Published 23 June 2003. doi:10.1083/jcb.200301099
© The Rockefeller University Press,
0021-9525/2003/6/1035 $5.00
The Journal of Cell Biology, Volume 161, Number 6, 1035-1040
Yeast osmosensor Sln1 and plant cytokinin receptor Cre1 respond to changes in turgor pressure
Vladimír Reiser1,
Desmond C. Raitt1 and
Haruo Saito1,2
1 Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02115
2 Institute of Medical Science, University of Tokyo, Tokyo 108-8639, Japan
Address correspondence to Dr. Haruo Saito, Dana-Farber Cancer Institute, 44 Binney Street, Boston, MA 02115. Tel.: (617) 632-3814. Fax: (617) 632-5951. E-mail: h-saito{at}ims.u-tokyo.ac.jp
Very little is known about how cellular osmosensors monitor changes in osmolarity of the environment. Here, we report that in yeast, Sln1 osmosensor histidine kinase monitors changes in turgor pressures. Reductions in turgor caused by either hyperosmotic stress, nystatin, or removal of cell wall activate MAPK Hog1 specifically through the SLN1 branch, but not through the SHO1 branch of the high osmolarity glycerol pathway. The integrity of the periplasmic region of Sln1 was essential for its sensor function. We found that activity of the plant histidine kinase cytokinin response 1 (Cre1) is also regulated by changes in turgor pressure, in a manner identical to that of Sln1, in the presence of cytokinin. We propose that Sln1 and Cre1 are turgor sensors, and that similar turgor-sensing mechanisms might regulate hyperosmotic stress responses both in yeast and plants.
Key Words: signal transduction; high osmolarity stress; histidine kinase; two-component system; HOG MAPK pathway
The online version of this article includes supplemental material.
* Abbreviations used in this paper: Cre1, cytokinin response 1; HOG, high osmolarity glycerol; TM, transmembrane.

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Abdullah, U., Cullen, P. J.
(2009). The tRNA Modification Complex Elongator Regulates the Cdc42-Dependent Mitogen-Activated Protein Kinase Pathway That Controls Filamentous Growth in Yeast. Eukaryot Cell
8: 1362-1372
[Abstract]
[Full Text]
-
Vyroubalova, S., Vaclavikova, K., Tureckova, V., Novak, O., Smehilova, M., Hluska, T., Ohnoutkova, L., Frebort, I., Galuszka, P.
(2009). Characterization of New Maize Genes Putatively Involved in Cytokinin Metabolism and Their Expression during Osmotic Stress in Relation to Cytokinin Levels. Plant Physiol.
151: 433-447
[Abstract]
[Full Text]
-
Roman, E., Cottier, F., Ernst, J. F., Pla, J.
(2009). Msb2 Signaling Mucin Controls Activation of Cek1 Mitogen-Activated Protein Kinase in Candida albicans. Eukaryot Cell
8: 1235-1249
[Abstract]
[Full Text]
-
Pitoniak, A., Birkaya, B., Dionne, H. M., Vadaie, N., Cullen, P. J.
(2009). The Signaling Mucins Msb2 and Hkr1 Differentially Regulate the Filamentation Mitogen-activated Protein Kinase Pathway and Contribute to a Multimodal Response. Mol. Biol. Cell
20: 3101-3114
[Abstract]
[Full Text]
-
Ferguson, B. J., Beveridge, C. A.
(2009). Roles for Auxin, Cytokinin, and Strigolactone in Regulating Shoot Branching. Plant Physiol.
149: 1929-1944
[Abstract]
[Full Text]
-
Horie, T., Tatebayashi, K., Yamada, R., Saito, H.
(2008). Phosphorylated Ssk1 Prevents Unphosphorylated Ssk1 from Activating the Ssk2 Mitogen-Activated Protein Kinase Kinase Kinase in the Yeast High-Osmolarity Glycerol Osmoregulatory Pathway. Mol. Cell. Biol.
28: 5172-5183
[Abstract]
[Full Text]
-
Wohlbach, D. J., Quirino, B. F., Sussman, M. R.
(2008). Analysis of the Arabidopsis Histidine Kinase ATHK1 Reveals a Connection between Vegetative Osmotic Stress Sensing and Seed Maturation. Plant Cell
20: 1101-1117
[Abstract]
[Full Text]
-
Burg, M. B., Ferraris, J. D.
(2008). Intracellular Organic Osmolytes: Function and Regulation. J. Biol. Chem.
283: 7309-7313
[Abstract]
[Full Text]
-
Bermejo, C., Rodriguez, E., Garcia, R., Rodriguez-Pena, J. M., Rodriguez de la Concepcion, M. L., Rivas, C., Arias, P., Nombela, C., Posas, F., Arroyo, J.
(2008). The Sequential Activation of the Yeast HOG and SLT2 Pathways Is Required for Cell Survival to Cell Wall Stress. Mol. Biol. Cell
19: 1113-1124
[Abstract]
[Full Text]
-
Narang, S. S., Malone, C. L., Deschenes, R. J., Fassler, J. S.
(2008). Modulation of Yeast Sln1 Kinase Activity by the Ccw12 Cell Wall Protein. J. Biol. Chem.
283: 1962-1973
[Abstract]
[Full Text]
-
Tran, L.-S. P., Urao, T., Qin, F., Maruyama, K., Kakimoto, T., Shinozaki, K., Yamaguchi-Shinozaki, K.
(2007). Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc. Natl. Acad. Sci. USA
104: 20623-20628
[Abstract]
[Full Text]
-
Bettinger, B. T., Clark, M. G., Amberg, D. C.
(2007). Requirement for the Polarisome and Formin Function in Ssk2p-Mediated Actin Recovery From Osmotic Stress in Saccharomyces cerevisiae. Genetics
175: 1637-1648
[Abstract]
[Full Text]
-
Cao, W.-H., Liu, J., He, X.-J., Mu, R.-L., Zhou, H.-L., Chen, S.-Y., Zhang, J.-S.
(2007). Modulation of Ethylene Responses Affects Plant Salt-Stress Responses. Plant Physiol.
143: 707-719
[Abstract]
[Full Text]
-
Mascher, T., Helmann, J. D., Unden, G.
(2006). Stimulus Perception in Bacterial Signal-Transducing Histidine Kinases. Microbiol. Mol. Biol. Rev.
70: 910-938
[Abstract]
[Full Text]
-
Reiser, V., D'Aquino, K. E., Ee, L.-S., Amon, A.
(2006). The Stress-activated Mitogen-activated Protein Kinase Signaling Cascade Promotes Exit from Mitosis. Mol. Biol. Cell
17: 3136-3146
[Abstract]
[Full Text]
-
Hayashi, M., Maeda, T.
(2006). Activation of the HOG Pathway upon Cold Stress in Saccharomyces cerevisiae.. J Biochem
139: 797-803
[Abstract]
[Full Text]
-
Pischke, M. S., Huttlin, E. L., Hegeman, A. D., Sussman, M. R.
(2006). A Transcriptome-Based Characterization of Habituation in Plant Tissue Culture. Plant Physiol.
140: 1255-1278
[Abstract]
[Full Text]
-
Panadero, J., Pallotti, C., Rodriguez-Vargas, S., Randez-Gil, F., Prieto, J. A.
(2006). A Downshift in Temperature Activates the High Osmolarity Glycerol (HOG) Pathway, Which Determines Freeze Tolerance in Saccharomyces cerevisiae. J. Biol. Chem.
281: 4638-4645
[Abstract]
[Full Text]
-
MacRobbie, E. A. C.
(2006). From the Cover: Osmotic effects on vacuolar ion release in guard cells. Proc. Natl. Acad. Sci. USA
103: 1135-1140
[Abstract]
[Full Text]
-
Hoffmann, X.-K., Beck, C. F.
(2005). Mating-Induced Shedding of Cell Walls, Removal of Walls from Vegetative Cells, and Osmotic Stress Induce Presumed Cell Wall Genes in Chlamydomonas. Plant Physiol.
139: 999-1014
[Abstract]
[Full Text]
-
Boudsocq, M., Lauriere, C.
(2005). Osmotic Signaling in Plants. Multiple Pathways Mediated by Emerging Kinase Families. Plant Physiol.
138: 1185-1194
[Full Text]
-
Levin, D. E.
(2005). Cell Wall Integrity Signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev.
69: 262-291
[Abstract]
[Full Text]
-
Anjard, C., Loomis, W. F.
(2005). Peptide signaling during terminal differentiation of Dictyostelium. Proc. Natl. Acad. Sci. USA
102: 7607-7611
[Abstract]
[Full Text]
-
Karlgren, S., Pettersson, N., Nordlander, B., Mathai, J. C., Brodsky, J. L., Zeidel, M. L., Bill, R. M., Hohmann, S.
(2005). Conditional Osmotic Stress in Yeast: A SYSTEM TO STUDY TRANSPORT THROUGH AQUAGLYCEROPORINS AND OSMOSTRESS SIGNALING. J. Biol. Chem.
280: 7186-7193
[Abstract]
[Full Text]
-
Maeta, K., Izawa, S., Inoue, Y.
(2005). Methylglyoxal, a Metabolite Derived from Glycolysis, Functions as a Signal Initiator of the High Osmolarity Glycerol-Mitogen-activated Protein Kinase Cascade and Calcineurin/Crz1-mediated Pathway in Saccharomyces cerevisiae. J. Biol. Chem.
280: 253-260
[Abstract]
[Full Text]
-
Lu, J. M.-Y., Deschenes, R. J., Fassler, J. S.
(2004). Role for the Ran Binding Protein, Mog1p, in Saccharomyces cerevisiae SLN1-SKN7 Signal Transduction. Eukaryot Cell
3: 1544-1556
[Abstract]
[Full Text]
-
Herrlich, A., Leitch, V., King, L. S.
(2004). Role of proneuregulin 1 cleavage and human epidermal growth factor receptor activation in hypertonic aquaporin induction. Proc. Natl. Acad. Sci. USA
101: 15799-15804
[Abstract]
[Full Text]
-
Saito, H., Tatebayashi, K.
(2004). Regulation of the Osmoregulatory HOG MAPK Cascade in Yeast. J Biochem
136: 267-272
[Abstract]
[Full Text]
-
Lamitina, S. T., Morrison, R., Moeckel, G. W., Strange, K.
(2004). Adaptation of the nematode Caenorhabditis elegans to extreme osmotic stress. Am. J. Physiol. Cell Physiol.
286: C785-C791
[Abstract]
[Full Text]