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Plant Cell. Sep 1999; 11(9): 1743–1754.
PMCID: PMC144312

A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor.

Abstract

Water deficit and the resulting osmotic stress affect plant growth. To understand how plant cells monitor and respond to osmotic change from water stress, we isolated a cDNA from dehydrated Arabidopsis plants. This cDNA encodes a novel hybrid-type histidine kinase, ATHK1. Restriction fragment length polymorphism mapping showed that the ATHK1 gene is on chromosome 2. The predicted ATHK1 protein has two putative transmembrane regions in the N-terminal half and has structural similarity to the yeast osmosensor synthetic lethal of N-end rule 1 (SLN1). The ATHK1 transcript was more abundant in roots than other tissues under normal growth conditions and accumulated under conditions of high or low osmolarity. Histochemical analysis of beta-glucuronidase activities driven by the ATHK1 promoter further indicates that the ATHK1 gene is transcriptionally upregulated in response to changes in external osmolarity. Overexpression of the ATHK1 cDNA suppressed the lethality of the temperature-sensitive osmosensing-defective yeast mutant sln1-ts. By contrast, ATHK1 cDNAs in which conserved His or Asp residues had been substituted failed to complement the sln1-ts mutant, indicating that ATHK1 functions as a histidine kinase. Introduction of the ATHK1 cDNA into the yeast double mutant sln1Delta sho1Delta, which lacks two osmosensors, suppressed lethality in high-salinity media and activated the high-osmolarity glycerol response 1 (HOG1) mitogen-activated protein kinase (MAPK). These results imply that ATHK1 functions as an osmosensor and transmits the stress signal to a downstream MAPK cascade.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Alex LA, Simon MI. Protein histidine kinases and signal transduction in prokaryotes and eukaryotes. Trends Genet. 1994 Apr;10(4):133–138. [PubMed]
  • Alex LA, Borkovich KA, Simon MI. 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. [PMC free article] [PubMed]
  • Brandstatter I, Kieber JJ. Two genes with similarity to bacterial response regulators are rapidly and specifically induced by cytokinin in Arabidopsis. Plant Cell. 1998 Jun;10(6):1009–1019. [PMC free article] [PubMed]
  • Chang C, Meyerowitz EM. The ethylene hormone response in Arabidopsis: a eukaryotic two-component signaling system. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4129–4133. [PMC free article] [PubMed]
  • Chang C, Stewart RC. The two-component system. Regulation of diverse signaling pathways in prokaryotes and eukaryotes. Plant Physiol. 1998 Jul;117(3):723–731. [PMC free article] [PubMed]
  • Chang C, Kwok SF, Bleecker AB, Meyerowitz EM. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science. 1993 Oct 22;262(5133):539–544. [PubMed]
  • Hrabak EM, Willis DK. The lemA gene required for pathogenicity of Pseudomonas syringae pv. syringae on bean is a member of a family of two-component regulators. J Bacteriol. 1992 May;174(9):3011–3020. [PMC free article] [PubMed]
  • Hua J, Meyerowitz EM. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell. 1998 Jul 24;94(2):261–271. [PubMed]
  • Hua J, Chang C, Sun Q, Meyerowitz EM. Ethylene insensitivity conferred by Arabidopsis ERS gene. Science. 1995 Sep 22;269(5231):1712–1714. [PubMed]
  • Hua J, Sakai H, Nourizadeh S, Chen QG, Bleecker AB, Ecker JR, Meyerowitz EM. EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. Plant Cell. 1998 Aug;10(8):1321–1332. [PMC free article] [PubMed]
  • Imamura A, Hanaki N, Umeda H, Nakamura A, Suzuki T, Ueguchi C, Mizuno T. Response regulators implicated in His-to-Asp phosphotransfer signaling in Arabidopsis. Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2691–2696. [PMC free article] [PubMed]
  • Ingram J, Bartels D. THE MOLECULAR BASIS OF DEHYDRATION TOLERANCE IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):377–403. [PubMed]
  • Ito H, Fukuda Y, Murata K, Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. [PMC free article] [PubMed]
  • Jonak C, Kiegerl S, Ligterink W, Barker PJ, Huskisson NS, Hirt H. Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):11274–11279. [PMC free article] [PubMed]
  • Johnston M. A model fungal gene regulatory mechanism: the GAL genes of Saccharomyces cerevisiae. Microbiol Rev. 1987 Dec;51(4):458–476. [PMC free article] [PubMed]
  • Kakimoto T. CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science. 1996 Nov 8;274(5289):982–985. [PubMed]
  • Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K. Cloning of cDNAs for genes that are early-responsive to dehydration stress (ERDs) in Arabidopsis thaliana L.: identification of three ERDs as HSP cognate genes. Plant Mol Biol. 1994 Aug;25(5):791–798. [PubMed]
  • Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. [PubMed]
  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA, Newburg L. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics. 1987 Oct;1(2):174–181. [PubMed]
  • Lashbrook CC, Tieman DM, Klee HJ. Differential regulation of the tomato ETR gene family throughout plant development. Plant J. 1998 Jul;15(2):243–252. [PubMed]
  • Lauter FR, Ninnemann O, Bucher M, Riesmeier JW, Frommer WB. Preferential expression of an ammonium transporter and of two putative nitrate transporters in root hairs of tomato. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):8139–8144. [PMC free article] [PubMed]
  • Liu YG, Mitsukawa N, Lister C, Dean C, Whittier RF. Isolation and mapping of a new set of 129 RFLP markers in Arabidopsis thaliana using recombinant inbred lines. Plant J. 1996 Oct;10(4):733–736. [PubMed]
  • Maeda T, Wurgler-Murphy SM, Saito H. A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature. 1994 May 19;369(6477):242–245. [PubMed]
  • Maeda T, Takekawa M, Saito H. Activation of yeast PBS2 MAPKK by MAPKKKs or by binding of an SH3-containing osmosensor. Science. 1995 Jul 28;269(5223):554–558. [PubMed]
  • Miyata S, Urao T, Yamaguchi-Shinozaki K, Shinozaki K. Characterization of genes for two-component phosphorelay mediators with a single HPt domain in Arabidopsis thaliana. FEBS Lett. 1998 Oct 16;437(1-2):11–14. [PubMed]
  • Mizoguchi T, Irie K, Hirayama T, Hayashida N, Yamaguchi-Shinozaki K, Matsumoto K, Shinozaki K. A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):765–769. [PMC free article] [PubMed]
  • Mizoguchi T, Ichimura K, Shinozaki K. Environmental stress response in plants: the role of mitogen-activated protein kinases. Trends Biotechnol. 1997 Jan;15(1):15–19. [PubMed]
  • Mizuno T. Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli. DNA Res. 1997 Apr 28;4(2):161–168. [PubMed]
  • Mizuno T. His-Asp phosphotransfer signal transduction. J Biochem. 1998 Apr;123(4):555–563. [PubMed]
  • Mizuno T, Kaneko T, Tabata S. Compilation of all genes encoding bacterial two-component signal transducers in the genome of the cyanobacterium, Synechocystis sp. strain PCC 6803. DNA Res. 1996 Dec 31;3(6):407–414. [PubMed]
  • Muchhal US, Pardo JM, Raghothama KG. Phosphate transporters from the higher plant Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10519–10523. [PMC free article] [PubMed]
  • Nagasawa S, Tokishita S, Aiba H, Mizuno T. A novel sensor-regulator protein that belongs to the homologous family of signal-transduction proteins involved in adaptive responses in Escherichia coli. Mol Microbiol. 1992 Mar;6(6):799–807. [PubMed]
  • Ota IM, Varshavsky A. A yeast protein similar to bacterial two-component regulators. Science. 1993 Oct 22;262(5133):566–569. [PubMed]
  • Parkinson JS. Signal transduction schemes of bacteria. Cell. 1993 Jun 4;73(5):857–871. [PubMed]
  • Parkinson JS, Kofoid EC. Communication modules in bacterial signaling proteins. Annu Rev Genet. 1992;26:71–112. [PubMed]
  • Payton S, Fray RG, Brown S, Grierson D. Ethylene receptor expression is regulated during fruit ripening, flower senescence and abscission. Plant Mol Biol. 1996 Sep;31(6):1227–1231. [PubMed]
  • Posas F, Wurgler-Murphy SM, Maeda T, Witten EA, Thai TC, 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. [PubMed]
  • Rosenberg S, Coit D, Tekamp-Olson P. Glyceraldehyde-3-phosphate dehydrogenase-derived expression cassettes for constitutive synthesis of heterologous proteins. Methods Enzymol. 1990;185:341–351. [PubMed]
  • Sakai H, Hua J, Chen QG, Chang C, Medrano LJ, Bleecker AB, Meyerowitz EM. ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis. Proc Natl Acad Sci U S A. 1998 May 12;95(10):5812–5817. [PMC free article] [PubMed]
  • Sakakibara H, Suzuki M, Takei K, Deji A, Taniguchi M, Sugiyama T. A response-regulator homologue possibly involved in nitrogen signal transduction mediated by cytokinin in maize. Plant J. 1998 May;14(3):337–344. [PubMed]
  • Schuster SC, Noegel AA, Oehme F, Gerisch G, Simon MI. 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]
  • Shinozaki K, Yamaguchi-Shinozaki K. Molecular responses to drought and cold stress. Curr Opin Biotechnol. 1996 Apr;7(2):161–167. [PubMed]
  • Shinozaki K, Yamaguchi-Shinozaki K. Gene Expression and Signal Transduction in Water-Stress Response. Plant Physiol. 1997 Oct;115(2):327–334. [PMC free article] [PubMed]
  • Stout V, Gottesman S. RcsB and RcsC: a two-component regulator of capsule synthesis in Escherichia coli. J Bacteriol. 1990 Feb;172(2):659–669. [PMC free article] [PubMed]
  • Suzuki T, Imamura A, Ueguchi C, Mizuno T. Histidine-containing phosphotransfer (HPt) signal transducers implicated in His-to-Asp phosphorelay in Arabidopsis. Plant Cell Physiol. 1998 Dec;39(12):1258–1268. [PubMed]
  • Swanson RV, Alex LA, Simon MI. Histidine and aspartate phosphorylation: two-component systems and the limits of homology. Trends Biochem Sci. 1994 Nov;19(11):485–490. [PubMed]
  • Urao T, Yakubov B, Yamaguchi-Shinozaki K, Shinozaki K. Stress-responsive expression of genes for two-component response regulator-like proteins in Arabidopsis thaliana. FEBS Lett. 1998 May 8;427(2):175–178. [PubMed]
  • Valvekens D, Montagu MV, Van Lijsebettens M. Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5536–5540. [PMC free article] [PubMed]
  • Vriezen WH, van Rijn CP, Voesenek LA, Mariani C. A homolog of the Arabidopsis thaliana ERS gene is actively regulated in Rumex palustris upon flooding. Plant J. 1997 Jun;11(6):1265–1271. [PubMed]
  • Wang N, Shaulsky G, Escalante R, Loomis WF. A two-component histidine kinase gene that functions in Dictyostelium development. EMBO J. 1996 Aug 1;15(15):3890–3898. [PMC free article] [PubMed]
  • Wilkinson JQ, Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ. An ethylene-inducible component of signal transduction encoded by never-ripe. Science. 1995 Dec 15;270(5243):1807–1809. [PubMed]
  • Wurgler-Murphy SM, Saito H. Two-component signal transducers and MAPK cascades. Trends Biochem Sci. 1997 May;22(5):172–176. [PubMed]

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