Skip to main content
PMC home page
The Plant Cell logoLink to The Plant Cell
. 1998 Jun;10(6):1009–1019. doi: 10.1105/tpc.10.6.1009

Two genes with similarity to bacterial response regulators are rapidly and specifically induced by cytokinin in Arabidopsis.

I Brandstatter 1, J J Kieber 1
PMCID: PMC144033  PMID: 9634588

Abstract

Cytokinins are central regulators of plant growth and development, but little is known about their mode of action. By using differential display, we identified a gene, IBC6 (for induced by cytokinin), from etiolated Arabidopsis seedlings, that is induced rapidly by cytokinin. The steady state level of IBC6 mRNA was elevated within 10 min by the exogenous application of cytokinin, and this induction did not require de novo protein synthesis. IBC6 was not induced by other plant hormones or by light. A second Arabidopsis gene with a sequence highly similar to IBC6 was identified. This IBC7 gene also was induced by cytokinin, although with somewhat slower kinetics and to a lesser extent. The pattern of expression of the two genes was similar, with higher expression in leaves, rachises, and flowers and lower transcript levels in roots and siliques. Sequence analysis revealed that IBC6 and IBC7 are similar to the receiver domain of bacterial two-component response regulators. This homology, coupled with previously published work on the CKI1 histidine kinase homolog, suggests that these proteins may play a role in early cytokinin signaling.

Full Text

The Full Text of this article is available as a PDF (1.8 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abel S., Oeller P. W., Theologis A. Early auxin-induced genes encode short-lived nuclear proteins. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):326–330. doi: 10.1073/pnas.91.1.326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ainley W. M., McNeil K. J., Hill J. W., Lingle W. L., Simpson R. B., Brenner M. L., Nagao R. T., Key J. L. Regulatable endogenous production of cytokinins up to 'toxic' levels in transgenic plants and plant tissues. Plant Mol Biol. 1993 Apr;22(1):13–23. doi: 10.1007/BF00038992. [DOI] [PubMed] [Google Scholar]
  3. Alex L. A., Borkovich K. A., Simon M. I. Hyphal development in Neurospora crassa: involvement of a two-component histidine kinase. Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3416–3421. doi: 10.1073/pnas.93.8.3416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brown J. L., Bussey H., Stewart R. C. Yeast Skn7p functions in a eukaryotic two-component regulatory pathway. EMBO J. 1994 Nov 1;13(21):5186–5194. doi: 10.1002/j.1460-2075.1994.tb06849.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. 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 Oct 22;262(5133):539–544. doi: 10.1126/science.8211181. [DOI] [PubMed] [Google Scholar]
  6. Chory J., Reinecke D., Sim S., Washburn T., Brenner M. A Role for Cytokinins in De-Etiolation in Arabidopsis (det Mutants Have an Altered Response to Cytokinins). Plant Physiol. 1994 Feb;104(2):339–347. doi: 10.1104/pp.104.2.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Franco A. R., Gee M. A., Guilfoyle T. J. Induction and superinduction of auxin-responsive mRNAs with auxin and protein synthesis inhibitors. J Biol Chem. 1990 Sep 15;265(26):15845–15849. [PubMed] [Google Scholar]
  8. Gómez-Lim M. A., Valdés-López V., Cruz-Hernandez A., Saucedo-Arias L. J. Isolation and characterization of a gene involved in ethylene biosynthesis from Arabidopsis thaliana. Gene. 1993 Dec 8;134(2):217–221. doi: 10.1016/0378-1119(93)90096-l. [DOI] [PubMed] [Google Scholar]
  9. Hua J., Chang C., Sun Q., Meyerowitz E. M. Ethylene insensitivity conferred by Arabidopsis ERS gene. Science. 1995 Sep 22;269(5231):1712–1714. doi: 10.1126/science.7569898. [DOI] [PubMed] [Google Scholar]
  10. Joshi C. P., Zhou H., Huang X., Chiang V. L. Context sequences of translation initiation codon in plants. Plant Mol Biol. 1997 Dec;35(6):993–1001. doi: 10.1023/a:1005816823636. [DOI] [PubMed] [Google Scholar]
  11. Kakimoto T. CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science. 1996 Nov 8;274(5289):982–985. doi: 10.1126/science.274.5289.982. [DOI] [PubMed] [Google Scholar]
  12. Kende H. Enzymes of ethylene biosynthesis. Plant Physiol. 1989 Sep;91(1):1–4. doi: 10.1104/pp.91.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kieber J. J., Rothenberg M., Roman G., Feldmann K. A., Ecker J. R. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell. 1993 Feb 12;72(3):427–441. doi: 10.1016/0092-8674(93)90119-b. [DOI] [PubMed] [Google Scholar]
  14. Li Y., Hagen G., Guilfoyle T. J. Altered morphology in transgenic tobacco plants that overproduce cytokinins in specific tissues and organs. Dev Biol. 1992 Oct;153(2):386–395. doi: 10.1016/0012-1606(92)90123-x. [DOI] [PubMed] [Google Scholar]
  15. Liang P., Pardee A. B. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science. 1992 Aug 14;257(5072):967–971. doi: 10.1126/science.1354393. [DOI] [PubMed] [Google Scholar]
  16. 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. EMBO J. 1987 Jan;6(1):43–48. doi: 10.1002/j.1460-2075.1987.tb04716.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Maeda T., Wurgler-Murphy S. M., Saito H. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature. 1994 May 19;369(6477):242–245. doi: 10.1038/369242a0. [DOI] [PubMed] [Google Scholar]
  18. Makino K., Shinagawa H., Amemura M., Nakata A. Nucleotide sequence of the phoB gene, the positive regulatory gene for the phosphate regulon of Escherichia coli K-12. J Mol Biol. 1986 Jul 5;190(1):37–44. doi: 10.1016/0022-2836(86)90073-2. [DOI] [PubMed] [Google Scholar]
  19. Medford J. I., Horgan R., El-Sawi Z., Klee H. J. Alterations of Endogenous Cytokinins in Transgenic Plants Using a Chimeric Isopentenyl Transferase Gene. Plant Cell. 1989 Apr;1(4):403–413. doi: 10.1105/tpc.1.4.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mutoh N., Simon M. I. Nucleotide sequence corresponding to five chemotaxis genes in Escherichia coli. J Bacteriol. 1986 Jan;165(1):161–166. doi: 10.1128/jb.165.1.161-166.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Newman T., de Bruijn F. J., Green P., Keegstra K., Kende H., McIntosh L., Ohlrogge J., Raikhel N., Somerville S., Thomashow M. Genes galore: a summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones. Plant Physiol. 1994 Dec;106(4):1241–1255. doi: 10.1104/pp.106.4.1241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ota I. M., Varshavsky A. A yeast protein similar to bacterial two-component regulators. Science. 1993 Oct 22;262(5133):566–569. doi: 10.1126/science.8211183. [DOI] [PubMed] [Google Scholar]
  23. Posas F., Wurgler-Murphy S. M., Maeda T., Witten E. A., Thai T. C., Saito H. Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 "two-component" osmosensor. Cell. 1996 Sep 20;86(6):865–875. doi: 10.1016/s0092-8674(00)80162-2. [DOI] [PubMed] [Google Scholar]
  24. Quail P. H., Boylan M. T., Parks B. M., Short T. W., Xu Y., Wagner D. Phytochromes: photosensory perception and signal transduction. Science. 1995 May 5;268(5211):675–680. doi: 10.1126/science.7732376. [DOI] [PubMed] [Google Scholar]
  25. Reith M., Munholland J. A High-Resolution Gene Map of the Chloroplast Genome of the Red Alga Porphyra purpurea. Plant Cell. 1993 Apr;5(4):465–475. doi: 10.1105/tpc.5.4.465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schaller G. E., Bleecker A. B. Ethylene-binding sites generated in yeast expressing the Arabidopsis ETR1 gene. Science. 1995 Dec 15;270(5243):1809–1811. doi: 10.1126/science.270.5243.1809. [DOI] [PubMed] [Google Scholar]
  27. Schneider-Poetsch H. A., Braun B., Marx S., Schaumburg A. Phytochromes and bacterial sensor proteins are related by structural and functional homologies. Hypothesis on phytochrome-mediated signal-transduction. FEBS Lett. 1991 Apr 9;281(1-2):245–249. doi: 10.1016/0014-5793(91)80403-p. [DOI] [PubMed] [Google Scholar]
  28. Schuster S. C., Noegel A. A., Oehme F., Gerisch G., Simon M. I. The hybrid histidine kinase DokA is part of the osmotic response system of Dictyostelium. EMBO J. 1996 Aug 1;15(15):3880–3889. [PMC free article] [PubMed] [Google Scholar]
  29. Shaulsky G., Escalante R., Loomis W. F. Developmental signal transduction pathways uncovered by genetic suppressors. Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15260–15265. doi: 10.1073/pnas.93.26.15260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shieh J. C., Wilkinson M. G., Buck V., Morgan B. A., Makino K., Millar J. B. The Mcs4 response regulator coordinately controls the stress-activated Wak1-Wis1-Sty1 MAP kinase pathway and fission yeast cell cycle. Genes Dev. 1997 Apr 15;11(8):1008–1022. doi: 10.1101/gad.11.8.1008. [DOI] [PubMed] [Google Scholar]
  31. Smart C. M., Scofield S. R., Bevan M. W., Dyer T. A. Delayed Leaf Senescence in Tobacco Plants Transformed with tmr, a Gene for Cytokinin Production in Agrobacterium. Plant Cell. 1991 Jul;3(7):647–656. doi: 10.1105/tpc.3.7.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Smigocki A. C. Cytokinin content and tissue distribution in plants transformed by a reconstructed isopentenyl transferase gene. Plant Mol Biol. 1991 Jan;16(1):105–115. doi: 10.1007/BF00017921. [DOI] [PubMed] [Google Scholar]
  33. Smigocki A. C., Owens L. D. Cytokinin gene fused with a strong promoter enhances shoot organogenesis and zeatin levels in transformed plant cells. Proc Natl Acad Sci U S A. 1988 Jul;85(14):5131–5135. doi: 10.1073/pnas.85.14.5131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Stock A. M., Mottonen J. M., Stock J. B., Schutt C. E. Three-dimensional structure of CheY, the response regulator of bacterial chemotaxis. Nature. 1989 Feb 23;337(6209):745–749. doi: 10.1038/337745a0. [DOI] [PubMed] [Google Scholar]
  35. Stock J. B., Ninfa A. J., Stock A. M. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev. 1989 Dec;53(4):450–490. doi: 10.1128/mr.53.4.450-490.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Stock J. B., Stock A. M., Mottonen J. M. Signal transduction in bacteria. Nature. 1990 Mar 29;344(6265):395–400. doi: 10.1038/344395a0. [DOI] [PubMed] [Google Scholar]
  37. Theologis A., Huynh T. V., Davis R. W. Rapid induction of specific mRNAs by auxin in pea epicotyl tissue. J Mol Biol. 1985 May 5;183(1):53–68. doi: 10.1016/0022-2836(85)90280-3. [DOI] [PubMed] [Google Scholar]
  38. Vogel J. P., Schuerman P., Woeste K., Brandstatter I., Kieber J. J. Isolation and characterization of Arabidopsis mutants defective in the induction of ethylene biosynthesis by cytokinin. Genetics. 1998 May;149(1):417–427. doi: 10.1093/genetics/149.1.417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Vogel J. P., Woeste K. E., Theologis A., Kieber J. J. Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4766–4771. doi: 10.1073/pnas.95.8.4766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wang N., Shaulsky G., Escalante R., Loomis W. F. A two-component histidine kinase gene that functions in Dictyostelium development. EMBO J. 1996 Aug 1;15(15):3890–3898. [PMC free article] [PubMed] [Google Scholar]
  41. Wilkinson J. Q., Lanahan M. B., Yen H. C., Giovannoni J. J., Klee H. J. An ethylene-inducible component of signal transduction encoded by never-ripe. Science. 1995 Dec 15;270(5243):1807–1809. doi: 10.1126/science.270.5243.1807. [DOI] [PubMed] [Google Scholar]
  42. Wong Y. S., Cheng H. C., Walsh D. A., Lagarias J. C. Phosphorylation of Avena phytochrome in vitro as a probe of light-induced conformational changes. J Biol Chem. 1986 Sep 15;261(26):12089–12097. [PubMed] [Google Scholar]
  43. Wong Y. S., McMichael R. W., Lagarias J. C. Properties of a polycation-stimulated protein kinase associated with purified Avena phytochrome. Plant Physiol. 1989 Oct;91(2):709–718. doi: 10.1104/pp.91.2.709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yeh K. C., Wu S. H., Murphy J. T., Lagarias J. C. A cyanobacterial phytochrome two-component light sensory system. Science. 1997 Sep 5;277(5331):1505–1508. doi: 10.1126/science.277.5331.1505. [DOI] [PubMed] [Google Scholar]
  45. Zhou D., Kalaitzís P., Mattoo A. K., Tucker M. L. The mRNA for an ETR1 homologue in tomato is constitutively expressed in vegetative and reproductive tissues. Plant Mol Biol. 1996 Mar;30(6):1331–1338. doi: 10.1007/BF00019564. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES