Summary
The perception of environmental stress and the subsequent transduction of stress signals are primary events in the acclimation of all organisms to changes in their environment. Many of the molecular sensors and transducers of environmental stress cannot be identified by traditional and conventional methods. Based on genomic information, a systematic approach has been applied to the solution of this problem in cyanobacteria, involving mutagenesis of potential sensors and signal transducers in combination with DNA microarray analyses for the genome-wide expression of genes. Almost all of the histidine kinases (Hiks) and response regulators (Rres) have been successfully inactivated by targeted mutagenesis in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Screening of mutant libraries by genome-wide DNA microarray analysis under various stress and non-stress conditions has allowed identification of the Hiks and Rres that perceive and transduce signals of environmental stress. In this chapter, we summarize recent progress in the identification of regulatory two-component systems. In addition, we discuss the potential roles of Spks, DNA supercoiling, sigma factors and transcription factors in the regulation of the responses of cyanobacterial cells to various types of stress.
Keywords
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- cph -:
-
gene for cyanobacterial phytochrome;
- crt -:
-
gene for carotenoid metabolism; phytoene desaturase;
- etr -:
-
gene for ethylene-receptor;
- fab -:
-
gene for fatty-acid biosynthesis;
- feo -:
-
gene for ferrous iron transport;
- FTIR-:
-
Fourier-transform infrared spectrometry;
- Fus -:
-
gene for fusion;
- glo -:
-
gene for glyoxylase (lactoylglutathione lyase);
- htp -:
-
gene for heat-tolerance protein;
- Hik-:
-
histidine kinase;
- hli- :
-
gene for high light-inducible protein;
- kdp -:
-
gene for high-affinity potassium transporter;
- nbl -:
-
gene for phycobilisome degradation protein;
- ndh -:
-
gene for NADH dehydrogenase;
- pgr -:
-
gene for plant growth regulator;
- pho -:
-
gene for low affinity to ortho-phosphate;
- rbp -:
-
gene for RNA binding protein;
- Rre-:
-
response regulator;
- sig -:
-
RNA polymerase sigma factor;
- sph -:
-
gene for Synechocystis phosphate sensor/regulator;
- Spk-:
-
serine/threonine protein kinase;
- Tyr-:
-
tyrosine protein kinases
References
Adamcik J, Viglasky V, Valle F, Antalik M, Podhradsky D, Dietler G (2002) Effect of bacteria growth temperature on the distribution of supercoiled DNA and its thermal stability. Electrophoresis 23:3300-3309
Aguilar PS, Hernandez-Arriaga AM, Cybulski LE, Erazo AC, de Mendoza D (2001) Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J 20:1681-1691
Allakhverdiev SI, Nishiyama Y, Miyairi S, Yamamoto H, Inagaki N, Kanesaki Y, Murata N (2002) Salt stress inhibits the repair of photodamaged Photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiol 130:1443-1453
Aoyama T, Takanami M (1988) Supercoiling response of E. coli promoters with different spacer lengths. Biochim Biophys Acta 949:311-317
Aravind L, Anantharaman V, Iyer LM (2003) Evolutionary connections between bacterial and eukaryotic signaling systems: a genomic perspective. Curr Opin Microbiol 6:490-497
Bartsevich VV, Pakrasi HB (1995) Molecular identification of an ABC transporter complex for manganese: analysis of a cyanobacterial mutant strain impaired in the photosynthetic oxygen evolution process. EMBO J 14:1845-1853
Bartsevich VV, Pakrasi HB (1996) Manganese transport in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 271:26057-26061
Bartsevich VV, Shestakov SV (1995) The dspA gene product of the cyanobacterium Synechocystis sp. strain PCC 6803 influences sensitivity to chemically different growth inhibitors and has amino acid similarity to histidine protein kinases. Microbiology 141:2915-2920
Cheung KJ, Badarinarayana V, Selinger DW, Janse D, Church GM (2003) A microarray-based antibiotic screen identifies a regulatory role for supercoiling in the osmotic stress response of Escherichia coli. Genome Res 13206-215
Conter A, Menchon C, Gutierrez C (1997) Role of DNA supercoiling and rpoS sigma factor in the osmotic and growth phase-dependent induction of the gene osmE of Escherichia coli K12. J Mol Biol 273:75-83
Dorman CJ (1996) Flexible response: DNA supercoiling, transcription and bacterial adaptation to environmental stress. Trends Microbiol 4:214-216
Duplessis MR, Karol KG, Adman ET, Choi LY, Jacobs MA, Cattolico RA (2007) Chloroplast His-to-Asp signal transduction: a potential mechanism for plastid gene regulation in Heterosigma akashiwo (Raphidophyceae). BMC Evol Biol 7:70. http://www.biomedcentral.com/1471-2148/7/70 (May 3, 2007)
Elhai J, Wolk CP (1988) Conjugal transfer of DNA into cyanobacteria. Methods Enzymol 167:747-765
Fiedler B, Broc D, Schubert H, Rediger A, Boerner T, Wilde A (2004) Involvement of cyanobacterial phytochromes in growth under different light qualities and quantities. Photochem Photobiol 79:551-555
Franco RJ, Drlica K (1989) Gyrase inhibitors can increase gyrA expression and DNA supercoiling. J Bacteriol 171:6573-6579
Galkin AN, Mikheeva LE, Shestakov SV (2003) Insertional inactivation of genes encoding eukaryotic-type serine/threonine protein kinases in the cyanobacterium Synechocystis sp. PCC 6803. Mikrobiologiia 72:64-69
Gellert M, O’Dea MH, Itoh T, Tomizawa J (1976) Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase. Proc Natl Acad Sci USA 73:4474-4478
Gilmour D, Gellert M (1961) The binding of p-chloromercuribenzoate by myosin. Arch Biochem Biophys 93:605-616
Glatz A, Vass I, Los DA, Vigh L (1999) The Synechocystis model of stress: from molecular chaperons to membranes. Plant Physiol Biochem 37:1-12
Graeme-Cook KA, May G, Bremer E, Higgins CF (1989) Osmotic regulation of porin expression: a role for DNA supercoiling. Mol Microbiol 3:1287-1294
Grau R, Gardiol D, Glikin GC, de Mendoza D (1994) DNA supercoiling and thermal regulation of unsaturated fatty acid synthesis in Bacillus subtilis. Mol Microbiol 11:933-941
Haselkorn R (1991) Genetic systems in cyanobacteria. Methods Enzymol 204:418-430
Hecker M, Schumann W, Volker U (1996) Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol 19:417-428
Higgins CF, Dorman CJ, Stirling DA, Waddell L, Booth IR, May G, Bremer E (1988) A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell 52:569-584
Hirani TA, Suzuki I, Murata N, Hayashi H, Eaton-Rye JJ (2001) Characterization of a two-component signal transduction system involved in the induction of alkaline phosphatase under phosphate-limiting conditions in Synechocystis sp. PCC 6803. Plant Mol Biol 45:133-144
Hsiao HY, He Q, Van Waasbergen LG, Grossman AR (2004) Control of photosynthetic and high light-responsive genes by the histidine kinase DspA: negative and positive regulation and interactions between signal transduction pathways. J Bacteriol 186:3882-3888
Hübschmann T, Yamamoto H, Gieler T, Murata N, Börner T (2005) Red and far-red light alter the transcript profile in the cyanobacterium Synechocystis sp. PCC 6803: impact of cyanobacterial phytochromes. FEBS Lett 579:1613-1618
Hughes J, Lamparter T, Mittmann F, Hartmann E, Gartner W, Wilde A, Boerner T (1997) A prokaryotic phytochrome. Nature 386:663
Hulko M, Berndt F, Gruber M, Linder JU, Truffault V, Schultz A, Martin J, Schultz JE, Lupas AN, Coles M (2006) The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126:929-940
Inaba M, Suzuki I, Szalontai B, Kanesaki Y, Los DA, Hayashi H, Murata N (2003) Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J Biol Chem 278:12191-12198
Iwasaki H, Williams SB, Kitayama Y, Ishiura M, Golden SS, Kondo T (2000) A kaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobacteria. Cell 101:223-233
Jorissen HJ, Quest B, Remberg A, Coursin T, Braslavsky SE, Schaffner K, Tandeau de Marsac N, Gartner W (2002) Two independent, light-sensing, two-component systems in a filamentous cyanobacterium. Eur J Biochem 269:2662-2671
Jung K, Veen M, Altendorf K (2000) K+ and ionic strength directly influence the autophosphorylation activity of the putative turgor sensor KdpD of Escherichia coli. J Biol Chem 275:40142-40147
Juntarajumnong W, Hirani TA, Simpson JM, Incharoensakdi A, Eaton-Rye JJ (2007) Phosphate sensing in Synechocystis sp. PCC 6803: SphU and the SphS-SphR two-component regulatory system. Arch Microbiol 188:389-402
Kamei A, Yuasa T, Orikawa K, Geng XX, Ikeuchi M (2001) A eukaryotic-type protein kinase, SpkA, is required for normal motility of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183:1505-1510
Kamei A, Yoshihara S, Yuasa T, Geng X, Ikeuchi M (2003) Biochemical and functional characterization of a eukaryotic-type protein kinase, SpkB, in the cyanobacterium Synechocystis sp. PCC 6803. Curr Microbiol 46:296-301
Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:185-209
Kaneko T, Nakamura Y, Sasamoto S, Watanabe A, Kohara M, Matsumoto M, Shimpo S, Yamada M, Tabata S (2003) Structural analysis of four large plasmids harboring in a unicellular cyanobacterium, Synechocystis sp. PCC 6803. DNA Res 10:221-228
Kanesaki Y, Suzuki I, Allakhverdiev SI, Mikami K, Murata N (2002) Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803. Biochem Biophys Res Commun 290:339-348
Kanesaki Y, Yamamoto H, Paithoonrangsarid K, Shoumskaya M, Suzuki I, Hayashi H, Murata N (2007) Histidine kinases play important roles in the perception and signal transduction of H2O2 in the cyanobacterium Synechocystis. Plant J 49:313-324
Kappell AD, van Waasbergen LG (2007) The response regulator RpaB binds the high light regulatory 1 sequence upstream of the high light-inducible hliB gene from the cyanobacterium Synechocystis PCC 6803. Arch Microbiol 187:337-342
Kehoe DM, Grossman AR (1994) Complementary chromatic adaptation: photoperception to gene regulation. Semin Cell Biol 5:303-313
Kehoe DM, Grossman AR (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273:1409-1412
Koretke KK, Lupas AN, Warren PV, Rosenberg M, Brown JR (2000) Evolution of two-component signal transduction. Mol Biol Evol 17:1956-1970
Leonard CJ, Aravind L, Koonin EV (1998) Novel families of putative protein kinases in bacteria and archaea: evolution of the “eukaryotic” protein kinase superfamily. Genome Res 8:1038-1047
Li H, Sherman LA (2000) A redox-responsive regulator of photosynthesis gene expression in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 182:4268-4277
Lopez-Maury L, Garcia-Dominguez M, Florencio FJ, Reyes JC (2002) A two-component signal transduction system involved in nickel sensing in the cyanobacterium Synechocystis sp. PCC 6803. Mol Microbiol 43:247-256
López-Maury L, Florencio FJ, Reyes JC (2003) Arsenic sensing and resistance system in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 185:5363-5371
Los DA (2004) The effect of low-temperature-induced DNA supercoiling on the expression of the desaturase genes in Synechocystis. Cell Mol Biol 50:605-612
Los DA, Murata N (1999) Responses to cold shock in cyanobacteria. J Mol Microbiol Biotechnol 1:221-230
Los DA, Murata N (2000) Regulation of enzymatic activity and gene expression by membrane fluidity. Science’s Signal Transduction Knowledge Environment 62: PE1. http://www.stke.org/cgi/content/full/OC_sigtrans;2000/62/pe1
Los DA, Murata N (2002) Sensing and response to low temperature in cyanobacteria. In: Storey KB, Storey JM (eds) Cell and molecular responses to stress, sensing, signaling and cell adaptation, vol 3. Elsevier, Amsterdam, pp 139-153
Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666:142-157
Marin K, Suzuki I, Yamaguchi K, Ribbeck K, Yamamoto H, Kanesaki Y, Hagemann M, Murata N (2003) Identification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp. PCC 6803. Proc Natl Acad Sci USA 100:9061-9066
Mikami K, Murata N (2003) Membrane fluidity and the perception of environmental signals in cyanobacteria and plants. Prog Lipid Res 42:527-543
Mikami K, Kanesaki Y, Suzuki I, Murata N (2002) The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp. PCC 6803. Mol Microbiol 46:905-915
Mizuno T, Kaneko T, Tabata S (1996) Compilation of all genes encoding bacterial two-component signal transducers in the genome of the cyanobacterium Synechocystis sp. strain PCC 6803. DNA Res 3:407-414
Murata N, Los DA (2006) Histidine kinase Hik33 is an important participant in cold signal transduction in cyanobacteria. Physiol Plant 126:17-27
Murata N, Suzuki I (2006) Exploitation of genomic sequences in a systematic analysis to access how cyanobacteria sense environmental stress. J Exp Bot 57:235-247
Murata N, Wada H (1995) Acyl-lipid desaturases, their importance in the tolerance and acclimatization to cold of cyanobacteria. Biochem J 308:1-8
Nakamoto H, Suzuki M, Kojima K (2003) Targeted inactivation of the hrcA repressor gene in cyanobacteria. FEBS Lett 549:57-62
Ogawa T, Bao DH, Katoh H, Shibata M, Pakrasi HB, Bhattacharyya-Pakrasi M (2002) A two-component signal transduction pathway regulates manganese homeostasis in Synechocystis 6803, a photosynthetic organism. J Biol Chem 277:28981-28986
Okamoto S, Ikeuchi M, Ohmori M (1999) Experimental analysis of recently transposed insertion sequences in the cyanobacterium Synechocystis sp. PCC 6803. DNA Res 6:265-273
Osanai T, Kanesaki Y, Nakano T, Takahashi H, Asayama M, Shirai M, Kanehisa M, Suzuki I, Murata N, Tanaka K (2005) Positive regulation of sugar catabolic pathways in the cyanobacterium Synechocystis sp. PCC 6803 by the group 2 sigma factor sigE. J Biol Chem 280:30653-30659
Paithoonrangsarid K, Shoumskaya MA, Kanesaki Y, Satoh S, Tabata S, Los DA, Zinchenko VV, Hayashi H, Tanticharoen M, Suzuki I, Murata N (2004) Five histidine kinases perceive osmotic stress and regulate distinct sets of genes in Synechocystis. J Biol Chem 279:53078-53086
Panichkin VB, Arakawa-Kobayashi S, Kanaseki T, Suzuki I, Los DA, Shestakov SV, Murata N (2006) Serine/threonine protein kinase, SpkA, in Synechocystis sp. PCC 6803 is a regulator of expression of three putative pilA operons, formation of thick pili and cell motility. J Bacteriol 188:7696-7699
Schmitz O, Katayama M, Williams SB, Kondo T, Golden SS (2000) CikA, a bacterio-phytochrome, that resets the cyanobacterial circadian clock. Science 289:765-768
Shi L, Potts M, Kennelly PJ (1998) The serine, threonine and/or tyrosine-specific protein kinases and protein phosphatases of prokaryotic organisms: A family portrait. FEMS Microbiol Rev 22:229-253
Shoumskaya MA, Paithoonrangsarid K, Kanesaki Y, Los DA, Zinchenko VV, Tanticharoen M, Suzuki I, Murata N (2005) Identical Hik-Rre systems are involved in perception and transduction of salt signals and hyperosmotic signals but regulate the expression of individual genes to different extents in Synechocystis. J Biol Chem 80:21531-21538
Sineshchekov V, Hughes J, Hartmann E, Lamparter T (1998) Fluorescence and photochemistry of recombinant phytochrome from the cyanobacterium Synechocystis. Photochem Photobiol 67:263-267
Sineshchekov OA, Trivedi VD, Sasaki J, Spudich JL (2005) Photochromicity of Anabaena sensory rhodopsin, an atypical microbial receptor with a cis-retinal light-adapted form. J Biol Chem 280:14663-14668
Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183-215
Suzuki I, Los DA, Kanesaki Y, Mikami K, Murata N (2000) The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J 19:1327-1334
Suzuki I, Kanesaki Y, Mikami K, Kanehisa M, Murata N (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Microbiol 40:235-244
Suzuki S, Ferjani A, Suzuki I, Murata N (2004) The SphS-SphR two component system is the exclusive sensor for the induction of gene expression in response to phosphate limitation in Synechocystis. J Biol Chem 279:13234-13240
Suzuki I, Kanesaki Y, Hayashi H, Hall JJ, Simon WJ, Slabas AR, Murata N (2005) The histidine kinase Hik34 is involved in thermotolerance by regulating the expression of heat-shock genes in Synechocystis. Plant Physiol 138:1409-1421
Szalontai B, Nishiyama Y, Gombos Z, Murata N (2000) Membrane dynamics as seen by Fourier Transform Infrared Spectroscopy in a cyanobacterium, Synechocystis PCC 6803: The effects of lipid unsaturation and the protein-to-lipid ratio. Biochim Biophys Acta 1509:409-419
Takai N, Nakajima M, Oyama T, Kito R, Sugita C, Sugita M, Kondo T, Iwasaki H (2006) A KaiC-associating SasA-RpaA two-component regulatory system as a major circadian timing mediator in cyanobacteria. Proc Natl Acad Sci USA 103:12109-12114
Tao W, Malone CL, Ault AD, Deschenes RJ, Fassler JS (2002) A cytoplasmic coiled-coil domain is required for histidine kinase activity of the yeast osmosensor SLN1. Mol Microbiol 43:459-473
Tasaka Y, Gombos Z, Nishiyama Y, Mohanty P, Ohba T, Ohki K, Murata N (1996) Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: Evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis. EMBO J 15:6416-6425
Taylor BL, Zhulin IB (1999) PAS domains: internal sensors of oxygen, redox potential and light. Microbiol Mol Biol Rev 63:479-506
Tu CJ, Shrager J, Burnap RL, Postier BL, Grossman AR (2004) Consequences of a deletion in dspA on transcript accumulation in Synechocystis sp. strain PCC 6803. J Bacteriol 186:3889-3902
van Waasbergen LG, Dolganov N, Grossman AR (2002) nblS, a gene involved in controlling photosynthesis-related gene expression during high light and nutrient stress in Synechococcus elongatus PCC 7942. J Bacteriol 184:2481-2490
Vermaas WF (1998) Gene modifications and mutation mapping to study the function of photosystem II. Methods Enzymol 297:293-310
Vogeley L, Sineshchekov OA, Trivedi VD, Sasaki J, Spudich JL, Luecke H (2004) Anabaena sensory rhodopsin: a photochromic color sensor at 2.0 A. Science 306:1390-1393
Walderhaug MO, Polarek JW, Voelkner P, Daniel JM, Hesse JE, Altendorf K, Epstein W (1992) KdpD and KdpE, proteins that control expression of the kdpABC operon, are members of the two-component sensor-effector class of regulators. J Bacteriol 174:2152-2159
Wang HL, Postier BL, Burnap RL (2004a) Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. J Biol Chem 279:5739-5751
Wang JC, Lynch AS (1993) Transcription and DNA supercoiling. Curr Opin Genet Dev 3:764-768
Wang T, Shen G, Balasubramanian R, McIntosh L, Bryant DA, Golbeck JH (2004b) The sufR gene (sll0088 in Synechocystis sp. strain PCC 6803) functions as a repressor of the sufBCDS operon in iron-sulfur cluster biogenesis in cyanobacteria. J Bacteriol 186:956-967
Weinstein-Fischer D, Elgrably-Weiss M, Altuvia S (2000) Escherichia coli response to hydrogen peroxide: a role for DNA supercoiling, topoisomerase I and Fis. Mol Microbiol 35:1413-1420
Widmann C, Gibson S, Jarpe MB, Johnson GL (1999) Mitogen activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79:143-180
Wilde A, Churin Y, Schubert H, Boerner T (1997) Disruption of a Synechocystis sp. PCC 6803 gene with partial similarity to phytochrome genes alters growth under changing light qualities. FEBS Lett 406:89-92
Williams JGK (1988) Construction of specific mutations in Photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis PCC6803. Methods Enzymol 167:766-778
Williams SB, Stewart V (1999) Functional similarities among two-component sensors and methyl-accepting chemotaxis proteins suggest a role for linker region amphipathic helices in transmembrane signal transduction. Mol Microbiol 33:1093-1102
Yamaguchi K, Suzuki I, Yamamoto H, Lyukevich A, Bodrova I, Los DA, Piven I, Zinchenko V, Kanehisa M, Murata N (2002) A two-component Mn2+-sensing system negatively regulates expression of the mntCAB operon in Synechocystis. Plant Cell 14:2901-2913
Yeh KC, Wu SH, Murphy JT, Lagarias JC (1997) A cyanobacterial phytochrome two-component light-sensory system. Science 277:1505-1508
Zabulon G, Richaud C, Guidi-Rontani C, Thomas JC (2007) NblA gene expression in Synechocystis PCC 6803 strains lacking DspA (Hik33) and an NblR-like protein. Curr Microbiol 54:36-41
Zhang CC, Gonzalez L, Phalip V (1998) Survey, analysis and genetic organization of genes encoding eukaryotic-like signaling proteins on a cyanobacterial genome. Nucleic Acids Res 26:3619-3625
Zhang CC, Jang J, Sakr S, Wang L (2005) Protein phosphorylation on Ser, Thr and Tyr residues in cyanobacteria. J Mol Microbiol Biotechnol 9:154-166
Acknowledgements
This work has been supported by the Cooperative Research Program of the National Institute for Basic Biology, Japan, by a Sasagawa Scientific Research Grant from the Japan Science Society to Y.K., a grant from the Russian Foundation for Basic Research (no. 09-04-01074) and a grant from the “Molecular and Cell Biology Program” of the Russian Academy of Sciences to D.A.L.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Kanesaki, Y., Los, D.A., Suzuki, I., Murata, N. (2009). Sensors and Signal Transducers of Environmental Stress in Cyanobacteria. In: Pareek, A., Sopory, S., Bohnert, H. (eds) Abiotic Stress Adaptation in Plants. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3112-9_2
Download citation
DOI: https://doi.org/10.1007/978-90-481-3112-9_2
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-90-481-3111-2
Online ISBN: 978-90-481-3112-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)