon N., Senoussi M. M., Andreu F., Rideau M., Chénieux J. C., Crèche J.. The expression of a gene encoding a putative ethylene receptor in plant and cell culture of Catharanthus roseus.  Biologia Plantarum. (2004 a);  48 345-350
• 22 Papon N., Vansiri A., Gantet P., Chénieux J. C., Rideau M., Crèche J.. Histidine-containing phosphotransfer domain extinction by RNA interference turns off a cytokinin signalling circuitry in Catharanthus roseus suspension cells.  Federation of European Biochemical Societies Letters. (2004 b);  558 85-88
• 23 Pischke M. S., Jones L. G., Otsuga D., Fernandez D. E., Drews G. N., Sussman M. R.. An Arabidopsis histidine kinase is essential for megagametogenesis.  Proceedings of the National Academy of Sciences of the USA. (2002);  99 15800-15805
• 24 Schaller G. E., Ladd A. N., Lanahan M. B., Spanbauer J. M., Bleecker A. B.. The ethylene response mediator ETR1 from Arabidopsis forms a disulfide-linked dimmer.  Journal of Biological Chemistry. (1995);  270 12526-12530
• 25 Smith J. I., Smart N. J., Kurz W. G. W., Misawa M.. The use of organic and inorganic compounds to increase the accumulation of indole alkaloids in Catharanthus roseus (L.) G. Don cell suspension cultures.  Journal of Experimental Botany. (1987);  38 1501-1506
• 26 Stock A. M., Robinson V. L., Goudreau P. N.. Two-component signal transduction.  Annual Revue of Biochemistry. (2000);  69 183-215
• 27 Thompson J. D., Higgins D. G., Gibson T. J.. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice.  Nucleic Acids Research. (1994);  22 4673-4680
• 28 Urao T., Yakubov B., Satoh R., Yamaguchi-Shinozaki K., Seki K., Hirayama T., Shinozaki K.. A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor.  Plant Cell. (1999);  11 1743-1754
• 29 West A. H., Stock A. M.. Histidine kinases and response regulator proteins in two-component signaling systems.  Trends in Biochemical Sciences. (2001);  26 369-376
• 30 Yahia A., Kevers C., Gaspar T., Chénieux J. C., Rideau M., Crèche J.. Cytokinins and ethylene stimulate indole alkaloïds accumulation in cell suspension cultures of Catharanthus roseus by two distinct mechanisms.  Plant Sciences. (1998);  133 9-15

Editor: G. Thiel